Advertisement

Chromosoma

pp 1–19 | Cite as

Epigenetic changes in mammalian gametes throughout their lifetime: the four seasons metaphor

  • Peera Wasserzug-Pash
  • Michael KlutsteinEmail author
Original Article

Abstract

The ability to reproduce is a major trait of living organisms. This ability is carried out by specialized reproductive cells—gametes. In mammals, gametes develop through a unique developmental pathway. Extensive changes in the epigenome of gametes occur during embryonic development. With birth, gametes continue to mature and develop until puberty. This growth process is accompanied by further epigenetic changes. When gametes mature, they reside within specialized organs—the gonads—and are exposed to both internal and external signals. The gametes’ epigenome reacts to these signals, and epigenetic changes which occur can alter gene expression and the ability of the cells to go through the cell cycle. The epigenome also ages and may be one of the key players in gamete aging, which, at least for females, occurs relatively early in life. The journey gametes undertake throughout the life of the organism is thus full of epigenetic changes. In this review, we depict these changes and the mechanisms involved in them. We focus on four stages of gamete development: gametes in embryonic development, during puberty and until sexual maturity, in adulthood, and during the process of aging. In each stage, we focus on one aspect of epigenetic changes and discuss it in more detail. These four stages include many different molecular players, lots of enzymatic activity, and abrupt changes. By this, these stages resemble the four seasons of the year. Thus, we describe epigenetic changes in gametes as changes throughout four seasons of life.

Keywords

Gametes Epigenetics Aging Embryonic development Environmental influence Puberty Spermatogenesis Spermiogenesis Oogenesis Genital ridge DNA methylation Histones 

Notes

Acknowledgments

The authors would like to thank Dr. N Mayorek for the critical reading of our manuscript. We would like to apologize to many colleagues who, due to a lack of space, their work could not be cited.

References

  1. Adenot PG, Mercier Y, Renard JP, Thompson EM (1997) Differential H4 acetylation of paternal and maternal chromatin precedes DNA replication and differential transcriptional activity in pronuclei of 1-cell mouse embryos. Development 124:4615–4625PubMedGoogle Scholar
  2. Agarwal DK, Lawrence WH, Autian J (1985) Antifertility and mutagenic effects in mice from parenteral administration of di-2-ethylhexyl phthalate (DEHP). J Toxicol Environ Health 16:71–84.  https://doi.org/10.1080/15287398509530720 CrossRefPubMedGoogle Scholar
  3. Anas MK, Suzuki C, Yoshioka K, Iwamura S (2003) Effect of mono-(2-ethylhexyl) phthalate on bovine oocyte maturation in vitro. Reprod Toxicol 17:305–310CrossRefPubMedGoogle Scholar
  4. Aoki VW, Liu L, Carrell DT (2005) Identification and evaluation of a novel sperm protamine abnormality in a population of infertile males. Hum Reprod 20:1298–1306.  https://doi.org/10.1093/humrep/deh798 CrossRefPubMedGoogle Scholar
  5. Armstrong S, Akande V (2013) What is the best treatment option for infertile women aged 40 and over? J Assist Reprod Genet 30:667–671.  https://doi.org/10.1007/s10815-013-9980-6 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Arnaud P, Hata K, Kaneda M, Li E, Sasaki H, Feil R, Kelsey G (2006) Stochastic imprinting in the progeny of Dnmt3L-/- females. Hum Mol Genet 15:589–598.  https://doi.org/10.1093/hmg/ddi475 CrossRefPubMedGoogle Scholar
  7. Bar Oz M, Kumar A, Elayyan J, Reich E, Binyamin M, Kandel L, Liebergall M, Steinmeyer J, Lefebvre V, Dvir-Ginzberg M (2016) Acetylation reduces SOX9 nuclear entry and ACAN gene transactivation in human chondrocytes. Aging Cell 15:499–508.  https://doi.org/10.1111/acel.12456 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Becker M, Becker A, Miyara F, Han Z, Kihara M, Brown DT, Hager GL, Latham K, Adashi EY, Misteli T (2005) Differential in vivo binding dynamics of somatic and oocyte-specific linker histones in oocytes and during ES cell nuclear transfer. Mol Biol Cell 16:3887–3895.  https://doi.org/10.1091/mbc.e05-04-0350 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bell EL, Nagamori I, Williams EO, del Rosario AM, Bryson BD, Watson N, White FM, Sassone-Corsi P, Guarente L (2014) SirT1 is required in the male germ cell for differentiation and fecundity in mice. Development 141:3495–3504.  https://doi.org/10.1242/dev.110627 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bonnet-Garnier A, Feuerstein P, Chebrout M, Fleurot R, Jan HU, Debey P, Beaujean N (2012) Genome organization and epigenetic marks in mouse germinal vesicle oocytes. Int J Dev Biol 56:877–887.  https://doi.org/10.1387/ijdb.120149ab CrossRefPubMedGoogle Scholar
  11. Borgel J, Guibert S, Li Y, Chiba H, Schübeler D, Sasaki H, Forné T, Weber M (2010) Targets and dynamics of promoter DNA methylation during early mouse development. Nat Genet 42:1093–1100.  https://doi.org/10.1038/ng.708 CrossRefPubMedGoogle Scholar
  12. Bourc’his D, Xu GL, Lin CS, Bollman B, Bestor TH (2001) Dnmt3L and the establishment of maternal genomic imprints. Science 294:2536–2539.  https://doi.org/10.1126/science.1065848 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Brons IG et al (2007) Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448:191–195.  https://doi.org/10.1038/nature05950 CrossRefPubMedGoogle Scholar
  14. Brunner AM, Nanni P, Mansuy IM (2014) Epigenetic marking of sperm by post-translational modification of histones and protamines. Epigenetics Chromatin 7:2.  https://doi.org/10.1186/1756-8935-7-2 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Bui HT, van Thuan N, Kishigami S, Wakayama S, Hikichi T, Ohta H, Mizutani E, Yamaoka E, Wakayama T, Miyano T (2007) Regulation of chromatin and chromosome morphology by histone H3 modifications in pig oocytes. Reproduction 133:371–382.  https://doi.org/10.1530/REP-06-0099 CrossRefPubMedGoogle Scholar
  16. Bullejos M, Koopman P (2005) Delayed Sry and Sox9 expression in developing mouse gonads underlies B6-Y(DOM) sex reversal. Dev Biol 278:473–481.  https://doi.org/10.1016/j.ydbio.2004.11.030 CrossRefPubMedGoogle Scholar
