Advertisement

Preclinical Models of Altered Early Life Nutrition and Development of Reproductive Disorders in Female Offspring

  • Pania E. Bridge-Comer
  • Mark H. VickersEmail author
  • Clare M. Reynolds
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1134)

Abstract

Early epidemiology studies in humans have and continue to offer valuable insight into the Developmental Origins of Health and Disease (DOHaD) hypothesis, which emphasises the importance of early-life nutritional and environmental changes on the increased risk of metabolic and reproductive disease in later life. Human studies are limited and constrained by a range of factors which do not apply to preclinical research. Animal models therefore offer a unique opportunity to fully investigate the mechanisms associated with developmental programming, helping to elucidate the developmental processes which influence reproductive diseases, and highlight potential biomarkers which can be translated back to the human condition. This review covers the use and limitations of a number of animal models frequently utilised in developmental programming investigations, with an emphasis on dietary manipulations which can lead to reproductive dysfunction in offspring.

Keywords

Reproductive health Animal model Early-life nutrition Biomarkers Fertility Diet 

References

  1. 1.
    Gluckman PD, Hanson MA, Spencer HG (2005) Predictive adaptive responses and human evolution. Trends Ecol Evol 20:527–533PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    Stocker CJ, Arch JRS, Cawthorne MA (2005) Fetal origins of insulin resistance and obesity. Proc Nutr Soc 64(2):143–151PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    Gluckman PD, Lillycrop KA, Vickers MH, Pleasants AB, Phillips ES, Beedle AS et al (2007) Metabolic plasticity during mammalian development is directionally dependent on early nutritional status. Proc Natl Acad Sci U S A 104:12796–12800PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Vickers MH, Reddy S, Ikenasio BA, Breier BH (2001) Dysregulation of the adipoinsular axis - a mechanism for the pathogenesis of hyperleptinemia and adipogenic diabetes induced by fetal programming. J Endocrinol 170:323–332PubMedCrossRefPubMedCentralGoogle Scholar
  5. 5.
    Osmond C, Barker DJ, Winter PD, Fall CH, Simmonds SJ (1993) Early growth and death from cardiovascular disease in women. BMJ 307:1519–1524PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Barker DJP, Osmond C, Winter PD, Margetts B, Simmonds SJ (1989) Weight in infancy and death from ischaemic heart disease. Lancet 334:577–580CrossRefGoogle Scholar
  7. 7.
    Lumey LH, Van Poppel FW (1994) The Dutch famine of 1944–45: mortality and morbidity in past and present generations. Soc Hist Med 7:229–246PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    Rooij SR, Wouters H, Yonker JE, Painter RC, Roseboom TJ (2010) Prenatal undernutrition and cognitive function in late adulthood. Proc Natl Acad Sci U S A 107:16881–16886PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Duleba AJ (2012) Medical management of metabolic dysfunction in PCOS. Steroids 77:306–311PubMedCrossRefPubMedCentralGoogle Scholar
  10. 10.
    Poretsky L, Cataldo NA, Rosenwaks Z, Giudice LC (1999) The insulin-related ovarian regulatory system in health and disease. Endocr Rev 20:535–582PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Barbieri RL, Makris A, Ryan KJ (1983) Effects of insulin on steroidogenesis in cultured porcine ovarian theca. Fertil Steril 40:237–241PubMedCrossRefPubMedCentralGoogle Scholar
  12. 12.
    Hohos NM, Skaznik-Wikiel ME (2017) High-fat diet and female fertility. Endocrinology 158:2407–2419PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Tsoulis MW, Chang PE, Moore CJ, Chan KA, Gohir W, Petrik JJ et al (2016) Maternal high-fat diet-induced loss of fetal oocytes is associated with compromised follicle growth in adult rat offspring. Biol Reprod 94:94.  https://doi.org/10.1095/biolreprod.115.135004
  14. 14.
    Rockett JC, Lynch CD, Buck GM (2003) Biomarkers for assessing reproductive development and health: part 1--pubertal development. Environ Health Perspect 112:105–112CrossRefGoogle Scholar
  15. 15.
    Metwally M, Li TC, Ledger WL (2007) The impact of obesity on female reproductive function. Obes Rev 8:515–523PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Feng Li X, Lin YS, Kinsey-Jones JS, O'Byrne KT (2012) High-fat diet increases LH pulse frequency and kisspeptin-neurokinin B expression in puberty-advanced female rats. Endocrinology 153:4422–4431CrossRefGoogle Scholar
  17. 17.
