1932

Abstract

Drastic epigenetic reprogramming occurs during human gametogenesis and early embryo development. Advances in low-input and single-cell epigenetic techniques have provided powerful tools to dissect the genome-wide dynamics of different epigenetic molecular layers in these processes. In this review, we focus mainly on the most recent progress in understanding the dynamics of DNA methylation, chromatin accessibility, and histone modifications in human gametogenesis and early embryo development. Deficiencies in remodeling of the epigenomes can cause severe developmental defects, infertility, and long-term health issues in offspring. Aspects of the external environment, including assisted reproductive technology procedures, parental diets, and unhealthy parental habits, may disturb the epigenetic reprogramming processes and lead to an aberrant epigenome in the offspring. Here, we review the current knowledge of the potential risk factors of aberrant epigenomes in humans.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-genom-083118-015143
2019-08-31
2024-06-12
Loading full text...

Full text loading...

/deliver/fulltext/genom/20/1/annurev-genom-083118-015143.html?itemId=/content/journals/10.1146/annurev-genom-083118-015143&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Andreu-Vieyra CV, Chen RH, Agno JE, Glaser S, Anastassiadis K et al. 2010. MLL2 is required in oocytes for bulk histone 3 lysine 4 trimethylation and transcriptional silencing. PLOS Biol 8:e1000453
    [Google Scholar]
  2. 2.
    Barker D. 1997. Maternal nutrition, fetal nutrition, and disease in later life. Nutrition 13:807–13
    [Google Scholar]
  3. 3.
    Barlow DP, Bartolomei MS. 2014. Genomic imprinting in mammals. Cold Spring Harb. Perspect. Biol. 6:a018382
    [Google Scholar]
  4. 4.
    Biechele S, Lin CJ, Rinaudo PF, Ramalho-Santos M 2015. Unwind and transcribe: chromatin reprogramming in the early mammalian embryo. Curr. Opin. Genet. Dev. 34:17–23
    [Google Scholar]
  5. 5.
    Borengasser SJ, Zhong Y, Kang P, Lindsey F, Ronis MJ et al. 2013. Maternal obesity enhances white adipose tissue differentiation and alters genome-scale DNA methylation in male rat offspring. Endocrinology 154:4113–25
    [Google Scholar]
  6. 6.
    Bourc'his D, Bestor TH. 2004. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431:96–99
    [Google Scholar]
  7. 7.
    Bowdin S, Allen C, Kirby G, Brueton L, Afnan M et al. 2007. A survey of assisted reproductive technology births and imprinting disorders. Hum. Reprod. 22:3237–40
    [Google Scholar]
  8. 8.
    Burton A, Torres-Padilla ME. 2014. Chromatin dynamics in the regulation of cell fate allocation during early embryogenesis. Nat. Rev. Mol. Cell Biol. 15:723–34
    [Google Scholar]
  9. 9.
    Canovas S, Ivanova E, Romar R, García-Martínez S, Soriano-Úbeda C et al. 2017. DNA methylation and gene expression changes derived from assisted reproductive technologies can be decreased by reproductive fluids. eLife 6:e23670
    [Google Scholar]
  10. 10.
    Capra E, Turri F, Lazzari B, Cremonesi P, Gliozzi TM et al. 2017. Small RNA sequencing of cryopre-served semen from single bull revealed altered miRNAs and piRNAs expression between high- and low-motile sperm populations. BMC Genom 18:14
    [Google Scholar]
  11. 11.
    Carrell DT, Hammoud SS. 2010. The human sperm epigenome and its potential role in embryonic development. Mol. Hum. Reprod. 16:37–47
    [Google Scholar]
  12. 12.
    Catalano PM, Ehrenberg HM. 2006. The short- and long-term implications of maternal obesity on the mother and her offspring. BJOG 113:1126–33
    [Google Scholar]
  13. 13.
    Chen S, Sun FZ, Huang X, Wang X, Tang N et al. 2015. Assisted reproduction causes placental maldevelopment and dysfunction linked to reduced fetal weight in mice. Sci. Rep. 5:10596
    [Google Scholar]
  14. 14.