  17. Burkhardt S, Borsos M, Szydlowska A, Godwin J, Williams SA, Cohen PE, Hirota T, Saitou M, Tachibana-Konwalski K (2016) Chromosome cohesion established by Rec8-cohesin in fetal oocytes is maintained without detectable turnover in oocytes arrested for months in mice. Curr Biol 26:678–685.  https://doi.org/10.1016/j.cub.2015.12.073 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Cantu AV, Laird DJ (2017) A pilgrim’s progress: seeking meaning in primordial germ cell migration. Stem Cell Res 24:181–187.  https://doi.org/10.1016/j.scr.2017.07.017 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Capalbo A, Hoffmann ER, Cimadomo D, Ubaldi FM, Rienzi L (2017) Human female meiosis revised: new insights into the mechanisms of chromosome segregation and aneuploidies from advanced genomics and time-lapse imaging. Hum Reprod Update 23:706–722.  https://doi.org/10.1093/humupd/dmx026 CrossRefPubMedGoogle Scholar
  20. Cheng JM, Liu YX (2017) Age-related loss of cohesion: causes and effects. Int J Mol Sci 18.  https://doi.org/10.3390/ijms18071578
  21. Ciccarone F, Tagliatesta S, Caiafa P, Zampieri M (2018) DNA methylation dynamics in aging: how far are we from understanding the mechanisms? Mech Ageing Dev 174:3–17.  https://doi.org/10.1016/j.mad.2017.12.002 CrossRefPubMedGoogle Scholar
  22. Crain DA, Janssen SJ, Edwards TM, Heindel J, Ho SM, Hunt P, Iguchi T, Juul A, McLachlan JA, Schwartz J, Skakkebaek N, Soto AM, Swan S, Walker C, Woodruff TK, Woodruff TJ, Giudice LC, Guillette LJ Jr (2008) Female reproductive disorders: the roles of endocrine-disrupting compounds and developmental timing. Fertil Steril 90:911–940.  https://doi.org/10.1016/j.fertnstert.2008.08.067 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Crawford NM, Steiner AZ (2015) Age-related infertility. Obstet Gynecol Clin N Am 42:15–25.  https://doi.org/10.1016/j.ogc.2014.09.005 CrossRefGoogle Scholar
  24. Dada R, Kumar M, Jesudasan R, Fernandez JL, Gosalvez J, Agarwal A (2012) Epigenetics and its role in male infertility. J Assist Reprod Genet 29:213–223.  https://doi.org/10.1007/s10815-012-9715-0 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Dahl JA, Jung I, Aanes H, Greggains GD, Manaf A, Lerdrup M, Li G, Kuan S, Li B, Lee AY, Preissl S, Jermstad I, Haugen MH, Suganthan R, Bjørås M, Hansen K, Dalen KT, Fedorcsak P, Ren B, Klungland A (2016) Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition. Nature 537:548–552.  https://doi.org/10.1038/nature19360 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Das N, Kumar TR (2018) Molecular regulation of follicle-stimulating hormone synthesis, secretion and action. J Mol Endocrinol 60:R131–R155.  https://doi.org/10.1530/JME-17-0308 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Davis BJ, Maronpot RR, Heindel JJ (1994) Di-(2-ethylhexyl) phthalate suppresses estradiol and ovulation in cycling rats. Toxicol Appl Pharmacol 128:216–223.  https://doi.org/10.1006/taap.1994.1200 CrossRefPubMedGoogle Scholar
  28. Dawlaty MM, Ganz K, Powell BE, Hu YC, Markoulaki S, Cheng AW, Gao Q, Kim J, Choi SW, Page DC, Jaenisch R (2011) Tet1 is dispensable for maintaining pluripotency and its loss is compatible with embryonic and postnatal development. Cell Stem Cell 9:166–175.  https://doi.org/10.1016/j.stem.2011.07.010 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Dawlaty MM, Breiling A, le T, Raddatz G, Barrasa MI, Cheng AW, Gao Q, Powell BE, Li Z, Xu M, Faull KF, Lyko F, Jaenisch R (2013) Combined deficiency of Tet1 and Tet2 causes epigenetic abnormalities but is compatible with postnatal development. Dev Cell 24:310–323.  https://doi.org/10.1016/j.devcel.2012.12.015 CrossRefPubMedPubMedCentralGoogle Scholar
  30. de la Rochebrochard E, Thonneau P (2002) Paternal age and maternal age are risk factors for miscarriage; results of a multicentre European study. Hum Reprod 17:1649–1656CrossRefPubMedGoogle Scholar
  31. Denomme MM, White CR, Gillio-Meina C, Macdonald WA, Deroo BJ, Kidder GM, Mann MR (2012) Compromised fertility disrupts Peg1 but not Snrpn and Peg3 imprinted methylation acquisition in mouse oocytes. Front Genet 3:129.  https://doi.org/10.3389/fgene.2012.00129 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Dor Y, Cedar H (2018) Principles of DNA methylation and their implications for biology and medicine. Lancet 392:777–786.  https://doi.org/10.1016/S0140-6736(18)31268-6 CrossRefPubMedGoogle Scholar
  33. Dovey OM, Foster CT, Cowley SM (2010) Histone deacetylase 1 (HDAC1), but not HDAC2, controls embryonic stem cell differentiation. Proc Natl Acad Sci U S A 107:8242–8247.  https://doi.org/10.1073/pnas.1000478107 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Eguizabal C, Herrera L, De Onate L, Montserrat N, Hajkova P, Izpisua Belmonte JC (2016) Characterization of the epigenetic changes during human gonadal primordial germ cells reprogramming. Stem Cells 34:2418–2428.  https://doi.org/10.1002/stem.2422 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Feng CW, Bowles J, Koopman P (2014) Control of mammalian germ cell entry into meiosis. Mol Cell Endocrinol 382:488–497.  https://doi.org/10.1016/j.mce.2013.09.026 CrossRefPubMedGoogle Scholar
  36. Ford WC, North K, Taylor H, Farrow A, Hull MG, Golding J (2000) Increasing paternal age is associated with delayed conception in a large population of fertile couples: evidence for declining fecundity in older men. The ALSPAC Study Team (Avon Longitudinal Study of Pregnancy and Childhood). Hum Reprod 15:1703–1708CrossRefPubMedGoogle Scholar
  37. Frans EM, Sandin S, Reichenberg A, Langstrom N, Lichtenstein P, McGrath JJ, Hultman CM (2013) Autism risk across generations: a population-based study of advancing grandpaternal and paternal age. JAMA Psychiatry 70:516–521.  https://doi.org/10.1001/jamapsychiatry.2013.1180 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Frattarelli JL, Miller KA, Miller BT, Elkind-Hirsch K, Scott RT Jr (2008) Male age negatively impacts embryo development and reproductive outcome in donor oocyte assisted reproductive technology cycles. Fertil Steril 90:97–103.  https://doi.org/10.1016/j.fertnstert.2007.06.009 CrossRefPubMedGoogle Scholar
  39. Funaya S, Ooga M, Suzuki MG, Aoki F (2018) Linker histone H1FOO regulates the chromatin structure in mouse zygotes. FEBS Lett 592:2414–2424.  https://doi.org/10.1002/1873-3468.13175 CrossRefPubMedGoogle Scholar