    Ahima RS, Dushay J, Flier SN, Prabakaran D, Flier JS (1997) Leptin accelerates the onset of puberty in normal female mice. J Clin Invest 99:391–395PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Moschos S, Chan JL, Mantzoros CS (2002) Leptin and reproduction: a review. Fertil Steril 77:433–444.  https://doi.org/10.1016/S0015-0282(01)03010-2CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Barash IA, Cheung CC, Weigle DS, Ren H, Kabigting EB, Kuijper JL et al (1996) Leptin is a metabolic signal to the reproductive system. Endocrinology 137:3144–3147.  https://doi.org/10.1210/en.137.7.3144CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Cunningham MJ, Clifton DK, Steiner RA (1999) Leptin’s actions on the reproductive axis: perspectives and mechanisms. Biol Reprod 60:216–222PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Brannian JD, Hansen KA (2002) Leptin and ovarian folliculogenesis: implications for ovulation induction and ART outcomes. Semin Reprod Med 20:103–112PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Duggal PS, Hoek Vd HK, Milner CR, Ryan NK, Armstrong DT, Magoffin DA et al (2000) The in vivo and in vitro effects of exogenous leptin on ovulation in the rat. Endocrinology 141:1971–1976PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG (2010) Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160:1577–1579PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Suvorov A, Vandenberg LN (2016) To cull or not to cull? Considerations for studies of endocrine-disrupting chemicals. Endocrinology 157:2586–2594PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Chahoud I, Paumgartten FJR (2009) Influence of litter size on the postnatal growth of rat pups: is there a rationale for litter-size standardization in toxicity studies? Environ Res 109:1021–1027PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Kirkpatrick BW, Rutledge JJ (1988) Influences of prenatal and postnatal fraternity size on ovarian development in the mouse. Biol Reprod 39:1027–1031PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    Holt M, Vangen O, Farstad W (2004) Components of litter size in mice after 110 generations of selection. Reproduction 127:587–592PubMedCrossRefPubMedCentralGoogle Scholar
  28. 28.
    Walker C, Bath KG, Joels M, Korosi A, Larauche M, Lucassen PJ et al (2017) Chronic early life stress induced by limited bedding and nesting (LBN) material in rodents: critical considerations of methodology, outcomes and translational potential. Stress 20:421–448PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Naninck EFG, Hoeijmakers L, Kakava-Georgiadou N, Meesters A, Lazic SE, Lucassen PJ et al (2015) Chronic early life stress alters developmental and adult neurogenesis and impairs cognitive function in mice. Hippocampus 25:309–328PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Committee for the Update of the Guide for the Care and Use of Laboratory Animals (2010) Guide for the care and use of laboratory animals: eighth edition. National Academies Press; 8th ed. (January 27, 2011). ISBN-10: 0309154006Google Scholar
  31. 31.
    Renaud HJ, Cui JY, Lu H, Klaassen CD (2014) Effect of diet on expression of genes involved in lipid metabolism, oxidative stress, and inflammation in mouse liver–insights into mechanisms of hepatic steatosis. PLoS One 9(2):e88584.  https://doi.org/10.1371/journal.pone.0088584CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Syed R, Shibata NM, Kharbanda KK, Su RJ, Olson K, Yokoyama A et al (2016) Effects of nonpurified and choline supplemented or nonsupplemented purified diets on hepatic steatosis and methionine metabolism in C3H mice. Metab Syndr Relat Disord 14:202–209PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Wainwright PE (1998) Issues of design and analysis relating to the use of multiparous species in developmental nutritional studies. J Nutr 128:661–663PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Roseboom TJ, van der Meulen JH, Ravelli AC, Osmond C, Barker DJ, Bleker OP (2001) Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Mol Cell Endocrinol 185:93–98PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Passos MCF, Ramos CF, Moura EG (2000) Short and long term effects of malnutrition in rats during lactation on the body weight of offspring. Nutr Res 20:1603–1612.  https://doi.org/10.1016/S0271-5317(00)00246-3CrossRefGoogle Scholar
  36. 36.
