Skip to main content
SpringerLink
Log in

Advances in research into gamete and embryo-fetal origins of adult diseases

  • Review
  • From CAS & CAE Members
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

The fetal and infant origins of adult disease hypothesis proposed that the roots of adult chronic disease lie in the effects of adverse environments in fetal life and early infancy. In addition to the fetal period, fertilization and early embryonic stages, the critical time windows of epigenetic reprogramming, rapid cell differentiation and organogenesis, are the most sensitive stages to environmental disturbances. Compared with embryo and fetal development, gametogenesis and maturation take decades and are more vulnerable to potential damage for a longer exposure period. Therefore, we should shift the focus of adult disease occurrence and pathogenesis further back to gametogenesis and embryonic development events, which may result in intergenerational, even transgenerational, epigenetic re-programming with transmission of adverse traits and characteristics to offspring. Here, we focus on the research progress relating to diseases that originated from events in the gametes and early embryos and the potential epigenetic mechanisms involved.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bahous, R.H., Jadavji, N.M., Deng, L., Cosín-Tomás, M., Lu, J., Malysheva, O., Leung, K.Y., Ho, M.K., Pallàs, M., Kaliman, P., et al. (2017). High dietary folate in pregnant mice leads to pseudo-MTHFR deficiency and altered methyl metabolism, with embryonic growth delay and short-term memory impairment in offspring. Hum Mol Genet 26, 888–900.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barker, D.J., Osmond, C., and Law, C.M. (1989a). The intrauterine and early postnatal origins of cardiovascular disease and chronic bronchitis. J Epidemiol Commun Health 43, 237–240.

    Article  CAS  Google Scholar 

  • Barker, D.J.P., Osmond, C., Winter, P.D., Margetts, B., and Simmonds, S.J. (1989b). Weight in infancy and death from ischaemic heart disease. Lancet 334, 577–580.

    Article  Google Scholar 

  • Barker, D. J., ed. (1992). Fetal and Infant Origins of Adult Disease. London: BMJ Books.

    Google Scholar 

  • Canani, R.B., Di Costanzo, M., Leone, L., Bedogni, G., Brambilla, P., Cianfarani, S., Nobili, V., Pietrobelli, A., and Agostoni, C. (2011). Epigenetic mechanisms elicited by nutrition in early life. Nutr Res Rev 24, 198–205.

    Article  CAS  PubMed  Google Scholar 

  • Cardozo, E.R., Karmon, A.E., Gold, J., Petrozza, J.C., and Styer, A.K. (2015). Reproductive outcomes in oocyte donation cycles are associated with donor BMI. Hum Reprod 207, dev298.

    Article  Google Scholar 

  • Chen, H., Zhang, L., Deng, T., Zou, P., Wang, Y., Quan, F., and Zhang, Y. (2016). Effects of oocyte vitrification on epigenetic status in early bovine embryos. Theriogenology 86, 868–878.

    Article  CAS  PubMed  Google Scholar 

  • Chen, Q., Yan, M., Cao, Z., Li, X., Zhang, Y., Shi, J., Feng, G., Peng, H., Zhang, X., Zhang, Y., et al. (2016). Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science 351, 397–400.

    Article  CAS  PubMed  Google Scholar 

  • Ding, G.L., Wang, F.F., Shu, J., Tian, S., Jiang, Y., Zhang, D., Wang, N., Luo, Q., Zhang, Y., Jin, F., et al. (2012). Transgenerational glucose intolerance with Igf2/H19 epigenetic alterations in mouse islet induced by intrauterine hyperglycemia. Diabetes 61, 1133–1142.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du, Z., Zheng, H., Huang, B., Ma, R., Wu, J., Zhang, X., He, J., Xiang, Y., Wang, Q., Li, Y., et al. (2017). Allelic reprogramming of 3D chromatin architecture during early mammalian development. Nature 547, 232–235.

    Article  CAS  PubMed  Google Scholar 

  • Eckersley-Maslin, M.A., Alda-Catalinas, C., and Reik, W. (2018). Dynamics of the epigenetic landscape during the maternal-to-zygotic transition. Nat Rev Mol Cell Biol 19, 436–450.

