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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Calorie restriction during gestation affects ovarian reserve in offspring in the mouse

Bianka M. Zanini A , Kelvin R. S. Andrade A , Jorgea Pradiee A , Gabriel B. Veiga A , Driele N. Garcia B , Rafael G. Mondadori C , Luís A. X. Cruz C , Joao A. Alvarado-Rincón D , Renata P. Ramirez A , Tatiana D. Saccon B , Michal M. Masternak E , Carlos C. Barros A and Augusto Schneider https://orcid.org/0000-0002-3410-2860 A F
+ Author Affiliations
- Author Affiliations

A Faculdade de Nutrição, Universidade Federal de Pelotas, Pelotas, RS, Brazil.

B Centro de Desenvolvimento Tecnológico, Universidade Federal de Pelotas, Pelotas, RS, Brazil.

C Instituto de Biologia, Universidade Federal de Pelotas, Pelotas, RS, Brazil.

D Faculdade de Veterinária, Universidade Federal de Pelotas, Pelotas, RS, Brazil.

E Burnett School of Biomedical Sciences, College of Medicine, University of Central Florida, Orlando, FL, USA.

F Corresponding author. Email: augusto.schneider@ufpel.edu.br

Reproduction, Fertility and Development 32(18) 1338-1349 https://doi.org/10.1071/RD20107
Submitted: 17 April 2020  Accepted: 27 October 2020   Published: 27 November 2020

Abstract

The aim of this study was to investigate the effect of calorie restriction (CR) during pregnancy in mice on metabolism and ovarian function in the offspring. Pregnant female mice were divided into two groups, a control group and a CR group (n = 7 in each). Mice in the CR group were fed 50% of the amount consumed by control females from Day 10 of gestation until delivery. After weaning, the offspring received diet ad libitum until 3 months of age, when ovaries were collected. Ovaries were serially cut and every sixth section was used for follicle counting. Female offspring from CR dams tended to have increased bodyweight compared with offspring from control females (P = 0.08). Interestingly, fewer primordial follicles (60% reduction; P = 0.001), transitional follicles (P = 0.0006) and total follicles (P = 0.006) were observed in offspring from CR mothers. The number of primary, secondary and tertiary follicles did not differ between the groups (P > 0.05). The CR offspring had fewer DNA double-strand breaks in primary follicle oocytes (P = 0.03). In summary, CR during the second half of gestation decreased primordial ovarian follicle reserve in female offspring. These findings suggest that undernutrition during the second half of gestation may decrease the reproductive lifespan of female offspring.

Graphical Abstract Image

Keywords: calorie restriction, diet, intrauterine, primordial follicles.


References

Baker, T. G. (1963). A quantitative and cytological study of germ cells in human ovaries. Proc. R. Soc. Lond. B Biol. Sci. 158, 417–433.
A quantitative and cytological study of germ cells in human ovaries.Crossref | GoogleScholarGoogle Scholar | 14070052PubMed |

Barker, D. J. (2004). The developmental origins of chronic adult disease. Acta Paediatr. 93, 26–33.
The developmental origins of chronic adult disease.Crossref | GoogleScholarGoogle Scholar |

Barker, D. J., Osmond, C., Forsén, T. J., Kajantie, E., and Eriksson, J. G. (2005). Trajectories of growth among children who have coronary events as adults. N. Engl. J. Med. 353, 1802–1809.
Trajectories of growth among children who have coronary events as adults.Crossref | GoogleScholarGoogle Scholar | 16251536PubMed |

Barros, C. C., Haro, A., Russo, F. J., Schadock, I., Almeida, S. S., Ribeiro, R. A., Vanzela, E. C., Lanzoni, V. P., Barros, F. C., Moraes, M. R., Mori, M. A., Bacurau, R. F. P., Wurtele, M., Boschero, A. C., Carneiro, E. M., Bader, M., Pesquero, J. B., and Araujo, R. C. (2012). Altered glucose homeostasis and hepatic function in obese mice deficient for both kinin receptor genes. PLoS One 7, e40573.
Altered glucose homeostasis and hepatic function in obese mice deficient for both kinin receptor genes.Crossref | GoogleScholarGoogle Scholar | 22829877PubMed |

Bernal, A. B., Vickers, M. H., Hampton, M. B., Poynton, R. A., and Sloboda, D. M. (2010). Maternal undernutrition significantly impacts ovarian follicle number and increases ovarian oxidative stress in adult rat offspring. PLoS One 5, e15558.
Maternal undernutrition significantly impacts ovarian follicle number and increases ovarian oxidative stress in adult rat offspring.Crossref | GoogleScholarGoogle Scholar | 21179452PubMed |