    Sloboda DM, Howie GJ, Pleasants A, Gluckman PD, Vickers MH (2009) Pre- and postnatal nutritional histories influence reproductive maturation and ovarian function in the rat. PLoS One 4(8):e6744.  https://doi.org/10.1371/journal.pone.0006744CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Guzmán C, García-Becerra R, Aguilar-Medina MA, Méndez I, Merchant-Larios H, Zambrano E (2014) Maternal protein restriction during pregnancy and/or lactation negatively affects follicular ovarian development and steroidogenesis in the prepubertal rat offspring. Arch Med Res 45:294–300PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Bispham J, Gopalakrishnan GS, Dandrea J, Wilson V, Budge H, Keisler DH et al (2003) Maternal endocrine adaptation throughout pregnancy to nutritional manipulation: consequences for maternal plasma leptin and cortisol and the programming of fetal adipose tissue development. Endocrinology 144:3575–3585PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Miller AE, Riegle GD (1980) Serum progesterone during pregnancy and pseudopregnancy and gestation length in the aging rat. Biol Reprod 22:751–758PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Parker CR, Mahesh VB (1976) Hormonal events surrounding the natural onset of puberty in female rats. Biol Reprod 14:347–353PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Singh KB (2005) Persistent estrus rat models of polycystic ovary disease: an update. Fertil Steril 84:1228–1234PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Winterhager E, Gellhaus A (2017) Transplacental nutrient transport mechanisms of intrauterine growth restriction in rodent models and humans. Front Physiol 8:951.  https://doi.org/10.3389/fphys.2017.00951CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Alfaradhi MZ, Ozanne SE (2011) Developmental programming in response to maternal overnutrition. Front Genet 2:27.  https://doi.org/10.3389/fgene.2011.00027CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Dickinson H, Moss TJ, Gatford KL, Moritz KM, Akison L, Fullston T et al (2016) A review of fundamental principles for animal models of DOHaD research: an Australian perspective. J Dev Orig Health Dis 7:449–472PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Sarraj MA, Drummond AE (2012) Mammalian foetal ovarian development: consequences for health and disease. Reproduction 143:151–163PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Hubscher C, Brooks D, Johnson J (2005) A quantitative method for assessing stages of the rat estrous cycle. Biotech Histochem 80:79–87PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Colledge WH, Mei H, de Tassigny XDA (2010) Mouse models to study the central regulation of puberty. Mol Cell Endocrinol 324:12–20Google Scholar
  48. 48.
    McLean AC, Valenzuela N, Fai S, Bennett SAL (2012) Performing vaginal lavage, crystal violet staining, and vaginal cytological evaluation for mouse estrous cycle staging identification. J Vis Exp (67):e4389.  https://doi.org/10.3791/4389
  49. 49.
    Bellofiore N, Ellery S, Mamrot J, Walker D, Temple-Smith P, Dickinson H (2016) First evidence of a menstruating rodent: the spiny mouse (Acomys cahirinus). Am J Obstet Gynecol 216(1):40.e1–40.e11.  https://doi.org/10.1016/j.ajog.2016.07.041CrossRefGoogle Scholar
  50. 50.
    Webb R, Woad KJ, Armstrong DG (2002) Corpus luteum (CL) function: local control mechanisms. Domest Anim Endocrinol 23:277–285PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Sangha GK, Sharma RK, Guraya SS (2002) Biology of corpus luteum in small ruminants. Small Rumin Res 43:53–64CrossRefGoogle Scholar
  52. 52.
    Accialini P, Hernandez SF, Abramovich D, Tesone M (2017) The rodent corpus luteum. 117–131.  https://doi.org/10.1007/978-3-319-43238-0_7. In: The life cycle of the corpus luteum. Springer; 1st ed. 2017 edition (November 2, 2016). ASIN: B01M7Y7028
  53. 53.
    Mess A (2014) Placental evolution within the supraordinal clades of eutheria with the perspective of alternative animal models for human placentation. Adv Biol 2014:639274. https://www.hindawi.com/journals/ab/2014/639274/. Accessed Jun 3, 2018.CrossRefGoogle Scholar
  54. 54.
    Varcoe TJ, Boden MJ, Voultsios A, Salkeld MD, Rattanatray L, Kennaway DJ (2013) Characterisation of the maternal response to chronic phase shifts during gestation in the rat: implications for fetal metabolic programming. PLoS One 8(1):e53800.  https://doi.org/10.1371/journal.pone.0053800CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Festing MFW (2006) Design and statistical methods in studies using animal models of development. ILAR J 47:5–14PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Lapatto R, Pallais JC, Zhang D, Chan Y, Mahan A, Cerrato F et al (2007) Kiss1−/− mice exhibit more variable hypogonadism than Gpr54−/− mice. Endocrinology 148:4927–4936PubMedCrossRefPubMedCentralGoogle Scholar
  57. 57.
    Morel O, Laporte-Broux B, Tarrade A, Chavatte-Palmer P (2012) The use of ruminant models in biomedical perinatal research. Theriogenology 78:1763–1773PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    Chavatte-Palmer P, Tarrade A, Rousseau-Ralliard D (2016) Diet before and during pregnancy and offspring health: the importance of animal models and what can be learned from them. Int J Environ Res Public Health 13(6):pii: E586.  https://doi.org/10.3390/ijerph13060586CrossRefGoogle Scholar
  59. 59.