  40. Gasca S, Canizares J, De Santa Barbara P, Mejean C, Poulat F, Berta P, Boizet-Bonhoure B (2002) A nuclear export signal within the high mobility group domain regulates the nucleocytoplasmic translocation of SOX9 during sexual determination. Proc Natl Acad Sci U S A 99:11199–11204.  https://doi.org/10.1073/pnas.172383099 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Ge ZJ, Schatten H, Zhang CL, Sun QY (2015) Oocyte ageing and epigenetics. Reproduction 149:R103–R114.  https://doi.org/10.1530/REP-14-0242 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Grabole N, Tischler J, Hackett JA, Kim S, Tang F, Leitch HG, Magnúsdóttir E, Surani MA (2013) Prdm14 promotes germline fate and naive pluripotency by repressing FGF signalling and DNA methylation. EMBO Rep 14:629–637.  https://doi.org/10.1038/embor.2013.67 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Greenfield R, Tabib A, Keshet I, Moss J, Sabag O, Goren A, Cedar H (2018) Role of transcription complexes in the formation of the basal methylation pattern in early development. Proc Natl Acad Sci U S A 115:10387–10391.  https://doi.org/10.1073/pnas.1804755115 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Group ECW (2008) Genetic aspects of female reproduction. Hum Reprod Update 14:293–307.  https://doi.org/10.1093/humupd/dmn009 CrossRefGoogle Scholar
  45. Gu C, Tong Q, Zheng L, Liang Z, Pu J, Mei H, Hu T, du Z, Tian F, Zeng F (2010a) TSEG-1, a novel member of histone H2A variants, participates in spermatogenesis via promoting apoptosis of spermatogenic cells. Genomics 95:278–289.  https://doi.org/10.1016/j.ygeno.2010.02.005 CrossRefPubMedGoogle Scholar
  46. Gu L, Wang Q, Sun QY (2010b) Histone modifications during mammalian oocyte maturation: dynamics, regulation and functions. Cell Cycle 9:1942–1950.  https://doi.org/10.4161/cc.9.10.11599 CrossRefPubMedGoogle Scholar
  47. Guarente L, Kenyon C (2000) Genetic pathways that regulate ageing in model organisms. Nature 408:255–262.  https://doi.org/10.1038/35041700 CrossRefPubMedGoogle Scholar
  48. Guglielmino MR, Santonocito M, Vento M, Ragusa M, Barbagallo D, Borzì P, Casciano I, Banelli B, Barbieri O, Astigiano S, Scollo P, Romani M, Purrello M, di Pietro C (2011) TAp73 is downregulated in oocytes from women of advanced reproductive age. Cell Cycle 10:3253–3256.  https://doi.org/10.4161/cc.10.19.17585 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Guo F, Yan L, Guo H, Li L, Hu B, Zhao Y, Yong J, Hu Y, Wang X, Wei Y, Wang W, Li R, Yan J, Zhi X, Zhang Y, Jin H, Zhang W, Hou Y, Zhu P, Li J, Zhang L, Liu S, Ren Y, Zhu X, Wen L, Gao YQ, Tang F, Qiao J (2015a) The transcriptome and DNA methylome landscapes of human primordial germ cells. Cell 161:1437–1452.  https://doi.org/10.1016/j.cell.2015.05.015 CrossRefPubMedGoogle Scholar
  50. Guo X, Wang L, Li J, Ding Z, Xiao J, Yin X, He S, Shi P, Dong L, Li G, Tian C, Wang J, Cong Y, Xu Y (2015b) Structural insight into autoinhibition and histone H3-induced activation of DNMT3A. Nature 517:640–644.  https://doi.org/10.1038/nature13899 CrossRefGoogle Scholar
  51. Guo J, Grow EJ, Yi C, Mlcochova H, Maher GJ, Lindskog C, Murphy PJ, Wike CL, Carrell DT, Goriely A, Hotaling JM, Cairns BR (2017) Chromatin and single-cell RNA-Seq profiling reveal dynamic signaling and metabolic transitions during human spermatogonial stem cell development. Cell Stem Cell 21:533–546 e536.  https://doi.org/10.1016/j.stem.2017.09.003 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Hamatani T, Falco G, Carter MG, Akutsu H, Stagg CA, Sharov AA, Dudekula DB, VanBuren V, Ko MSH (2004) Age-associated alteration of gene expression patterns in mouse oocytes. Hum Mol Genet 13:2263–2278.  https://doi.org/10.1093/hmg/ddh241 CrossRefGoogle Scholar
  53. Hammoud SS, Nix DA, Hammoud AO, Gibson M, Cairns BR, Carrell DT (2011) Genome-wide analysis identifies changes in histone retention and epigenetic modifications at developmental and imprinted gene loci in the sperm of infertile men. Hum Reprod 26:2558–2569.  https://doi.org/10.1093/humrep/der192 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Hammoud SS, Low DH, Yi C, Carrell DT, Guccione E, Cairns BR (2014) Chromatin and transcription transitions of mammalian adult germline stem cells and spermatogenesis. Cell Stem Cell 15:239–253.  https://doi.org/10.1016/j.stem.2014.04.006 CrossRefPubMedGoogle Scholar
  55. Hassan MA, Killick SR (2003) Effect of male age on fertility: evidence for the decline in male fertility with increasing age. Fertil Steril 79(Suppl 3):1520–1527CrossRefPubMedGoogle Scholar
  56. Hayakawa K, Ohgane J, Tanaka S, Yagi S, Shiota K (2012) Oocyte-specific linker histone H1foo is an epigenomic modulator that decondenses chromatin and impairs pluripotency. Epigenetics 7:1029–1036.  https://doi.org/10.4161/epi.21492 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Hayashi K, Surani MA (2009) Self-renewing epiblast stem cells exhibit continual delineation of germ cells with epigenetic reprogramming in vitro. Development 136:3549–3556.  https://doi.org/10.1242/dev.037747 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M (2011) Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell 146:519–532.  https://doi.org/10.1016/j.cell.2011.06.052 CrossRefGoogle Scholar
  59. Hekimi S, Guarente L (2003) Genetics and the specificity of the aging process. Science 299:1351–1354.  https://doi.org/10.1126/science.1082358 CrossRefGoogle Scholar
  60. Hemminki K, Kyyronen P, Vaittinen P (1999) Parental age as a risk factor of childhood leukemia and brain cancer in offspring. Epidemiology 10:271–275CrossRefPubMedGoogle Scholar
  61. Henderson SA, Edwards RG (1968) Chiasma frequency and maternal age in mammals. Nature 218:22–28CrossRefPubMedPubMedCentralGoogle Scholar
  62. Hill PWS, Leitch HG, Requena CE, Sun Z, Amouroux R, Roman-Trufero M, Borkowska M, Terragni J, Vaisvila R, Linnett S, Bagci H, Dharmalingham G, Haberle V, Lenhard B, Zheng Y, Pradhan S, Hajkova P (2018) Epigenetic reprogramming enables the transition from primordial germ cell to gonocyte. Nature 555:392–396.  https://doi.org/10.1038/nature25964 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Holubcova Z, Blayney M, Elder K, Schuh M (2015) Human oocytes. Error-prone chromosome-mediated spindle assembly favors chromosome segregation defects in human oocytes. Science 348:1143–1147.  https://doi.org/10.1126/science.aaa9529 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Hong E, Lim Y, Lee E, Oh M, Kwon D (2012) Tissue-specific and age-dependent expression of protein arginine methyltransferases (PRMTs) in male rat tissues. Biogerontology 13:329–336.  https://doi.org/10.1007/s10522-012-9379-2 CrossRefPubMedGoogle Scholar
