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Intergenerational response of steroidogenesis-related genes to maternal malnutrition

Published online by Cambridge University Press:  21 February 2019

Abdel Halim Harrath*
Affiliation:
Department of Zoology, College of Science, King Saud University, Riyadh, Saudi Arabia Institute of Biological Sciences of Tunis, University of Tunis El Manar, Tunis, Tunisia
Abdulkarem Alrezaki
Affiliation:
Department of Zoology, College of Science, King Saud University, Riyadh, Saudi Arabia
Saleh H. Alwasel
Affiliation:
Department of Zoology, College of Science, King Saud University, Riyadh, Saudi Arabia
Abdelhabib Semlali
Affiliation:
Groupe de Recherche en Écologie Buccale, Département de stomatologie, Faculté de Médecine Dentaire, Université Laval, Québec, QC, Canada
*
Address for correspondence: Prof. A. H. Harrath, Department of Zoology, College of Science, King Saud University, P. O. Box 2455, Riyadh 11451, Saudi Arabia. E-mail: [email protected]

Abstract

We sought to examine whether rat maternal food restriction (MFR) affects the expression of steroidogenesis-related genes Cyp19, Cyp17a1, Insl3 and Gdf-9 in the ovaries of offspring from the first (FRG1) and second (FRG2) generations at pre-pubertal age (week 4) and during adulthood (week 8). At week 4, MFR significantly increased the expression of RNAs for all analyzed genes in both FRG1 and FRG2 females, which may indicate that MFR affects the onset of the reproductive lifespan, by inducing early pubertal onset. At week 8, the Cyp19 gene was still upregulated in MRF-subjected animals (Cyp19: P=0.0049 and P=0.0508 in FRG1 and FRG2, respectively), but MFR induced a significant decrease in Cyp17 and Gdf-9 gene expression in the offspring of both FRG1 and FRG2 females when compared with the controls (Cyp17: P=0.0018 and P=0.0016, respectively; Gdf-9: P=0.0047 and P=0.0023, respectively). This suggests that females at week 8, which should normally be in their optimal reproductive capacity, experience premature ovarian aging. At week 4, the activation of Cyp19 and Cyp17 was higher in the FRG1 ovaries than in the FRG2 ovaries, whereas the extent of Insl3 and Gdf-9 activation was lower in the FRG1 ovaries. This may indicate that FRG2 females were more vulnerable to MFR than their mothers (FRG1) and grandmothers, which is consistent with the ‘predictive adaptive response’ hypothesis. Our findings reveal that MFR may induce intergenerational ovarian changes as an adaptive response to ensure reproductive success before death.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2019 

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References

Barker, DJP. The malnourished baby and infant. Br Med Bull. 2001; 60, 6988.CrossRefGoogle ScholarPubMed
Ergaz, Z, Avgil, M, Ornoy, A. Intrauterine growth restriction-etiology and consequences: what do we know about the human situation and experimental animal models? Reprod Toxicol. 2005; 20, 301322.CrossRefGoogle ScholarPubMed
Thorn, SR, Regnault, TRH, Brown, LD, et al. Intrauterine growth restriction increases fetal hepatic gluconeogenic capacity and reduces messenger ribonucleic acid translation initiation and nutrient sensing in fetal liver and skeletal muscle. Endocrinology. 2009; 150, 30213030.CrossRefGoogle ScholarPubMed
Xu, G, Umezawa, M, Takeda, K. Early development origins of adult disease caused by malnutrition and environmental chemical substances. J Health Sci. 2009; 55, 1119.CrossRefGoogle Scholar