    Nestor CC, Briscoe AMS, Davis SM, Valent M, Goodman RL, Hileman SM (2012) Evidence of a role for kisspeptin and neurokinin B in puberty of female sheep. Endocrinology 153:2756–2765PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Di R, He J, Song S, Tian D, Liu Q, Liang X et al (2014) Characterization and comparative profiling of ovarian microRNAs during ovine anestrus and the breeding season. BMC Genomics 15:899.  https://doi.org/10.1186/1471-2164-15-899CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Rosa HJD, Bryant MJ (2003) Seasonality of reproduction in sheep. Small Rumin Res 48:155–171.  https://doi.org/10.1016/S0921-4488(03)00038-5CrossRefGoogle Scholar
  62. 62.
    Foster DL, Karsch FJ, Olster DH, Ryan KD, Yellon SM (1986) Determinants of puberty in a seasonal breeder. Recent Prog Horm Res 42:331–384PubMedPubMedCentralGoogle Scholar
  63. 63.
    Bartlewski PM, Baby TE, Giffin JL (2011) Reproductive cycles in sheep. Anim Reprod Sci 124:259–268PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Barry JS, Anthony RV (2008) The pregnant sheep as a model for human pregnancy. Theriogenology 69:55–67PubMedCrossRefPubMedCentralGoogle Scholar
  65. 65.
    Reynolds LP, Borowicz PP, Vonnahme KA, Johnson ML, Grazul-Bilska AT, Wallace JM et al (2005) Animal models of placental angiogenesis. Placenta 26:689–708PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Stouffer RL, Woodruff TK (2017) Nonhuman primates: a vital model for basic and applied research on female reproduction, prenatal development, and women’s health. ILAR J 58:281–294PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Bauer C (2015) The baboon (Papio sp.) as a model for female reproduction studies. Contraception 92:120–123PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Li C, Nathanielsz PW, Kuo AH, Gaser C, Schwab M, Clarke GD et al (2017) Premature brain aging in baboons resulting from moderate fetal undernutrition. Front Aging Neurosci 9:92.  https://doi.org/10.3389/fnagi.2017.00092CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Tardif S, Carville A, Elmore D, Williams L, Rice K (2012) Reproduction and breeding of nonhuman Primates. In: Nonhuman primates in biomedical research, pp 197–249. Academic Press; 2 edition (March 29, 2012). ASIN: B00BLHF6DM.CrossRefGoogle Scholar
  70. 70.
    VandeBerg JL, Williams-Blangero S, Tardif SD, SpringerLink (Online service) (2009) The baboon in biomedical research. Springer; 2009 edition (June 4, 2009). ASIN: B008BAQCIA.Google Scholar
  71. 71.
    Plant TM (2012) A comparison of the neuroendocrine mechanisms underlying the initiation of the preovulatory LH surge in the human, Old World monkey and rodent. Front Neuroendocrinol 33:160–168PubMedCrossRefPubMedCentralGoogle Scholar
  72. 72.
    Phillips KA, Bales KL, Capitanio JP, Conley A, Czoty PW, ‘t Hart BA et al (2014) Why primate models matter. Am J Primatol 76:801–827PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Cox LA, Li C, Glenn JP, Lange K, Spradling KD, Nathanielsz PW et al (2013) Expression of the placental transcriptome in maternal nutrient reduction in baboons is dependent on fetal sex. J Nutr 143:1698–1708PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Danilovich N, Babu PS, Xing W, Gerdes M, Krishnamurthy H, Sairam MR (2000) Estrogen deficiency, obesity, and skeletal abnormalities in follicle-stimulating hormone receptor knockout (FORKO) female mice. Endocrinology 141:4295–4308PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    Balen A, Homburg R, Franks S (2009) Defining polycystic ovary syndrome. BMJ 338:a2968.  https://doi.org/10.1136/bmj.a2968CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Dumesic D, Abbott D, Padmanabhan V (2007) Polycystic ovary syndrome and its developmental origins. Rev Endocr Metab Disord 8:127–141PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Shi D, Vine DF (2012) Animal models of polycystic ovary syndrome: a focused review of rodent models in relationship to clinical phenotypes and cardiometabolic risk. Fertil Steril 98:193.e2.  https://doi.org/10.1016/j.fertnstert.2012.04.006CrossRefGoogle Scholar
  78. 78.
    Roberts JS, Perets RA, Sarfert KS, Bowman JJ, Ozark PA, Whitworth GB et al (2017) High-fat high-sugar diet induces polycystic ovary syndrome in a rodent model. Biol Reprod 96:551–562Google Scholar
  79. 79.
    Gunn RG, Sim DA, Hunter EA (1995) Effects of nutrition in utero and in early life on the subsequent lifetime reproductive performance of Scottish Blackface ewes in two management systems. Anim Sci 60:223–230CrossRefGoogle Scholar
  80. 80.
