Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-24T20:10:02.793Z Has data issue: false hasContentIssue false
  • English
  • Français

A review of fundamental principles for animal models of DOHaD research: an Australian perspective

Part of: DOHaD ANZ Conference 2015

Published online by Cambridge University Press:  30 September 2016

H. Dickinson ,
T. J. Moss ,
K. L. Gatford ,
K. M. Moritz ,
L. Akison ,
T. Fullston ,
D. H. Hryciw ,
C. A. Maloney ,
M. J. Morris  and
A. L. Wooldridge
...Show all authors
H. Dickinson*
Affiliation:
The Ritchie Centre, Hudson Institute of Medical Research, Monash University, Clayton, VIC, Australia
T. J. Moss
Affiliation:
The Ritchie Centre, Hudson Institute of Medical Research, Monash University, Clayton, VIC, Australia
K. L. Gatford
Affiliation:
School of Medicine and Robinson Research Institute, University of Adelaide, Adelaide, SA, Australia
K. M. Moritz
Affiliation:
School of Biomedical Sciences, The University of Queensland, St Lucia, QLD, Australia
L. Akison
Affiliation:
School of Biomedical Sciences, The University of Queensland, St Lucia, QLD, Australia
T. Fullston
Affiliation:
School of Medicine and Robinson Research Institute, University of Adelaide, Adelaide, SA, Australia
D. H. Hryciw
Affiliation:
Department of Physiology, University of Melbourne, Parkville, VIC, Australia
C. A. Maloney
Affiliation:
School of Medical Sciences, UNSW Australia, Sydney, NSW, Australia
M. J. Morris
Affiliation:
School of Medical Sciences, UNSW Australia, Sydney, NSW, Australia
A. L. Wooldridge
Affiliation:
School of Medicine and Robinson Research Institute, University of Adelaide, Adelaide, SA, Australia
J. E. Schjenken
Affiliation:
School of Medicine and Robinson Research Institute, University of Adelaide, Adelaide, SA, Australia
S. A. Robertson
Affiliation:
School of Medicine and Robinson Research Institute, University of Adelaide, Adelaide, SA, Australia
B. J. Waddell
Affiliation:
Faculty of Science, The University of Western Australia, Crawley, WA, Australia
P. J. Mark
Affiliation:
Faculty of Science, The University of Western Australia, Crawley, WA, Australia
C. S. Wyrwoll
Affiliation:
Faculty of Science, The University of Western Australia, Crawley, WA, Australia
S. J. Ellery
Affiliation:
The Ritchie Centre, Hudson Institute of Medical Research, Monash University, Clayton, VIC, Australia
K. L. Thornburg
Affiliation:
Heart Research Center, Oregon Health & Science University, Portland, OR, USA
B. S. Muhlhausler
Affiliation:
School of Agriculture, Food and Wine, FOODplus Research Centre, The University of Adelaide, Adelaide, SA, Australia
J. L. Morrison
Affiliation:
School of Pharmacy and Medical Sciences, Sansom Institute for Health Research, University of South Australia, Adelaide, SA, Australia
*
*Address for correspondence: H. Dickinson, The Ritchie Centre, Hudson Institute of Medical Research, Monash University, 27-31 Wright Street, Clayton, VIC 3168, Australia. (Email [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Epidemiology formed the basis of ‘the Barker hypothesis’, the concept of ‘developmental programming’ and today’s discipline of the Developmental Origins of Health and Disease (DOHaD). Animal experimentation provided proof of the underlying concepts, and continues to generate knowledge of underlying mechanisms. Interventions in humans, based on DOHaD principles, will be informed by experiments in animals. As knowledge in this discipline has accumulated, from studies of humans and other animals, the complexity of interactions between genome, environment and epigenetics, has been revealed. The vast nature of programming stimuli and breadth of effects is becoming known. As a result of our accumulating knowledge we now appreciate the impact of many variables that contribute to programmed outcomes. To guide further animal research in this field, the Australia and New Zealand DOHaD society (ANZ DOHaD) Animals Models of DOHaD Research Working Group convened at the 2nd Annual ANZ DOHaD Congress in Melbourne, Australia in April 2015. This review summarizes the contributions of animal research to the understanding of DOHaD, and makes recommendations for the design and conduct of animal experiments to maximize relevance, reproducibility and translation of knowledge into improving health and well-being.

Keywords

developmental stageoutcome/systemdevelopmental origins of health and diseaseprogramming
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 7 , Issue 5: Themed Issue: Australia/New Zealand 2015 DOHaD Scientific Meeting: Advances and Updates , October 2016 , pp. 449 - 472
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Prescott, SL, Allen, K, Armstrong, K, et al. The establishment of DOHaD working groups in Australia and New Zealand. J Dev Orig Health Dis. 2016; 1–7. doi:10.1017/S2040174416000167.Google ScholarPubMed
2. Fleming, A, Copp, AJ. Embryonic folate metabolism and mouse neural tube defects. Science. 1998; 280, 2107–2109.CrossRefGoogle ScholarPubMed
3. Denny, KJ, Jeanes, A, Fathe, K, et al. Neural tube defects, folate, and immune modulation. Birth Defects Res A Clin Mol Teratol. 2013; 97, 602–609.CrossRefGoogle ScholarPubMed
4. Kilkenny, C, Browne, WJ, Cuthill, IC, Emerson, M, Altman, DG. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 2010; 8, e1000412.CrossRefGoogle ScholarPubMed
5. Dobbing, J, Sands, J. Comparative aspects of the brain growth spurt. Early Hum Dev. 1979; 3, 79–83.CrossRefGoogle ScholarPubMed
6. Ballesteros, MC, Hansen, PE, Soila, K. MR imaging of the developing human brain. Part 2. Postnatal development. Radiographics. 1993; 13, 611–622.CrossRefGoogle ScholarPubMed
7. Derrick, M, Luo, NL, Bregman, JC, et al. Preterm fetal hypoxia-ischemia causes hypertonia and motor deficits in the neonatal rabbit: a model for human cerebral palsy? J Neurosci. 2004; 24, 24–34.CrossRefGoogle Scholar
8. Chung, Y, So, K, Kim, E, Kim, S, Jeon, Y. Immunoreactivity of neurogenic factor in the guinea pig brain after prenatal hypoxia. Ann Anat. 2015; 200, 66–72.CrossRefGoogle ScholarPubMed
9. Quinn, TA, Ratnayake, U, Dickinson, H, Castillo-Melendez, M, Walker, DW. Ontogenetic change in the regional distribution of dehydroepiandrosterone-synthesizing enzyme and the glucocorticoid receptor in the brain of the spiny mouse (Acomys cahirinus). Dev Neurosci. 2016; 38, 54–73.CrossRefGoogle ScholarPubMed
10. Barlow, RM. The foetal sheep: morphogenesis of the nervous system and histochemical aspects of myelination. J Comp Neurol. 1969; 135, 249–262.CrossRefGoogle ScholarPubMed
11. Watson, RE, Desesso, JM, Hurtt, ME, Cappon, GD. Postnatal growth and morphological development of the brain: a species comparison. Birth Defects Res B Dev Reprod Toxicol. 2006; 77, 471–484.CrossRefGoogle Scholar
12. Hunter, DS, Hazel, SJ, Kind, KL, et al. Programming the brain: common outcomes and gaps in knowledge from animal studies of IUGR. Physiol Behav. 2016; 164(Pt A), 233–248.CrossRefGoogle ScholarPubMed
13. Sinclair, KD, Allegrucci, C, Singh, R, et al. DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci U S A. 2007; 104, 19351–19356.CrossRefGoogle ScholarPubMed
14. Morton, AJ, Rudiger, SR, Wood, NI, et al. Early and progressive circadian abnormalities in Huntington’s disease sheep are unmasked by social environment. Hum Mol Genet. 2014; 23, 3375–3383.CrossRefGoogle ScholarPubMed
15. Hernandez, CE, Matthews, LR, Oliver, MH, Bloomfield, FH, Harding, JE. Effects of sex, litter size and periconceptional ewe nutrition on offspring behavioural and physiological response to isolation. Physiol Behav. 2010; 101, 588–594.CrossRefGoogle ScholarPubMed
16. Burton, GJ, Fowden, AL. Review: the placenta and developmental programming: balancing fetal nutrient demands with maternal resource allocation. Placenta. 2012; 33(Suppl), S23–S27.CrossRefGoogle ScholarPubMed
17. Wallace, JM, Regnault, TR, Limesand, SW, Hay, WW Jr, Anthony, RV. Investigating the causes of low birth weight in contrasting ovine paradigms. J Physiol. 2005; 565(Pt 1), 19–26.CrossRefGoogle ScholarPubMed
18. Woods, LL. Maternal glucocorticoids and prenatal programming of hypertension. Am J Physiol Regul Integr Comp Physiol. 2006; 291, R1069–R1075.CrossRefGoogle ScholarPubMed
19. Gray, SP, Denton, KM, Cullen-McEwen, L, Bertram, JF, Moritz, KM. Prenatal exposure to alcohol reduces nephron number and raises blood pressure in progeny. J Am Soc Nephrol. 2010; 21, 1891–1902.CrossRefGoogle ScholarPubMed
20. Varcoe, TJ, Boden, MJ, Voultsios, A, et al. Characterisation of the maternal response to chronic phase shifts during gestation in the rat: implications for fetal metabolic programming. PLoS One. 2013; 8, e53800.CrossRefGoogle ScholarPubMed
21. Barclay, JL, Husse, J, Bode, B, et al. Circadian desynchrony promotes metabolic disruption in a mouse model of shiftwork. PLoS One. 2012; 7, e37150.CrossRefGoogle Scholar
22. Constancia, M, Hemberger, M, Hughes, J, et al. Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature. 2002; 417, 945–948.CrossRefGoogle Scholar
23. Sibley, CP, Coan, PM, Ferguson-Smith, AC, et al. Placental-specific insulin-like growth factor 2 (Igf2) regulates the diffusional exchange characteristics of the mouse placenta. Proc Natl Acad Sci U S A. 2004; 101, 8204–8208.CrossRefGoogle ScholarPubMed
24. Montgomery, MK, Hallahan, NL, Brown, SH, et al. Mouse strain-dependent variation in obesity and glucose homeostasis in response to high-fat feeding. Diabetologia. 2013; 56, 1129–1139.CrossRefGoogle ScholarPubMed
25. Stringer, JM, Pask, AJ, Shaw, G, Renfree, MB. Post-natal imprinting: evidence from marsupials. Heredity. 2014; 113, 145–155.CrossRefGoogle ScholarPubMed
26. Bennett, GA, Palliser, HK, Shaw, JC, Walker, D, Hirst, JJ. Prenatal stress alters hippocampal neuroglia and increases anxiety in childhood. Dev Neurosci. 2015; 37, 533–545.CrossRefGoogle ScholarPubMed
27. Shaw, JC, Palliser, HK, Walker, DW, Hirst, JJ. Preterm birth affects GABAA receptor subunit mRNA levels during the foetal-to-neonatal transition in guinea pigs. J Dev Orig Health Dis. 2015; 6, 250–260.CrossRefGoogle ScholarPubMed
28. Kind, KL, Clifton, PM, Grant, PA, et al. Effect of maternal feed restriction during pregnancy on glucose tolerance in the adult guinea pig. Am J Physiol Regul Integr Comp Physiol. 2003; 284, R140–R152.CrossRefGoogle ScholarPubMed
29. Sferruzzi-Perri, AN, Owens, JA, Pringle, KG, Robinson, JS, Roberts, CT. Maternal insulin-like growth factors-I and -II act via different pathways to promote fetal growth. Endocrinology. 2006; 147, 3344–3355.CrossRefGoogle ScholarPubMed