Buckler, H. (2005). The menopause transition: endocrine changes and clinical symptoms. J. Br. Menopause Soc. 11, 61–65.
The menopause transition: endocrine changes and clinical symptoms.Crossref | GoogleScholarGoogle Scholar | 15970017PubMed |

Castrillon, D. H., Miao, L., Kollipara, R., Horner, J. W., and DePinho, R. A. (2003). Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 301, 215–218.
Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a.Crossref | GoogleScholarGoogle Scholar | 12855809PubMed |

Chan, K. A., Bernal, A. B., Vickers, M. H., Gohir, W., Petrik, J. J., and Sloboda, D. M. (2015). Early life exposure to undernutrition induces ER stress, apoptosis, and reduced vascularization in ovaries of adult rat offspring. Biol. Reprod. 92, 110–111.
Early life exposure to undernutrition induces ER stress, apoptosis, and reduced vascularization in ovaries of adult rat offspring.Crossref | GoogleScholarGoogle Scholar | 25810471PubMed |

Chan, K. A., Jazwiec, P. A., Gohir, W., Petrik, J. J., and Sloboda, D. M. (2018). Maternal nutrient restriction impairs young adult offspring ovarian signaling resulting in reproductive dysfunction and follicle loss. Biol. Reprod. 98, 664–682.
Maternal nutrient restriction impairs young adult offspring ovarian signaling resulting in reproductive dysfunction and follicle loss.Crossref | GoogleScholarGoogle Scholar | 29351580PubMed |

Choi, G. Y., Tosh, D. N., Garg, A., Mansano, R., Ross, M. G., and Desai, M. (2007). Gender-specific programmed hepatic lipid dysregulation in intrauterine growth-restricted offspring. Am. J. Obstet. Gynecol. 196, 477.e1–477.e7.
Gender-specific programmed hepatic lipid dysregulation in intrauterine growth-restricted offspring.Crossref | GoogleScholarGoogle Scholar |

Cohen, P. E., and Holloway, J. K. (2010). Predicting gene networks in human oocyte meiosis. Biol. Reprod. 82, 469–472.
Predicting gene networks in human oocyte meiosis.Crossref | GoogleScholarGoogle Scholar | 20032284PubMed |

de Rooij, S. R., Wouters, H., Yonker, J. E., Painter, R. C., and Roseboom, T. J. (2010). Prenatal undernutrition and cognitive function in late adulthood. Proc. Natl Acad. Sci. USA 107, 16881–16886.
Prenatal undernutrition and cognitive function in late adulthood.Crossref | GoogleScholarGoogle Scholar | 20837515PubMed |

Desai, M., Gayle, D., Babu, J., and Ross, M. G. (2005). Programmed obesity in intrauterine growth-restricted newborns: modulation by newborn nutrition. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R91–R96.
Programmed obesity in intrauterine growth-restricted newborns: modulation by newborn nutrition.Crossref | GoogleScholarGoogle Scholar | 15297266PubMed |

Evans, A. C., Mossa, F., Walsh, S. W., Scheetz, D., Jimenez-Krassel, F., Ireland, J. L., Smith, G. W., and Ireland, J. J. (2012). Effects of maternal environment during gestation on ovarian folliculogenesis and consequences for fertility in bovine offspring. Reprod. Domest. Anim. 47, 31–37.
Effects of maternal environment during gestation on ovarian folliculogenesis and consequences for fertility in bovine offspring.Crossref | GoogleScholarGoogle Scholar | 22827347PubMed |

Fortune, J. E., Yang, M. Y., Allen, J. J., and Herrick, S. L. (2013). Triennial Reproduction Symposium: the ovarian follicular reserve in cattle: what regulates its formation and size? J. Anim. Sci. 91, 3041–3050.
Triennial Reproduction Symposium: the ovarian follicular reserve in cattle: what regulates its formation and size?Crossref | GoogleScholarGoogle Scholar | 23736047PubMed |

García, A. P., Palou, M., Sánchez, J., Priego, T., Palou, A., and Picó, C. (2011). Moderate caloric restriction during gestation in rats alters adipose tissue sympathetic innervation and later adiposity in offspring. PLoS One 6, e17313.
Moderate caloric restriction during gestation in rats alters adipose tissue sympathetic innervation and later adiposity in offspring.Crossref | GoogleScholarGoogle Scholar | 21364997PubMed |