    Vickers MH, Breier BH, Cutfield WS, Hofman PL, Gluckman PD (2000) Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol Endocrinol Metab 279(1):E83–E87PubMedCrossRefPubMedCentralGoogle Scholar
  81. 81.
    Taylor PD, Poston L (2007) Developmental programming of obesity in mammals. Exp Physiol 92:287–298.  https://doi.org/10.1113/expphysiol.2005.032854CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Barker DJP, Godfrey KM, Gluckman PD, Harding JE, Owens JA, Robinson JS (1993) Fetal nutrition and cardiovascular disease in adult life. Lancet 341:938–941PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Yarde F, Broekmans FJM, van der Pal-de Bruin KM, Schönbeck Y, te Velde ER, Stein AD et al (2013) Prenatal famine, birthweight, reproductive performance and age at menopause: the Dutch hunger winter families study. Hum Reprod 28:3328–3336PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Rhind SM, Elston DA, Jones JR, Rees ME, McMillen SR, Gunn RG (1998) Effects of restriction of growth and development of Brecon Cheviot ewe lambs on subsequent lifetime reproductive performance. Small Rumin Res 30:121–126CrossRefGoogle Scholar
  85. 85.
    Wang J, Yu X, Wu R, Sun X, Cheng S, Ge W et al (2018) Starvation during pregnancy impairs fetal oogenesis and folliculogenesis in offspring in the mouse. Cell Death Dis 9:452.  https://doi.org/10.1038/s41419-018-0492-2CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Meikle D, Westberg M (2001) Maternal nutrition and reproduction of daughters in wild house mice (Mus musculus). Reproduction 122:437–442PubMedCrossRefPubMedCentralGoogle Scholar
  87. 87.
    Khorram O, Keen-Rinehart E, Chuang T, Ross MG, Desai M (2015) Maternal undernutrition induces premature reproductive senescence in adult female rat offspring. Fertil Steril 103:298.e2.  https://doi.org/10.1016/j.fertnstert.2014.09.026CrossRefGoogle Scholar
  88. 88.
    Léonhardt M, Lesage J, Croix D, Dutriez-Casteloot I, Beauvillain JC, Dupouy JP (2003) Effects of perinatal maternal food restriction on pituitary-gonadal axis and plasma leptin level in rat pup at birth and weaning and on timing of puberty. Biol Reprod 68:390–400PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Bernal AB, Vickers MH, Hampton MB, Poynton RA, Sloboda DM (2010) Maternal undernutrition significantly impacts ovarian follicle number and increases ovarian oxidative stress in adult rat offspring. PLoS One 5:e15558.  https://doi.org/10.1371/journal.pone.0015558CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Rae MT, Kyle CE, Miller DW, Hammond AJ, Brooks AN, Rhind SM (2002) The effects of undernutrition, in utero, on reproductive function in adult male and female sheep. Anim Reprod Sci 72:63–71PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Borwick SC, Rhind SM, McMillen SR, Racey PA (1997) Effect of undernutrition of ewes from the time of mating on fetal ovarian development in mid gestation. Reprod Fertil Dev 9:711–716PubMedCrossRefPubMedCentralGoogle Scholar
  92. 92.
    Rae MT, Palassio S, Kyle CE, Brooks AN, Lea RG, Miller DW et al (2001) Effect of maternal undernutrition during pregnancy on early ovarian development and subsequent follicular development in sheep fetuses. Reproduction 122:915–922PubMedCrossRefPubMedCentralGoogle Scholar
  93. 93.
    Puttabyatappa M, Cardoso RC, Herkimer C, Veiga-Lopez A, Padmanabhan V (2016) Developmental programming: postnatal estradiol modulation of prenatally organized reproductive neuroendocrine function in sheep. Reproduction 152:139–150PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Iwasa T, Matsuzaki T, Murakami M, Fujisawa S, Kinouchi R, Gereltsetseg G et al (2010) Effects of intrauterine undernutrition on hypothalamic Kiss1 expression and the timing of puberty in female rats. J Physiol 588:821–829PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Chan KA, Bernal AB, Vickers MH, Gohir W, Petrik JJ, Sloboda DM (2015) Early life exposure to undernutrition induces ER stress, apoptosis, and reduced vascularization in ovaries of adult rat offspring. Biol Reprod 92(4):110.  https://doi.org/10.1095/biolreprod.114.124149CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Miller BH, Olson SL, Turek FW, Levine JE, Horton TH, Takahashi JS (2004) Circadian clock mutation disrupts estrous cyclicity and maintenance of pregnancy. Curr Biol 14:1367–1373PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Deligeorgis SG, Chadio S, Menegatos J (1996) Pituitary responsiveness to GnRH in lambs undernourished during fetal life. Anim Reprod Sci 43:113–121CrossRefGoogle Scholar
  98. 98.