30. Sferruzzi-Perri, AN, Owens, JA, Standen, P, et al. Early treatment of the pregnant guinea pig with IGFs promotes placental transport and nutrient partitioning near term. Am J Physiol Endocrinol Metab. 2007; 292, E668–E676.CrossRefGoogle ScholarPubMed
31. Sferruzzi-Perri, AN, Owens, JA, Standen, P, et al. Early pregnancy maternal endocrine insulin-like growth factor I programs the placenta for increased functional capacity throughout gestation. Endocrinology. 2007; 148, 4362–4370.CrossRefGoogle ScholarPubMed
32. Dickinson, H, Ellery, S, Ireland, Z, et al. Creatine supplementation during pregnancy: summary of experimental studies suggesting a treatment to improve fetal and neonatal morbidity and reduce mortality in high-risk human pregnancy. BMC Pregnancy Childbirth. 2014; 14, 150.CrossRefGoogle ScholarPubMed
33. Bellofiore, N, Ellery, SJ, Mamrot, J, et al. First report of a menstruating rodent: the spiny mouse (Acomys cahirinus). BioRxiv. 2016; 056895.Google ScholarPubMed
34. Dickinson, H, Walker, DW, Wintour, EM, Moritz, K. Maternal dexamethasone treatment at midgestation reduces nephron number and alters renal gene expression in the fetal spiny mouse. Am J Physiol Regul Integr Comp Physiol. 2007; 292, R453–R461.CrossRefGoogle ScholarPubMed
35. Quinn, TA, Ratnayake, U, Castillo-Melendez, M, et al. Adrenal steroidogenesis following prenatal dexamethasone exposure in the spiny mouse. J Endocrinol. 2014; 221, 347–362.CrossRefGoogle ScholarPubMed
36. O’Connell, BA, Moritz, KM, Walker, DW, Dickinson, H. Synthetic glucocorticoid dexamethasone inhibits branching morphogenesis in the spiny mouse placenta. Biol Reprod. 2013; 88, 26.Google ScholarPubMed
37. Dodic, M, Abouantoun, T, O’Connor, A, Wintour, EM, Moritz, KM. Programming effects of short prenatal exposure to dexamethasone in sheep. Hypertension. 2002; 40, 729–734.CrossRefGoogle ScholarPubMed
38. O’Sullivan, L, Cuffe, JS, Paravicini, TM, et al. Prenatal exposure to dexamethasone in the mouse alters cardiac growth patterns and increases pulse pressure in aged male offspring. PLoS One. 2013; 8, e69149.CrossRefGoogle ScholarPubMed
39. Singh, RR, Moritz, KM, Bertram, JF, Cullen-McEwen, LA. Effects of dexamethasone exposure on rat metanephric development: in vitro and in vivo studies. Am J Physiol Renal Physiol. 2007; 293, F548–F554.CrossRefGoogle ScholarPubMed
40. Rivera, HM, Kievit, P, Kirigiti, MA, et al. Maternal high-fat diet and obesity impact palatable food intake and dopamine signaling in nonhuman primate offspring. Obesity. 2015; 23, 2157–2164.CrossRefGoogle ScholarPubMed
41. Moritz, KM, Wintour, EM, Black, MJ, Bertram, JF, Caruana, G. Factors influencing mammalian kidney development: implications for health in adult life. Adv Anat Embryol Cell Biol. 2008; 196, 1–78.Google ScholarPubMed
42. Gatford, KL, Simmons, RA, De Blasio, MJ, Robinson, JS, Owens, JA. Review: placental programming of postnatal diabetes and impaired insulin action after IUGR. Placenta. 2010; 31(Suppl), S60–S65.CrossRefGoogle ScholarPubMed
43. Paus, T, Collins, DL, Evans, AC, et al. Maturation of white matter in the human brain: a review of magnetic resonance studies. Brain Res Bull. 2001; 54, 255–266.CrossRefGoogle Scholar
44. Rattanatray, L, MacLaughlin, SM, Kleemann, DO, et al. Impact of maternal periconceptional overnutrition on fat mass and expression of adipogenic and lipogenic genes in visceral and subcutaneous fat depots in the postnatal lamb. Endocrinology. 2010; 151, 5195–5205.CrossRefGoogle ScholarPubMed
45. Zhang, S, Rattanatray, L, MacLaughlin, SM, et al. Periconceptional undernutrition in normal and overweight ewes leads to increased adrenal growth and epigenetic changes in adrenal IGF2/H19 gene in offspring. FASEB J. 2010; 24, 2772–2782.CrossRefGoogle ScholarPubMed
46. Garg, M, Thamotharan, M, Dai, Y, Lee, PW, Devaskar, SU. Embryo-transfer of the F2 postnatal calorie restricted female rat offspring into a control intra-uterine environment normalizes the metabolic phenotype. Metabolism. 2013; 62, 432–441.CrossRefGoogle ScholarPubMed
47. Thamotharan, M, Garg, M, Oak, S, et al. Transgenerational inheritance of the insulin-resistant phenotype in embryo-transferred intrauterine growth-restricted adult female rat offspring. Am J Physiol Endocrinol Metab. 2007; 292, E1270–E1279.CrossRefGoogle ScholarPubMed
48. Tran, M, Gallo, LA, Hanvey, AN, et al. Embryo transfer cannot delineate between the maternal pregnancy environment and germ line effects in the transgenerational transmission of disease in rats. Am J Physiol Regul Integr Comp Physiol. 2014; 306, R607–R618.CrossRefGoogle ScholarPubMed
49. Sjoblom, C, Roberts, CT, Wikland, M, Robertson, SA. Granulocyte-macrophage colony-stimulating factor alleviates adverse consequences of embryo culture on fetal growth trajectory and placental morphogenesis. Endocrinology. 2005; 146, 2142–2153.CrossRefGoogle ScholarPubMed
50. Calle, A, Fernandez-Gonzalez, R, Ramos-Ibeas, P, et al. Long-term and transgenerational effects of in vitro culture on mouse embryos. Theriogenology. 2012; 77, 785–793.CrossRefGoogle ScholarPubMed
51. Fauque, P, Ripoche, MA, Tost, J, et al. Modulation of imprinted gene network in placenta results in normal development of in vitro manipulated mouse embryos. Hum Mol Genet. 2010; 19, 1779–1790.CrossRefGoogle ScholarPubMed
52. Rivera, RM, Stein, P, Weaver, JR, et al. Manipulations of mouse embryos prior to implantation result in aberrant expression of imprinted genes on day 9.5 of development. Hum Mol Genet. 2008; 17, 1–14.CrossRefGoogle ScholarPubMed
53. Chen, M, Wu, L, Zhao, J, et al. Altered glucose metabolism in mouse and humans conceived by IVF. Diabetes. 2014; 63, 3189–3198.CrossRefGoogle ScholarPubMed
54. Davies, MJ, Moore, VM, Willson, KJ, et al. Reproductive technologies and the risk of birth defects. N Engl J Med. 2012; 366, 1803–1813.CrossRefGoogle ScholarPubMed
55. Lazaraviciute, G, Kauser, M, Bhattacharya, S, Haggarty, P, Bhattacharya, S. A systematic review and meta-analysis of DNA methylation levels and imprinting disorders in children conceived by IVF/ICSI compared with children conceived spontaneously. Hum Reprod Update. 2014; 20, 840–852.CrossRefGoogle ScholarPubMed
56. Combelles, CM, Albertini, DF. Assessment of oocyte quality following repeated gonadotropin stimulation in the mouse. Biol Reprod. 2003; 68, 812–821.CrossRefGoogle ScholarPubMed
57. Kalthur, G, Salian, SR, Nair, R, et al. Distribution pattern of cytoplasmic organelles, spindle integrity, oxidative stress, octamer-binding transcription factor 4 (Oct4) expression and developmental potential of oocytes following multiple superovulation. Reprod Fertil Dev. 2015; doi:10.1071/RD15184 (e-pub ahead of print).Google Scholar
58. Kanayama, K, Osada, H. The yield of abnormal unfertilized eggs observed after repeated gonadotrophin-induced ovulation. J Int Med Res. 2000; 28, 24–27.CrossRefGoogle ScholarPubMed
59. Van Blerkom, J, Davis, P. Differential effects of repeated ovarian stimulation on cytoplasmic and spindle organization in metaphase II mouse oocytes matured in vivo and in vitro. Hum Reprod. 2001; 16, 757–764.CrossRefGoogle ScholarPubMed
60. Albertini, DF, Sanfins, A, Combelles, CM. Origins and manifestations of oocyte maturation competencies. Reprod Biomed Online. 2003; 6, 410–415.CrossRefGoogle ScholarPubMed
61. Elbling, L, Colot, M. Abnormal development and transport and increased sister-chromatid exchange in preimplantation embryos following superovulation in mice. Mutat Res. 1985; 147, 189–195.CrossRefGoogle ScholarPubMed
62. Vogel, R, Spielmann, H. Genotoxic and embryotoxic effects of gonadotropin-hyperstimulated ovulation of murine oocytes, preimplantation embryos, and term fetuses. Reprod Toxicol. 1992; 6, 329–333.CrossRefGoogle ScholarPubMed
63. Ertzeid, G, Storeng, R. The impact of ovarian stimulation on implantation and fetal development in mice. Hum Reprod. 2001; 16, 221–225.CrossRefGoogle ScholarPubMed
64. Van der Auwera, I, D’Hooghe, T. Superovulation of female mice delays embryonic and fetal development. Hum Reprod. 2001; 16, 1237–1243.CrossRefGoogle ScholarPubMed
65. McKiernan, SH, Bavister, BD. Gonadotrophin stimulation of donor females decreases post-implantation viability of cultured one-cell hamster embryos. Hum Reprod. 1998; 13, 724–729.CrossRefGoogle ScholarPubMed
66. Santos, MA, Kuijk, EW, Macklon, NS. The impact of ovarian stimulation for IVF on the developing embryo. Reproduction. 2010; 139, 23–34.CrossRefGoogle ScholarPubMed
67. Boomsma, CM, Kavelaars, A, Eijkemans, MJ, et al. Ovarian stimulation for in vitro fertilization alters the intrauterine cytokine, chemokine, and growth factor milieu encountered by the embryo. Fertil Steril. 2010; 94, 1764–1768.CrossRefGoogle ScholarPubMed
68. Sibug, RM, Helmerhorst, FM, Tijssen, AM, de Kloet, ER, de Koning, J. Gonadotrophin stimulation reduces VEGF(120) expression in the mouse uterus during the peri-implantation period. Hum Reprod. 2002; 17, 1643–1648.CrossRefGoogle ScholarPubMed
69. Miller, BG, Armstrong, DT. Superovulatory doses of pregnant mare serum gonadotropin cause delayed implantation and infertility in immature rats. Biol Reprod. 1981; 25, 253–260.CrossRefGoogle ScholarPubMed
70. Cora, MC, Kooistra, L, Travlos, G. Vaginal cytology of the laboratory rat and mouse: review and criteria for the staging of the estrous cycle using stained vaginal smears. Toxicol Pathol. 2015; 43, 776–793.CrossRefGoogle ScholarPubMed
71. Mamrot, J, Pangestu, M, Walker, D, Gardner, DK, Dickinson, H. Confirmed dioestrus in pseudopregnant mice using vaginal exfoliative cytology improves embryo transfer implantation rate. Reprod Biomed Online. 2015; 31, 538–543.CrossRefGoogle ScholarPubMed
72. Rezac, P. Potential applications of electrical impedance techniques in female mammalian reproduction. Theriogenology. 2008; 70, 1–14.CrossRefGoogle ScholarPubMed
73. Bartos, L. Vaginal impedance measurement used for mating in the rat. Lab Anim. 1977; 11, 53–55.CrossRefGoogle ScholarPubMed
74. Jaramillo, LM, Balcazar, IB, Duran, C. Using vaginal wall impedance to determine estrous cycle phase in Lewis rats. Lab Anim. 2012; 41, 122–128.CrossRefGoogle ScholarPubMed
75. Roulo, RM, Fishburn, JD, Alworth, L, Hoberman, AM, Smith, MA. Producing timed-pregnant Mongolian gerbils for developmental studies. Lab Anim. 2013; 42, 380–383.CrossRefGoogle ScholarPubMed
76. Stiles, RJ, Schrum, AG, Gil, D. A co-housing strategy to improve fecundity of mice in timed matings. Lab Anim. 2013; 42, 62–65.CrossRefGoogle ScholarPubMed
77. Scharmann, W, Wolff, D. Production of timed pregnant mice by utilization of the Whitten effect and a simple cage system. Lab Anim Sci. 1980; 30(Pt 1), 206–208.Google Scholar