    Chen X, Huang Y, Huang H, Guan Y, Li M et al. 2018. Effects of superovulation, in vitro fertilization, and oocyte in vitro maturation on imprinted gene Grb10 in mouse blastocysts. Arch. Gynecol. Obstet. 98:1219–27
    [Google Scholar]
  15. 15.
    Chen Z, Hagen DE, Ji T, Elsik CG, Rivera RM 2017. Global misregulation of genes largely uncoupled to DNA methylome epimutations characterizes a congenital overgrowth syndrome. Sci. Rep. 7:12667
    [Google Scholar]
  16. 16.
    Clark SJ, Smallwood SA, Lee HJ, Krueger F, Reik W, Kelsey G 2017. Genome-wide base-resolution mapping of DNA methylation in single cells using single-cell bisulfite sequencing (scBS-seq). Nat. Protoc. 12:534–47
    [Google Scholar]
  17. 17.
    Clarke HJ, Vieux KF. 2015. Epigenetic inheritance through the female germ-line: the known, the unknown, and the possible. Semin. Cell Dev. Biol. 43:106–16
    [Google Scholar]
  18. 18.
    Dahl JA, Jung I, Aanes H, Greggains GD, Manaf A et al. 2016. Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition. Nature 537:548–52
    [Google Scholar]
  19. 19.
    Davies MJ, Moore VM, Willson KJ, Van Essen P, Priest K et al. 2012. Reproductive technologies and the risk of birth defects. N. Engl. J. Med. 366:1803–13
    [Google Scholar]
  20. 20.
    de Waal E, Vrooman LA, Fischer E, Ord T, Mainigi MA et al. 2015. The cumulative effect of assisted reproduction procedures on placental development and epigenetic perturbations in a mouse model. Hum. Mol. Genet. 24:6975–85
    [Google Scholar]
  21. 21.
    DeChiara TM, Robertson EJ, Efstratiadis A 1991. Parental imprinting of the mouse insulin-like growth factor II gene. Cell 64:849–59
    [Google Scholar]
  22. 22.
    Derakhshan-Horeh M, Abolhassani F, Jafarpour F, Moini A, Karbalaie K et al. 2016. Vitrification at Day3 stage appears not to affect the methylation status of H19/IGF2 differentially methylated region of in vitro produced human blastocysts. Cryobiology 73:168–74
    [Google Scholar]
  23. 23.
    Drake AJ, Reynolds RM. 2010. Impact of maternal obesity on offspring obesity and cardiometabolic disease risk. Reproduction 140:387–98
    [Google Scholar]
  24. 24.
    Dumesic DA, Goodarzi MO, Chazenbalk GD, Abbott DH 2014. Intrauterine environment and polycystic ovary syndrome. Semin. Reprod. Med. 32:159–65
    [Google Scholar]
  25. 25.
    Dunn GA, Bale TL. 2009. Maternal high-fat diet promotes body length increases and insulin insensitivity in second-generation mice. Endocrinology 150:4999–5009
    [Google Scholar]
  26. 26.
    Dunn GA, Bale TL. 2011. Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology 152:2228–36
    [Google Scholar]
  27. 27.
    Farhangniya M, Dortaj Rabori E, Mozafari Kermani R, Haghdoost AA, Bahrampour A et al. 2013. Comparison of congenital abnormalities of infants conceived by assisted reproductive techniques versus infants with natural conception in Tehran. Int. J. Fertil. Steril. 7:217–24
    [Google Scholar]
  28. 28.
    Farthing CR, Ficz G, Ng RK, Chan CF, Andrews S et al. 2008. Global mapping of DNA methylation in mouse promoters reveals epigenetic reprogramming of pluripotency genes. PLOS Genet 4:e1000116
    [Google Scholar]
  29. 29.
    Fernandez M, Zambrano MJ, Riquelme J, Castiglioni C, Kottler M-L et al. 2017. Pseudohypoparathyroidism type 1B associated with assisted reproductive technology. J. Pediatr. Endocrinol. Metab. 30:1125–32
    [Google Scholar]
  30. 30.