    Rae MT, Rhind SM, Kyle CE, Miller DW, Brooks AN (2002) Maternal undernutrition alters triiodothyronine concentrations and pituitary response to GnRH in fetal sheep. J Endocrinol 173:449–455PubMedCrossRefPubMedCentralGoogle Scholar
  99. 99.
    Jahan-Mihan A, Luhovyy BL, El Khoury D, Anderson GH (2011) Dietary proteins as determinants of metabolic and physiologic functions of the gastrointestinal tract. Nutrients 3:574–603PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Zambrano E, Bautista CJ, Deás M, Martínez-Samayoa PM, González-Zamorano M, Ledesma H et al (2006) A low maternal protein diet during pregnancy and lactation has sex- and window of exposure-specific effects on offspring growth and food intake, glucose metabolism and serum leptin in the rat. J Physiol Lond 571:221–230PubMedCrossRefPubMedCentralGoogle Scholar
  101. 101.
    Winship AL, Gazzard SE, Cullen McEwen LA, Bertram JF, Hutt KJ (2018) Maternal low protein diet programmes low ovarian reserve in offspring. Reproduction . pii: REP-18-0247.  https://doi.org/10.1530/REP-18-0247
  102. 102.
    Jahan-Mihan A, Smith CE, Anderson GH (2011) Effect of protein source in diets fed during gestation and lactation on food intake regulation in male offspring of Wistar rats. Am J Physiol Regul Integr Comp Physiol 300:1175.  https://doi.org/10.1152/ajpregu.00744.2010CrossRefGoogle Scholar
  103. 103.
    Jahan-Mihan A, Szeto IMY, Luhovyy BL, Huot PSP, Anderson GH (2012) Soya protein- and casein-based nutritionally complete diets fed during gestation and lactation differ in effects on characteristics of the metabolic syndrome in male offspring of Wistar rats. Br J Nutr 107:284–294PubMedCrossRefPubMedCentralGoogle Scholar
  104. 104.
    Jahan-Mihan A, Rodriguez J, Christie C, Sadeghi M, Zerbe T (2015) The role of maternal dietary proteins in development of metabolic syndrome in offspring. Nutrients 7(11):9185–9217PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Guzmán C, Cabrera R, Cárdenas M, Larrea F, Nathanielsz PW, Zambrano E (2006) Protein restriction during fetal and neonatal development in the rat alters reproductive function and accelerates reproductive ageing in female progeny. J Physiol Lond 572:97–108PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Brasil FB, Faria TS, Costa WS, Sampaio FJB, Ramos CF (2005) The pups’ endometrium morphology is affected by maternal malnutrition during suckling. Maturitas 51:405–412PubMedCrossRefPubMedCentralGoogle Scholar
  107. 107.
    Smith JT, Waddell BJ (2000) Increased fetal glucocorticoid exposure delays puberty onset in postnatal life. Endocrinology 141:2422–2428PubMedCrossRefPubMedCentralGoogle Scholar
  108. 108.
    Ferreira RV, Gombar FM, da Silva Faria T, Costa WS, Sampaio FJB, da Fonte Ramos C (2010) Metabolic programming of ovarian angiogenesis and folliculogenesis by maternal malnutrition during lactation. Fertil Steril 93:2572–2580PubMedCrossRefPubMedCentralGoogle Scholar
  109. 109.
    Catalano PM (2003) Obesity and pregnancy—the propagation of a viscous cycle? J Clin Endocrinol Metab 88:3505–3506PubMedCrossRefPubMedCentralGoogle Scholar
  110. 110.
    Gluckman PD, Hanson MA (2008) Developmental and epigenetic pathways to obesity: an evolutionary-developmental perspective. Int J Obes 32(Suppl 7):S62–S71.  https://doi.org/10.1038/ijo.2008.240CrossRefGoogle Scholar
  111. 111.
    Lain KY, Catalano PM (2007) Metabolic changes in pregnancy. Clin Obstet Gynecol 50(4):938–948PubMedCrossRefPubMedCentralGoogle Scholar
  112. 112.
    Kubo A, Ferrara A, Laurent CA, Windham GC, Greenspan LC, Deardorff J et al (2016) Associations between maternal pregravid obesity and gestational diabetes and the timing of pubarche in daughters. Am J Epidemiol 184:7–14PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Buettner R, Schölmerich J, Bollheimer LC (2007) High-fat diets: modeling the metabolic disorders of human obesity in rodents. Obesity (Silver Spring) 15:798–808CrossRefGoogle Scholar
  114. 114.