78. Gangrade, BK, Dominic, CJ. Studies of the male-originating pheromones involved in the Whitten effect and Bruce effect in mice. Biol Reprod. 1984; 31, 89–96.CrossRefGoogle ScholarPubMed
79. Whitten, WK. Modification of the oestrous cycle of the mouse by external stimuli associated with the male. J Endocrinol. 1956; 13, 399–404.CrossRefGoogle ScholarPubMed
80. Dalal, SJ, Estep, JS, Valentin-Bon, IE, Jerse, AE. Standardization of the Whitten effect to induce susceptibility to Neisseria gonorrhoeae in female mice. Contemp Top Lab Anim Sci. 2001; 40, 13–17.Google ScholarPubMed
81. Iida, K, Kobayashi, N, Kohno, H, Miyamoto, A, Fukui, Y. A comparative study of induction of estrus and ovulation by three different intravaginal devices in ewes during the non-breeding season. J Reprod Dev. 2004; 50, 63–69.CrossRefGoogle ScholarPubMed
82. Schjenken, JE, Robertson, SA. Seminal fluid signalling in the female reproductive tract: implications for reproductive success and offspring health. Adv Exp Med Biol. 2015; 868, 127–158.CrossRefGoogle ScholarPubMed
83. Casas, E, Vavouri, T. Sperm epigenomics: challenges and opportunities. Front Genet. 2014; 5, 330.CrossRefGoogle ScholarPubMed
84. Sung, TI, Wang, JD, Chen, PC. Increased risks of infant mortality and of deaths due to congenital malformation in the offspring of male electronics workers. Birth Defects Res A Clin Mol Teratol. 2009; 85, 119–124.CrossRefGoogle ScholarPubMed
85. Chang, JS. Parental smoking and childhood leukemia. Methods Mol Biol. 2009; 472, 103–137.CrossRefGoogle ScholarPubMed
86. Linschooten, JO, Verhofstad, N, Gutzkow, K, et al. Paternal lifestyle as a potential source of germline mutations transmitted to offspring. FASEB J. 2013; 27, 2873–2879.CrossRefGoogle ScholarPubMed
87. Danielzik, S, Langnase, K, Mast, M, Spethmann, C, Muller, MJ. Impact of parental BMI on the manifestation of overweight 5-7 year old children. Eur J Nutr. 2002; 41, 132–138.CrossRefGoogle ScholarPubMed
88. Ng, SF, Lin, RC, Laybutt, DR, et al. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature. 2010; 467, 963–966.CrossRefGoogle ScholarPubMed
89. Fullston, T, Ohlsson Teague, EM, Palmer, NO, et al. Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content. FASEB J. 2013; 27, 4226–4243.CrossRefGoogle Scholar
90. Gapp, K, Soldado-Magraner, S, Alvarez-Sanchez, M, et al. Early life stress in fathers improves behavioural flexibility in their offspring. Nat Commun. 2014; 5, 5466.CrossRefGoogle ScholarPubMed
91. Kong, A, Frigge, ML, Masson, G, et al. Rate of de novo mutations and the importance of father’s age to disease risk. Nature. 2012; 488, 471–475.CrossRefGoogle ScholarPubMed
92. Bromfield, JJ, Schjenken, JE, Chin, PY, et al. Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring. Proc Natl Acad Sci U S A. 2014; 111, 2200–2205.CrossRefGoogle ScholarPubMed
93. Brykczynska, U, Hisano, M, Erkek, S, et al. Repressive and active histone methylation mark distinct promoters in human and mouse spermatozoa. Nat Struct Mol Biol. 2010; 17, 679–687.CrossRefGoogle ScholarPubMed
94. Siklenka, K, Erkek, S, Godmann, M, et al. Disruption of histone methylation in developing sperm impairs offspring health transgenerationally. Science. 2015; 350, aab2006.CrossRefGoogle ScholarPubMed
95. Trasler, JM. Epigenetics in spermatogenesis. Mol Cell Endocrinol. 2009; 306, 33–36.CrossRefGoogle ScholarPubMed
96. Jenkins, TG, Carrell, DT. The sperm epigenome and potential implications for the developing embryo. Reproduction. 2012; 143, 727–734.CrossRefGoogle ScholarPubMed
97. Filkowski, JN, Ilnytskyy, Y, Tamminga, J, et al. Hypomethylation and genome instability in the germline of exposed parents and their progeny is associated with altered miRNA expression. Carcinogenesis. 2010; 31, 1110–1115.CrossRefGoogle ScholarPubMed
98. Grandjean, V, Gounon, P, Wagner, N, et al. The miR-124-Sox9 paramutation: RNA-mediated epigenetic control of embryonic and adult growth. Development. 2009; 136, 3647–3655.CrossRefGoogle ScholarPubMed
99. Rassoulzadegan, M, Grandjean, V, Gounon, P, et al. RNA-mediated non-Mendelian inheritance of an epigenetic change in the mouse. Nature. 2006; 441, 469–474.CrossRefGoogle ScholarPubMed
100. Rodgers, AB, Morgan, CP, Leu, NA, Bale, TL. Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc Natl Acad Sci U S A. 2015; 112, 13699–13704.CrossRefGoogle ScholarPubMed
101. Wagner, KD, Wagner, N, Ghanbarian, H, et al. RNA induction and inheritance of epigenetic cardiac hypertrophy in the mouse. Dev Cell. 2008; 14, 962–969.CrossRefGoogle ScholarPubMed
102. Wang, Y, Medvid, R, Melton, C, Jaenisch, R, Blelloch, R. DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat Genet. 2007; 39, 380–385.CrossRefGoogle ScholarPubMed
103. O’Dowd, R, Wlodek, ME, Nicholas, KR. Uteroplacental insufficiency alters the mammary gland response to lactogenic hormones in vitro. Reprod Fertil Dev. 2008; 20, 460–465.CrossRefGoogle ScholarPubMed
104. Briffa, JF, McAinch, AJ, Romano, T, Wlodek, ME, Hryciw, DH. Leptin in pregnancy and development: a contributor to adulthood disease? Am J Physiol Endocrinol Metab. 2015; 308, E335–E350.CrossRefGoogle ScholarPubMed
105. Hager, R, Cheverud, JM, Wolf, JB. Change in maternal environment induced by cross-fostering alters genetic and epigenetic effects on complex traits in mice. Proc Biol Sci. 2009; 276, 2949–2954.Google ScholarPubMed
106. Siebel, AL, Gallo, LA, Guan, TC, Owens, JA, Wlodek, ME. Cross-fostering and improved lactation ameliorates deficits in endocrine pancreatic morphology in growth-restricted adult male rat offspring. J Dev Orig Health Dis. 2010; 1, 234–244.CrossRefGoogle ScholarPubMed
107. Denenberg, VH, Grota, LJ, Zarrow, MX. Maternal behaviour in the rat: analysis of cross-fostering. J Reprod Fertil. 1963; 5, 133–141.CrossRefGoogle ScholarPubMed
108. Smith, JT, Waddell, BJ. Increased fetal glucocorticoid exposure delays puberty onset in postnatal life. Endocrinology. 2000; 141, 2422–2428.CrossRefGoogle ScholarPubMed
109. Barbazanges, A, Vallee, M, Mayo, W, et al. Early and later adoptions have different long-term effects on male rat offspring. J Neurosci. 1996; 16, 7783–7790.CrossRefGoogle ScholarPubMed
110. Matsumoto, M, Higuchi, K, Togashi, H, et al. Early postnatal stress alters the 5-HTergic modulation to emotional stress at postadolescent periods of rats. Hippocampus. 2005; 15, 775–781.CrossRefGoogle ScholarPubMed
111. Romano, T, Wark, JD, Owens, JA, Wlodek, ME. Prenatal growth restriction and postnatal growth restriction followed by accelerated growth independently program reduced bone growth and strength. Bone. 2009; 45, 132–141.CrossRefGoogle ScholarPubMed
112. Siebel, AL, Mibus, A, De Blasio, MJ, et al. Improved lactational nutrition and postnatal growth ameliorates impairment of glucose tolerance by uteroplacental insufficiency in male rat offspring. Endocrinology. 2008; 149, 3067–3076.CrossRefGoogle ScholarPubMed
113. Oben, JA, Mouralidarane, A, Samuelsson, AM, et al. Maternal obesity during pregnancy and lactation programs the development of offspring non-alcoholic fatty liver disease in mice. J Hepatol. 2010; 52, 913–920.CrossRefGoogle ScholarPubMed
114. Champagne, FA, Francis, DD, Mar, A, Meaney, MJ. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav. 2003; 79, 359–371.CrossRefGoogle ScholarPubMed
115. Babicky, A, Ostadalova, I, Parizek, J, Kolar, J, Bibr, B. Onset and duration of the physiological weaning period for infant rats reared in nests of different sizes. Physiol Bohemoslov. 1973; 22, 449–456.Google ScholarPubMed
116. Boubred, F, Daniel, L, Buffat, C, et al. Early postnatal overfeeding induces early chronic renal dysfunction in adult male rats. Am J Physiol Renal Physiol. 2009; 297, F943–F951.CrossRefGoogle ScholarPubMed
117. Munoz-Valverde, D, Rodriguez-Rodriguez, P, Gutierrez-Arzapalo, PY, et al. Effect of fetal undernutrition and postnatal overfeeding on rat adipose tissue and organ growth at early stages of postnatal development. Physiol Res. 2015; 64, 547–559.CrossRefGoogle ScholarPubMed
118. O’Dowd, R, Kent, JC, Moseley, JM, Wlodek, ME. Effects of uteroplacental insufficiency and reducing litter size on maternal mammary function and postnatal offspring growth. Am J Physiol Regul Integr Comp Physiol. 2008; 294, R539–R548.CrossRefGoogle ScholarPubMed
119. Wadley, GD, Siebel, AL, Cooney, GJ, et al. Uteroplacental insufficiency and reducing litter size alters skeletal muscle mitochondrial biogenesis in a sex-specific manner in the adult rat. Am J Physiol Endocrinol Metab. 2008; 294, E861–E869.CrossRefGoogle Scholar
120. Bai, SL, Campbell, SE, Moore, JA, Morales, MC, Gerdes, AM. Influence of age, growth, and sex on cardiac myocyte size and number in rats. Anat Rec. 1990; 226, 207–212.CrossRefGoogle ScholarPubMed
121. Velkoska, E, Cole, TJ, Dean, RG, Burrell, LM, Morris, MJ. Early undernutrition leads to long-lasting reductions in body weight and adiposity whereas increased intake increases cardiac fibrosis in male rats. J Nutr. 2008; 138, 1622–1627.CrossRefGoogle ScholarPubMed
122. Alleva, E, Caprioli, A, Laviola, G. Litter gender composition affects maternal behavior of the primiparous mouse dam (Mus musculus). J Comp Psychol. 1989; 103, 83–87.CrossRefGoogle ScholarPubMed
123. Federation of Animal Science Societies 2010. Guide for the care and use of agricultural animals in research and teaching. Champaign (IL): Federation of Animal Science Societies.Google Scholar
124. Toth, LA. The influence of the cage environment on rodent physiology and behavior: implications for reproducibility of pre-clinical rodent research. Exp Neurol. 2015; 270, 72–77.CrossRefGoogle ScholarPubMed
125. Skinner, MK. Environmental stress and epigenetic transgenerational inheritance. BMC Med. 2014; 12, 153.CrossRefGoogle ScholarPubMed
126. Gallo, LA, Tran, M, Cullen-McEwen, LA, et al. Transgenerational programming of fetal nephron deficits and sex-specific adult hypertension in rats. Reprod Fertil Dev. 2014; 26, 1032–1043.CrossRefGoogle ScholarPubMed
127. Weyrich, A, Lenz, D, Jeschek, M, et al. Paternal intergenerational epigenetic response to heat exposure in male wild guinea pigs. Mol Ecol. 2016; 25, 1729–1740.CrossRefGoogle ScholarPubMed
128. Long, NM, Shasa, DR, Ford, SP, Nathanielsz, PW. Growth and insulin dynamics in two generations of female offspring of mothers receiving a single course of synthetic glucocorticoids. Am J Obstet Gynecol. 2012; 207, 203 e201–203 e208.CrossRefGoogle ScholarPubMed
129. Long, NM, Ford, SP, Nathanielsz, PW. Multigenerational effects of fetal dexamethasone exposure on the hypothalamic-pituitary-adrenal axis of first- and second-generation female offspring. Am J Obstet Gynecol. 2013; 208, 217 e211–217 e218.CrossRefGoogle ScholarPubMed