  65. Hunt PA, Koehler KE, Susiarjo M, Hodges CA, Ilagan A, Voigt RC, Thomas S, Thomas BF, Hassold TJ (2003) Bisphenol a exposure causes meiotic aneuploidy in the female mouse. Curr Biol 13:546–553CrossRefPubMedGoogle Scholar
  66. Idring S, Magnusson C, Lundberg M, Ek M, Rai D, Svensson AC, Dalman C, Karlsson H, Lee BK (2014) Parental age and the risk of autism spectrum disorders: findings from a Swedish population-based cohort. Int J Epidemiol 43:107–115.  https://doi.org/10.1093/ije/dyt262 CrossRefPubMedGoogle Scholar
  67. Irie N, Weinberger L, Tang WWC, Kobayashi T, Viukov S, Manor YS, Dietmann S, Hanna JH, Surani MA (2015) SOX17 is a critical specifier of human primordial germ cell fate. Cell 160:253–268.  https://doi.org/10.1016/j.cell.2014.12.013 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Jenkins TG, Carrell DT (2012) The sperm epigenome and potential implications for the developing embryo. Reproduction 143:727–734.  https://doi.org/10.1530/REP-11-0450 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Jenkins TG, Aston KI, Pflueger C, Cairns BR, Carrell DT (2014) Age-associated sperm DNA methylation alterations: possible implications in offspring disease susceptibility. PLoS Genet 10:e1004458.  https://doi.org/10.1371/journal.pgen.1004458 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Jenkins TG, Aston KI, Carrell DT (2018) Sperm epigenetics and aging. Transl Androl Urol 7:S328–S335.  https://doi.org/10.21037/tau.2018.06.10 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Kageyama S, Liu H, Kaneko N, Ooga M, Nagata M, Aoki F (2007) Alterations in epigenetic modifications during oocyte growth in mice. Reproduction 133:85–94.  https://doi.org/10.1530/REP-06-0025 CrossRefPubMedGoogle Scholar
  72. Kalo D, Roth Z (2017) Low level of mono(2-ethylhexyl) phthalate reduces oocyte developmental competence in association with impaired gene expression. Toxicology 377:38–48.  https://doi.org/10.1016/j.tox.2016.12.005 CrossRefPubMedGoogle Scholar
  73. Kalo D, Hadas R, Furman O, Ben-Ari J, Maor Y, Patterson DG, Tomey C, Roth Z (2015) Carryover effects of acute DEHP exposure on ovarian function and oocyte developmental competence in lactating cows. PLoS One 10:e0130896.  https://doi.org/10.1371/journal.pone.0130896 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, Li E, Sasaki H (2004) Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429:900–903.  https://doi.org/10.1038/nature02633 CrossRefPubMedGoogle Scholar
  75. Kanfi Y, Naiman S, Amir G, Peshti V, Zinman G, Nahum L, Bar-Joseph Z, Cohen HY (2012) The sirtuin SIRT6 regulates lifespan in male mice. Nature 483:218–221.  https://doi.org/10.1038/nature10815 CrossRefGoogle Scholar
  76. Kawasaki Y, Lee J, Matsuzawa A, Kohda T, Kaneko-Ishino T, Ishino F (2014) Active DNA demethylation is required for complete imprint erasure in primordial germ cells. Sci Rep 4:3658.  https://doi.org/10.1038/srep03658 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Kelsey G, Feil R (2013) New insights into establishment and maintenance of DNA methylation imprints in mammals. Philos Trans R Soc Lond Ser B Biol Sci 368:20110336.  https://doi.org/10.1098/rstb.2011.0336 CrossRefGoogle Scholar
  78. Kim JH, Jee BC, Lee JM, Suh CS, Kim SH (2014) Histone acetylation level and histone acetyltransferase/deacetylase activity in ejaculated sperm from normozoospermic men. Yonsei Med J 55:1333–1340.  https://doi.org/10.3349/ymj.2014.55.5.1333 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Kirchhof N, Carnwath JW, Lemme E, Anastassiadis K, Scholer H, Niemann H (2000) Expression pattern of Oct-4 in preimplantation embryos of different species. Biol Reprod 63:1698–1705CrossRefPubMedGoogle Scholar
  80. Klutstein M, Fennell A, Fernandez-Alvarez A, Cooper JP (2015) The telomere bouquet regulates meiotic centromere assembly. Nat Cell Biol 17:458–469.  https://doi.org/10.1038/ncb3132 CrossRefPubMedGoogle Scholar
  81. Kobayashi H, Sakurai T, Imai M, Takahashi N, Fukuda A, Yayoi O, Sato S, Nakabayashi K, Hata K, Sotomaru Y, Suzuki Y, Kono T (2012) Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS Genet 8:e1002440.  https://doi.org/10.1371/journal.pgen.1002440 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Kobayashi H, Sakurai T, Miura F, Imai M, Mochiduki K, Yanagisawa E, Sakashita A, Wakai T, Suzuki Y, Ito T, Matsui Y, Kono T (2013) High-resolution DNA methylome analysis of primordial germ cells identifies gender-specific reprogramming in mice. Genome Res 23:616–627.  https://doi.org/10.1101/gr.148023.112 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R (1991) Male development of chromosomally female mice transgenic for Sry. Nature 351:117–121.  https://doi.org/10.1038/351117a0 CrossRefPubMedGoogle Scholar
  84. Koskenniemi JJ, Virtanen HE, Toppari J (2017) Testicular growth and development in puberty. Curr Opin Endocrinol Diabetes Obes 24:215–224.  https://doi.org/10.1097/MED.0000000000000339 CrossRefPubMedGoogle Scholar
  85. Kuliev A, Cieslak J, Verlinsky Y (2005) Frequency and distribution of chromosome abnormalities in human oocytes. Cytogenet Genome Res 111:193–198.  https://doi.org/10.1159/000086889 CrossRefPubMedGoogle Scholar
  86. Kunitomi A, Yuasa S, Sugiyama F, Saito Y, Seki T, Kusumoto D, Kashimura S, Takei M, Tohyama S, Hashimoto H, Egashira T, Tanimoto Y, Mizuno S, Tanaka S, Okuno H, Yamazawa K, Watanabe H, Oda M, Kaneda R, Matsuzaki Y, Nagai T, Okano H, Yagami KI, Tanaka M, Fukuda K (2016) H1foo has a pivotal role in qualifying induced pluripotent stem cells. Stem Cell Rep 6:825–833.  https://doi.org/10.1016/j.stemcr.2016.04.015 CrossRefGoogle Scholar
  87. Kurimoto K, Yabuta Y, Ohinata Y, Shigeta M, Yamanaka K, Saitou M (2008) Complex genome-wide transcription dynamics orchestrated by Blimp1 for the specification of the germ cell lineage in mice. Genes Dev 22:1617–1635.  https://doi.org/10.1101/gad.1649908 CrossRefPubMedPubMedCentralGoogle Scholar