    George LA, Uthlaut AB, Long NM, Zhang L, Ma Y, Smith DT et al (2010) Different levels of overnutrition and weight gain during pregnancy have differential effects on fetal growth and organ development. Reprod Biol Endocrinol 8:75.  https://doi.org/10.1186/1477-7827-8-75
  115. 115.
    Jungheim ES, Schoeller EL, Marquard KL, Louden ED, Schaffer JE, Moley KH (2010) Diet-induced obesity model: abnormal oocytes and persistent growth abnormalities in the offspring. Endocrinology 151:4039–4046PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Cheong Y, Sadek KH, Bruce KD, Macklon N, Cagampang FR (2014) Diet-induced maternal obesity alters ovarian morphology and gene expression in the adult mouse offspring. Fertil Steril 102:899–907PubMedCrossRefPubMedCentralGoogle Scholar
  117. 117.
    Reynolds CM, Segovia SA, Zhang XD, Gray C, Vickers MH (2015) Conjugated linoleic acid supplementation during pregnancy and lactation reduces maternal high-fat-diet-induced programming of early-onset puberty and hyperlipidemia in female rat offspring. Biol Reprod 92(2):40.  https://doi.org/10.1095/biolreprod.114.125047CrossRefPubMedPubMedCentralGoogle Scholar
  118. 118.
    Connor KL, Vickers MH, Beltrand J, Meaney MJ, Sloboda DM (2012) Nature, nurture or nutrition? Impact of maternal nutrition on maternal care, offspring development and reproductive function. J Physiol 590:2167–2180PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Da Silva P, Aitken RP, Rhind SM, Racey PA, Wallace JM (2003) Effect of maternal overnutrition during pregnancy on pituitary gonadotrophin gene expression and gonadal morphology in female and male foetal sheep at day 103 of gestation. Placenta 24:248–257.  https://doi.org/10.1053/plac.2002.0897CrossRefPubMedPubMedCentralGoogle Scholar
  120. 120.
    Shasa DR, Odhiambo JF, Long NM, Tuersunjiang N, Nathanielsz PW, Ford SP (2015) Multigenerational impact of maternal overnutrition/obesity in the sheep on the neonatal leptin surge in granddaughters. Int J Obes 39:695–701CrossRefGoogle Scholar
  121. 121.
    Uri-Belapolsky S, Shaish A, Eliyahu E, Grossman H, Levi M, Chuderland D et al (2014) Interleukin-1 deficiency prolongs ovarian lifespan in mice. Proc Natl Acad Sci U S A 111:12492–12497PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Ludwig DS, Peterson KE, Gortmaker SL (2001) Relation between consumption of sugar-sweetened drinks and childhood obesity: a prospective, observational analysis. Lancet 357:505–508PubMedCrossRefPubMedCentralGoogle Scholar
  123. 123.
    Sloboda DM, Li M, Patel R, Clayton ZE, Yap C, Vickers MH (2014) Early life exposure to fructose and offspring phenotype: implications for long term metabolic homeostasis. J Obes 2014:203474.  https://doi.org/10.1155/2014/203474CrossRefPubMedPubMedCentralGoogle Scholar
  124. 124.
    Rendeiro C, Masnik AM, Mun JG, Du K, Clark D, Dilger RN et al (2015) Fructose decreases physical activity and increases body fat without affecting hippocampal neurogenesis and learning relative to an isocaloric glucose diet. Sci Rep 5:9589.  https://doi.org/10.1038/srep09589CrossRefPubMedPubMedCentralGoogle Scholar
  125. 125.
    Vickers MH, Clayton ZE, Yap C, Sloboda DM (2011) Maternal fructose intake during pregnancy and lactation alters placental growth and leads to sex-specific changes in fetal and neonatal endocrine function. Endocrinology 152:1378–1387PubMedCrossRefPubMedCentralGoogle Scholar
  126. 126.
    Galipeau D, Verma S, McNeill JH (2002) Female rats are protected against fructose-induced changes in metabolism and blood pressure. Am J Physiol Heart Circ Physiol 283:2478CrossRefGoogle Scholar
  127. 127.
    Munetsuna E, Yamada H, Yamazaki M, Ando Y, Mizuno G, Ota T et al (2018) Maternal fructose intake disturbs ovarian estradiol synthesis in rats. Life Sci 202:117–123PubMedCrossRefPubMedCentralGoogle Scholar
  128. 128.
    Gomez-Smith M, Corbett D, Karthikeyan S, Jeffers MS, Janik R, Thomason LA et al (2016) A physiological characterization of the cafeteria diet model of metabolic syndrome in the rat. Physiol Behav 167:382–391Google Scholar
  129. 129.