130. Long, NM, Smith, DT, Ford, SP, Nathanielsz, PW. Elevated glucocorticoids during ovine pregnancy increase appetite and produce glucose dysregulation and adiposity in their granddaughters in response to ad libitum feeding at 1 year of age. Am J Obstet Gynecol. 2013; 209, 353 e351–353 e359.CrossRefGoogle ScholarPubMed
131. Beery, AK, Zucker, I. Sex bias in neuroscience and biomedical research. Neurosci Biobehav Rev. 2011; 35, 565–572.CrossRefGoogle ScholarPubMed
132. Farkas, RH, Unger, EF, Temple, R. Zolpidem and driving impairment – identifying persons at risk. N Engl J Med. 2013; 369, 689–691.CrossRefGoogle ScholarPubMed
133. Prendergast, BJ, Onishi, KG, Zucker, I. Female mice liberated for inclusion in neuroscience and biomedical research. Neurosci Biobehav Rev. 2014; 40, 1–5.CrossRefGoogle ScholarPubMed
134. Aiken, CE, Ozanne, SE. Sex differences in developmental programming models. Reproduction. 2013; 145, R1–R13.CrossRefGoogle ScholarPubMed
135. Dunn, GA, Morgan, CP, Bale, TL. Sex-specificity in transgenerational epigenetic programming. Horm Behav. 2011; 59, 290–295.CrossRefGoogle ScholarPubMed
136. Clifton, VL. Review: sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta. 2010; 31(Suppl), S33–S39.CrossRefGoogle ScholarPubMed
137. Bermejo-Alvarez, P, Rizos, D, Rath, D, Lonergan, P, Gutierrez-Adan, A. Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. Proc Natl Acad Sci U S A. 2010; 107, 3394–3399.CrossRefGoogle ScholarPubMed
138. Mulla, ZD, Plavsic, SK, Ortiz, M, Nuwayhid, BS, Ananth, CV. Fetal sex pairing and adverse perinatal outcomes in twin gestations. Ann Epidemiol. 2013; 23, 7–12.CrossRefGoogle ScholarPubMed
139. Jost, A, Vigier, B, Prepin, J. Freemartins in cattle: the first steps of sexual organogenesis. J Reprod Fertil. 1972; 29, 349–379.CrossRefGoogle ScholarPubMed
140. Ryan, BC, Vandenbergh, JG. Intrauterine position effects. Neurosci Biobehav Rev. 2002; 26, 665–678.CrossRefGoogle ScholarPubMed
141. Madeja, Z, Yadi, H, Apps, R, et al. Paternal MHC expression on mouse trophoblast affects uterine vascularization and fetal growth. Proc Natl Acad Sci U S A. 2011; 108, 4012–4017.CrossRefGoogle ScholarPubMed
142. Ober, C, Hyslop, T, Elias, S, Weitkamp, LR, Hauck, WW. Human leukocyte antigen matching and fetal loss: results of a 10 year prospective study. Hum Reprod. 1998; 13, 33–38.CrossRefGoogle ScholarPubMed
143. Robertson, SA. Seminal plasma and male factor signalling in the female reproductive tract. Cell Tissue Res. 2005; 322, 43–52.CrossRefGoogle ScholarPubMed
144. Woidacki, K, Meyer, N, Schumacher, A, et al. Transfer of regulatory T cells into abortion-prone mice promotes the expansion of uterine mast cells and normalizes early pregnancy angiogenesis. Sci Rep. 2015; 5, 13938.CrossRefGoogle ScholarPubMed
145. Wedekind, C, Seebeck, T, Bettens, F, Paepke, AJ. MHC-dependent mate preferences in humans. Proc Biol Sci. 1995; 260, 245–249.Google ScholarPubMed
146. O’Regan, D, Kenyon, CJ, Seckl, JR, Holmes, MC. Prenatal dexamethasone ‘programmes’ hypotension, but stress-induced hypertension in adult offspring. J Endocrinol. 2008; 196, 343–352.CrossRefGoogle ScholarPubMed
147. Bol, V, Desjardins, F, Reusens, B, Balligand, JL, Remacle, C. Does early mismatched nutrition predispose to hypertension and atherosclerosis, in male mice? PLoS One. 2010; 5, pii: e12656. doi: 10.1371/journal.pone.0012656.CrossRefGoogle ScholarPubMed
148. Varcoe, TJ, Gatford, KL, Voultsios, A, et al. Rapidly alternating photoperiods disrupt central and peripheral rhythmicity and decrease plasma glucose, but do not affect glucose tolerance or insulin secretion in sheep. Exp Physiol. 2014; 99, 1214–1228.CrossRefGoogle ScholarPubMed
149. Orozco-Solis, R, Matos, RJ, Lopes de Souza, S, et al. Perinatal nutrient restriction induces long-lasting alterations in the circadian expression pattern of genes regulating food intake and energy metabolism. Int J Obes. 2011; 35, 990–1000.CrossRefGoogle ScholarPubMed
150. Thompson, JA, Sarr, O, Piorkowska, K, Gros, R, Regnault, TR. Low birth weight followed by postnatal over-nutrition in the guinea pig exposes a predominant player in the development of vascular dysfunction. J Physiol. 2014; 592(Pt 24), 5429–5443.CrossRefGoogle ScholarPubMed
151. Howat, WJ, Wilson, BA. Tissue fixation and the effect of molecular fixatives on downstream staining procedures. Methods. 2014; 70, 12–19.CrossRefGoogle ScholarPubMed
152. Suvarna, SK, Layton, C, Bancroft, JD. Bancroft’s Theory and Practice of Histological Techniques. 2013. Elsevier: Churchill Livingstone: Oxford.Google Scholar
153. Hernandez, CE, Harding, JE, Oliver, MH, et al. Effects of litter size, sex and periconceptional ewe nutrition on side preference and cognitive flexibility in the offspring. Behav Brain Res. 2009; 204, 82–87.CrossRefGoogle ScholarPubMed
154. Hunter, DS, Hazel, SJ, Kind, KL, et al. Placental and fetal growth restriction, size at birth and neonatal growth alter cognitive function and behaviour in sheep in an age- and sex-specific manner. Physiol Behav. 2015; 152(Pt A), 1–10.CrossRefGoogle Scholar
155. Vickers, MH, Breier, BH, Cutfield, WS, Hofman, PL, Gluckman, PD. Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol Endocrinol Metab. 2000; 279, E83–E87.CrossRefGoogle ScholarPubMed
156. Gugusheff, JR, Ong, ZY, Muhlhausler, BS. The early origins of food preferences: targeting the critical windows of development. FASEB J. 2015; 29, 365–373.CrossRefGoogle ScholarPubMed
157. McPherson, NO, Bell, VG, Zander-Fox, DL, et al. When two obese parents are worse than one! Impacts on embryo and fetal development. Am J Physiol Endocrinol Metab. 2015; 309, E568–E581.CrossRefGoogle ScholarPubMed
158. Wallace, JM, Milne, JS, Adam, CL, Aitken, RP. Adverse metabolic phenotype in low-birth-weight lambs and its modification by postnatal nutrition. Br J Nutr. 2012; 107, 510–522.CrossRefGoogle ScholarPubMed
159. Wyrwoll, CS, Mark, PJ, Mori, TA, Puddey, IB, Waddell, BJ. Prevention of programmed hyperleptinemia and hypertension by postnatal dietary omega-3 fatty acids. Endocrinology. 2006; 147, 599–606.CrossRefGoogle ScholarPubMed
160. Hunter, DS, Hazel, SJ, Kind, KL, et al. Do I turn left or right? Effects of sex, age, experience and exit route on maze test performance in sheep. Physiol Behav. 2015; 139, 244–253.CrossRefGoogle ScholarPubMed
161. Bouwknecht, JA, Spiga, F, Staub, DR, et al. Differential effects of exposure to low-light or high-light open-field on anxiety-related behaviors: relationship to c-Fos expression in serotonergic and non-serotonergic neurons in the dorsal raphe nucleus. Brain Res Bull. 2007; 72, 32–43.CrossRefGoogle ScholarPubMed
162. Bonuccelli, S, Muscelli, E, Gastaldelli, A, et al. Improved tolerance to sequential glucose loading (Staub-Traugott effect): size and mechanisms. Am J Physiol Endocrinol Metab. 2009; 297, E532–E537.CrossRefGoogle ScholarPubMed
163. Banjanin, S, Kapoor, A, Matthews, SG. Prenatal glucocorticoid exposure alters hypothalamic-pituitary-adrenal function and blood pressure in mature male guinea pigs. J Physiol. 2004; 558(Pt 1), 305–318.CrossRefGoogle ScholarPubMed
164. Kapoor, A, Matthews, SG. Short periods of prenatal stress affect growth, behaviour and hypothalamo-pituitary-adrenal axis activity in male guinea pig offspring. J Physiol. 2005; 566(Pt 3), 967–977.CrossRefGoogle ScholarPubMed
165. Welberg, LA, Seckl, JR, Holmes, MC. Inhibition of 11beta-hydroxysteroid dehydrogenase, the foeto-placental barrier to maternal glucocorticoids, permanently programs amygdala GR mRNA expression and anxiety-like behaviour in the offspring. Eur J Neurosci. 2000; 12, 1047–1054.CrossRefGoogle ScholarPubMed
166. Waddell, BJ, Bollen, M, Wyrwoll, CS, Mori, TA, Mark, PJ. Developmental programming of adult adrenal structure and steroidogenesis: effects of fetal glucocorticoid excess and postnatal dietary omega-3 fatty acids. J Endocrinol. 2010; 205, 171–178.CrossRefGoogle ScholarPubMed
167. Poore, KR, Boullin, JP, Cleal, JK, et al. Sex- and age-specific effects of nutrition in early gestation and early postnatal life on hypothalamo-pituitary-adrenal axis and sympathoadrenal function in adult sheep. J Physiol. 2010; 588(Pt 12), 2219–2237.CrossRefGoogle ScholarPubMed
168. Bloomfield, FH, Oliver, MH, Giannoulias, CD, et al. Brief undernutrition in late-gestation sheep programs the hypothalamic-pituitary-adrenal axis in adult offspring. Endocrinology. 2003; 144, 2933–2940.CrossRefGoogle ScholarPubMed
169. Bloomfield, FH, Oliver, MH, Harding, JE. Effects of twinning, birth size, and postnatal growth on glucose tolerance and hypothalamic-pituitary-adrenal function in postpubertal sheep. Am J Physiol Endocrinol Metab. 2007; 292, E231–E237.CrossRefGoogle ScholarPubMed
170. Esler, M, Eikelis, N, Schlaich, M, et al. Chronic mental stress is a cause of essential hypertension: presence of biological markers of stress. Clin Exp Pharmacol Physiol. 2008; 35, 498–502.CrossRefGoogle ScholarPubMed
171. Nowotny, B, Cavka, M, Herder, C, et al. Effects of acute psychological stress on glucose metabolism and subclinical inflammation in patients with post-traumatic stress disorder. Horm Metab Res. 2010; 42, 746–753.CrossRefGoogle ScholarPubMed
172. Schilling, TM, Kolsch, M, Larra, MF, et al. For whom the bell (curve) tolls: cortisol rapidly affects memory retrieval by an inverted U-shaped dose-response relationship. Psychoneuroendocrinology. 2013; 38, 1565–1572.CrossRefGoogle ScholarPubMed
173. Bailey, CJ, Flatt, PR. Insulin and glucagon during pentobarbitone anaesthesia. Diabete Metab. 1980; 6, 91–95.Google ScholarPubMed
174. Liu, H, Schultz, CG, De Blasio, MJ, et al. Effect of placental restriction and neonatal exendin-4 treatment on postnatal growth, adult body composition, and in vivo glucose metabolism in the sheep. Am J Physiol Endocrinol Metab. 2015; 309, E589–E600.CrossRefGoogle ScholarPubMed
175. Moss, TJ, Doherty, DA, Nitsos, I, et al. Effects into adulthood of single or repeated antenatal corticosteroids in sheep. Am J Obstet Gynecol. 2005; 192, 146–152.CrossRefGoogle ScholarPubMed
176. Owens, JA, Thavaneswaran, P, De Blasio, MJ, et al. Sex-specific effects of placental restriction on components of the metabolic syndrome in young adult sheep. Am J Physiol Endocrinol Metab. 2007; 292, E1879–E1889.CrossRefGoogle ScholarPubMed
177. Brunton, PJ, Sullivan, KM, Kerrigan, D, et al. Sex-specific effects of prenatal stress on glucose homoeostasis and peripheral metabolism in rats. J Endocrinol. 2013; 217, 161–173.CrossRefGoogle ScholarPubMed
178. Smith, JW, Seckl, JR, Evans, AT, Costall, B, Smythe, JW. Gestational stress induces post-partum depression-like behaviour and alters maternal care in rats. Psychoneuroendocrinology. 2004; 29, 227–244.CrossRefGoogle ScholarPubMed