  88. Kuroki S, Matoba S, Akiyoshi M, Matsumura Y, Miyachi H, Mise N, Abe K, Ogura A, Wilhelm D, Koopman P, Nozaki M, Kanai Y, Shinkai Y, Tachibana M (2013) Epigenetic regulation of mouse sex determination by the histone demethylase Jmjd1a. Science 341:1106–1109.  https://doi.org/10.1126/science.1239864 CrossRefPubMedGoogle Scholar
  89. Kutchy NA, Menezes ESB, Chiappetta A, Tan W, Wills RW, Kaya A, Topper E, Moura AA, Perkins AD, Memili E (2018) Acetylation and methylation of sperm histone 3 lysine 27 (H3K27ac and H3K27me3) are associated with bull fertility. Andrologia 50.  https://doi.org/10.1111/and.12915
  90. Lee RD (2003) Rethinking the evolutionary theory of aging: transfers, not births, shape senescence in social species. Proc Natl Acad Sci U S A 100:9637–9642.  https://doi.org/10.1073/pnas.1530303100 CrossRefPubMedPubMedCentralGoogle Scholar
  91. Li BZ, Huang Z, Cui QY, Song XH, du L, Jeltsch A, Chen P, Li G, Li E, Xu GL (2011) Histone tails regulate DNA methylation by allosterically activating de novo methyltransferase. Cell Res 21:1172–1181.  https://doi.org/10.1038/cr.2011.92 CrossRefPubMedPubMedCentralGoogle Scholar
  92. Li Y, Zheng M, Lau YF (2014) The sex-determining factors SRY and SOX9 regulate similar target genes and promote testis cord formation during testicular differentiation. Cell Rep 8:723–733.  https://doi.org/10.1016/j.celrep.2014.06.055 CrossRefPubMedGoogle Scholar
  93. Lin Q, Sirotkin A, Skoultchi AI (2000) Normal spermatogenesis in mice lacking the testis-specific linker histone H1t. Mol Cell Biol 20:2122–2128CrossRefPubMedPubMedCentralGoogle Scholar
  94. Lin CJ, Koh FM, Wong P, Conti M, Ramalho-Santos M (2014) Hira-mediated H3.3 incorporation is required for DNA replication and ribosomal RNA transcription in the mouse zygote. Dev Cell 30:268–279.  https://doi.org/10.1016/j.devcel.2014.06.022 CrossRefPubMedPubMedCentralGoogle Scholar
  95. Lister LM, Kouznetsova A, Hyslop LA, Kalleas D, Pace SL, Barel JC, Nathan A, Floros V, Adelfalk C, Watanabe Y, Jessberger R, Kirkwood TB, Höög C, Herbert M (2010) Age-related meiotic segregation errors in mammalian oocytes are preceded by depletion of cohesin and Sgo2. Curr Biol 20:1511–1521.  https://doi.org/10.1016/j.cub.2010.08.023 CrossRefPubMedGoogle Scholar
  96. Liu S, Brind’Amour J, Karimi MM, Shirane K, Bogutz A, Lefebvre L, Sasaki H, Shinkai Y, Lorincz MC (2014) Setdb1 is required for germline development and silencing of H3K9me3-marked endogenous retroviruses in primordial germ cells. Genes Dev 28:2041–2055.  https://doi.org/10.1101/gad.244848.114 CrossRefPubMedPubMedCentralGoogle Scholar
  97. Liu Z, Chen X, Zhou S, Liao L, Jiang R, Xu J (2015) The histone H3K9 demethylase Kdm3b is required for somatic growth and female reproductive function. Int J Biol Sci 11:494–507.  https://doi.org/10.7150/ijbs.11849 CrossRefPubMedPubMedCentralGoogle Scholar
  98. Liu Y, Giannopoulou EG, Wen D, Falciatori I, Elemento O, Allis CD, Rafii S, Seandel M (2016) Epigenetic profiles signify cell fate plasticity in unipotent spermatogonial stem and progenitor cells. Nat Commun 7:11275.  https://doi.org/10.1038/ncomms11275 CrossRefPubMedPubMedCentralGoogle Scholar
  99. Lucifero D, Mertineit C, Clarke HJ, Bestor TH, Trasler JM (2002) Methylation dynamics of imprinted genes in mouse germ cells. Genomics 79:530–538.  https://doi.org/10.1006/geno.2002.6732 CrossRefPubMedGoogle Scholar
  100. Luense LJ, Wang X, Schon SB, Weller AH, Lin Shiao E, Bryant JM, Bartolomei MS, Coutifaris C, Garcia BA, Berger SL (2016) Comprehensive analysis of histone post-translational modifications in mouse and human male germ cells. Epigenetics Chromatin 9:24.  https://doi.org/10.1186/s13072-016-0072-6 CrossRefPubMedPubMedCentralGoogle Scholar
  101. Luke L, Tourmente M, Dopazo H, Serra F, Roldan ER (2016) Selective constraints on protamine 2 in primates and rodents. BMC Evol Biol 16:21.  https://doi.org/10.1186/s12862-016-0588-1 CrossRefPubMedPubMedCentralGoogle Scholar
  102. Ma P, Schultz RM (2008) Histone deacetylase 1 (HDAC1) regulates histone acetylation, development, and gene expression in preimplantation mouse embryos. Dev Biol 319:110–120.  https://doi.org/10.1016/j.ydbio.2008.04.011 CrossRefPubMedPubMedCentralGoogle Scholar
  103. Ma P, Schultz RM (2013) Histone deacetylase 2 (HDAC2) regulates chromosome segregation and kinetochore function via H4K16 deacetylation during oocyte maturation in mouse. PLoS Genet 9:e1003377.  https://doi.org/10.1371/journal.pgen.1003377 CrossRefPubMedPubMedCentralGoogle Scholar
  104. Machida S, Hayashida R, Takaku M, Fukuto A, Sun J, Kinomura A, Tashiro S, Kurumizaka H (2016) Relaxed chromatin formation and weak suppression of homologous pairing by the testis-specific linker histone H1T. Biochemistry 55:637–646.  https://doi.org/10.1021/acs.biochem.5b01126 CrossRefPubMedGoogle Scholar
  105. Maezawa S, Yukawa M, Alavattam KG, Barski A, Namekawa SH (2018) Dynamic reorganization of open chromatin underlies diverse transcriptomes during spermatogenesis. Nucleic Acids Res 46:593–608.  https://doi.org/10.1093/nar/gkx1052 CrossRefPubMedGoogle Scholar
  106. Malekinejad H, Van Tol HT, Colenbrander B, Fink-Gremmels J (2006) Expression of 3alpha- and 3beta-hydroxy steroid dehydrogenase mRNA in COCs and granulosa cells determines zearalenone biotransformation. Toxicol in Vitro 20:458–463.  https://doi.org/10.1016/j.tiv.2005.09.007 CrossRefPubMedGoogle Scholar
  107. Manosalva I, Gonzalez A (2010) Aging changes the chromatin configuration and histone methylation of mouse oocytes at germinal vesicle stage. Theriogenology 74:1539–1547.  https://doi.org/10.1016/j.theriogenology.2010.06.024 CrossRefGoogle Scholar
  108. Marcho C, Cui W, Mager J (2015) Epigenetic dynamics during preimplantation development. Reproduction 150:R109–R120.  https://doi.org/10.1530/REP-15-0180 CrossRefPubMedPubMedCentralGoogle Scholar
  109. Miller B, Messias E, Miettunen J, Alaräisänen A, Järvelin MR, Koponen H, Räsänen P, Isohanni M, Kirkpatrick B (2011) Meta-analysis of paternal age and schizophrenia risk in male versus female offspring. Schizophr Bull 37:1039–1047.  https://doi.org/10.1093/schbul/sbq011 CrossRefPubMedGoogle Scholar
  110. Morais da Silva S, Hacker A, Harley V, Goodfellow P, Swain A, Lovell-Badge R (1996) Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds. Nat Genet 14:62–68.  https://doi.org/10.1038/ng0996-62 CrossRefPubMedGoogle Scholar