    Fortunato A, Leo R, Liguori F 2012. Effects of cryostorage on human sperm chromatin integrity. Zygote 21:330–36
    [Google Scholar]
  31. 31.
    Friedler S, Schachter M, Strassburger D, Esther K, Ron El R, Raziel A 2007. A randomized clinical trial comparing recombinant hyaluronan/recombinant albumin versus human tubal fluid for cleavage stage embryo transfer in patients with multiple IVF-embryo transfer failure. Hum. Reprod. 22:2444–48
    [Google Scholar]
  32. 32.
    Gan H, Wen L, Liao S, Lin X, Ma T et al. 2013. Dynamics of 5-hydroxymethylcytosine during mouse spermatogenesis. Nat. Commun. 4:1995
    [Google Scholar]
  33. 33.
    Gao L, Wu K, Liu Z, Yao X, Yuan S et al. 2018. Chromatin accessibility landscape in human early embryos and its association with evolution. Cell 173:248–59.e15
    [Google Scholar]
  34. 34.
    Gkountela S, Zhang KX, Shafiq TA, Liao WW, Hargan-Calvopina J et al. 2015. DNA demethylation dynamics in the human prenatal germline. Cell 161:1425–36
    [Google Scholar]
  35. 35.
    Goel NJ, Meyers LL, Frangos M 2018. Pseudohypoparathyroidism type 1B in a patient conceived by in vitro fertilization: another imprinting disorder reported with assisted reproductive technology. J. Assist. Reprod. Genet. 35:975–79
    [Google Scholar]
  36. 36.
    Guo F, Li L, Li J, Wu X, Hu B et al. 2017. Single-cell multi-omics sequencing of mouse early embryos and embryonic stem cells. Cell Res 27:967–88
    [Google Scholar]
  37. 37.
    Guo F, Yan L, Guo H, Li L, Hu B et al. 2015. The transcriptome and DNA methylome landscapes of human primordial germ cells. Cell 161:1437–52
    [Google Scholar]
  38. 38.
    Guo H, Hu B, Yan L, Yong J, Wu Y et al. 2017. DNA methylation and chromatin accessibility profiling of mouse and human fetal germ cells. Cell Res 27:165–83
    [Google Scholar]
  39. 39.
    Guo H, Zhu P, Yan L, Li R, Hu B et al. 2014. The DNA methylation landscape of human early embryos. Nature 511:606–10
    [Google Scholar]
  40. 40.
    Han JY, Park J, Jang W, Chae H, Kim M, Kim Y 2016. A twin sibling with Prader-Willi syndrome caused by type 2 microdeletion following assisted reproductive technology: a case report. Biomed. Rep. 5:18–22
    [Google Scholar]
  41. 41.
    Hanna CW, Demond H, Kelsey G 2018. Epigenetic regulation in development: Is the mouse a good model for the human. ? Hum. Reprod. Update 24:556–76
    [Google Scholar]
  42. 42.
    Hansen M, Kurinczuk JJ, Bower C, Webb S 2002. The risk of major birth defects after intracytoplasmic sperm injection and in vitro fertilization. N. Engl. J. Med. 346:725–30
    [Google Scholar]
  43. 43.
    Hargan-Calvopina J, Taylor S, Cook H, Hu Z, Lee SA et al. 2016. Stage-specific demethylation in primordial germ cells safeguards against precocious differentiation. Dev. Cell 39:75–86
    [Google Scholar]
  44. 44.
    Heerwagen MJ, Miller MR, Barbour LA, Friedman JE 2010. Maternal obesity and fetal metabolic programming: a fertile epigenetic soil. Am. J. Physiol. Regulat. Integr. Comp. Physiol. 299:R711–22
    [Google Scholar]
  45. 45.
    Heisey AS, Bell EM, Herdt-Losavio ML, Druschel C 2015. Surveillance of congenital malformations in infants conceived through assisted reproductive technology or other fertility treatments. Birth Defects Res. A 103:119–26
    [Google Scholar]
  46. 46.
    Hewitson L, Takahashi D, Dominko T, Simerly C, Schatten G 1998. Fertilization and embryo development to blastocysts after intracytoplasmic sperm injection in the rhesus monkey. Hum. Reprod. 13:3449–55
    [Google Scholar]
  47. 47.