179. Nicholas, LM, Rattanatray, L, MacLaughlin, SM, et al. Differential effects of maternal obesity and weight loss in the periconceptional period on the epigenetic regulation of hepatic insulin-signaling pathways in the offspring. FASEB J. 2013; 27, 3786–3796.CrossRefGoogle ScholarPubMed
180. Nicholas, LM, Rattanatray, L, Morrison, JL, et al. Maternal obesity or weight loss around conception impacts hepatic fatty acid metabolism in the offspring. Obesity (Silver Spring). 2014; 22, 1685–1693.CrossRefGoogle ScholarPubMed
181. Nicholas, LM, Morrison, JL, Rattanatray, L, et al. Differential effects of exposure to maternal obesity or maternal weight loss during the periconceptional period in the sheep on insulin signalling molecules in skeletal muscle of the offspring at 4 months of age. PLoS One. 2013; 8, e84594.CrossRefGoogle ScholarPubMed
182. Zhang, S, Rattanatray, L, MacLaughlin, SM, et al. Periconceptional undernutrition in normal and overweight ewes leads to increased adrenal growth and epigenetic changes in adrenal IGF2/H19 gene in offspring. FASEB J. 2010; 24, 2772–2782.CrossRefGoogle ScholarPubMed
183. Dong, F, Ford, SP, Fang, CX, et al. Maternal nutrient restriction during early to mid gestation up-regulates cardiac insulin-like growth factor (IGF) receptors associated with enlarged ventricular size in fetal sheep. Growth Horm IGF Res. 2005; 15, 291–299.CrossRefGoogle ScholarPubMed
184. Ford, SP, Zhang, L, Zhu, M, et al. Maternal obesity accelerates fetal pancreatic beta-cell but not alpha-cell development in sheep: prenatal consequences. Am J Physiol Regul Integr Comp Physiol. 2009; 297, R835–R843.CrossRefGoogle Scholar
185. George, LA, TUthlaut, AB, Long, NM, et al. Different levels of overnutrition and weight gain during pregnancy have differential effects on fetal growth and organ development. Reprod Biol Endocrinol. 2010; 8, 75–85.CrossRefGoogle ScholarPubMed
186. Long, NM, Nathanielsz, PW, Ford, SP. The impact of maternal overnutrition and obesity on hypothalamic-pituitary-adrenal axis response of offspring to stress. Domest Anim Endocrinol. 2012; 42, 195–202.CrossRefGoogle ScholarPubMed
187. Ma, Y, Zhu, MJ, Zhang, L, et al. Maternal obesity and overnutrition alter fetal growth rate and cotyledonary vascularity and angiogenic factor expression in the ewe. Am J Physiol Regul Integr Comp Physiol. 2010; 299, R249–R258.CrossRefGoogle ScholarPubMed
188. Muhlhausler, BS, Adam, CL, Findlay, PA, Duffield, JA, McMillen, IC. Increased maternal nutrition alters development of the appetite-regulating network in the brain. FASEB J. 2006; 20, 1257–1259.CrossRefGoogle ScholarPubMed
189. Muhlhausler, BS, Roberts, CT, Yuen, BS, et al. Determinants of fetal leptin synthesis, fat mass, and circulating leptin concentrations in well-nourished ewes in late pregnancy. Endocrinology. 2003; 144, 4947–4954.CrossRefGoogle ScholarPubMed
190. Muhlhausler, BS, Duffield, JA, McMillen, IC. Increased maternal nutrition increases leptin expression in perirenal and subcutaneous adipose tissue in the postnatal lamb. Endocrinology. 2007; 148, 6157–6163.CrossRefGoogle ScholarPubMed
191. Fernandez-Twinn, DS, Blackmore, HL, Siggens, L, et al. The programming of cardiac hypertrophy in the offspring by maternal obesity is associated with hyperinsulinemia, AKT, ERK, and mTOR activation. Endocrinology. 2012; 153, 5961–5971.CrossRefGoogle ScholarPubMed
192. Alfaradhi, MZ, Fernandez-Twinn, DS, Martin-Gronert, MS, et al. Oxidative stress and altered lipid homeostasis in the programming of offspring fatty liver by maternal obesity. Am J Physiol Regul Integr Comp Physiol. 2014; 307, R26–R34.CrossRefGoogle ScholarPubMed
193. Desai, M, Jellyman, JK, Han, G, et al. Maternal obesity and high-fat diet program offspring metabolic syndrome. Am J Obstet Gynecol. 2014; 211, 237.e231–237.e213.CrossRefGoogle ScholarPubMed
194. Gugusheff, JR, Ong, ZY, Muhlhausler, BS. A maternal ‘junk-food’ diet reduces sensitivity to the opioid antagonist naloxone in offspring postweaning. FASEB J. 2013; 27, 1275–1284.CrossRefGoogle Scholar
195. Simar, D, Chen, H, Lambert, K, Mercier, J, Morris, MJ. Interaction between maternal obesity and post-natal over-nutrition on skeletal muscle metabolism. Nutr Metab Cardiovasc Dis. 2012; 22, 269–276.CrossRefGoogle ScholarPubMed
196. Chen, H, Simar, D, Lambert, K, Mercier, J, Morris, MJ. Maternal and postnatal overnutrition differentially impact appetite regulators and fuel metabolism. Endocrinology. 2008; 149, 5348–5356.CrossRefGoogle ScholarPubMed
197. Morris, MJ, Chen, H. Established maternal obesity in the rat reprograms hypothalamic appetite regulators and leptin signaling at birth. Int J Obes (Lond). 2009; 33, 115–122.CrossRefGoogle ScholarPubMed
198. Chen, H, Morris, MJ. Differential responses of orexigenic neuropeptides to fasting in offspring of obese mothers. Obesity (Silver Spring). 2009; 17, 1356–1362.CrossRefGoogle ScholarPubMed
199. Gugusheff, JR, Vithayathil, M, Ong, ZY, Muhlhausler, BS. The effects of prenatal exposure to a ‘junk food’ diet on offspring food preferences and fat deposition can be mitigated by improved nutrition during lactation. J Dev Orig Health Dis. 2013; 4, 348–357.CrossRefGoogle ScholarPubMed
200. Clayton, ZE, Vickers, MH, Bernal, A, Yap, C, Sloboda, DM. Early life exposure to fructose alters maternal, fetal and neonatal hepatic gene expression and leads to sex-dependent changes in lipid metabolism in rat offspring. PLoS One. 2015; 10, e0141962.CrossRefGoogle ScholarPubMed
201. Gray, C, Harrison, CJ, Segovia, SA, Reynolds, CM, Vickers, MH. Maternal salt and fat intake causes hypertension and sustained endothelial dysfunction in fetal, weanling and adult male resistance vessels. Sci Rep. 2015; 5, 9753.CrossRefGoogle ScholarPubMed
202. Howie, GJ, Sloboda, DM, Reynolds, CM, Vickers, MH. Timing of maternal exposure to a high fat diet and development of obesity and hyperinsulinemia in male rat offspring: same metabolic phenotype, different developmental pathways? J Nutr Metab. 2013; 2013, 517384.CrossRefGoogle ScholarPubMed
203. Fullston, T, McPherson, NO, Owens, JA, et al. Paternal obesity induces metabolic and sperm disturbances in male offspring that are exacerbated by their exposure to an ‘obesogenic’ diet. Physiol Rep. 2015; 3, pii: e12336. doi: 10.14814/phy2.12336.CrossRefGoogle Scholar
204. Ng, SF, Lin, RC, Maloney, CA, et al. Paternal high-fat diet consumption induces common changes in the transcriptomes of retroperitoneal adipose and pancreatic islet tissues in female rat offspring. FASEB J. 2014; 28, 1830–1841.CrossRefGoogle ScholarPubMed
205. Fullston, T, Palmer, NO, Owens, JA, et al. Diet-induced paternal obesity in the absence of diabetes diminishes the reproductive health of two subsequent generations of mice. Hum Reprod. 2012; 27, 1391–1400.CrossRefGoogle ScholarPubMed
206. Fullston, T, Shehadeh, H, Sandeman, LY, et al. Female offspring sired by diet induced obese male mice display impaired blastocyst development with molecular alterations to their ovaries, oocytes and cumulus cells. J Assist Reprod Genet. 2015; 32, 725–735.CrossRefGoogle ScholarPubMed
207. Grissom, NM, Lyde, R, Christ, L, et al. Obesity at conception programs the opioid system in the offspring brain. Neuropsychopharmacology. 2014; 39, 801–810.CrossRefGoogle ScholarPubMed
208. Muhlhausler, BS, Adam, CL, Marrocco, EM, et al. Impact of glucose infusion on the structural and functional characteristics of adipose tissue and on hypothalamic gene expression for appetite regulatory neuropeptides in the sheep fetus during late gestation. J Physiol. 2005; 565, 185–195.CrossRefGoogle ScholarPubMed
209. McGillick, EV, Morrison, JL, McMillen, IC, Orgeig, S. Intrafetal glucose infusion alters glucocorticoid signaling and reduces surfactant protein mRNA expression in the lung of the late-gestation sheep fetus. Am J Physiol Regul Integr Comp Physiol. 2014; 307, R538–R545.CrossRefGoogle ScholarPubMed
210. Edwards, LJ, McMillen, IC. Maternal undernutrition increases arterial blood pressure in the sheep fetus during late gestation. J Physiol. 2001; 533(Pt 2), 561–570.CrossRefGoogle ScholarPubMed
211. Lie, S, Morrison, JL, Williams-Wyss, O, et al. Impact of embryo number and periconceptional undernutrition on insulin signalling and gluconeogenic factors and microRNAs in the liver of fetal sheep. Am J Physiol Endocrinol Metab. 2014; 306, E1013–E1024.CrossRefGoogle ScholarPubMed
212. Lie, S, Morrison, JL, Williams-Wyss, O, et al. Impact of embryo number and maternal undernutrition around the time of conception on insulin signaling and gluconeogenic factors and microRNAs in the liver of fetal sheep. Am J Physiol Endocrinol Metab. 2014; 306, E1013–E1024.CrossRefGoogle ScholarPubMed
213. Lie, S, Morrison, JL, Williams-Wyss, O, et al. Impact of maternal undernutrition around the time of conception on factors regulating hepatic lipid metabolism and microRNAs in singleton and twin fetuses. Am J Physiol Endocrinol Metab. 2016; 310, E148–E159.CrossRefGoogle ScholarPubMed
214. Lie, S, Morrison, JL. Impact of periconceptional and preimplantation undernutrition on factors regulating myogenesis and protein synthesis in muscle of singleton and twin fetal sheep. Physiol Rep. 2015; 3, pii: e12495. doi: 10.14814/phy2.12495.CrossRefGoogle ScholarPubMed
215. Lie, S, Morrison, JL, Williams-Wyss, O, et al. Periconceptional undernutrition programs changes in insulin-signaling molecules and microRNAs in skeletal muscle in singleton and twin fetal sheep. Biol Reprod. 2014; 90, 5.CrossRefGoogle ScholarPubMed
216. Lie, S, Morrison, JL, Williams-Wyss, O, et al. Impact of embryo number and periconceptional undernutrition on factors regulating adipogenesis, lipogenesis, and metabolism in adipose tissue in the sheep fetus. Am J Physiol Endocrinol Metab. 2013; 305, E931–E941.CrossRefGoogle ScholarPubMed
217. Lie, S, Sim, SM, McMillen, IC, et al. Maternal undernutrition around the time of conception and embryo number each impact on the abundance of key regulators of cardiac growth and metabolism in the fetal sheep heart. J Dev Orig Health Dis. 2013; 4, 377–390.CrossRefGoogle ScholarPubMed
218. Edwards, LJ, McMillen, IC. Periconceptional nutrition programs development of the cardiovascular system in the fetal sheep. Am J Physiol. 2002; 283, R669–R679.Google ScholarPubMed
219. Jaquiery, AL, Oliver, MH, Honeyfield-Ross, M, Harding, JE, Bloomfield, FH. Periconceptional undernutrition in sheep affects adult phenotype only in males. J Nutr Metab. 2012; 2012, 123610.CrossRefGoogle ScholarPubMed