    Article  CAS  PubMed  Google Scholar 

  • Eckert, J.J., Porter, R., Watkins, A.J., Burt, E., Brooks, S., Leese, H.J., Humpherson, P.G., Cameron, I.T., and Fleming, T.P. (2012). Metabolic induction and early responses of mouse blastocyst developmental programming following maternal low protein diet affecting life-long health. PLoS ONE 7, e52791.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fleming, T. P., Eckert, J. J. and Denisenko, O. (2017). The role of maternal nutrition during the periconceptional period and its effect on offspring phenotype. Adv Exp Med Biol 1014: 87–105.

    Article  CAS  PubMed  Google Scholar 

  • Fleming, T.P., Velazquez, M.A., Eckert, J.J., Lucas, E.S., and Watkins, A.J. (2012). Nutrition of females during the peri-conceptional period and effects on foetal programming and health of offspring. Anim Reprod Sci 130, 193–197.

    Article  CAS  PubMed  Google Scholar 

  • Flyamer, I.M., Gassler, J., Imakaev, M., Brandão, H.B., Ulianov, S.V., Abdennur, N., Razin, S.V., Mirny, L.A., and Tachibana-Konwalski, K. (2017). Single-nucleus Hi-C reveals unique chromatin reorganization at oocyte-to-zygote transition. Nature 544, 110–114.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao, L., Zhao, Y.C., Liang, Y., Lin, X.H., Tan, Y.J., Wu, D.D., Li, X.Z., Ye, B.Z., Kong, F.Q., Sheng, J.Z., et al. (2016). The impaired myocardial ischemic tolerance in adult offspring of diabetic pregnancy is restored by maternal melatonin treatment. J Pineal Res 61, 340–352.

    Article  CAS  PubMed  Google Scholar 

  • Gapp, K., Jawaid, A., Sarkies, P., Bohacek, J., Pelczar, P., Prados, J., Farinelli, L., Miska, E., and Mansuy, I.M. (2014). Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat Neurosci 17, 667–669.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ge, Z.J., Liang, X.W., Guo, L., Liang, Q.X., Luo, S.M., Wang, Y.P., Wei, Y. C., Han, Z.M., Schatten, H., and Sun, Q.Y. (2013). Maternal diabetes causes alterations of DNA methylation statuses of some imprinted genes in murine oocytes. Biol Reprod 88, 117.

    Article  PubMed  Google Scholar 

  • Gkountela, S., Zhang, K.X., Shafiq, T.A., Liao, W.W., Hargan-Calvopiña, J., Chen, P.Y., and Clark, A.T. (2015). DNA demethylation dynamics in the human prenatal germline. Cell 161, 1425–1436.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gluckman, P., and Harding, J. (1994). Nutritional and hormonal regulation of fetal growth—evolving concepts. Acta Paediatr 83, 60–63.

    Article  Google Scholar 

  • Gould, J.M., Smith, P.J., Airey, C.J., Mort, E.J., Airey, L.E., Warricker, F.D. M., Pearson-Farr, J.E., Weston, E.C., Gould, P.J.W., Semmence, O.G., et al. (2018). Mouse maternal protein restriction during preimplantation alone permanently alters brain neuron proportion and adult short-term memory. Proc Natl Acad Sci USA 115, E7398–E7407.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grandjean, V., Fourré, S., De Abreu, D.A.F., Derieppe, M.A., Remy, J.J., and Rassoulzadegan, M. (2015). RNA-mediated paternal heredity of diet-induced obesity and metabolic disorders. Sci Rep 5, 18193.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu, T.P., Guo, F., Yang, H., Wu, H.P., Xu, G.F., Liu, W., Xie, Z.G., Shi, L., He, X., Jin, S., et al. (2011). The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 477, 606–610.

    Article  CAS  PubMed  Google Scholar 

  • Guo, F., Yan, L., Guo, H., Li, L., Hu, B., Zhao, Y., Yong, J., Hu, Y., Wang, X., Wei, Y., et al. (2015). The transcriptome and DNA methylome landscapes of human primordial germ cells. Cell 161, 1437–1452.

    Article  CAS  PubMed  Google Scholar 

  • Han, L., Ren, C., Li, L., Li, X., Ge, J., Wang, H., Miao, Y.L., Guo, X., Moley, K.H., Shu, W., et al. (2018). Embryonic defects induced by maternal obesity in mice derive from Stella insufficiency in oocytes. Nat Genet 50, 432–442.