Lee, S, You, YA, Kwon, EJ, et al. Maternal food restriction during pregnancy and lactation adversely affect hepatic growth and lipid metabolism in three-week-old rat offspring. Int J Mol Sci. 2016; 17(12), 2115.CrossRefGoogle ScholarPubMed
Sundrani, DP, Roy, SS, Jadhav, AT, Joshi, SR. Sex-specific differences and developmental programming for diseases in later life. Reprod Fertil Dev. 2017; 11, 20852099.CrossRefGoogle Scholar
Chan, KA, Tsoulis, MW, Sloboda, DM. Early-life nutritional effects on the female reproductive system. J Endocrinol. 2015; 224, R45R62.CrossRefGoogle ScholarPubMed
Grzesiak, M, Knapczyk-Stwora, K, Duda, M, Slomczynska, M. Elevated level of 17-beta-estradiol is associated with overexpression of FSHR, CYP19A1, and CTNNB1 genes in porcine ovarian follicles after prenatal and neonatal flutamide exposure. Theriogenology. 2012; 78, 20502060.CrossRefGoogle ScholarPubMed
Bernal, AB, Vickers, MH, Hampton, MB, Poynton, RA, Sloboda, DM. Maternal undernutrition significantly impacts ovarian follicle number and increases ovarian oxidative stress in adult rat offspring. PLoS One. 2010; 5, e15558.CrossRefGoogle ScholarPubMed
Sloboda, DM, Hickey, M, Hart, R. Reproduction in females: the role of the early life environment. Hum Reprod Update. 2011; 17, 210227.CrossRefGoogle ScholarPubMed
Sirotkin, AV, Harrath, AH. Phytoestrogens and their effects. Eur J Pharmacol. 2014; 741, 230236.CrossRefGoogle ScholarPubMed
Sharov, AA, Falco, G, Piao, Y, et al. Effects of aging and calorie restriction on the global gene expression profiles of mouse testis and ovary. BMC Biol. 2008; 6, 24.CrossRefGoogle ScholarPubMed
Guzman, C, Garcia-Becerra, R, Aguilar-Medina, MA, et al. Maternal protein restriction during pregnancy and/or lactation negatively affects follicular ovarian development and steroidogenesis in the prepubertal rat offspring. Arch Med Res. 2014; 45, 294300.CrossRefGoogle ScholarPubMed
Cordier, AG, Leveille, P, Dupont, C, et al. Dietary lipid and cholesterol induce ovarian dysfunction and abnormal LH response to stimulation in rabbits. PLos One. 2013; 8, e63101.CrossRefGoogle ScholarPubMed
Pisani, LF, Antonini, S, Pocar, P, et al. Effects of pre-mating nutrition on mRNA levels of developmentally relevant genes in sheep oocytes and granulosa cells. Reproduction. 2008; 136, 303312.CrossRefGoogle ScholarPubMed
Godwin, J. Social determination of sex in reef fishes. Semin Cell Dev Biol. 2009; 20, 264270.CrossRefGoogle ScholarPubMed
Fitzpatrick, SL, Carlone, DL, Robker, RL, Richards, JS. Expression of aromatase in the ovary: down-regulation of mRNA by the ovulatory luteinizing hormone surge. Steroids. 1997; 62, 197206.CrossRefGoogle ScholarPubMed
Stocco, C. Aromatase expression in the ovary: hormonal and molecular regulation. Steroids. 2008; 73, 473487.CrossRefGoogle ScholarPubMed
Guigon, CJ, Mazaud, S, Forest, MG, et al. Unaltered development of the initial follicular waves and normal pubertal onset in female rats after neonatal deletion of the follicular reserve. Endocrinology. 2003; 144, 36513662.CrossRefGoogle ScholarPubMed
Bathgate, R, Balvers, M, Hunt, N, Ivell, R. Relaxin-like factor gene is highly expressed in the bovine ovary of the cycle and pregnancy: sequence and messenger ribonucleic acid analysis. Biol Reprod. 1996; 55, 14521457.CrossRefGoogle ScholarPubMed
Balvers, M, Spiess, AN, Domagalski, R, et al. Relaxin-like factor expression as a marker of differentiation in the mouse testis and ovary. Endocrinology. 1998; 139, 29602970.CrossRefGoogle ScholarPubMed