  111. Mostoslavsky R (2008) DNA repair, insulin signaling and sirtuins: at the crossroads between cancer and aging. Front Biosci 13:6966–6990CrossRefPubMedGoogle Scholar
  112. Nacarelli T, Liu P, Zhang R (2017) Epigenetic basis of cellular senescence and its implications in aging. Genes (Basel) 8.  https://doi.org/10.3390/genes8120343
  113. Naserbakht M, Ahmadkhaniha HR, Mokri B, Smith CL (2011) Advanced paternal age is a risk factor for schizophrenia in Iranians. Ann General Psychiatry 10:15.  https://doi.org/10.1186/1744-859X-10-15 CrossRefGoogle Scholar
  114. Nashun B, Hill PWS, Smallwood SA, Dharmalingam G, Amouroux R, Clark SJ, Sharma V, Ndjetehe E, Pelczar P, Festenstein RJ, Kelsey G, Hajkova P (2015) Continuous histone replacement by Hira is essential for normal transcriptional regulation and de novo DNA methylation during mouse oogenesis. Mol Cell 60:611–625.  https://doi.org/10.1016/j.molcel.2015.10.010 CrossRefPubMedPubMedCentralGoogle Scholar
  115. Ng JH, Kumar V, Muratani M, Kraus P, Yeo JC, Yaw LP, Xue K, Lufkin T, Prabhakar S, Ng HH (2013) In vivo epigenomic profiling of germ cells reveals germ cell molecular signatures. Dev Cell 24:324–333.  https://doi.org/10.1016/j.devcel.2012.12.011 CrossRefPubMedGoogle Scholar
  116. Nishino K, Hattori N, Tanaka S, Shiota K (2004) DNA methylation-mediated control of Sry gene expression in mouse gonadal development. J Biol Chem 279:22306–22313.  https://doi.org/10.1074/jbc.M309513200 CrossRefPubMedGoogle Scholar
  117. North BJ, Rosenberg MA, Jeganathan KB, Hafner AV, Michan S, Dai J, Baker DJ, Cen Y, Wu LE, Sauve AA, van Deursen JM, Rosenzweig A, Sinclair DA (2014) SIRT2 induces the checkpoint kinase BubR1 to increase lifespan. EMBO J 33:1438–1453.  https://doi.org/10.15252/embj.201386907 CrossRefPubMedPubMedCentralGoogle Scholar
  118. Ohta H, Kurimoto K, Okamoto I, Nakamura T, Yabuta Y, Miyauchi H, Yamamoto T, Okuno Y, Hagiwara M, Shirane K, Sasaki H, Saitou M (2017) In vitro expansion of mouse primordial germ cell-like cells recapitulates an epigenetic blank slate. EMBO J 36:1888–1907.  https://doi.org/10.15252/embj.201695862 CrossRefPubMedPubMedCentralGoogle Scholar
  119. Okano M, Bell DW, Haber DA, Li E (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247–257CrossRefGoogle Scholar
  120. Olsen J (1990) Subfecundity according to the age of the mother and the father. Dan Med Bull 37:281–282PubMedGoogle Scholar
  121. Ottolini CS, Newnham LJ, Capalbo A, Natesan SA, Joshi HA, Cimadomo D, Griffin DK, Sage K, Summers MC, Thornhill AR, Housworth E, Herbert AD, Rienzi L, Ubaldi FM, Handyside AH, Hoffmann ER (2015) Genome-wide maps of recombination and chromosome segregation in human oocytes and embryos show selection for maternal recombination rates. Nat Genet 47:727–735.  https://doi.org/10.1038/ng.3306 CrossRefPubMedPubMedCentralGoogle Scholar
  122. Patel S, Homaei A, Raju AB, Meher BR (2018) Estrogen: the necessary evil for human health, and ways to tame it. Biomed Pharmacother 102:403–411.  https://doi.org/10.1016/j.biopha.2018.03.078 CrossRefPubMedGoogle Scholar
  123. Patino-Parrado I, Gomez-Jimenez A, Lopez-Sanchez N, Frade JM (2017) Strand-specific CpG hemimethylation, a novel epigenetic modification functional for genomic imprinting. Nucleic Acids Res 45:8822–8834.  https://doi.org/10.1093/nar/gkx518 CrossRefPubMedPubMedCentralGoogle Scholar
  124. Peretz J, Vrooman L, Ricke WA, Hunt PA, Ehrlich S, Hauser R, Padmanabhan V, Taylor HS, Swan SH, VandeVoort CA, Flaws JA (2014) Bisphenol a and reproductive health: update of experimental and human evidence, 2007-2013. Environ Health Perspect 122:775–786.  https://doi.org/10.1289/ehp.1307728 CrossRefPubMedPubMedCentralGoogle Scholar
  125. Qiao J, Wang ZB, Feng HL, Miao YL, Wang Q, Yu Y, Wei YC, Yan J, Wang WH, Shen W, Sun SC, Schatten H, Sun QY (2014) The root of reduced fertility in aged women and possible therapentic options: current status and future perspects. Mol Asp Med 38:54–85.  https://doi.org/10.1016/j.mam.2013.06.001 CrossRefGoogle Scholar
  126. Reizel Y, Spiro A, Sabag O, Skversky Y, Hecht M, Keshet I, Berman BP, Cedar H (2015) Gender-specific postnatal demethylation and establishment of epigenetic memory. Genes Dev 29:923–933.  https://doi.org/10.1101/gad.259309.115 CrossRefPubMedPubMedCentralGoogle Scholar
  127. Richardson BE, Lehmann R (2010) Mechanisms guiding primordial germ cell migration: strategies from different organisms. Nat Rev Mol Cell Biol 11:37–49.  https://doi.org/10.1038/nrm2815 CrossRefPubMedPubMedCentralGoogle Scholar
  128. SanMiguel JM, Abramowitz LK, Bartolomei MS (2018) Imprinted gene dysregulation in a Tet1 null mouse model is stochastic and variable in the germline and offspring. Development 145:dev160622.  https://doi.org/10.1242/dev.160622 CrossRefPubMedPubMedCentralGoogle Scholar
  129. Santos F, Hendrich B, Reik W, Dean W (2002) Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol 241:172–182.  https://doi.org/10.1006/dbio.2001.0501 CrossRefGoogle Scholar
  130. Seisenberger S, Andrews S, Krueger F, Arand J, Walter J, Santos F, Popp C, Thienpont B, Dean W, Reik W (2012) The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol Cell 48:849–862.  https://doi.org/10.1016/j.molcel.2012.11.001 CrossRefPubMedPubMedCentralGoogle Scholar
  131. 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 278:440–458.  https://doi.org/10.1016/j.ydbio.2004.11.025 CrossRefPubMedGoogle Scholar
  132. Sekido R, Lovell-Badge R (2008) Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453:930–934.  https://doi.org/10.1038/nature06944 CrossRefPubMedGoogle Scholar
  133. Sekido R, Bar I, Narvaez V, Penny G, Lovell-Badge R (2004) SOX9 is up-regulated by the transient expression of SRY specifically in Sertoli cell precursors. Dev Biol 274:271–279.  https://doi.org/10.1016/j.ydbio.2004.07.011 CrossRefPubMedGoogle Scholar
  134. Selemani M, Mwanyangala MA, Mrema S, Shamte A, Kajungu D, Mkopi A, Mahande MJ, Nathan R (2014) The effect of mother’s age and other related factors on neonatal survival associated with first and second birth in rural, Tanzania: evidence from Ifakara health and demographic surveillance system in rural Tanzania. BMC Pregnancy Childbirth 14:240.  https://doi.org/10.1186/1471-2393-14-240 CrossRefPubMedPubMedCentralGoogle Scholar