Garcia, D. N., Saccon, T. D., Pradiee, J., Rincon, J. A. A., Andrade, K. R. S., Rovani, M. T., Mondadori, R. G., Cruz, L. A. X., Barros, C. C., Masternak, M. M., Bartke, A., Mason, J. B., and Schneider, A. (2019). Effect of caloric restriction and rapamycin on ovarian aging in mice. Geroscience 41, 395–408.
Effect of caloric restriction and rapamycin on ovarian aging in mice.Crossref | GoogleScholarGoogle Scholar | 31359237PubMed |

Gardner, D. S., Ozanne, S. E., and Sinclair, K. D. (2009). Effect of the early-life nutritional environment on fecundity and fertility of mammals. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 3419–3427.
Effect of the early-life nutritional environment on fecundity and fertility of mammals.Crossref | GoogleScholarGoogle Scholar | 19833652PubMed |

Gluckman, P. D., Hanson, M. A., Cooper, C., and Thornburg, K. L. (2008). Effect of in utero and early-life conditions on adult health and disease. N. Engl. J. Med. 359, 61–73.
Effect of in utero and early-life conditions on adult health and disease.Crossref | GoogleScholarGoogle Scholar | 18596274PubMed |

Godfrey, K. M., Gluckman, P. D., and Hanson, M. A. (2010). Developmental origins of metabolic disease: life course and intergenerational perspectives. Trends Endocrinol. Metab. 21, 199–205.
Developmental origins of metabolic disease: life course and intergenerational perspectives.Crossref | GoogleScholarGoogle Scholar | 20080045PubMed |

Griffin, J., Emery, B. R., Huang, I., Peterson, C. M., and Carrell, D. T. (2006). Comparative analysis of follicle morphology and oocyte diameter in four mammalian species (mouse, hamster, pig, and human). J. Exp. Clin. Assist. Reprod. 3, 2.
Comparative analysis of follicle morphology and oocyte diameter in four mammalian species (mouse, hamster, pig, and human).Crossref | GoogleScholarGoogle Scholar | 16509981PubMed |

Grive, K. J., and Freiman, R. N. (2015). The developmental origins of the mammalian ovarian reserve. Development 142, 2554–2563.
The developmental origins of the mammalian ovarian reserve.Crossref | GoogleScholarGoogle Scholar | 26243868PubMed |

Guzmán, C., Cabrera, R., Cárdenas, M., Larrea, F., Nathanielsz, P. W., and 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. 572, 97–108.
Protein restriction during fetal and neonatal development in the rat alters reproductive function and accelerates reproductive ageing in female progeny.Crossref | GoogleScholarGoogle Scholar | 16497715PubMed |

Guzmán, C., García-Becerra, R., Aguilar-Medina, M. A., Méndez, I., Merchant-Larios, H., and 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, 294–300.
Maternal protein restriction during pregnancy and/or lactation negatively affects follicular ovarian development and steroidogenesis in the prepubertal rat offspring.Crossref | GoogleScholarGoogle Scholar | 24819035PubMed |

Harrath, A. H., Alrezaki, A., Mansour, L., Alwasel, S. H., and Palomba, S. (2017). Food restriction during pregnancy and female offspring fertility: adverse effects of reprogrammed reproductive lifespan. J. Ovarian Res. 10, 77.
Food restriction during pregnancy and female offspring fertility: adverse effects of reprogrammed reproductive lifespan.Crossref | GoogleScholarGoogle Scholar | 29282125PubMed |

Hofman, P. L., Cutfield, W. S., Robinson, E. M., Bergman, R. N., Menon, R. K., Sperling, M. A., and Gluckman, P. D. (1997). Insulin resistance in short children with intrauterine growth retardation. J. Clin. Endocrinol. Metab. 82, 402–406.
Insulin resistance in short children with intrauterine growth retardation.Crossref | GoogleScholarGoogle Scholar | 9024226PubMed |

Howie, G. J., Sloboda, D. M., and Vickers, M. H. (2012). Maternal undernutrition during critical windows of development results in differential and sex-specific effects on postnatal adiposity and related metabolic profiles in adult rat offspring. Br. J. Nutr. 108, 298–307.
Maternal undernutrition during critical windows of development results in differential and sex-specific effects on postnatal adiposity and related metabolic profiles in adult rat offspring.Crossref | GoogleScholarGoogle Scholar | 22018052PubMed |