    Article  CAS  PubMed  Google Scholar 

  • Hanna, C.W., Demond, H., and Kelsey, G. (2018). Epigenetic regulation in development: is the mouse a good model for the human? Human Reprod Update 24, 556–576.

    Article  Google Scholar 

  • Hanson, M.A., and Gluckman, P.D. (2014). Early developmental conditioning of later health and disease: physiology or pathophysiology? Physiol Rev 94, 1027–1076.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hou, Y.J., Zhu, C.C., Duan, X., Liu, H.L., Wang, Q., and Sun, S.C. (2016). Both diet and gene mutation induced obesity affect oocyte quality in mice. Sci Rep 6, 18858.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu, X.L., Feng, C., Lin, X.H., Zhong, Z.X., Zhu, Y.M., Lv, P.P., Lv, M., Meng, Y., Zhang, D., Lu, X.E., et al. (2014). High maternal serum estradiol environment in the first trimester is associated with the increased risk of small-for-gestational-age birth. J Clin Endocrinol Metab 99, 2217–2224.

    Article  CAS  PubMed  Google Scholar 

  • Huypens, P., Sass, S., Wu, M., Dyckhoff, D., Tschöp, M., Theis, F., Marschall, S., Hrabe de Angelis, M., and Beckers, J. (2016). Epigenetic germline inheritance of diet-induced obesity and insulin resistance. Nat Genet 48, 497–499.

    Article  CAS  PubMed  Google Scholar 

  • Joubert, B.R., den Dekker, H.T., Felix, J.F., Bohlin, J., Ligthart, S., Beckett, E., Tiemeier, H., van Meurs, J.B., Uitterlinden, A.G., Hofman, A., et al. (2016). Maternal plasma folate impacts differential DNA methylation in an epigenome-wide meta-analysis of newborns. Nat Commun 7, 10577.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jungheim, E.S., Schoeller, E.L., Marquard, K.L., Louden, E.D., Schaffer, J. E., and Moley, K.H. (2010). Diet-induced obesity model: abnormal oocytes and persistent growth abnormalities in the offspring. Endocrinology 151, 4039–4046.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kanaka-gantenbein, C., Mastorakos, G., and Chrousos, G.P. (2003). Endocrine-related causes and consequences of intrauterine growth retardation. Ann New York Acad Sci 997, 150–157.

    Article  Google Scholar 

  • Ke, Y., Xu, Y., Chen, X., Feng, S., Liu, Z., Sun, Y., Yao, X., Li, F., Zhu, W., Gao, L., et al. (2017). 3D chromatin structures of mature gametes and structural reprogramming during mammalian embryogenesis. Cell 170, 367–381.e20.

    Article  CAS  PubMed  Google Scholar 

  • Krishnaveni, G.V., Veena, S.R., Karat, S.C., Yajnik, C.S., and Fall, C.H.D. (2014). Association between maternal folate concentrations during pregnancy and insulin resistance in Indian children. Diabetologia 57, 110–121.

    Article  CAS  PubMed  Google Scholar 

  • Kuhtz, J., Romero, S., De Vos, M., Smitz, J., Haaf, T., and Anckaert, E. (2014). Human in vitro oocyte maturation is not associated with increased imprinting error rates at LIT1, SNRPN, PEG3 and GTL2. Hum Reprod 29, 1995–2005.

    Article  CAS  PubMed  Google Scholar 

  • Li, W., Li, Z., Li, S., Wang, X., Wilson, J.X., and Huang, G. (2018). Periconceptional folic acid supplementation benefit to development of early sensory-motor function through increase DNA methylation in rat offspring. Nutrients 10, 292.

    Article  CAS  PubMed Central  Google Scholar 

  • Liu, X., Wang, C., Liu, W., Li, J., Li, C., Kou, X., Chen, J., Zhao, Y., Gao, H., Wang, H., et al. (2016). Distinct features of H3K4me3 and H3K27me3 chromatin domains in pre-implantation embryos. Nature 537, 558–562.