Bathgate, R, Moniac, N, Bartlick, B, et al. Expression and regulation of relaxin-like factor gene transcripts in the bovine ovary: differentiation-dependent expression in theca cell cultures. Biol Reprod. 1999; 61, 10901098.CrossRefGoogle ScholarPubMed
Zarreh-Hoshyari-Khah, MR, Einspanier, A, Ivell, R. Differential splicing and expression of the relaxin-like factor gene in reproductive tissues of the marmoset monkey (Callithrix jacchus). Biol Reprod. 1999; 60, 445453.CrossRefGoogle Scholar
Hanna, CB, Yao, S, Patta, MC, Jensen, JT, Wu, X. Expression of insulin-like 3 (INSL3) and differential splicing of its receptor in the ovary of rhesus macaques. Reprod Biol Endocrinol. 2010; 8, 150.CrossRefGoogle ScholarPubMed
Glister, C, Satchell, L, Bathgate, RA, et al. Functional link between bone morphogenetic proteins and insulin-like peptide 3 signaling in modulating ovarian androgen production. Proc Natl Acad Sci U S A. 2013; 110, E1426E1435.CrossRefGoogle ScholarPubMed
Kawamura, K, Kumagai, J, Sudo, S, et al. Paracrine regulation of mammalian oocyte maturation and male germ cell survival. Proc Natl Acad Sci U S A. 2004; 101, 73237328.CrossRefGoogle ScholarPubMed
Gilchrist, RB, Lane, M, Thompson, JG. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update. 2008; 14, 159177.CrossRefGoogle ScholarPubMed
Hosoe, M, Kaneyama, K, Ushizawa, K, Hayashi, KG, Takahashi, T. Quantitative analysis of bone morphogenetic protein 15 (BMP15) and growth differentiation factor 9 (GDF9) gene expression in calf and adult bovine ovaries. Reprod Biol Endocrinol. 2011; 9, 33.CrossRefGoogle ScholarPubMed
Lin, ZL, Li, YH, Xu, YN, et al. Effects of growth differentiation factor 9 and bone morphogenetic protein 15 on the in vitro maturation of porcine oocytes. Reprod Domest Anim. 2014; 49, 219227.CrossRefGoogle ScholarPubMed
Orisaka, M, Tajima, K, Tsang, BK, Kotsuji, F. Oocyte-granulosa-theca cell interactions during preantral follicular development. J Ovarian Res. 2009b; 2, 9.CrossRefGoogle ScholarPubMed
McGrath, SA, Esquela, AF, Lee, SJ. Oocyte-specific expression of growth/differentiation factor-9. Mol Endocrinol. 1995; 9, 131136.Google ScholarPubMed
Orisaka, M, Jiang, JY, Orisaka, S, Kotsuji, F, Tsang, BK. Growth differentiation factor 9 promotes rat preantral follicle growth by up-regulating follicular androgen biosynthesis. Endocrinology. 2009a; 150, 27402748.CrossRefGoogle ScholarPubMed
Miller, WL. Androgen biosynthesis from cholesterol to DHEA. Mol Cell Endocrinol. 2002; 198, 714.CrossRefGoogle Scholar
Rainey, WE, Carr, BR, Sasano, H, Suzuki, T, Mason, JI. Trends Endocrinol Metab. 2002; 13, 234239.CrossRefGoogle Scholar
Fernandez, T, Palomino, J, Parraguez, VH, Peralta, OA. De los Reyes M. Differential expression of GDF-9 and BMP-15 during follicular development in canine ovaries evaluated by flow cytometry. Anim Reprod Sci. 2016; 167, 5967.CrossRefGoogle ScholarPubMed
Sui, S, Jia, Y, He, B, et al. Maternal low-protein diet alters ovarian expression of folliculogenic and steroidogenic genes and their regulatory microRNAs in neonatal piglets. Asian-Australas J Anim Sci. 2014; 27, 16951704.CrossRefGoogle ScholarPubMed
Ellison, PT. Energetics and reproductive effort. Am J Hum Biol. 2003; 15, 342351.CrossRefGoogle ScholarPubMed
Ellis, BJ. Timing of pubertal maturation in girls: an integrated life history approach. Psychol Bull. 2004; 130, 920958.CrossRefGoogle ScholarPubMed