    Hiura H, Okae H, Chiba H, Miyauchi N, Sato F et al. 2014. Imprinting methylation errors in ART. Reprod. Med. Biol. 13:193–202
    [Google Scholar]
  48. 48.
    Inoue A, Jiang L, Lu FL, Suzuki T, Zhang Y 2017. Maternal H3K27me3 controls DNA methylation-independent imprinting. Nature 547:419–24
    [Google Scholar]
  49. 49.
    Jackson RA, Gibson KA, Wu YW, Croughan MS 2004. Perinatal outcomes in singletons following in vitro fertilization: a meta-analysis. Obstet. Gynecol. 103:551–63
    [Google Scholar]
  50. 50.
    Jeyaseelan K, Bansal SK, Gupta N, Sankhwar SN, Rajender S 2015. Differential genes expression between fertile and infertile spermatozoa revealed by transcriptome analysis. PLOS ONE 10:e0127007
    [Google Scholar]
  51. 51.
    Ji M, Wang X, Wu W, Guan Y, Liu J et al. 2018. ART manipulation after controlled ovarian stimulation may not increase the risk of abnormal expression and DNA methylation at some CpG sites of H19,IGF2 and SNRPN in foetuses: a pilot study. Reprod. Biol. Endocrinol. 16:63
    [Google Scholar]
  52. 52.
    Joubert BR, Haberg SE, Nilsen RM, Wang X, Vollset SE et al. 2012. 450K epigenome-wide scan identifies differential DNA methylation in newborns related to maternal smoking during pregnancy. Environ. Health Perspect. 120:1425–31
    [Google Scholar]
  53. 53.
    Kagiwada S, Kurimoto K, Hirota T, Yamaji M, Saitou M 2013. Replication-coupled passive DNA demethylation for the erasure of genome imprints in mice. EMBO J 32:340–53
    [Google Scholar]
  54. 54.
    Kaminen-Ahola N, Ahola A, Maga M, Mallitt KA, Fahey P et al. 2010. Maternal ethanol consumption alters the epigenotype and the phenotype of offspring in a mouse model. PLOS Genet 6:e1000811
    [Google Scholar]
  55. 55.
    Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N et al. 2004. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429:900–3
    [Google Scholar]
  56. 56.
    Kato Y, Kaneda M, Hata K, Kumaki K, Hisano M et al. 2007. Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse. Hum. Mol. Genet. 16:2272–80
    [Google Scholar]
  57. 57.
    Kelly TK, Liu Y, Lay FD, Liang G, Berman BP, Jones PA 2012. Genome-wide mapping of nucleosome positioning and DNA methylation within individual DNA molecules. Genome Res 22:2497–506
    [Google Scholar]
  58. 58.
    Kitamura E, Igarashi J, Morohashi A, Hida N, Oinuma T et al. 2007. Analysis of tissue-specific differentially methylated regions (TDMs) in humans. Genomics 89:326–37
    [Google Scholar]
  59. 59.
    Knezovich JG, Ramsay M. 2012. The effect of preconception paternal alcohol exposure on epigenetic remodeling of the H19 and Rasgrf1 imprinting control regions in mouse offspring. Front. Genet. 3:10
    [Google Scholar]
  60. 60.
    Krausz C, Guarducci E, Becherini L, Degl'Innocenti S, Gerace L et al. 2011. The clinical significance of the POLG gene polymorphism in male infertility. J. Clin. Endocrinol. Metab. 89:4292–97
    [Google Scholar]
  61. 61.
    Leitch HG, Tang WW, Surani MA 2013. Primordial germ-cell development and epigenetic reprogramming in mammals. Curr. Top. Dev. Biol. 104:149–87
    [Google Scholar]
  62. 62.
    Li E, Beard C, Jaenisch R 1993. Role for DNA methylation in genomic imprinting. Nature 366:362–65
    [Google Scholar]
  63. 63.
    Li L, Guo F, Gao Y, Ren YX, Yuan P et al. 2018. Single-cell multi-omics sequencing of human early embryos. Nat. Cell Biol. 20:847–58
    [Google Scholar]
  64. 64.