    Article  CAS  PubMed  Google Scholar 

  • Lv, P.P., Meng, Y., Lv, M., Feng, C., Liu, Y., Li, J.Y., Yu, D.Q., Shen, Y., Hu, X.L., Gao, Q., et al. (2014). Altered thyroid hormone profile in offspring after exposure to high estradiol environment during the first trimester of pregnancy: a cross-sectional study. BMC Med 12, 240.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lv, P.P., Tian, S., Feng, C., Li, J.Y., Yu, D.Q., Jin, L., Shen, Y., Yu, T.T., Meng, Y., Ding, G.L., et al. (2016). Maternal high estradiol exposure is associated with elevated thyroxine and Pax8 in mouse offspring. Sci Rep 6, 36805.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marshall, K.L., and Rivera, R.M. (2018). The effects of superovulation and reproductive aging on the epigenome of the oocyte and embryo. Mol Reprod Dev 85, 90–105.

    Article  CAS  PubMed  Google Scholar 

  • Meng, Y., Lv, P.P., Ding, G.L., Yu, T.T., Liu, Y., Shen, Y., Hu, X.L., Lin, X. H., Tian, S., Lv, M., et al. (2015). High maternal serum estradiol levels induce dyslipidemia in human newborns via a hepatic HMGCR estrogen response element. Sci Rep 5, 10086.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morgan, H.D., Sutherland, H.G.E., Martin, D.I.K., and Whitelaw, E. (1999). Epigenetic inheritance at the agouti locus in the mouse. Nat Genet 23, 314–318.

    Article  CAS  PubMed  Google Scholar 

  • Motrenko, T. (2010). Embryo-fetal origin of diseases–new approach on epigenetic reprogramming. Arch Perinat Med 6.

    Google Scholar 

  • Padmanabhan, N., Jia, D., Geary-Joo, C., Wu, X., Ferguson-Smith, A.C., Fung, E., Bieda, M.C., Snyder, F.F., Gravel, R.A., Cross, J.C., et al. (2013). Mutation in folate metabolism causes epigenetic instability and transgenerational effects on development. Cell 155, 81–93.

    Article  CAS  PubMed  Google Scholar 

  • Paneth, N., and Susser, M. (1995). Early origin of coronary heart disease (the “Barker hypothesis”). Br Med J 310, 411–412.

    Article  CAS  Google Scholar 

  • Pliushch, G., Schneider, E., Schneider, T., El Hajj, N., Rösner, S., Strowitzki, T., and Haaf, T. (2015). In vitro maturation of oocytes is not associated with altered deoxyribonucleic acid methylation patterns in children from in vitro fertilization or intracytoplasmic sperm injection. Fertil Steril 103, 720–727.e1.

    Article  PubMed  Google Scholar 

  • Radford, E.J., Ito, M., Shi, H., Corish, J.A., Yamazawa, K., Isganaitis, E., Seisenberger, S., Hore, T.A., Reik, W., Erkek, S., et al. (2014). In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science 345, 1255903.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rechavi, O., Houri-Ze’evi, L., Anava, S., Goh, W.S.S., Kerk, S.Y., Hannon, G.J., and Hobert, O. (2014). Starvation-induced transgenerational inheritance of small RNAs in C. elegans. Cell 158, 277–287.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren, J., Cheng, Y., Ming, Z.H., Dong, X.Y., Zhou, Y.Z., Ding, G.L., Pang, H.Y., Rahman, T.U., Akbar, R., Huang, H.F., et al. (2018). Intrauterine hyperglycemia exposure results in intergenerational inheritance via DNA methylation reprogramming on F1 PGCs. Epigenets Chromatin 11, 20.

    Article  CAS  Google Scholar 

  • Rodgers, A.B., Morgan, C.P., Leu, N.A., and Bale, T.L. (2015). Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc Natl Acad Sci USA 112, 13699–13704.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siklenka, K., Erkek, S., Godmann, M., Lambrot, R., McGraw, S., Lafleur, C., Cohen, T., Xia, J., Suderman, M., Hallett, M., et al. (2015). Disruption of histone methylation in developing sperm impairs offspring health transgenerationally. Science 350, aab2006.

    Article  CAS  PubMed  Google Scholar 

  • Skinner, M.K., Guerrero-Bosagna, C., and Haque, M.M. (2015). Environmentally induced epigenetic transgenerational inheritance of sperm epimutations promote genetic mutations. Epigenetics 10, 762–771.

    Article  PubMed  PubMed Central  Google Scholar 

  • Soubry, A. (2018). POHaD: why we should study future fathers. Environ Epigenets 4, dvy007.