220. Kumarasamy, V, Mitchell, MD, Bloomfield, FH, et al. Effects of periconceptional undernutrition on the initiation of parturition in sheep. Am J Physiol Regul Integr Comp Physiol. 2005; 288, R67–R72.CrossRefGoogle ScholarPubMed
221. Thorstensen, EB, Derraik, JG, Oliver, MH, et al. Effects of periconceptional undernutrition on maternal taurine concentrations in sheep. Br J Nutr. 2012; 107, 466–472.CrossRefGoogle ScholarPubMed
222. Dong, F, Ford, SP, Nijland, MJ, Nathanielsz, PW, Ren, J. Influence of maternal undernutrition and overfeeding on cardiac ciliary neurotrophic factor receptor and ventricular size in fetal sheep. J Nutr Biochem. 2008; 19, 409–414.CrossRefGoogle ScholarPubMed
223. Han, HC, Austin, KJ, Nathanielsz, PW, et al. Maternal nutrient restriction alters gene expression in the ovine fetal heart. J Physiol. 2004; 558(Pt 1), 111–121.CrossRefGoogle ScholarPubMed
224. George, LA, Zhang, L, Tuersunjiang, N, et al. Early maternal undernutrition programs increased feed intake, altered glucose metabolism and insulin secretion, and liver function in aged female offspring. Am J Physiol Regul Integr Comp Physiol. 2012; 302, R795–R804.CrossRefGoogle ScholarPubMed
225. Hawkins, P, Steyn, C, McGarrigle, HH, et al. Effect of maternal nutrient restriction in early gestation on responses of the hypothalamic-pituitary-adrenal axis to acute isocapnic hypoxaemia in late gestation fetal sheep. Exp Physiol. 2000; 85, 85–96.CrossRefGoogle ScholarPubMed
226. Huang, Y, Yan, X, Zhao, JX, et al. Maternal obesity induces fibrosis in fetal myocardium of sheep. Am J Physiol Endocrinol Metab. 2010; 299, E968–E975.CrossRefGoogle ScholarPubMed
227. Huang, Y, Yan, X, Zhu, MJ, et al. Enhanced transforming growth factor-beta signaling and fibrogenesis in ovine fetal skeletal muscle of obese dams at late gestation. Am J Physiol Endocrinol Metab. 2010; 298, E1254–E1260.CrossRefGoogle ScholarPubMed
228. Huang, Y, Zhao, JX, Yan, X, et al. Maternal obesity enhances collagen accumulation and cross-linking in skeletal muscle of ovine offspring. PLoS One. 2012; 7, e31691.CrossRefGoogle ScholarPubMed
229. Edwards, LJ, Bryce, AE, Coulter, CL, McMillen, IC. Maternal undernutrition throughout pregnancy increases adrenocorticotrophin receptor and steroidogenic acute regulatory protein gene expression in the adrenal gland of twin fetal sheep during late gestation. Mol Cell Endocrinol. 2002; 196, 1–10.CrossRefGoogle ScholarPubMed
230. Nguyen, LT, Muhlhausler, BS, Botting, KJ, Morrison, JL. Maternal undernutrition alters fat cell size distribution, but not lipogenic gene expression, in the visceral fat of the late gestation guinea pig fetus. Placenta. 2010; 31, 902–909.CrossRefGoogle Scholar
231. Soo, PS, Hiscock, J, Botting, KJ, et al. Maternal undernutrition reduces P-glycoprotein in guinea pig placenta and developing brain in late gestation. Reprod Toxicol. 2012; 33, 374–381.CrossRefGoogle ScholarPubMed
232. Sohlstrom, A, Katsman, A, Kind, KL, et al. Food restriction alters pregnancy-associated changes in IGF and IGFBP in the guinea pig. Am J Physiol. 1998; 274(Pt 1), E410–E416.Google ScholarPubMed
233. Chan, LL, Sebert, SP, Hyatt, MA, et al. Effect of maternal nutrient restriction from early to midgestation on cardiac function and metabolism after adolescent-onset obesity. Am J Physiol Regul Integr Comp Physiol. 2009; 296, R1455–R1463.CrossRefGoogle ScholarPubMed
234. Hyatt, MA, Gopalakrishnan, GS, Bispham, J, et al. Maternal nutrient restriction in early pregnancy programs hepatic mRNA expression of growth-related genes and liver size in adult male sheep. J Endocrinol. 2007; 192, 87–97.CrossRefGoogle ScholarPubMed
235. Whorwood, CB, Firth, KM, Budge, H, Symonds, ME. Maternal undernutrition during early to midgestation programs tissue-specific alterations in the expression of the glucocorticoid receptor, 11beta-hydroxysteroid dehydrogenase isoforms, and type 1 angiotensin ii receptor in neonatal sheep. Endocrinology. 2001; 142, 2854–2864.CrossRefGoogle ScholarPubMed
236. Gardner, DS, Pearce, S, Dandrea, J, et al. Peri-implantation undernutrition programs blunted angiotensin II evoked baroreflex responses in young adult sheep. Hypertension. 2004; 43, 1290–1296.CrossRefGoogle ScholarPubMed
237. Edwards, LJ, McMillen, IC. Impact of maternal undernutrition during the periconceptional period, fetal number, and fetal sex on the development of the hypothalamo-pituitary adrenal axis in sheep during late gestation. Biol Reprod. 2002; 66, 1562–1569.CrossRefGoogle ScholarPubMed
238. Berends, LM, Fernandez-Twinn, DS, Martin-Gronert, MS, Cripps, RL, Ozanne, SE. Catch-up growth following intra-uterine growth-restriction programmes an insulin-resistant phenotype in adipose tissue. Int J Obes (Lond). 2013; 37, 1051–1057.CrossRefGoogle ScholarPubMed
239. Ferland-McCollough, D, Fernandez-Twinn, DS, Cannell, IG, et al. Programming of adipose tissue miR-483-3p and GDF-3 expression by maternal diet in type 2 diabetes. Cell Death Differ. 2012; 19, 1003–1012.CrossRefGoogle ScholarPubMed
240. Ivanova, E, Chen, JH, Segonds-Pichon, A, Ozanne, SE, Kelsey, G. DNA methylation at differentially methylated regions of imprinted genes is resistant to developmental programming by maternal nutrition. Epigenetics. 2012; 7, 1200–1210.CrossRefGoogle Scholar
241. Belkacemi, L, Jelks, A, Chen, CH, Ross, MG, Desai, M. Altered placental development in undernourished rats: role of maternal glucocorticoids. Reprod Biol Endocrinol. 2011; 9, 105.CrossRefGoogle ScholarPubMed
242. Khorram, O, Keen-Rinehart, E, Chuang, TD, Ross, MG, Desai, M. Maternal undernutrition induces premature reproductive senescence in adult female rat offspring. Fertil Steril. 2015; 103, 291–298.e292.CrossRefGoogle ScholarPubMed
243. Tosh, DN, Fu, Q, Callaway, CW, et al. Epigenetics of programmed obesity: alteration in IUGR rat hepatic IGF1 mRNA expression and histone structure in rapid vs. delayed postnatal catch-up growth. Am J Physiol Gastrointest Liver Physiol. 2010; 299, G1023–G1029.CrossRefGoogle ScholarPubMed
244. Yamada, M, Wolfe, D, Han, G, et al. Early onset of fatty liver in growth-restricted rat fetuses and newborns. Congenit Anom (Kyoto). 2011; 51, 167–173.CrossRefGoogle ScholarPubMed
245. Desai, M, Crowther, NJ, Lucas, A, Hales, CN. Organ-selective growth in the offspring of protein-restricted mothers. Br J Nutr. 1996; 76, 591–603.CrossRefGoogle ScholarPubMed
246. Williams, SJ, Campbell, ME, McMillen, IC, Davidge, ST. Differential effects of maternal hypoxia or nutrient restriction on carotid and femoral vascular function in neonatal rats. Am J Physiol. 2004; 4, 4.Google Scholar
247. Williams, SJ, Davidge, ST, Morrison, JL, McMillen, IC. Chronic hypoxia increases sensitivity to noradrenaline in small mesenteric arteries from fetal sheep in late gestation. Pediatr Res. 2005; 58, 1040.Google Scholar
248. Williams, SJ, Hemmings, DG, Mitchell, JM, McMillen, IC, Davidge, ST. Effects of maternal hypoxia or nutrient restriction during pregnancy on endothelial function in adult male rat offspring. J Physiol. 2005; 565(Pt 1), 125–135.CrossRefGoogle ScholarPubMed
249. Xu, Y, Williams, SJ, O’Brien, D, Davidge, ST. Hypoxia or nutrient restriction during pregnancy in rats leads to progressive cardiac remodeling and impairs postischemic recovery in adult male offspring. FASEB J. 2006; 20, 1251–1253.CrossRefGoogle ScholarPubMed
250. Browne, VA, Stiffel, VM, Pearce, WJ, Longo, LD, Gilbert, RD. Cardiac beta-adrenergic receptor function in fetal sheep exposed to long-term high-altitude hypoxemia. Am J Physiol. 1997; 273(Pt 2), R2022–R2031.Google ScholarPubMed
251. Gilbert, RD. Fetal myocardial responses to long-term hypoxemia. Comp Biochem Physiol A Mol Integr Physiol. 1998; 119, 669–674.CrossRefGoogle ScholarPubMed
252. Kamitomo, M, Longo, LD, Gilbert, RD. Right and left ventricular function in fetal sheep exposed to long-term high-altitude hypoxemia. Am J Physiol. 1992; 262(Pt 2), H399–H405.Google ScholarPubMed
253. Ducsay, CA, Mlynarczyk, M, Kaushal, KM, et al. Long-term hypoxia enhances ACTH response to arginine vasopressin but not corticotropin-releasing hormone in the near-term ovine fetus. Am J Physiol Regul Integr Comp Physiol. 2009; 297, R892–R899.CrossRefGoogle Scholar
254. Myers, DA, Bell, PA, Hyatt, K, Mlynarczyk, M, Ducsay, CA. Long-term hypoxia enhances proopiomelanocortin processing in the near-term ovine fetus. Am J Physiol Regul Integr Comp Physiol. 2005; 288, R1178–R1184.CrossRefGoogle ScholarPubMed
255. Myers, DA, Hyatt, K, Mlynarczyk, M, Bird, IM, Ducsay, CA. Long-term hypoxia represses the expression of key genes regulating cortisol biosynthesis in the near-term ovine fetus. Am J Physiol Regul Integr Comp Physiol. 2005; 289, R1707–R1714.CrossRefGoogle ScholarPubMed
256. Hu, XQ, Longo, LD, Gilbert, RD, Zhang, L. Effects of long-term high-altitude hypoxemia on alpha 1-adrenergic receptors in the ovine uterine artery. Am J Physiol. 1996; 270(Pt 2), H1001–H1007.Google ScholarPubMed
257. Hull, AD, Longo, LD, Long, DM, Pearce, WJ. Pregnancy alters cerebrovascular adaptation to high-altitude hypoxia. Am J Physiol. 1994; 266(Pt 2), R765–R772.Google ScholarPubMed
258. Kamitomo, M, Alonso, JG, Okai, T, Longo, LD, Gilbert, RD. Effects of long-term, high-altitude hypoxemia on ovine fetal cardiac output and blood flow distribution. Am J Obstet Gynecol. 1993; 169, 701–707.CrossRefGoogle ScholarPubMed
259. Penninga, L, Longo, LD. Ovine placentome morphology: effect of high altitude, long-term hypoxia. Placenta. 1998; 19, 187–193.CrossRefGoogle ScholarPubMed
260. Herrera, EA, Rojas, RT, Krause, BJ, et al. Cardiovascular function in term fetal sheep conceived, gestated and studied in the hypobaric hypoxia of the Andean altiplano. J Physiol. 2016; 594, 1231–1245.CrossRefGoogle ScholarPubMed
261. Thompson, JA, Gros, R, Richardson, BS, Piorkowska, K, Regnault, TR. Central stiffening in adulthood linked to aberrant aortic remodeling under suboptimal intrauterine conditions. Am J Physiol Regul Integr Comp Physiol. 2011; 301, R1731–R1737.CrossRefGoogle ScholarPubMed
262. Thompson, L, Dong, Y, Evans, L. Chronic hypoxia increases inducible NOS-derived nitric oxide in fetal guinea pig hearts. Pediatr Res. 2009; 65, 188–192.CrossRefGoogle ScholarPubMed
263. Thompson, LP, Dong, Y. Chronic hypoxia decreases endothelial nitric oxide synthase protein expression in fetal guinea pig hearts. J Soc Gynecol Investig. 2005; 12, 388–395.CrossRefGoogle ScholarPubMed
264. Herrera, EA, Pulgar, VM, Riquelme, RA, et al. High altitude chronic hypoxia during gestation and after birth modifies cardiovascular responses in newborn sheep. Am J Physiol Regul Integr Comp Physiol. 2007; 292, R2234–R2240.CrossRefGoogle ScholarPubMed
