Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-23T20:05:52.211Z Has data issue: false hasContentIssue false
  • English
  • Français

From Mice to Men: research models of developmental programming

Published online by Cambridge University Press:  13 July 2012

C. Rabadán-Diehl  and
P. Nathanielsz
C. Rabadán-Diehl*
Affiliation:
Office of Global Health, National Heart, Lung, and Blood Institute, NIH, Bethesda, MD, USA
P. Nathanielsz
Affiliation:
Department of Obstetrics and Gynecology, Center for Pregnancy and Newborn Research, University of Texas Health Science Center, San Antonio, TX, USA
*
*Address for correspondence: Dr C. Rabadán-Diehl, Deputy Director, Office of Global Health, National Heart, Lung, and Blood Institute, NIH, 31 Center Drive, Suite 5A06C, Bethesda, MD 20982, USA. (Email [email protected])
Get access Rights & Permissions [Opens in a new window]

Abstract

Developmental programming can be defined as a response to a specific challenge to the mammalian organism during a critical developmental time window that alters the trajectory of development with persistent effects on offspring phenotype and predisposition to future illness. We focus on the need for studies in relevant, well-characterized animal models in the context of recent research discoveries on the challenges, mechanisms and outcomes of developmental programming. We discuss commonalities and differences in general principles of developmental programming as they apply to several species, including humans. The consequences of these differences are discussed. Obesity, metabolic disorders and cardiovascular diseases are associated with the highest percentage of morbidity and mortality worldwide. Although many of the causes are associated with lifestyle, high-energy diets and lack of physical activity, recent evidence has linked developmental programming to the epidemic of metabolic diseases. A better understanding of comparative systems physiology of mother, fetus and neonate using information provided by rapid advances in molecular biology has the potential to improve the lifetime health of future generations by providing better women's health, diagnostic tools and preventative and therapeutic interventions in individuals exposed during their development to programming influences.

Keywords

modelsopportunitiesprogramming
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 4 , Issue 1 , February 2013 , pp. 3 - 9
Copyright
Copyright © Cambridge University Press [2012]. This is a work of the U.S. Government and is not subject to copyright protection in the United States. 2012 