    Jacobs S, Teixeira DS, Guilherme C, Rocha d, Claudio FK, Aranda BCC et al (2014) The impact of maternal consumption of cafeteria diet on reproductive function in the offspring. Physiol Behav 129:280–286PubMedCrossRefPubMedCentralGoogle Scholar
  130. 130.
    Sampey BP, Vanhoose AM, Winfield HM, Freemerman AJ, Muehlbauer MJ, Fueger PT et al (2011) Cafeteria diet is a robust model of human metabolic syndrome with liver and adipose inflammation: comparison to high-fat diet. Obesity (Silver Spring) 19:1109–1117CrossRefGoogle Scholar
  131. 131.
    Barrett P, Mercer JG, Morgan PJ (2016) Preclinical models for obesity research. Dis Model Mech 9:1245–1255PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    Bayol SA, Simbi BH, Stickland NC (2005) A maternal cafeteria diet during gestation and lactation promotes adiposity and impairs skeletal muscle development and metabolism in rat offspring at weaning. J Physiol 567:951–961PubMedPubMedCentralCrossRefGoogle Scholar
  133. 133.
    Bayol SA, Simbi BH, Bertrand JA, Stickland NC (2008) Offspring from mothers fed a ‘junk food’ diet in pregnancy and lactation exhibit exacerbated adiposity that is more pronounced in females. J Physiol 586:3219–3230PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Sagae SC, Menezes EF, Bonfleur ML, Vanzela EC, Zacharias P, Lubaczeuski C et al (2012) Early onset of obesity induces reproductive deficits in female rats. Physiol Behav 105:1104–1111Google Scholar
  135. 135.
    Bazzano MV, Torelli C, Pustovrh MC, Paz DA, Elia EM (2015) Obesity induced by cafeteria diet disrupts fertility in the rat by affecting multiple ovarian targets. Reprod Biomed Online 31:655–667PubMedCrossRefPubMedCentralGoogle Scholar
  136. 136.
    Henriksen T, Clausen T (2002) The fetal origins hypothesis: placental insufficiency and inheritance versus maternal malnutrition in well-nourished populations. Acta Obstet Gynecol Scand 81:112–114PubMedCrossRefPubMedCentralGoogle Scholar
  137. 137.
    Vuguin PM (2007) Animal models for small for gestational age and fetal programing of adult disease. Horm Res 68:113–123PubMedPubMedCentralGoogle Scholar
  138. 138.
    Janot M, Cortes-Dubly M, Rodriguez S, Huynh-Do U (2014) Bilateral uterine vessel ligation as a model of intrauterine growth restriction in mice. Reprod Biol Endocrinol 12:62.  https://doi.org/10.1186/1477-7827-12-62CrossRefPubMedPubMedCentralGoogle Scholar
  139. 139.
    O’Dowd R, Kent JC, Moseley JM, Wlodek ME (2008) Effects of uteroplacental insufficiency and reducing litter size on maternal mammary function and postnatal offspring growth. Am J Physiol Regul Integr Comp Physiol 294:539.  https://doi.org/10.1152/ajpregu.00628.2007CrossRefGoogle Scholar
  140. 140.
    Engelbregt MJ, Houdijk ME, Popp-Snijders C, Delemarre-van de Waal HA (2000) The effects of intra-uterine growth retardation and postnatal undernutrition on onset of puberty in male and female rats. Pediatr Res 48:803–807PubMedCrossRefPubMedCentralGoogle Scholar
  141. 141.
    Romano T, Hryciw DH, Westcott KT, Wlodek ME (2017) Puberty onset is delayed following uteroplacental insufficiency and occurs earlier with improved lactation and growth for pups born small. Reprod Fertil Dev 29:307–318PubMedCrossRefPubMedCentralGoogle Scholar
  142. 142.
    Morrison JL (2008) Sheep models of intrauterine growth restriction: fetal adaptations and consequences. Clin Exp Pharmacol Physiol 35(7):730–743PubMedCrossRefPubMedCentralGoogle Scholar
  143. 143.
    de Bruin JP, Dorland M, Bruinse HW, Spliet W, Nikkels PGJ, Te Velde ER (1998) Fetal growth retardation as a cause of impaired ovarian development. Early Hum Dev 51:39–46PubMedCrossRefPubMedCentralGoogle Scholar
  144. 144.
    Fowden AL, Giussani DA, Forhead AJ (2006) Intrauterine programming of physiological systems: causes and consequences. Physiology (Bethesda) 21:29–37Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Pania E. Bridge-Comer
    • 1
  • Mark H. Vickers
    • 1
    Email author
  • Clare M. Reynolds
    • 1
  1. 1.The Liggins Institute, University of AucklandAucklandNew Zealand

Personalised recommendations