265. Giussani, DA, Salinas, CE, Villena, M, Blanco, CE. The role of oxygen in prenatal growth: studies in the chick embryo. J Physiol. 2007; 585(Pt 3), 911–917.CrossRefGoogle ScholarPubMed
266. Herrera, EA, Salinas, CE, Blanco, CE, Villena, M, Giussani, DA. High altitude hypoxia and blood pressure dysregulation in adult chickens. J Dev Orig Health Dis. 2013; 4, 69–76.CrossRefGoogle ScholarPubMed
267. Mulder, AL, Golde, JM, Goor, AA, Giussani, DA, Blanco, CE. Developmental changes in plasma catecholamine concentrations during normoxia and acute hypoxia in the chick embryo. J Physiol. 2000; 527(Pt 3), 593–599.CrossRefGoogle ScholarPubMed
268. Morrison, JL, Botting, KJ, Dyer, JL, et al. Restriction of placental function alters heart development in the sheep fetus. Am J Physiol Regul Integr Comp Physiol. 2007; 293, R306–R313.CrossRefGoogle ScholarPubMed
269. Botting, KJ, McMillen, IC, Forbes, H, Nyengaard, JR, Morrison, JL. Chronic hypoxemia in late gestation decreases cardiomyocyte number but does not change expression of hypoxia-responsive genes. J Am Heart Assoc. 2014; 3, pii: e000531. doi: 10.1161/JAHA.113.000531.CrossRefGoogle Scholar
270. Wang, KC, Brooks, DA, Summers-Pearce, B, et al. Low birth weight activates the renin-angiotensin system, but limits cardiac angiogenesis in early postnatal life. Am J Physiol Regul Integr Comp Physiol. 2015; 3, pii: e12270. doi: 10.14814/phy2.12270.Google ScholarPubMed
271. Wang, KC, Lim, CH, McMillen, IC, et al. Alteration of cardiac glucose metabolism in association to low birth weight: experimental evidence in lambs with left ventricular hypertrophy. Metabolism. 2013; 62, 1662–1672.CrossRefGoogle ScholarPubMed
272. Wang, KC, Tosh, DN, Zhang, S, et al. IGFR-Galphaq signaling and cardiac hypertrophy in the low-birth-weight lamb. Am J Physiol Regul Integr Comp Physiol. 2015; 308, R627–R635.CrossRefGoogle ScholarPubMed
273. Wang, KC, Zhang, L, McMillen, IC, et al. Fetal growth restriction and the programming of heart growth and cardiac IGF-2 expression in the lamb. J Physiol. 2011; 589(Pt 19), 4709–4722.CrossRefGoogle ScholarPubMed
274. Muhlhausler, BS, Duffield, JA, Ozanne, SE, et al. The transition from fetal growth restriction to accelerated postnatal growth: a potential role for insulin signalling in skeletal muscle. J Physiol. 2009; 587(Pt 17), 4199–4211.CrossRefGoogle ScholarPubMed
275. De Blasio, MJ, Gatford, KL, Harland, ML, Robinson, JS, Owens, JA. Placental restriction reduces insulin sensitivity and expression of insulin signaling and glucose transporter genes in skeletal muscle, but not liver, in young sheep. Endocrinology. 2012; 153, 2142–2151.CrossRefGoogle Scholar
276. Gentili, S, Morrison, JL, McMillen, IC. Intrauterine growth restriction and differential patterns of hepatic growth and expression of IGF1, PCK2, and HSDL1 mRNA in the sheep fetus in late gestation. Biol Reprod. 2009; 80, 1121–1127.CrossRefGoogle ScholarPubMed
277. Orgeig, S, Crittenden, TA, Marchant, C, McMillen, IC, Morrison, JL. Intrauterine growth restriction delays surfactant protein maturation in the sheep fetus. Am J Physiol Lung Cell Mol Physiol. 2010; 298, L575–L583.CrossRefGoogle ScholarPubMed
278. Orgeig, S, McGillick, EV, Botting, KJ, et al. Increased lung prolyl hydroxylase and decreased glucocorticoid receptor are related to decreased surfactant protein in the growth-restricted sheep fetus. Am J Physiol Lung Cell Mol Physiol. 2015; 309, L84–L97.CrossRefGoogle ScholarPubMed
279. Butler, TG, Schwartz, J, McMillen, IC. Differential effects of the early and late intrauterine environment on corticotrophic cell development. J Clin Invest. 2002; 110, 783–791.CrossRefGoogle ScholarPubMed
280. Ross, JT, Phillips, ID, Simonetta, G, et al. Differential effects of placental restriction on IGF-II, ACTH receptor and steroidogenic enzyme mRNA levels in the foetal sheep adrenal. J Neuroendocrinol. 2000; 12, 79–85.CrossRefGoogle ScholarPubMed
281. Adams, MB, Ross, JT, Butler, TG, McMillen, IC. Glucocorticoids decrease phenylethanolamine N-methyltransferase mRNA expression in the immature foetal sheep adrenal. J Neuroendocrinol. 1999; 11, 569–575.CrossRefGoogle ScholarPubMed
282. Danielson, L, McMillen, IC, Dyer, JL, Morrison, JL. Restriction of placental growth results in greater hypotensive response to α-adrenergic blockade in fetal sheep during late gestation. J Physiol. 2005; 563(Pt 2), 611–620.CrossRefGoogle ScholarPubMed
283. Dyer, JL, McMillen, IC, Warnes, KE, Morrison, JL. No evidence for an enhanced role of endothelial nitric oxide in the maintenance of arterial blood pressure in the IUGR sheep fetus. Placenta. 2009; 30, 705–710.CrossRefGoogle ScholarPubMed
284. Owens, JA, Gatford, KL, De Blasio, MJ, et al. Restriction of placental growth in sheep impairs insulin secretion but not sensitivity before birth. J Physiol. 2007; 584(Pt 3), 935–949.CrossRefGoogle Scholar
285. Duffield, JA, Vuocolo, T, Tellam, R, et al. Intrauterine growth restriction and the sex specific programming of leptin and peroxisome proliferator-activated receptor gamma (PPARgamma) mRNA expression in visceral fat in the lamb. Pediatr Res. 2009; 66, 59–65.CrossRefGoogle ScholarPubMed
286. Duffield, JA, Vuocolo, T, Tellam, R, et al. Placental restriction of fetal growth decreases IGF1 and leptin mRNA expression in the perirenal adipose tissue of late gestation fetal sheep. Am J Physiol Regul Integr Comp Physiol. 2008; 294, R1413–R1419.CrossRefGoogle ScholarPubMed
287. Wooldridge, AL, Bischof, RJ, Meeusen, EN, et al. Placental restriction of fetal growth reduces cutaneous responses to antigen after sensitization in sheep. Am J Physiol Regul Integr Comp Physiol. 2014; 306, R441–R446.CrossRefGoogle ScholarPubMed
288. de Vrijer, B, Davidsen, ML, Wilkening, RB, Anthony, RV, Regnault, TR. Altered placental and fetal expression of IGFs and IGF-binding proteins associated with intrauterine growth restriction in fetal sheep during early and mid-pregnancy. Pediatr Res. 2006; 60, 507–512.CrossRefGoogle ScholarPubMed
289. Limesand, SW, Regnault, TR, Hay, WW Jr. Characterization of glucose transporter 8 (GLUT8) in the ovine placenta of normal and growth restricted fetuses. Placenta. 2004; 25, 70–77.CrossRefGoogle ScholarPubMed
290. Regnault, TR, Marconi, AM, Smith, CH, et al. Placental amino acid transport systems and fetal growth restriction–a workshop report. Placenta. 2005; 26(Suppl. A), S76–S80.CrossRefGoogle ScholarPubMed
291. muGalan, HL, Anthony, RV, Rigano, S, et al. Fetal hypertension and abnormal Doppler velocimetry in an ovine model of intrauterine growth restriction. Am J Obstet Gynecol. 2005; 192, 272–279.Google Scholar
292. Rozance, PJ, Limesand, SW, Barry, JS, et al. Chronic late-gestation hypoglycemia upregulates hepatic PEPCK associated with increased PGC1alpha mRNA and phosphorylated CREB in fetal sheep. Am J Physiol Endocrinol Metab. 2008; 294, E365–E370.CrossRefGoogle ScholarPubMed
293. Frost, MS, Zehri, AH, Limesand, SW, Hay, WW Jr, Rozance, PJ. Differential effects of chronic pulsatile versus chronic constant maternal hyperglycemia on fetal pancreatic beta-cells. J Pregnancy. 2012; 2012, 812094.CrossRefGoogle ScholarPubMed
294. Limesand, SW, Rozance, PJ, Macko, AR, et al. Reductions in insulin concentrations and beta-cell mass precede growth restriction in sheep fetuses with placental insufficiency. Am J Physiol Endocrinol Metab. 2013; 304, E516–E523.CrossRefGoogle ScholarPubMed
295. Gadd, TS, Aitken, RP, Wallace, JM, Wathes, DC. Effect of a high maternal dietary intake during mid-gestation on components of the utero-placental insulin-like growth factor (IGF) system in adolescent sheep with retarded placental development. J Reprod Fertil. 2000; 118, 407–416.CrossRefGoogle ScholarPubMed
296. Lea, RG, Hannah, LT, Redmer, DA, et al. Developmental indices of nutritionally induced placental growth restriction in the adolescent sheep. Pediatr Res. 2005; 57, 599–604.CrossRefGoogle ScholarPubMed
297. Redmer, DA, Aitken, RP, Milne, JS, Reynolds, LP, Wallace, JM. Influence of maternal nutrition on mRNA expression of placental angiogenic factors and their receptors at midgestation in adolescent sheep. Biol Reprod. 2005; 72, 1004–1009.CrossRefGoogle ScholarPubMed
298. Palmer, RM, Thompson, MG, Meallet, C, et al. Growth and metabolism of fetal and maternal muscles of adolescent sheep on adequate or high feed intake: possible role of protein kinase C-alpha in fetal muscle growth. Br J Nutr. 1998; 79, 351–357.CrossRefGoogle ScholarPubMed
299. Gagnon, R, Langridge, J, Inchley, K, Murotsuki, J, Possmayer, F. Changes in surfactant-associated protein mRNA profile in growth-restricted fetal sheep. Am J Physiol. 1999; 276(Pt 1), L459–L465.Google ScholarPubMed
300. Maritz, GS, Cock, ML, Louey, S, Suzuki, K, Harding, R. Fetal growth restriction has long-term effects on postnatal lung structure in sheep. Pediatr Res. 2004; 55, 287–295.CrossRefGoogle ScholarPubMed
301. Cock, ML, Albuquerque, CA, Joyce, BJ, Hooper, SB, Harding, R. Effects of intrauterine growth restriction on lung liquid dynamics and lung development in fetal sheep. Am J Obstet Gynecol. 2001; 184, 209–216.CrossRefGoogle ScholarPubMed
302. Joyce, BJ, Louey, S, Davey, MG, et al. Compromised respiratory function in postnatal lambs after placental insufficiency and intrauterine growth restriction. Pediatr Res. 2001; 50, 641–649.CrossRefGoogle ScholarPubMed
303. Murotsuki, J, Challis, JR, Han, VK, Fraher, LJ, Gagnon, R. Chronic fetal placental embolization and hypoxemia cause hypertension and myocardial hypertrophy in fetal sheep. Am J Physiol. 1997; 272(Pt 2), R201–R207.Google ScholarPubMed
304. Louey, S, Jonker, SS, Giraud, GD, Thornburg, KL. Placental insufficiency decreases cell cycle activity and terminal maturation in fetal sheep cardiomyocytes. J Physiol. 2007; 580(Pt 2), 639–648.CrossRefGoogle ScholarPubMed
305. Louey, S, Cock, ML, Stevenson, KM, Harding, R. Placental insufficiency and fetal growth restriction lead to postnatal hypotension and altered postnatal growth in sheep. Pediatr Res. 2000; 48, 808–814.CrossRefGoogle ScholarPubMed
306. Bubb, KJ, Cock, ML, Black, MJ, et al. Intrauterine growth restriction delays cardiomyocyte maturation and alters coronary artery function in the fetal sheep. J Physiol. 2007; 578(Pt 3), 871–881.CrossRefGoogle ScholarPubMed
307. Gagnon, R, Lamb, T, Richardson, B. Cerebral circulatory responses of near-term ovine fetuses during sustained fetal placental embolization. Am J Physiol. 1997; 273(Pt 2), H2001–H2008.Google ScholarPubMed
308. Gagnon, R, Murotsuki, J, Challis, JR, Fraher, L, Richardson, BS. Fetal sheep endocrine responses to sustained hypoxemic stress after chronic fetal placental embolization. Am J Physiol. 1997; 272(Pt 1), E817–E823.Google ScholarPubMed