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.Barker, DJP. EDITORIAL: the developmental origins of adult disease. Eur J Epidemiol. 2003; 18, 733–736.CrossRefGoogle ScholarPubMed
2.Wadhwa, PD, Buss, C, Entringer, S, Swanson, JM. Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin Reprod Med. 2009; 27, 358–368.CrossRefGoogle ScholarPubMed
3.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.Google Scholar
4.Igosheva, N, Abramov, AY, Poston, L, et al. Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS One. 2010; 5, e10074.Google Scholar
5.Godfrey, KM, Barker, DJ. Fetal programming and adult health. Public Health Nutr. 2001; 4, 611–624.Google Scholar
6.Rich-Edwards, JW, Stampfer, MJ, Manson, JE, et al. Birth weight and risk of cardiovascular disease in a cohort of women followed up since 1976. BMJ. 1997; 315, 396–400.Google Scholar
7.Curhan, GC, Willett, WC, Rimm, EB, et al. Birth weight and adult hypertension, diabetes mellitus, and obesity in US men. Circulation. 1996; 94, 3246–3250.Google Scholar
8.Stein, AD, Ravelli, AC, Lumey, LH. Famine, third-trimester pregnancy weight gain, and intrauterine growth: the Dutch Famine Birth Cohort Study. Hum Biol. 1995; 67, 135–150.Google ScholarPubMed
9.Roseboom, TJ, van der Meulen, JH, Ravelli, AC, et al. Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Mol Cell Endocrinol. 2001; 185, 93–98.CrossRefGoogle Scholar
10.Harvey, NC, Mahon, PA, Kim, M, et al. Intrauterine growth and postnatal skeletal development: findings from the Southampton Women's Survey. Paediatr Perinat Epidemiol. 2012; 26, 34–44.CrossRefGoogle ScholarPubMed
11.Salem, W, Adler, A, Lee, C, Smith, G. Maternal waist to hip ratio is a risk factor for macrosomia. BJOG. 2012; 119, 291–297.CrossRefGoogle ScholarPubMed
12.Cohen, JF, Rifas-Shiman, SL, Rimm, EB, et al. Maternal trans fatty acid intake and fetal growth. Am J Clin Nutr. 2011; 94, 1241–1247.Google Scholar
13.Chivers, P, Hands, B, Parker, H, et al. Body mass index, adiposity rebound and early feeding in a longitudinal cohort (Raine Study). Int J Obes (Lond). 2010; 34, 1169–1176.Google Scholar
14.Oken, E, Kleinman, KP, Belfort, MB, et al. Associations of gestational weight gain with short- and longer-term maternal and child health outcomes. Am J Epidemiol. 2009; 170, 173–180.Google Scholar
15. Rasmussen KM, Yaktine AL. Weight Gain During Pregancy: Reexamining the Guidelines, 2009. Committee to Reexamine IOM Pregnancy Weight Guidelines, Institute of Medicine, National Research Council.Google Scholar
16.Rasmussen, KM, Abrams, B, Bodnar, LM, et al. Recommendations for weight gain during pregnancy in the context of the obesity epidemic. Obstet Gynecol. 2010; 116, 1191–1195.Google Scholar
17.Rasmussen, KM, Catalano, PM, Yaktine, AL. New guidelines for weight gain during pregnancy: what obstetrician/gynecologists should know. Curr Opin Obstet Gynecol. 2009; 21, 521–526.CrossRefGoogle ScholarPubMed
18.Breslow, JL. Mouse models of atherosclerosis. Science. 1996; 272, 685–688.Google Scholar
19.Daugherty, A. Mouse models of atherosclerosis. Am J Med Sci. 2002; 323, 3–10.CrossRefGoogle ScholarPubMed
20.Ternel, RE, Rudel, LL. Diet effects on atherosclerosis in mice. Curr Drug Targets. 2007; 8, 1150–1160.Google Scholar
21.Jones, RH, Ozanne, SE. Fetal programming of glucose-insulin metabolism. Mol Cell Endocrinol. 2009; 297, 4–9.Google Scholar
22.Boney, CM, Verma, A, Tucker, R, Vohr, BR. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics. 2005; 115, e290–e296.CrossRefGoogle ScholarPubMed
23.Burt, BE, Hess, BW, Nathanielsz, PW, Ford, SP. Flock differences in the impact of maternal dietary restriction on offspring growth and glucose tolerance in female offspring. Soc Reprod Fertil Suppl. 2007; 64, 411–424.Google Scholar
24.Vonnahme, KA, Hess, BW, Nijland, MJ, et al. Placentomal differentiation may compensate for maternal nutrient restriction in ewes adapted to harsh range conditions. J Anim Sci. 2006; 84, 3451–3459.Google Scholar
25.Hales, CN, Barker, DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992; 35, 595–601.CrossRefGoogle ScholarPubMed
26.Fowden, AL. The role of insulin in fetal growth. Early Hum Dev. 1992; 29, 177–181.CrossRefGoogle ScholarPubMed
27.Jones, RH, Ozanne, SE. Fetal programming of glucose-insulin metabolism. Mol Cell Endocrinol. 2009; 297, 4–9.Google Scholar
28.Boney, CM, Verma, A, Tucker, R, Vohr, BR. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics. 2005; 115, e290–e296.Google Scholar
29.Dabelea, D, Knowler, WC, Pettitt, DJ. Effect of diabetes in pregnancy on offspring: follow-up research in the Pima Indians. J Matern Fetal Med. 2000; 9, 83–88.Google Scholar
30.Crowther, NJ, Cameron, N, Trusler, J, Gray, IP. Association between poor glucose tolerance and rapid post natal weight gain in seven-year-old children. Diabetologia. 1998; 41, 1163–1167.Google Scholar
31.Yajnik, C. Interactions of perturbations in intrauterine. Proc Nutr Soc. 2000; 59, 257–265.Google Scholar
32.Snoeck, A, Remacle, C, Reusens, B, Hoet, JJ. Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol Neonate. 1990; 57, 107–118.Google Scholar
33.Boujendar, S, Reusens, B, Merezak, S, et al. Taurine supplementation to a low protein diet during foetal and early postnatal life restores a normal proliferation and apoptosis of rat pancreatic islets. Diabetologia. 2002; 45, 856–866.CrossRefGoogle ScholarPubMed