  135. Sher G, Keskintepe L, Keskintepe M, Ginsburg M, Maassarani G, Yakut T, Baltaci V, Kotze D, Unsal E (2007) Oocyte karyotyping by comparative genomic hybridization [correction of hybrydization] provides a highly reliable method for selecting “competent” embryos, markedly improving in vitro fertilization outcome: a multiphase study. Fertil Steril 87:1033–1040.  https://doi.org/10.1016/j.fertnstert.2006.08.108 CrossRefPubMedGoogle Scholar
  136. Shirane K, Toh H, Kobayashi H, Miura F, Chiba H, Ito T, Kono T, Sasaki H (2013) Mouse oocyte methylomes at base resolution reveal genome-wide accumulation of non-CpG methylation and role of DNA methyltransferases. PLoS Genet 9:e1003439.  https://doi.org/10.1371/journal.pgen.1003439 CrossRefPubMedPubMedCentralGoogle Scholar
  137. Sim H, Argentaro A, Czech DP, Bagheri-Fam S, Sinclair AH, Koopman P, Boizet-Bonhoure B, Poulat F, Harley VR (2011) Inhibition of SRY-calmodulin complex formation induces ectopic expression of ovarian cell markers in developing XY gonads. Endocrinology 152:2883–2893.  https://doi.org/10.1210/en.2010-1475 CrossRefPubMedGoogle Scholar
  138. Simon L, Castillo J, Oliva R, Lewis SE (2011) Relationships between human sperm protamines, DNA damage and assisted reproduction outcomes. Reprod BioMed Online 23:724–734.  https://doi.org/10.1016/j.rbmo.2011.08.010 CrossRefPubMedGoogle Scholar
  139. Singh VP, Yueh WT, Gerton JL, Duncan FE (2019) Oocyte-specific deletion of Hdac8 in mice reveals stage-specific effects on fertility. Reproduction.  https://doi.org/10.1530/REP-18-0560
  140. Smallwood SA, Kelsey G (2012) De novo DNA methylation: a germ cell perspective. Trends Genet 28:33–42.  https://doi.org/10.1016/j.tig.2011.09.004 CrossRefPubMedGoogle Scholar
  141. Smits LJ, Zielhuis GA, Jongbloet PH, Van Poppel FW (2002) Mother’s age and daughter’s fecundity. An epidemiological analysis of late 19th to early 20th century family reconstitutions. Int J Epidemiol 31:349–358CrossRefPubMedGoogle Scholar
  142. Steger K, Balhorn R (2018) Sperm nuclear protamines: a checkpoint to control sperm chromatin quality. Anat Histol Embryol 47:273–279.  https://doi.org/10.1111/ahe.12361 CrossRefPubMedGoogle Scholar
  143. Stewart KR, Veselovska L, Kim J, Huang J, Saadeh H, Tomizawa SI, Smallwood SA, Chen T, Kelsey G (2015) Dynamic changes in histone modifications precede de novo DNA methylation in oocytes. Genes Dev 29:2449–2462.  https://doi.org/10.1101/gad.271353.115 CrossRefPubMedPubMedCentralGoogle Scholar
  144. Stewart KR, Veselovska L, Kelsey G (2016) Establishment and functions of DNA methylation in the germline. Epigenomics 8:1399–1413.  https://doi.org/10.2217/epi-2016-0056 CrossRefPubMedPubMedCentralGoogle Scholar
  145. Susiarjo M, Sasson I, Mesaros C, Bartolomei MS (2013) Bisphenol a exposure disrupts genomic imprinting in the mouse. PLoS Genet 9:e1003401.  https://doi.org/10.1371/journal.pgen.1003401 CrossRefPubMedPubMedCentralGoogle Scholar
  146. Swartz SZ, Wessel GM (2015) Germ line versus soma in the transition from egg to embryo. Curr Top Dev Biol 113:149–190.  https://doi.org/10.1016/bs.ctdb.2015.06.003 CrossRefPubMedPubMedCentralGoogle Scholar
  147. Tachiwana H, Kagawa W, Osakabe A, Kawaguchi K, Shiga T, Hayashi-Takanaka Y, Kimura H, Kurumizaka H (2010) Structural basis of instability of the nucleosome containing a testis-specific histone variant, human H3T. Proc Natl Acad Sci U S A 107:10454–10459.  https://doi.org/10.1073/pnas.1003064107 CrossRefPubMedPubMedCentralGoogle Scholar
  148. Tang WW et al (2015) A unique gene regulatory network resets the human germline epigenome for development. Cell 161:1453–1467.  https://doi.org/10.1016/j.cell.2015.04.053 CrossRefPubMedPubMedCentralGoogle Scholar
  149. 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.  https://doi.org/10.1038/nrg.2016.88 CrossRefPubMedGoogle Scholar
  150. Tang C, Klukovich R, Peng H, Wang Z, Yu T, Zhang Y, Zheng H, Klungland A, Yan W (2018) ALKBH5-dependent m6A demethylation controls splicing and stability of long 3′-UTR mRNAs in male germ cells. Proc Natl Acad Sci U S A 115:E325–E333.  https://doi.org/10.1073/pnas.1717794115 CrossRefPubMedGoogle Scholar
  151. Tarin JJ, Brines J, Cano A (1998) Long-term effects of delayed parenthood. Hum Reprod 13:2371–2376CrossRefPubMedGoogle Scholar
  152. Teperek M, Simeone A, Gaggioli V, Miyamoto K, Allen GE, Erkek S, Kwon T, Marcotte EM, Zegerman P, Bradshaw CR, Peters AHFM, Gurdon JB, Jullien J (2016) Sperm is epigenetically programmed to regulate gene transcription in embryos. Genome Res 26:1034–1046.  https://doi.org/10.1101/gr.201541.115 CrossRefPubMedPubMedCentralGoogle Scholar
  153. Tesar PJ, Chenoweth JG, Brook FA, Davies TJ, Evans EP, Mack DL, Gardner RL, McKay RDG (2007) New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448:196–199.  https://doi.org/10.1038/nature05972 CrossRefPubMedGoogle Scholar
  154. Toiber D, Erdel F, Bouazoune K, Silberman DM, Zhong L, Mulligan P, Sebastian C, Cosentino C, Martinez-Pastor B, Giacosa S, D’Urso A, Näär AM, Kingston R, Rippe K, Mostoslavsky R (2013) SIRT6 recruits SNF2H to DNA break sites, preventing genomic instability through chromatin remodeling. Mol Cell 51:454–468.  https://doi.org/10.1016/j.molcel.2013.06.018 CrossRefPubMedPubMedCentralGoogle Scholar
  155. Tomizawa S, Nowacka-Woszuk J, Kelsey G (2012) DNA methylation establishment during oocyte growth: mechanisms and significance. Int J Dev Biol 56:867–875.  https://doi.org/10.1387/ijdb.120152gk CrossRefPubMedGoogle Scholar
  156. Ueda T, Abe K, Miura A, Yuzuriha M, Zubair M, Noguchi M, Niwa K, Kawase Y, Kono T, Matsuda Y, Fujimoto H, Shibata H, Hayashizaki Y, Sasaki H (2000) The paternal methylation imprint of the mouse H19 locus is acquired in the gonocyte stage during foetal testis development. Genes Cells 5:649–659CrossRefPubMedGoogle Scholar
  157. Ueda J, Harada A, Urahama T, Machida S, Maehara K, Hada M, Makino Y, Nogami J, Horikoshi N, Osakabe A, Taguchi H, Tanaka H, Tachiwana H, Yao T, Yamada M, Iwamoto T, Isotani A, Ikawa M, Tachibana T, Okada Y, Kimura H, Ohkawa Y, Kurumizaka H, Yamagata K (2017) Testis-specific histone variant H3t gene is essential for entry into spermatogenesis. Cell Rep 18:593–600.  https://doi.org/10.1016/j.celrep.2016.12.065 CrossRefPubMedGoogle Scholar