    Li L, Wang L, Le F, Liu X, Yu P et al. 2011. Evaluation of DNA methylation status at differentially methylated regions in IVF-conceived newborn twins. Fertil. Steril. 95:1975–79
    [Google Scholar]
  65. 65.
    Lin Z, Hsu PJ, Xing X, Fang J, Lu Z et al. 2017. Mettl3-/Mettl14-mediated mRNA N6-methyladenosine modulates murine spermatogenesis. Cell Res 27:1216–30
    [Google Scholar]
  66. 66.
    Litzky JF, Deyssenroth MA, Everson TM, Lester BM, Lambertini L et al. 2018. Prenatal exposure to maternal depression and anxiety on imprinted gene expression in placenta and infant neurodevelopment and growth. Pediatr. Res. 83:1075–83
    [Google Scholar]
  67. 67.
    Liu X, Wang C, Liu W, Li J, Li C et al. 2016. Distinct features of H3K4me3 and H3K27me3 chromatin domains in pre-implantation embryos. Nature 537:558–62
    [Google Scholar]
  68. 68.
    Liu Y, Tang Y, Ye D, Ma W, Feng S et al. 2017. Impact of abnormal DNA methylation of imprinted loci on human spontaneous abortion. Reprod. Sci. 25:131–39
    [Google Scholar]
  69. 69.
    Ma P, Pan H, Montgomery RL, Olson EN, Schultz RM 2012. Compensatory functions of histone deacetylase 1 (HDAC1) and HDAC2 regulate transcription and apoptosis during mouse oocyte development. PNAS 109:E481–89
    [Google Scholar]
  70. 70.
    MacLean JA II, Wilkinson MF 2005. Gene regulation in spermatogenesis. Curr. Top. Dev. Biol. 71:131–97
    [Google Scholar]
  71. 71.
    Milagro FI, Mansego ML, De Miguel C, Martinez JA 2013. Dietary factors, epigenetic modifications and obesity outcomes: progresses and perspectives. Mol. Aspects Med. 34:782–812
    [Google Scholar]
  72. 72.
    Niakan KK, Han J, Pedersen RA, Simon C, Pera RA 2012. Human pre-implantation embryo development. Development 139:829–41
    [Google Scholar]
  73. 73.
    Oakes CC, La Salle S, Smiraglia DJ, Robaire B, Trasler JM 2007. Developmental acquisition of genome-wide DNA methylation occurs prior to meiosis in male germ cells. Dev. Biol. 307:368–79
    [Google Scholar]
  74. 74.
    Oakes CC, La Salle S, Smiraglia DJ, Robaire B, Trasler JM 2007. A unique configuration of genome-wide DNA methylation patterns in the testis. PNAS 104:228–33
    [Google Scholar]
  75. 75.
    Okano M, Bell DW, Haber DA, Li E 1999. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247–57
    [Google Scholar]
  76. 76.
    Panning B, Jaenisch R. 1996. DNA hypomethylation can activate Xist expression and silence X-linked genes. Genes Dev 10:1991–2002
    [Google Scholar]
  77. 77.
    Peters J. 2014. The role of genomic imprinting in biology and disease: an expanding view. Nat. Rev. Genet. 15:517–30
    [Google Scholar]
  78. 78.
    Rathke C, Baarends WM, Awe S, Renkawitz-Pohl R 2014. Chromatin dynamics during spermiogenesis. Biochim. Biophys. Acta 1839:155–68
    [Google Scholar]
  79. 79.
    Schieve LA, Meikle SF, Ferre C, Peterson HB, Jeng G, Wilcox LS 2002. Low and very low birth weight in infants conceived with use of assisted reproductive technology. N. Engl. J. Med. 346:731–37
    [Google Scholar]
  80. 80.
    Schuster A, Tang C, Xie Y, Ortogero N, Yuan S, Yan W 2016. SpermBase: a database for sperm-borne RNA contents. Biol. Reprod. 95:99
    [Google Scholar]
  81. 81.