34.Boujendar, S, Arany, E, Hill, D, Remacle, C, Reusens, B. Taurine supplementation of a low protein diet fed to rat dams normalizes the vascularization of the fetal endocrine pancreas. J Nutr. 2003; 133, 2820–2825.Google Scholar
35.Ozanne, SE, Olsen, GS, Hansen, LL, et al. Early growth restriction leads to down regulation of protein kinase C zeta and insulin resistance in skeletal muscle. J Endocrinol. 2003; 177, 235–241.Google Scholar
36.Petry, CJ, Dorling, MW, Pawlak, DB, Ozanne, SE, Hales, CN. Diabetes in old male offspring of rat dams fed a reduced protein diet. Int J Exp Diabetes Res. 2001; 2, 139–143.Google Scholar
37.Ozanne, SE, Dorling, MW, Wang, CI, Nave, BT. Impaired PI 3-kinase activation in adipocytes from early growth-restricted male rats. Am J Physiol Endocrinol Metab. 2001; 280, E534–E539.Google Scholar
38.Wadhwa, PD, Buss, C, Entringer, S, Swanson, JM. Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin Reprod Med. 2009; 27, 358–368.CrossRefGoogle ScholarPubMed
39. Wang J, Wu Z, Li D, et al. Nutrition, epigenetics, and metabolic syndrome. Antioxid Redox Signal. 2012; Jan 13 [Epub ahead of print].Google Scholar
40.Sen, S, Simmons, RA. Maternal antioxidant supplementation prevents adiposity in the offspring of Western diet-fed rats. Diabetes. 2010; 59, 3058–3065.CrossRefGoogle ScholarPubMed
41. Junien C, Nathanielsz P. Report on the IASO Stock Conference 2006: early and lifelong environmental epigenomic programming of metabolic syndrome, obesity and type II diabetes. Obes Rev. 2007; 8, 487–502.Google Scholar
42.Waterland, RA, Michels, KB. Epigenetic epidemiology of the developmental origins hypothesis. Annu Rev Nutr. 2007; 27, 363–388.Google Scholar
43.Gluckman, PD, Hanson, MA, Beedle, AS. Non-genomic transgenerational inheritance of disease risk. Bioessays. 2007; 29, 145–154.Google Scholar
44.Tobi, EW, Lumey, LH, Talens, RP, et al. DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum Mol Gent. 2009; 18, 4046–4053.CrossRefGoogle ScholarPubMed
45.Karowicz-Bilinska, A, Kedziora-Kornatowska, K, Bartosz, G. Indices of oxidative stress in pregnancy with fetal growth restriction. Free Radic Res. 2007; 41, 870–873.Google Scholar
46.Potdar, N, Singh, R, Mistry, V, et al. First-trimester increase in oxidative stress and risk of small-for-gestational-age fetus. BJOG. 2009; 116, 637–642.Google Scholar
47.Wang, Y, Walsh, SW. Increased superoxide generation is associated with decreased superoxide dismutase activity and mRNA expression in placental trophoblast cells in pre-eclampsia. Placenta. 2001; 22, 206–212.Google Scholar
48.Karowicz-Bilinska, A, Suzin, J, Sieroszewski, P. Evaluation of oxidative stress indices during treatment in pregnant women with intrauterine growth retardation. Med Sci Monit. 2002; 8, CR211–CR216.Google Scholar
49.Simmons, RA, Suponitsky-Kroyter, I, Selak, MA. Progressive accumulation of mitochondrial DNA mutations and decline in mitochondrial function lead to beta-cell failure. J Biol Chem. 2005; 280, 28785–28791.Google Scholar
50.Selak, MA, Storey, BT, Peterside, A, Simmons, RA. Impaired oxidative phosphorylation in skeletal muscle of intrauterine growth-retarded rats. Am J Physiol. 2003; 285, E130–E137.Google Scholar
51. WHO. Global Status Report on NCDs, 2010. Retrieved May 2, 2012, from http://www.who.int/chp/ncd_global_status_report/en/index.htmlGoogle Scholar
52. Institute of Medicine of the National Academies. Promoting Cardiovascular health in the Developing World: A Critical Challenge to Achieve Global Health, 2010. Retrieved May 2, 2012, from http://www.iom.edu/Reports/2010/Promoting-Cardiovascular-Health-in-the-Developing-World-A-Critical-Challenge-to-Achieve-Global-Health.aspxGoogle Scholar
53. National Heart, Lung, and Blood Institute. NHLBI Working Group: The Influence of Early Programming in the Development of Cardiovascular, Lung, Blood, and Sleep Disorders Executive Summary, 2005. Retrieved May 2, 2012, from http://www.nhlbi.nih.gov/meetings/workshops/earlyprg.htmGoogle Scholar
54. NIH. The Obese and Diabetic Intrauterine Environment: Long-term Metabolic or Cardiovascular Consequences in the Offspring Request for Applications (RFA-DK-05-014), 2005. Retrieved May 2, 2012, from http://grants.nih.gov/grants/guide/rfa-files/RFA-DK-05-014.htmlGoogle Scholar
55. National Institute of Child health and Human Development. Vision Themes: Developmental Origins of Health and Disease Workshop, 2011. Retrieved May 2, 2012, from http://www.nichd.nih.gov/vision/vision_themes/developmental_origins.cfmGoogle Scholar
56.Richter, LM, Victora, CG, Hallal, PC, et al. Cohort Profile: the consortium of health-oriented research in transitioning societies. Int J Epidemiol. 2011.Google Scholar
57.Chowdury, ME, Botlero, R, Koblinsky, M, et al. Determinants of reduction in maternal mortality in Matlab, Bangladesh: a 30 year cohort study. Lancet. 2007; 370, 1320–1328.CrossRefGoogle Scholar
58.Zhu, L, Ling, H. National neural tube defects prevention program in China. Food Nutr Bull. 2008; 29, S196–S204.Google Scholar
59.Huang, C, Li, Z, Wang, M, Martorell, R. Early life exposure to the 1959–1961 Chinese famine has long-term health consequences. J Nutr. 2010; 140, 1874–1878.Google Scholar
60.Friedlander, Y, Paltiel, O, Manor, O, et al. Birthweight of offspring and mortality of parents: the Jerusalem perinatal study cohort. Ann Epidemiol. 2007; 17, 914–922.Google Scholar