  158. Urdinguio RG, Bayón GF, Dmitrijeva M, Toraño EG, Bravo C, Fraga MF, Bassas L, Larriba S, Fernández AF (2015) Aberrant DNA methylation patterns of spermatozoa in men with unexplained infertility. Hum Reprod 30:1014–1028.  https://doi.org/10.1093/humrep/dev053 CrossRefPubMedGoogle Scholar
  159. Uysal F, Ozturk S, Akkoyunlu G (2018) Superovulation alters DNA methyltransferase protein expression in mouse oocytes and early embryos. J Assist Reprod Genet 35:503–513.  https://doi.org/10.1007/s10815-017-1087-z CrossRefPubMedGoogle Scholar
  160. van der Heijden GW, Derijck AA, Ramos L, Giele M, van der Vlag J, de Boer P (2006) Transmission of modified nucleosomes from the mouse male germline to the zygote and subsequent remodeling of paternal chromatin. Dev Biol 298:458–469.  https://doi.org/10.1016/j.ydbio.2006.06.051 CrossRefPubMedGoogle Scholar
  161. Veselovska L, Smallwood SA, Saadeh H, Stewart KR, Krueger F, Maupetit-Méhouas S, Arnaud P, Tomizawa SI, Andrews S, Kelsey G (2015) Deep sequencing and de novo assembly of the mouse oocyte transcriptome define the contribution of transcription to the DNA methylation landscape. Genome Biol 16:209.  https://doi.org/10.1186/s13059-015-0769-z CrossRefPubMedPubMedCentralGoogle Scholar
  162. Villeponteau B (1997) The heterochromatin loss model of aging. Exp Gerontol 32:383–394CrossRefPubMedGoogle Scholar
  163. Viner RM, Allen NB, Patton GC (2017) Puberty, developmental processes, hnd iealth Interventions. In: rd, Bundy DAP, Silva N, Horton S, Jamison DT, Patton GC (eds) Child and adolescent health and development. Washington (DC).  https://doi.org/10.1596/978-1-4648-0423-6/pt2.ch9
  164. Vrooman LA, Oatley JM, Griswold JE, Hassold TJ, Hunt PA (2015) Estrogenic exposure alters the spermatogonial stem cells in the developing testis, permanently reducing crossover levels in the adult. PLoS Genet 11:e1004949.  https://doi.org/10.1371/journal.pgen.1004949 CrossRefPubMedPubMedCentralGoogle Scholar
  165. Warburton D (2005) Biological aging and the etiology of aneuploidy. Cytogenet Genome Res 111:266–272.  https://doi.org/10.1159/000086899 CrossRefPubMedGoogle Scholar
  166. Wen D, Banaszynski LA, Liu Y, Geng F, Noh KM, Xiang J, Elemento O, Rosenwaks Z, Allis CD, Rafii S (2014) Histone variant H3.3 is an essential maternal factor for oocyte reprogramming. Proc Natl Acad Sci U S A 111:7325–7330.  https://doi.org/10.1073/pnas.1406389111 CrossRefPubMedPubMedCentralGoogle Scholar
  167. Weuve J, Hauser R, Calafat AM, Missmer SA, Wise LA (2010) Association of exposure to phthalates with endometriosis and uterine leiomyomata: findings from NHANES, 1999-2004. Environ Health Perspect 118:825–832.  https://doi.org/10.1289/ehp.0901543 CrossRefPubMedPubMedCentralGoogle Scholar
  168. Whitcomb BW, Turzanski-Fortner R, Richter KS, Kipersztok S, Stillman RJ, Levy MJ, Levens ED (2011) Contribution of male age to outcomes in assisted reproductive technologies. Fertil Steril 95:147–151.  https://doi.org/10.1016/j.fertnstert.2010.06.039 CrossRefPubMedGoogle Scholar
  169. Wu JY, Ribar TJ, Cummings DE, Burton KA, McKnight GS, Means AR (2000) Spermiogenesis and exchange of basic nuclear proteins are impaired in male germ cells lacking Camk4. Nat Genet 25:448–452.  https://doi.org/10.1038/78153 CrossRefPubMedGoogle Scholar
  170. Wu J, Yamauchi T, Izpisua Belmonte JC (2016) An overview of mammalian pluripotency. Development 143:1644–1648.  https://doi.org/10.1242/dev.132928 CrossRefPubMedGoogle Scholar
  171. Yamaguchi S, Hong K, Liu R, Shen L, Inoue A, Diep D, Zhang K, Zhang Y (2012) Tet1 controls meiosis by regulating meiotic gene expression. Nature 492:443–447.  https://doi.org/10.1038/nature11709 CrossRefPubMedPubMedCentralGoogle Scholar
  172. Yamaguchi S, Shen L, Liu Y, Sendler D, Zhang Y (2013) Role of Tet1 in erasure of genomic imprinting. Nature 504:460–464.  https://doi.org/10.1038/nature12805 CrossRefPubMedPubMedCentralGoogle Scholar
  173. Yamaji M, Seki Y, Kurimoto K, Yabuta Y, Yuasa M, Shigeta M, Yamanaka K, Ohinata Y, Saitou M (2008) Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat Genet 40:1016–1022.  https://doi.org/10.1038/ng.186 CrossRefGoogle Scholar
  174. Yip BH, Pawitan Y, Czene K (2006) Parental age and risk of childhood cancers: a population-based cohort study from Sweden. Int J Epidemiol 35:1495–1503.  https://doi.org/10.1093/ije/dyl177 CrossRefPubMedGoogle Scholar
  175. Yu A, Dang W (2017) Regulation of stem cell aging by SIRT1—linking metabolic signaling to epigenetic modifications. Mol Cell Endocrinol 455:75–82.  https://doi.org/10.1016/j.mce.2017.03.031 CrossRefPubMedGoogle Scholar
  176. Yue MX, Fu XW, Zhou GB, Hou YP, Du M, Wang L, Zhu SE (2012) Abnormal DNA methylation in oocytes could be associated with a decrease in reproductive potential in old mice. J Assist Reprod Genet 29:643–650.  https://doi.org/10.1007/s10815-012-9780-4 CrossRefPubMedPubMedCentralGoogle Scholar
  177. Yun Y, An P, Ning J, Zhao GM, Yang WL, Lei AM (2015) H1foo is essential for in vitro meiotic maturation of bovine oocytes. Zygote 23:416–425.  https://doi.org/10.1017/S0967199414000021 CrossRefPubMedGoogle Scholar
  178. Zhang L, Hou X, Ma R, Moley K, Schedl T, Wang Q (2014) Sirt2 functions in spindle organization and chromosome alignment in mouse oocyte meiosis. FASEB J 28:1435–1445.  https://doi.org/10.1096/fj.13-244111 CrossRefPubMedPubMedCentralGoogle Scholar
  179. Zhang Y, Han J, Zhu CC, Tang F, Cui XS, Kim NH, Sun SC (2016) Exposure to HT-2 toxin causes oxidative stress induced apoptosis/autophagy in porcine oocytes. Sci Rep 6:33904.  https://doi.org/10.1038/srep33904 CrossRefPubMedPubMedCentralGoogle Scholar
  180. Zhang K, Lu Y, Jiang C, Liu W, Shu J, Chen X, Shi Y, Wang E, Wang L, Hu Q, Dai Y, Xiong B (2017) HDAC8 functions in spindle assembly during mouse oocyte meiosis. Oncotarget 8:20092–20102.  https://doi.org/10.18632/oncotarget.15383 CrossRefPubMedPubMedCentralGoogle Scholar
  181. Ziv-Gal A, Wang W, Zhou C, Flaws JA (2015) The effects of in utero bisphenol A exposure on reproductive capacity in several generations of mice. Toxicol Appl Pharmacol 284:354–362.  https://doi.org/10.1016/j.taap.2015.03.003 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute of Dental Sciences, Faculty of Dental MedicineHebrew University of JerusalemJerusalemIsrael

Personalised recommendations