Kevenaar, M. E., Meerasahib, M. F., Kramer, P., van de Lang-Born, B. M., de Jong, F. H., Groome, N. P., and Visser, J. A. (2006). Serum anti-Mullerian hormone levels reflect the size of the primordial follicle pool in mice. Endocrinology 147, 3228–3234.
Serum anti-Mullerian hormone levels reflect the size of the primordial follicle pool in mice.Crossref | GoogleScholarGoogle Scholar | 16556768PubMed |

Lea, R. G., Andrade, L. P., Rae, M. T., Hannah, L. T., Kyle, C. E., Murray, J. F., Rhind, S. M., and Miller, D. W. (2006). Effects of maternal undernutrition during early pregnancy on apoptosis regulators in the ovine fetal ovary. Reproduction 131, 113–124.
Effects of maternal undernutrition during early pregnancy on apoptosis regulators in the ovine fetal ovary.Crossref | GoogleScholarGoogle Scholar | 16388015PubMed |

Lintern-Moore, S. U. E., and Moore, G. P. M. (1979). The initiation of follicle and oocyte growth in the mouse ovary. Biol. Reprod. 20, 773–778.
The initiation of follicle and oocyte growth in the mouse ovary.Crossref | GoogleScholarGoogle Scholar |

Lumey, L. H., and Stein, A. D. (1997). In utero exposure to famine and subsequent fertility: the Dutch Famine Birth Cohort Study. Am. J. Public Health 87, 1962–1966.
In utero exposure to famine and subsequent fertility: the Dutch Famine Birth Cohort Study.Crossref | GoogleScholarGoogle Scholar | 9431284PubMed |

Malo, E., Saukko, M., Santaniemi, M., Hietaniemi, M., Lammentausta, E., Sequeiros, R. B., Ukkola, O., and Kesäniemi, Y. A. (2013). Plasma lipid levels and body weight altered by intrauterine growth restriction and postnatal fructose diet in adult rats. Pediatr. Res. 73, 155.
Plasma lipid levels and body weight altered by intrauterine growth restriction and postnatal fructose diet in adult rats.Crossref | GoogleScholarGoogle Scholar | 23174704PubMed |

Masternak, M. M., Al-Regaiey, K. A., Del Rosario Lim, M. M., Bonkowski, M. S., Panici, J. A., Przybylski, G. K., and Bartke, A. (2005). Caloric restriction results in decreased expression of peroxisome proliferator-activated receptor superfamily in muscle of normal and long-lived growth hormone receptor/binding protein knockout mice. J. Gerontol. A Biol. Sci. Med. Sci. 60, 1238–1245.
Caloric restriction results in decreased expression of peroxisome proliferator-activated receptor superfamily in muscle of normal and long-lived growth hormone receptor/binding protein knockout mice.Crossref | GoogleScholarGoogle Scholar | 16282554PubMed |

McGee, E. A., and Hsueh, A. J. (2000). Initial and cyclic recruitment of ovarian follicles. Endocr. Rev. 21, 200–214.
Initial and cyclic recruitment of ovarian follicles.Crossref | GoogleScholarGoogle Scholar | 10782364PubMed |

Myers, M., Britt, K. L., Wreford, N. G. M., Ebling, F. J., and Kerr, J. B. (2004). Methods for quantifying follicular numbers within the mouse ovary. Reproduction 127, 569–580.
Methods for quantifying follicular numbers within the mouse ovary.Crossref | GoogleScholarGoogle Scholar | 15129012PubMed |

Navot, D., Bergh, R. A., Williams, M. A., Garrisi, G. J., Guzman, I., Sandler, B., and Grunfeld, L. (1991). Poor oocyte quality rather than implantation failure as a cause of age-related decline in female fertility. Lancet 337, 1375–1377.
Poor oocyte quality rather than implantation failure as a cause of age-related decline in female fertility.Crossref | GoogleScholarGoogle Scholar | 1674764PubMed |

Nteeba, J., Ross, J. W., Perfield Ii, J. W., and Keating, A. F. (2013). High fat diet induced obesity alters ovarian phosphatidylinositol-3 kinase signaling gene expression. Reprod. Toxicol. 42, 68–77.
High fat diet induced obesity alters ovarian phosphatidylinositol-3 kinase signaling gene expression.Crossref | GoogleScholarGoogle Scholar | 23954404PubMed |