    Seisenberger S, Andrews S, Krueger F, Arand J, Walter J et al. 2012. The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol. Cell 48:849–62
    [Google Scholar]
  82. 82.
    Seki Y, Hayashi K, Itoh K, Mizugaki M, Saitou M, Matsui Y 2005. Extensive and orderly reprogramming of genome-wide chromatin modifications associated with specification and early development of germ cells in mice. Dev. Biol. 278:440–58
    [Google Scholar]
  83. 83.
    Sharma U, Rando OJ. 2017. Metabolic inputs into the epigenome. Cell Metab 25:544–58
    [Google Scholar]
  84. 84.
    Shirane K, Toh H, Kobayashi H, Miura F, Chiba H, Ito T et al. 2013. Mouse oocyte methylomes at base resolution reveal genome-wide accumulation of non-CpG methylation and role of DNA methyltransferases. PLOS Genet 9:e1003439
    [Google Scholar]
  85. 85.
    Smith ZD, Chan MM, Humm KC, Karnik R, Mekhoubad S et al. 2014. DNA methylation dynamics of the human preimplantation embryo. Nature 511:611–15
    [Google Scholar]
  86. 86.
    Soellner L, Begemann M, Mackay DJ, Gronskov K, Tumer Z et al. 2017. Recent advances in imprinting disorders. Clin. Genet. 91:3–13
    [Google Scholar]
  87. 87.
    Soubry A. 2015. Epigenetic inheritance and evolution: a paternal perspective on dietary influences. Prog. Biophys. Mol. Biol. 118:79–85
    [Google Scholar]
  88. 88.
    Taberlay PC, Statham AL, Kelly TK, Clark SJ, Jones PA 2014. Reconfiguration of nucleosome-depleted regions at distal regulatory elements accompanies DNA methylation of enhancers and insulators in cancer. Genome Res 24:1421–32
    [Google Scholar]
  89. 89.
    Tang L, Liu Z, Zhang R, Su C, Yang W et al. 2017. Imprinting alterations in sperm may not significantly influence ART outcomes and imprinting patterns in the cord blood of offspring. PLOS ONE 12:e0187869
    [Google Scholar]
  90. 90.
    Tang WW, Dietmann S, Irie N, Leitch HG, Floros VI et al. 2015. A unique gene regulatory network resets the human germline epigenome for development. Cell 161:1453–67
    [Google Scholar]
  91. 91.
    Tang WW, Kobayashi T, Irie N, Dietmann S, Surani MA 2016. Specification and epigenetic programming of the human germ line. Nat. Rev. Genet. 17:585–600
    [Google Scholar]
  92. 92.
    Ventura-Juncá P, Irarrázaval I, Rolle AJ, Gutiérrez JI, Moreno RD, Santos MJ 2015. In vitro fertilization (IVF) in mammals: epigenetic and developmental alterations. Scientific and bioethical implications for IVF in humans. Biol. Res. 48:68
    [Google Scholar]
  93. 93.
    Vincent RN, Gooding LD, Louie K, Chan Wong E, Ma S 2016. Altered DNA methylation and expression of PLAGL1 in cord blood from assisted reproductive technology pregnancies compared with natural conceptions. Fertil. Steril. 106:739–48.e3
    [Google Scholar]
  94. 94.
    Vink JM, Sadrzadeh S, Lambalk CB, Boomsma DI 2006. Heritability of polycystic ovary syndrome in a Dutch twin-family study. J. Clin. Endocrinol. Metab. 91:2100–4
    [Google Scholar]
  95. 95.
    von Meyenn F, Reik W 2015. Forget the parents: epigenetic reprogramming in human germ cells. Cell 161:1248–51
    [Google Scholar]
  96. 96.
    Wadhwa PD, Buss C, Entringer S, Swanson JM 2009. Developmental origins of health and disease: brief history of the approach and current focus on epigenetic mechanisms. Semin. Reprod. Med. 27:358–68
    [Google Scholar]
  97. 97.
    Walsh CP, Chaillet JR, Bestor TH 1998. Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat. Genet. 20:116–17
    [Google Scholar]
  98. 98.