309. Murotsuki, J, Gagnon, R, Pu, X, Yang, K. Chronic hypoxemia selectively down-regulates 11beta-hydroxysteroid dehydrogenase type 2 gene expression in the fetal sheep kidney. Biol Reprod. 1998; 58, 234–239.CrossRefGoogle Scholar
310. Mitchell, EK, Louey, S, Cock, ML, Harding, R, Black, MJ. Nephron endowment and filtration surface area in the kidney after growth restriction of fetal sheep. Pediatr Res. 2004; 55, 769–773.CrossRefGoogle ScholarPubMed
311. Miller, SL, Supramaniam, VG, Jenkin, G, Walker, DW, Wallace, EM. Cardiovascular responses to maternal betamethasone administration in the intrauterine growth-restricted ovine fetus. Am J Obstet Gynecol. 2009; 201, 613 e611–613 e618.CrossRefGoogle ScholarPubMed
312. Miller, SL, Yawno, T, Alers, NO, et al. Antenatal antioxidant treatment with melatonin to decrease newborn neurodevelopmental deficits and brain injury caused by fetal growth restriction. J Pineal Res. 2014; 56, 283–294.CrossRefGoogle ScholarPubMed
313. Castillo-Melendez, M, Yawno, T, Allison, BJ, et al. Cerebrovascular adaptations to chronic hypoxia in the growth restricted lamb. Int J Dev Neurosci. 2015; 45, 55–65.CrossRefGoogle ScholarPubMed
314. Sutherland, AE, Crossley, KJ, Allison, BJ, et al. The effects of intrauterine growth restriction and antenatal glucocorticoids on ovine fetal lung development. Pediatr Res. 2012; 71, 689–696.CrossRefGoogle ScholarPubMed
315. Briscoe, TA, Rehn, AE, Dieni, S, et al. Cardiovascular and renal disease in the adolescent guinea pig after chronic placental insufficiency. Am J Obstet Gynecol. 2004; 191, 847–855.CrossRefGoogle ScholarPubMed
316. Sarr, O, Thompson, JA, Zhao, L, Lee, TY, Regnault, TR. Low birth weight male guinea pig offspring display increased visceral adiposity in early adulthood. PLoS One. 2014; 9, e98433.CrossRefGoogle ScholarPubMed
317. Mazzuca, MQ, Tare, M, Parkington, HC, et al. Uteroplacental insufficiency programmes vascular dysfunction in non-pregnant rats: compensatory adaptations in pregnancy. J Physiol. 2012; 590(Pt 14), 3375–3388.CrossRefGoogle ScholarPubMed
318. Tare, M, Parkington, HC, Bubb, KJ, Wlodek, ME. Uteroplacental insufficiency and lactational environment separately influence arterial stiffness and vascular function in adult male rats. Hypertension. 2012; 60, 378–386.CrossRefGoogle ScholarPubMed
319. Tran, M, Gallo, LA, Jefferies, AJ, Moritz, KM, Wlodek, ME. Transgenerational metabolic outcomes associated with uteroplacental insufficiency. J Endocrinol. 2013; 217, 105–118.CrossRefGoogle ScholarPubMed
320. Pinney, SE, Jaeckle Santos, LJ, Han, Y, Stoffers, DA, Simmons, RA. Exendin-4 increases histone acetylase activity and reverses epigenetic modifications that silence Pdx1 in the intrauterine growth retarded rat. Diabetologia. 2011; 54, 2606–2614.CrossRefGoogle ScholarPubMed
321. Tran, M, Young, ME, Jefferies, AJ, et al. Uteroplacental insufficiency leads to hypertension, but not glucose intolerance or impaired skeletal muscle mitochondrial biogenesis, in 12-month-old rats. Physiol Rep. 2015; 3, pii: e12556. doi: 10.14814/phy2.12556.CrossRefGoogle ScholarPubMed
322. van der Linde, S, Romano, T, Wadley, G, et al. Growth restriction in the rat alters expression of cardiac JAK/STAT genes in a sex-specific manner. J Dev Orig Health Dis. 2014; 5, 314–321.CrossRefGoogle Scholar
323. Kallapur, SG, Nitsos, I, Moss, TJ, et al. Chronic endotoxin exposure does not cause sustained structural abnormalities in the fetal sheep lungs. Am J Physiol Lung Cell Mol Physiol. 2005; 288, L966–L974.CrossRefGoogle Scholar
324. Clifton, VL, Moss, TJ, Wooldridge, AL, et al. Development of an experimental model of maternal allergic asthma during pregnancy. J Physiol. 2016; 594, 1311–1325.CrossRefGoogle ScholarPubMed
325. Chen, H, Iglesias, MA, Caruso, V, Morris, MJ. Maternal cigarette smoke exposure contributes to glucose intolerance and decreased brain insulin action in mice offspring independent of maternal diet. PLoS One. 2011; 6, e27260.CrossRefGoogle ScholarPubMed
326. Gray, SP, Kenna, K, Bertram, JF, et al. Repeated ethanol exposure during late gestation decreases nephron endowment in fetal sheep. Am J Physiol Regul Integr Comp Physiol. 2008; 295, R568–R574.CrossRefGoogle ScholarPubMed
327. Cullen, CL, Burne, TH, Lavidis, NA, Moritz, KM. Low dose prenatal ethanol exposure induces anxiety-like behaviour and alters dendritic morphology in the basolateral amygdala of rat offspring. PLoS One. 2013; 8, e54924.CrossRefGoogle ScholarPubMed
328. Cullen, CL, Burne, TH, Lavidis, NA, Moritz, KM. Low dose prenatal alcohol exposure does not impair spatial learning and memory in two tests in adult and aged rats. PLoS One. 2014; 9, e101482.CrossRefGoogle Scholar
329. Gardebjer, EM, Cuffe, JS, Pantaleon, M, Wlodek, ME, Moritz, KM. Periconceptional alcohol consumption causes fetal growth restriction and increases glycogen accumulation in the late gestation rat placenta. Placenta. 2014; 35, 50–57.CrossRefGoogle ScholarPubMed
330. Gray, SP, Denton, KM, Cullen-McEwen, L, Bertram, JF, Moritz, KM. Prenatal exposure to alcohol reduces nephron number and raises blood pressure in progeny. J Am Soc Nephrol. 2010; 21, 1891–1902.CrossRefGoogle ScholarPubMed
331. Nguyen, VB, Probyn, ME, Campbell, F, et al. Low-dose maternal alcohol consumption: effects in the hearts of offspring in early life and adulthood. Physiol Rep. 2014; 2, pii: e12087. doi: 10.14814/phy2.12087.CrossRefGoogle ScholarPubMed
332. Probyn, ME, Parsonson, KR, Gardebjer, EM, et al. Impact of low dose prenatal ethanol exposure on glucose homeostasis in Sprague-Dawley rats aged up to eight months. PLoS One. 2013; 8, e59718.CrossRefGoogle ScholarPubMed
333. Morrison, JL, Riggs, KW, Rurak, DW. Fluoxetine during pregnancy: impact on fetal development. Reprod Fertil Dev. 2005; 17, 641–650.CrossRefGoogle ScholarPubMed
334. Morrison, JL, Rurak, DW, Chien, C, et al. Maternal fluoxetine infusion does not alter fetal endocrine and biophysical circadian rhythms in pregnant sheep. J Soc Gynecol Investig. 2005; 12, 356–364.CrossRefGoogle Scholar
335. Morrison, JL, Chien, C, Gruber, N, Rurak, D, Riggs, W. Fetal behavioural state changes following maternal fluoxetine infusion in sheep. Brain Res Dev Brain Res. 2001; 131, 47–56.CrossRefGoogle ScholarPubMed
336. Susiarjo, M, Xin, F, Bansal, A, et al. Bisphenol a exposure disrupts metabolic health across multiple generations in the mouse. Endocrinology. 2015; 156, 2049–2058.CrossRefGoogle ScholarPubMed
337. Moisiadis, VG, Matthews, SG. Glucocorticoids and fetal programming part 1: outcomes. Nat Rev Endocrinol. 2014; 10, 391–402.CrossRefGoogle ScholarPubMed
338. Moss, TJ, Nitsos, I, Harding, R, Newnham, JP. Differential effects of maternal and fetal betamethasone injections in late-gestation fetal sheep. J Soc Gynecol Investig. 2003; 10, 474–479.CrossRefGoogle ScholarPubMed
339. Moritz, KM, Johnson, K, Douglas-Denton, R, Wintour, EM, Dodic, M. Maternal glucocorticoid treatment programs alterations in the renin-angiotensin system of the ovine fetal kidney. Endocrinology. 2002; 143, 4455–4463.CrossRefGoogle ScholarPubMed
340. De Blasio, MJ, Dodic, M, Jefferies, AJ, et al. Maternal exposure to dexamethasone or cortisol in early pregnancy differentially alters insulin secretion and glucose homeostasis in adult male sheep offspring. Am J Physiol Endocrinol Metab. 2007; 293, E75–E82.CrossRefGoogle ScholarPubMed
341. Moritz, KM, De Matteo, R, Dodic, M, et al. Prenatal glucocorticoid exposure in the sheep alters renal development in utero: implications for adult renal function and blood pressure control. Am J Physiol Regul Integr Comp Physiol. 2011; 301, R500–R509.CrossRefGoogle ScholarPubMed
342. O’Sullivan, L, Cuffe, JS, Koning, A, et al. Excess prenatal corticosterone exposure results in albuminuria, sex-specific hypotension, and altered heart rate responses to restraint stress in aged adult mice. Am J Physiol Renal Physiol. 2015; 308, F1065–F1073.CrossRefGoogle ScholarPubMed
343. Cuffe, JS, Dickinson, H, Simmons, DG, Moritz, KM. Sex specific changes in placental growth and MAPK following short term maternal dexamethasone exposure in the mouse. Placenta. 2011; 32, 981–989.CrossRefGoogle ScholarPubMed
344. Quinn, TA, Ratnayake, U, Castillo-Melendez, M, et al. Adrenal steroidogenesis following prenatal dexamethasone exposure in the spiny mouse. J Endocrinol. 2014; 221, 347–362.CrossRefGoogle ScholarPubMed
345. Dickinson, H, Walker, DW, Wintour, EM, Moritz, K. Maternal dexamethasone treatment at midgestation reduces nephron number and alters renal gene expression in the fetal spiny mouse. Am J Physiol Regul Integr Comp Physiol. 2007; 292, R453–R461.CrossRefGoogle ScholarPubMed
346. O’Connell, BA, Moritz, KM, Roberts, CT, Walker, DW, Dickinson, H. The placental response to excess maternal glucocorticoid exposure differs between the male and female conceptus in spiny mice. Biol Reprod. 2011; 85, 1040–1047.CrossRefGoogle ScholarPubMed
347. Owen, D, Matthews, SG. Glucocorticoids and sex-dependent development of brain glucocorticoid and mineralocorticoid receptors. Endocrinology. 2003; 144, 2775–2784.CrossRefGoogle ScholarPubMed
348. Benediktsson, R, Lindsay, RS, Noble, J, Seckl, JR, Edwards, CRW. Glucocorticoid exposure in utero: new model for adult hypertension. Lancet. 1993; 341, 339–341.CrossRefGoogle ScholarPubMed
349. Wyrwoll, CS, Mark, PJ, Mori, T, Puddey, I, Waddell, BJ. Prevention of programmed hypertension and hyperleptinemia by postnatal dietary omega-3 fatty acids. Endocrinology. 2006; 147, 599–606.CrossRefGoogle ScholarPubMed
350. Wyrwoll, CS, Mark, PJ, Waddell, BJ. Developmental programming of renal glucocorticoid sensitivity and the renin-angiotensin system. Hypertension. 2007; 50, 579–584.CrossRefGoogle ScholarPubMed
351. Wyrwoll, CS, Mark, PJ, Mori, TA, Waddell, BJ. Developmental programming of adult hyperinsulinemia, increased proinflammatory cytokine production and altered skeletal muscle expression of GLUT4 and uncoupling protein-3. J Endocrinol. 2008; 198, 571–579.CrossRefGoogle ScholarPubMed
352. Waddell, BJ, Bollen, M, Wyrwoll, CS, Mori, TA, Mark, PJ. Developmental programming of adrenal structure and steroidogenesis: effects of fetal glucocorticoid excess and postnatal dietary omega-3 fatty acids. J Endocrinol. 2010; 205, 171–178.CrossRefGoogle ScholarPubMed
353. Mark, PJ, Lewis, JL, Jones, ML, Keelan, JA, Waddell, BJ. The inflammatory state of the rat placenta increases in late gestation and is further enhanced by glucocorticoids in the labyrinth zone. Placenta. 2013; 34, 559–566.CrossRefGoogle ScholarPubMed