    Google Scholar 

  • Stein, A.D., Pierik, F.H., Verrips, G.H.W., Susser, E.S., and Lumey, L.H. (2009). Maternal exposure to the Dutch famine before conception and during pregnancy. Epidemiology 20, 909–915.

    Article  PubMed  Google Scholar 

  • Tan, Y.J., Zhang, X.Y., Ding, G.L., Li, R., Wang, L., Jin, L., Lin, X.H., Gao, L., Sheng, J.Z., and Huang, H.F. (2015). Aquaporin7 plays a crucial role in tolerance to hyperosmotic stress and in the survival of oocytes during cryopreservation. Sci Rep 5, 17741.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian, S., Lin, X.H., Xiong, Y.M., Liu, M.E., Yu, T.T., Lv, M., Zhao, W., Xu, G.F., Ding, G.L., Xu, C.M., et al. (2017). Prevalence of prediabetes risk in offspring born to mothers with hyperandrogenism. EBioMedicine 16, 275–283.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tobi, E.W., Slieker, R.C., Stein, A.D., Suchiman, H.E.D., Slagboom, P.E., van Zwet, E.W., Heijmans, B.T., and Lumey, L.H. (2015). Early gestation as the critical time-window for changes in the prenatal environment to affect the adult human blood methylome. Int J Epidemiol 44, 1211–1223.

    Article  PubMed  PubMed Central  Google Scholar 

  • Veenendaal, M.V.E., Painter, R.C., de Rooij, S.R., Bossuyt, P.M.M., van der Post, J.A.M., Gluckman, P.D., Hanson, M.A., and Roseboom, T.J. (2013). Transgenerational effects of prenatal exposure to the 1944–45 Dutch famine. BJOG 120, 548–554.

    Article  CAS  PubMed  Google Scholar 

  • Vickers, M.H. (2014). Early life nutrition, epigenetics and programming of later life disease. Nutrients 6, 2165–2178.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, C., Liu, X., Gao, Y., Yang, L., Li, C., Liu, W., Chen, C., Kou, X., Zhao, Y., Chen, J., et al. (2018). Reprogramming of H3K9me3-dependent heterochromatin during mammalian embryo development. Nat Cell Biol 20, 620–631.

    Article  CAS  PubMed  Google Scholar 

  • Wang, H.H., Zhou, C.L., Lv, M., Yang, Q., Li, J.X., Hou, M., Lin, J., Liu, X.M., Wu, Y.T., Sheng, J.Z., et al. (2018). Prenatal high estradiol exposure induces sex-specific and dietarily reversible insulin resistance through decreased hypothalamic INSR. Endocrinology 159, 465–476.

    Article  PubMed  Google Scholar 

  • Wang, Q., Tang, S.B., Song, X.B., Deng, T.F., Zhang, T.T., Yin, S., Luo, S. M., Shen, W., Zhang, C.L., and Ge, Z.J. (2018). High-glucose concentrations change DNA methylation levels in human IVM oocytes. Human Reprod 33, 474–481.

    Article  CAS  Google Scholar 

  • Watkins, A.J., Lucas, E.S., Torrens, C., Cleal, J.K., Green, L., Osmond, C., Eckert, J.J., Gray, W.P., Hanson, M.A., and Fleming, T.P. (2010). Maternal low-protein diet during mouse pre-implantation development induces vascular dysfunction and altered renin-angiotensin-system homeostasis in the offspring. Br J Nutr 103, 1762–1770.

    Article  CAS  PubMed  Google Scholar 

  • Watkins, A.J., Ursell, E., Panton, R., Papenbrock, T., Hollis, L., Cunningham, C., Wilkins, A., Perry, V.H., Sheth, B., Kwong, W.Y., et al. (2008a). Adaptive responses by mouse early embryos to maternal diet protect fetal growth but predispose to adult onset disease1. Biol Reprod 78, 299–306.