    Wang CF, Liu XY, Gao YW, Yang L, Li C et al. 2018. Reprogramming of H3K9me3-dependent heterochromatin during mammalian embryo development. Nat. Cell Biol. 20:620–31
    [Google Scholar]
  99. 99.
    Webster KE, O'Bryan MK, Fletcher S, Crewther PE, Aapola U et al. 2005. Meiotic and epigenetic defects in Dnmt3L-knockout mouse spermatogenesis. PNAS 102:4068–73
    [Google Scholar]
  100. 100.
    Wei Y, Yang CR, Wei YP, Zhao ZA, Hou Y et al. 2014. Paternally induced transgenerational inheritance of susceptibility to diabetes in mammals. PNAS 111:1873–78
    [Google Scholar]
  101. 101.
    White CR, Denomme MM, Tekpetey FR, Feyles V, Power SG, Mann MR 2015. High frequency of imprinted methylation errors in human preimplantation embryos. Sci. Rep. 5:17311
    [Google Scholar]
  102. 102.
    Wu J, Huang B, Chen H, Yin Q, Liu Y et al. 2016. The landscape of accessible chromatin in mammalian preimplantation embryos. Nature 534:652–57
    [Google Scholar]
  103. 103.
    Wu J, Xu J, Liu B, Yao G, Wang P et al. 2018. Chromatin analysis in human early development reveals epigenetic transition during ZGA. Nature 557:256–60
    [Google Scholar]
  104. 104.
    Xu GL, Bestor TH, Bourc'his D, Hsieh CL, Tommerup N et al. 1999. Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 402:187–91
    [Google Scholar]
  105. 105.
    Xu Q, Xie W. 2018. Epigenome in early mammalian development: inheritance, reprogramming and establishment. Trends Cell Biol 28:237–53
    [Google Scholar]
  106. 106.
    Xue Z, Huang K, Cai C, Cai L, Jiang CY et al. 2013. Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. Nature 500:593–97
    [Google Scholar]
  107. 107.
    Yamagata K, Yamazaki T, Miki H, Ogonuki N, Inoue K et al. 2007. Centromeric DNA hypomethylation as an epigenetic signature discriminates between germ and somatic cell lineages. Dev. Biol. 312:419–26
    [Google Scholar]
  108. 108.
    Yan L, Yang M, Guo H, Yang L, Wu J et al. 2013. Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat. Struct. Mol. Biol. 20:1131–39
    [Google Scholar]
  109. 109.
    Yu B, Dong X, Gravina S, Kartal O, Schimmel T et al. 2017. Genome-wide, single-cell DNA methylomics reveals increased non-CpG methylation during human oocyte maturation. Stem Cell Rep 9:397–407
    [Google Scholar]
  110. 110.
    Zambrano E, Martinez-Samayoa PM, Bautista CJ, Deas M, Guillen L et al. 2005. Sex differences in transgenerational alterations of growth and metabolism in progeny (F2) of female offspring (F1) of rats fed a low protein diet during pregnancy and lactation. J. Physiol. 566:225–36
    [Google Scholar]
  111. 111.
    Zhang B, Zheng H, Huang B, Li W, Xiang Y et al. 2016. Allelic reprogramming of the histone modification H3K4me3 in early mammalian development. Nature 537:553–57
    [Google Scholar]
  112. 112.
    Zhang X, San Gabriel M, Zini A 2006. Sperm nuclear histone to protamine ratio in fertile and infertile men: evidence of heterogeneous subpopulations of spermatozoa in the ejaculate. J. Androl. 27:414–20
    [Google Scholar]
  113. 113.
    Zheng H, Huang B, Zhang B, Xiang Y, Du Z et al. 2016. Resetting epigenetic memory by reprogramming of histone modifications in mammals. Mol. Cell 63:1066–79
    [Google Scholar]
  114. 114.
    Zhu P, Guo HS, Ren YX, Hou Y, Dong J et al. 2018. Single-cell DNA methylome sequencing of human preimplantation embryos. Nat. Genet. 50:12–19
    [Google Scholar]
/content/journals/10.1146/annurev-genom-083118-015143
Loading
/content/journals/10.1146/annurev-genom-083118-015143
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error