Palou, M., Konieczna, J., Torrens, J. M., Sanchez, J., Priego, T., Fernandes, M. L., Palou, A., and Picó, C. (2012). Impaired insulin and leptin sensitivity in the offspring of moderate caloric-restricted dams during gestation is early programmed. J. Nutr. Biochem. 23, 1627–1639.
Impaired insulin and leptin sensitivity in the offspring of moderate caloric-restricted dams during gestation is early programmed.Crossref | GoogleScholarGoogle Scholar | 22444870PubMed |

Pepling, M. E., Wilhelm, J. E., O’Hara, A. L., Gephardt, G. W., and Spradling, A. C. (2007). Mouse oocytes within germ cell cysts and primordial follicles contain a Balbiani body. Proc. Natl Acad. Sci. USA 104, 187–192.
Mouse oocytes within germ cell cysts and primordial follicles contain a Balbiani body.Crossref | GoogleScholarGoogle Scholar | 17189423PubMed |

Peters, H. (1969). The development of the mouse ovary from birth to maturity. Eur. J. Endocrinol. 62, 98–116.
The development of the mouse ovary from birth to maturity.Crossref | GoogleScholarGoogle Scholar |

Picó, C., Palou, M., Priego, T., Sánchez, J., and Palou, A. (2012). Metabolic programming of obesity by energy restriction during the perinatal period: different outcomes depending on gender and period, type and severity of restriction. Front. Physiol. 3, 436.
Metabolic programming of obesity by energy restriction during the perinatal period: different outcomes depending on gender and period, type and severity of restriction.Crossref | GoogleScholarGoogle Scholar | 23189059PubMed |

Rae, M. T., Palassio, S., Kyle, C. E., Brooks, A. N., Lea, R. G., Miller, D. W., and Rhind, S. M. (2001). Effect of maternal undernutrition during pregnancy on early ovarian development and subsequent follicular development in sheep fetuses. Reproduction 122, 915–922.
Effect of maternal undernutrition during pregnancy on early ovarian development and subsequent follicular development in sheep fetuses.Crossref | GoogleScholarGoogle Scholar | 11732987PubMed |

Richardson, M. C., Guo, M., Fauser, B. C. J. M., and Macklon, N. S. (2014). Environmental and developmental origins of ovarian reserve. Hum. Reprod. Update 20, 353–369.
Environmental and developmental origins of ovarian reserve.Crossref | GoogleScholarGoogle Scholar | 24287894PubMed |

Roseboom, T., de Rooij, S., and Painter, R. (2006). The Dutch famine and its long-term consequences for adult health. Early Hum. Dev. 82, 485–491.
The Dutch famine and its long-term consequences for adult health.Crossref | GoogleScholarGoogle Scholar | 16876341PubMed |

Schneider, A., Zhi, X., Moreira, F., Lucia, T., Mondadori, R. G., and Masternak, M. M. (2014). Primordial follicle activation in the ovary of Ames dwarf mice. J. Ovarian Res. 7, 120.
Primordial follicle activation in the ovary of Ames dwarf mice.Crossref | GoogleScholarGoogle Scholar | 25543533PubMed |

Schneider, A., Matkovich, S. J., Saccon, T., Victoria, B., Spinel, L., Lavasani, M., Bartke, A., Golusinski, P., and Masternak, M. M. (2017). Ovarian transcriptome associated with reproductive senescence in the long-living Ames dwarf mice. Mol. Cell. Endocrinol. 439, 328–336.
Ovarian transcriptome associated with reproductive senescence in the long-living Ames dwarf mice.Crossref | GoogleScholarGoogle Scholar | 27663076PubMed |

Skaznik-Wikiel, M. E., Swindle, D. C., Allshouse, A. A., Polotsky, A. J., and McManaman, J. L. (2016). High-fat diet causes subfertility and compromised ovarian function independent of obesity in mice. Biol. Reprod. 94, 108.
High-fat diet causes subfertility and compromised ovarian function independent of obesity in mice.Crossref | GoogleScholarGoogle Scholar | 27030045PubMed |

Sloboda, D. M., Hart, R., Doherty, D. A., Pennell, C. E., and Hickey, M. (2007). Age at menarche: influences of prenatal and postnatal growth. J. Clin. Endocrinol. Metab. 92, 46–50.
Age at menarche: influences of prenatal and postnatal growth.Crossref | GoogleScholarGoogle Scholar | 17062767PubMed |