Gluckman, PD, Hanson, MA. Changing times: the evolution of puberty. Mol Cell Endocrinol. 2006; 254–255, 2631.Google Scholar
Jasienska, G, Thune, I, Ellison, PT. Fatness at birth predicts adult susceptibility to ovarian suppression: an empirical test of the predictive adaptive response hypothesis. Proc Natl Acad Sci U S A. 2006; 103, 1275912762.CrossRefGoogle ScholarPubMed
Ozanne, SE, Nicholas Hales, C. Poor fetal growth followed by rapid postnatal catch-up growth leads to premature death. Mech Ageing Dev. 2005; 126, 852854.CrossRefGoogle ScholarPubMed
Gluckman, PD, Hanson, MA, Beedle, AS, Spencer, HG. Predictive adaptive responses in perspective. Trends Endocrinol Metab. 2008; 19, 109110, Author reply p. 112.CrossRefGoogle Scholar
Stearns, SC. The Evolution of Life Histories, 1992. Oxford University Press: New York.Google Scholar
Sloboda, DM, Howie, GJ, Pleasants, A, Gluckman, PD, Vickers, MH. Pre- and postnatal nutritional histories influence reproductive maturation and ovarian function in the rat. PLoS One. 2009; 4, e6744.CrossRefGoogle ScholarPubMed
Mcgrath, SA, Esquela, AF, Lee, SJ. Oocyte-specific expression of growth-differentiation factor-Ix. Mol Endocrinol. 1995a; 9, 131136.Google Scholar
Berberoglu, Z, Aktas, A, Fidan, Y, Yazici, AC, Aral, Y. Association of plasma GDF-9 or GDF-15 levels with bone parameters in polycystic ovary syndrome. J Bone Miner Metab. 2015; 33, 101108.CrossRefGoogle ScholarPubMed
Murray, AA, Gosden, RG, Allison, V, Spears, N. Effect of androgens on the development of mouse follicles growing in vitro. J Reprod Fertil. 1998; 113, 2733.CrossRefGoogle ScholarPubMed
Wang, H, Andoh, K, Hagiwara, H, et al. Effect of adrenal and ovarian androgens on type 4 follicles unresponsive to FSH in immature mice. Endocrinology. 2001; 142, 49304936.CrossRefGoogle ScholarPubMed
Yang, JL, Zhang, CP, Li, L, et al. Testosterone induces redistribution of Forkhead Box-3a and down-regulation of growth and differentiation factor 9 messenger ribonucleic acid expression at early stage of mouse folliculogenesis. Endocrinology. 2010; 151, 774782.CrossRefGoogle ScholarPubMed
Vitt, UA, McGee, EA, Hayashi, M, Hsueh, AJW. In vivo treatment with GDF-9 stimulates primordial and primary follicle progression and theca cell marker CYP17 in ovaries of immature rats. Endocrinology. 2000; 141, 38143820.CrossRefGoogle ScholarPubMed
Faria Tda, S, Brasil Fde, B, Sampaio, FJ, Ramos Cda, F. Maternal malnutrition during lactation alters the folliculogenesis and gonadotropins and estrogen isoforms ovarian receptors in the offspring at puberty. J Endocrinol. 2008; 198, 625634.CrossRefGoogle ScholarPubMed
Shaw, ND, Srouji, SS, Welt, CK, et al. Compensatory increase in ovarian aromatase in older regularly cycling women. J Clin Endocrinol Metab. 2015; 100, 35393547.CrossRefGoogle ScholarPubMed
Burger, HG, Dudley, E, Mamers, P, Groome, N, Robertson, DM. Early follicular phase serum FSH as a function of age: the roles of inhibin B, inhibin A and estradiol. Climacteric. 2000; 3, 1724.CrossRefGoogle ScholarPubMed
Randolph, JF Jr, Sowers, M, Bondarenko, IV, et al. Change in estradiol and follicle-stimulating hormone across the early menopausal transition: effects of ethnicity and age. J Clin Endocrinol Metab. 2004; 89, 15551561.CrossRefGoogle ScholarPubMed
Sowers, MR, Eyvazzadeh, AD, McConnell, D, et al. Anti-mullerian hormone and inhibin B in the definition of ovarian aging and the menopause transition. J Clin Endocrinol Metab. 2008a; 93, 34783483.CrossRefGoogle ScholarPubMed