    Article  CAS  PubMed  Google Scholar 

  • Watkins, A.J., Wilkins, A., Cunningham, C., Perry, V.H., Seet, M.J., Osmond, C., Eckert, J.J., Torrens, C., Cagampang, F.R.A., Cleal, J., et al. (2008b). Low protein diet fed exclusively during mouse oocyte maturation leads to behavioural and cardiovascular abnormalities in offspring. J Physiol 586, 2231–2244.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei, Y., Yang, C.R., Wei, Y.P., Zhao, Z.A., Hou, Y., Schatten, H., and Sun, Q.Y. (2014). Paternally induced transgenerational inheritance of susceptibility to diabetes in mammals. Proc Natl Acad Sci USA 111, 1873–1878.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, J., Huang, B., Chen, H., Yin, Q., Liu, Y., Xiang, Y., Zhang, B., Liu, B., Wang, Q., Xia, W., et al. (2016). The landscape of accessible chromatin in mammalian preimplantation embryos. Nature 534, 652–657.

    Article  CAS  PubMed  Google Scholar 

  • Wu, L.L., Russell, D.L., Wong, S.L., Chen, M., Tsai, T.S., St John, J.C., Norman, R.J., Febbraio, M.A., Carroll, J., and Robker, R.L. (2015). Mitochondrial dysfunction in oocytes of obese mothers: transmission to offspring and reversal by pharmacological endoplasmic reticulum stress inhibitors. Development 142, 681–691.

    Article  CAS  PubMed  Google Scholar 

  • Xu, G.F., Zhang, J.Y., Pan, H.T., Tian, S., Liu, M.E., Yu, T.T., Li, J.Y., Ying, W.W., Yao, W.M., Lin, X.H., et al. (2014). Cardiovascular dysfunction in offspring of ovarian-hyperstimulated women and effects of estradiol and progesterone: a retrospective cohort study and proteomics analysis. J Clin Endocrinol Metab 99, E2494–E2503.

    Article  CAS  PubMed  Google Scholar 

  • Xu, G.F., Zhou, C.L., Xiong, Y.M., Li, J.Y., Yu, T.T., Tian, S., Lin, X.H., Liao, Y., Lv, Y., Zhang, F.H., et al. (2017). Reduced intellectual ability in offspring of ovarian hyperstimulation syndrome: a cohort study. EBioMedicine 20, 263–267.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zamudio, N.M., Chong, S., and O’Bryan, M.K. (2008). Epigenetic regulation in male germ cells. Reproduction 136, 131–146.

    Article  CAS  PubMed  Google Scholar 

  • Zeltser, L.M. (2018). Feeding circuit development and early-life influences on future feeding behaviour. Nat Rev Neurosci 19, 302–316.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zenk, F., Loeser, E., Schiavo, R., Kilpert, F., Bogdanovic, O., and Iovino, N. (2017). Germ line-inherited H3K27me3 restricts enhancer function during maternal-to-zygotic transition. Science 357, 212–216.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, L., Han, L., Ma, R., Hou, X., Yu, Y., Sun, S., Xu, Y., Schedl, T., Moley, K.H., and Wang, Q. (2015). Sirt3 prevents maternal obesityassociated oxidative stress and meiotic defects in mouse oocytes. Cell Cycle 14, 2959–2968.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, Y., Zhang, X., Shi, J., Tuorto, F., Li, X., Liu, Y., Liebers, R., Zhang, L., Qu, Y., Qian, J., et al. (2018). Dnmt2 mediates intergenerational transmission of paternally acquired metabolic disorders through sperm small non-coding RNAs. Nat Cell Biol 20, 535–540.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu, P., Guo, H., Ren, Y., Hou, Y., Dong, J., Li, R., Lian, Y., Fan, X., Hu, B., Gao, Y., et al. (2018). Single-cell DNA methylome sequencing of human preimplantation embryos. Nat Genet 50, 12–19.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by Special Fund for the National Key Research and Development Plan (2017YFC1001303) and National Natural Science Foundation of China (81490742 and 31571556).

Author information

Author notes

  1. Contributed equally to this work

Authors and Affiliations

  1. The International Peace Maternity and Child Health Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200030, China

    Kexin Zou, Guolian Ding & Hefeng Huang

  2. Institute of Embryo-Fetal Original Adult Disease, School of Medicine, Shanghai Jiao Tong University, Shanghai, 200030, China

    Kexin Zou, Guolian Ding & Hefeng Huang

Authors
  1. Kexin Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guolian Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hefeng Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hefeng Huang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zou, K., Ding, G. & Huang, H. Advances in research into gamete and embryo-fetal origins of adult diseases. Sci. China Life Sci. 62, 360–368 (2019). https://doi.org/10.1007/s11427-018-9427-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-018-9427-4

Keywords

Search

Navigation