Sloboda, D. M., Howie, G. J., Pleasants, A., Gluckman, P. D., and Vickers, M. H. (2009). Pre-and postnatal nutritional histories influence reproductive maturation and ovarian function in the rat. PLoS One 4, e6744.
Pre-and postnatal nutritional histories influence reproductive maturation and ovarian function in the rat.Crossref | GoogleScholarGoogle Scholar | 19707592PubMed |

Stein, A. D., Ravelli, A. C., and Lumey, L. (1995). Famine, third-trimester pregnancy weight gain, and intrauterine growth: the Dutch Famine Birth Cohort Study. Hum. Biol. 67, 135–150.
| 7721275PubMed |

Symonds, M. E., Sebert, S. P., Hyatt, M. A., and Budge, H. (2009). Nutritional programming of the metabolic syndrome. Nat. Rev. Endocrinol. 5, 604.
Nutritional programming of the metabolic syndrome.Crossref | GoogleScholarGoogle Scholar | 19786987PubMed |

Szegda, K. L., Whitcomb, B. W., Purdue-Smithe, A. C., Boutot, M. E., Manson, J. E., Hankinson, S. E., Rosner, B. A., and Bertone-Johnson, E. R. (2017). Adult adiposity and risk of early menopause. Hum. Reprod. 32, 2522–2531.
Adult adiposity and risk of early menopause.Crossref | GoogleScholarGoogle Scholar | 29087465PubMed |

Szostaczuk, N., Priego, T., Palou, M., Palou, A., and Picó, C. (2017). Oral leptin supplementation throughout lactation in rats prevents later metabolic alterations caused by gestational calorie restriction. Int. J. Obes. 41, 360.
Oral leptin supplementation throughout lactation in rats prevents later metabolic alterations caused by gestational calorie restriction.Crossref | GoogleScholarGoogle Scholar |

Thompson, N. M., Norman, A. M., Donkin, S. S., Shankar, R. R., Vickers, M. H., Miles, J. L., and Breier, B. H. (2007). Prenatal and postnatal pathways to obesity: different underlying mechanisms, different metabolic outcomes. Endocrinology 148, 2345–2354.
Prenatal and postnatal pathways to obesity: different underlying mechanisms, different metabolic outcomes.Crossref | GoogleScholarGoogle Scholar | 17272392PubMed |

Titus, S., Li, F., Stobezki, R., Akula, K., Unsal, E., Jeong, K., Dickler, M., Robson, M., Moy, F., Goswami, S., and Oktay, K. (2013). Impairment of BRCA1-related DNA double-strand break repair leads to ovarian aging in mice and humans. Sci. Transl. Med. 5, 172ra21–172ra21.
Impairment of BRCA1-related DNA double-strand break repair leads to ovarian aging in mice and humans.Crossref | GoogleScholarGoogle Scholar | 23408054PubMed |

Tosh, D., Rani, H. S., Murty, U. S., Deenadayal, A., and Grover, P. (2015). Mutational analysis of the FIGLA gene in women with idiopathic premature ovarian failure. Menopause 22, 520–526.
Mutational analysis of the FIGLA gene in women with idiopathic premature ovarian failure.Crossref | GoogleScholarGoogle Scholar | 25314148PubMed |

Winship, A. L., Gazzard, S. E., McEwen, L. A. C., Bertram, J. F., and Hutt, K. J. (2018). Maternal low protein diet programmes low ovarian reserve in offspring. Reproduction 156, 299–311.
Maternal low protein diet programmes low ovarian reserve in offspring.Crossref | GoogleScholarGoogle Scholar | 30306601PubMed |

Yarde, F., Broekmans, F. J. M., Van der Pal-de Bruin, K. M., Schönbeck, Y., Te Velde, E. R., Stein, A. D., and Lumey, L. H. (2013). Prenatal famine, birthweight, reproductive performance and age at menopause: the Dutch hunger winter families study. Hum. Reprod. 28, 3328–3336.
Prenatal famine, birthweight, reproductive performance and age at menopause: the Dutch hunger winter families study.Crossref | GoogleScholarGoogle Scholar | 23966246PubMed |

Zhao, H., Chen, Z. J., Qin, Y., Shi, Y., Wang, S., Choi, Y., Simpson, J. L., and Rajkovic, A. (2008). Transcription factor FIGLA is mutated in patients with premature ovarian failure. Am. J. Hum. Genet. 82, 1342–1348.
Transcription factor FIGLA is mutated in patients with premature ovarian failure.Crossref | GoogleScholarGoogle Scholar | 18499083PubMed |