Sowers, MR, Zheng, H, McConnell, D, et al. Estradiol rates of change in relation to the final menstrual period in a population-based cohort of women. J Clin Endocrinol Metab. 2008b; 93, 38473852.CrossRefGoogle Scholar
Block, E. Quantitative morphological investigations of the follicular system in women; variations at different ages. Acta Anat (Basel). 1952; 14, 108123.CrossRefGoogle ScholarPubMed
Richardson, SJ, Senikas, V, Nelson, JF. Follicular depletion during the menopausal transition: evidence for accelerated loss and ultimate exhaustion. J Clin Endocrinol Metab. 1987; 65, 12311237.CrossRefGoogle ScholarPubMed
Gougeon, A, Ecochard, R, Thalabard, JC. Age-related changes of the population of human ovarian follicles: increase in the disappearance rate of non-growing and early-growing follicles in aging women. Biol Reprod. 1994; 50, 653663.CrossRefGoogle ScholarPubMed
Turner, KJ, Macpherson, S, Millar, MR, et al. Development and validation of a new monoclonal antibody to mammalian aromatase. J Endocrinol. 2002; 172, 2130.CrossRefGoogle ScholarPubMed
Sakurada, Y, Shirota, M, Inoue, K, Uchida, N, Shirota, K. New approach to in situ quantification of ovarian gene expression in rat using a laser microdissection technique: relationship between follicle types and regulation of inhibin-alpha and cytochrome P450 aromatase genes in the rat ovary. Histochem Cell Biol. 2006; 126, 735741.CrossRefGoogle ScholarPubMed
Kunz, TH, Orrell, KS. Reproduction, energy cost of. Encyclopedia of Energy. 2004; 5, 423442.CrossRefGoogle Scholar
Hales, CN, Barker, DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992; 35, 595601.CrossRefGoogle ScholarPubMed
Gluckman, PD, Hanson, MA. The developmental origins of the metabolic syndrome. Trends Endocrinol Metab. 2004; 15, 183187.CrossRefGoogle ScholarPubMed
Martin-Gronert, MS, Ozanne, SE. Maternal nutrition during pregnancy and health of the offspring. Biochem Soc Trans. 2006; 34, 779782.CrossRefGoogle ScholarPubMed
Vitt, UA, Mazerbourg, S, Klein, C, Hsueh, AJ. Bone morphogenetic protein receptor type II is a receptor for growth differentiation factor-9. Biol Reprod. 2002; 67, 473480.CrossRefGoogle ScholarPubMed
Abadjieva, D, Kistanova, E. Tribulus terrestris alters the expression of growth differentiation factor 9 and bone morphogenetic protein 15 in rabbit ovaries of mothers and F1 female offspring. PLoS One. 2016; 11, e0150400.CrossRefGoogle ScholarPubMed
Eppig, JJ, Wigglesworth, K, Pendola, FL. The mammalian oocyte orchestrates the rate of ovarian follicular development. Proc Natl Acad Sci U S A. 2002; 99, 28902894.CrossRefGoogle ScholarPubMed
Paulini, F, Melo, EO. The role of oocyte-secreted factors GDF9 and BMP15 in follicular development and oogenesis. Reprod Domest Anim. 2011; 46, 354361.CrossRefGoogle ScholarPubMed
Liang, H, Zhang, Z. Food restriction affects reproduction and survival of F1 and F2 offspring of Rat-like hamster (Cricetulus triton). Physiol Behav. 2006; 87, 607613.CrossRefGoogle Scholar
Meikle, D, Westberg, M. Maternal nutrition and reproduction of daughters in wild house mice (Mus musculus). Reproduction. 2001; 122, 437442.CrossRefGoogle Scholar
Rogers, EH, Hunter, ES, Rosen, MB, et al. Lack of evidence for intergenerational reproductive effects due to prenatal and postnatal undernutrition in the female CD-1 mouse. Reprod Toxicol. 2003; 17, 519525.CrossRefGoogle ScholarPubMed