Epigenetic inheritance through the female germ-line: The known, the unknown, and the possible

Seminars in Cell and Developmental Biology

Volumn 43, Issue , 2015, Pages 106-116

  Clarke, Hugh J ^a   Vieux, Karl Frédéric ^a  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

DNA methylation; Epigenetics; Histones; MicroRNA; Oogenesis; Transgenerational inheritance

Indexed keywords

DNA; HISTONE; MICRORNA; UNTRANSLATED RNA;

ARTICLE; DNA METHYLATION; EPIGENETICS; FEMALE; GERM LINE; HISTONE MODIFICATION; HUMAN; INHERITANCE; NONHUMAN; OOCYTE DEVELOPMENT; PROTEIN PROCESSING; ADVERSE EFFECTS; CYTOLOGY; ENVIRONMENTAL EXPOSURE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; OOCYTE;

DNA METHYLATION; ENVIRONMENTAL EXPOSURE; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONES; HUMANS; INHERITANCE PATTERNS; MICRORNAS; OOCYTES; OOGENESIS; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84948110887     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2015.07.003     Document Type: Article

References (121)

1. Messerschmidt D.M., Knowles B.B., Solter D. DNA methylation dynamics during epigenetic reprogramming in the germline and preimplantation embryos. Genes Dev. 2014, 28:812-828.
2. Mikedis M.M., Downs K.M. Mouse primordial germ cells: a reappraisal. Int. Rev. Cell Mol. Biol. 2014, 309:1-57.
3. Jorgensen J.S. Defining the neighborhoods that escort the oocyte through its early life events and into a functional follicle. Mol. Reprod. Dev. 2013, 80:960-976.
4. Kagiwada S., Kurimoto K., Hirota T., Yamaji M., Saitou M. Replication-coupled passive DNA demethylation for the erasure of genome imprints in mice. EMBO J. 2013, 32:340-353.
5. Baker T.G. A quantitative and cytological study of germ cells in human ovaries. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 1963, 158:417-433.
6. Lin Y.T., Capel B. Cell fate commitment during mammalian sex determination. Curr. Opin. Genet. Dev. 2015, 32:144-152.
7. Pepling M.E. Follicular assembly: mechanisms of action. Reproduction 2012, 143:139-149.
8. Pepling M.E. From primordial germ cell to primordial follicle: mammalian female germ cell development. Genesis 2006, 44:622-632.
9. Kerr J.B., Duckett R., Myers M., Britt K.L., Mladenovska T., Findlay J.K. Quantification of healthy follicles in the neonatal and adult mouse ovary: evidence for maintenance of primordial follicle supply. Reproduction 2006, 132:95-109.
10. Oktem O., Oktay K. The ovary: anatomy function throughout human life. Ann. N. Y. Acad. Sci. 2008, 1127:1-9.
11. Hanna C.B., Hennebold J.D. Ovarian germline stem cells: an unlimited source of oocytes?. Fertil. Steril. 2014, 101:20-30.
12. Zhang H., Zheng W., Shen Y., Adhikari D., Ueno H., Liu K. Experimental evidence showing that no mitotically active female germline progenitors exist in postnatal mouse ovaries. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:12580-12585.
13. Lei L., Spradling A.C. Female mice lack adult germ-line stem cells but sustain oogenesis using stable primordial follicles. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:8585-8590.
14. Zhang H., Liu L., Li X., Busayavalasa K., Shen Y., Hovatta O., et al. Life-long in vivo cell-lineage tracing shows that no oogenesis originates from putative germline stem cells in adult mice. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:17983-17988.
15. Hirshfield A.N. Development of follicles in the mammalian ovary. Int. Rev. Cytol. 1991, 124:43-101.
16. Adhikari D., Liu K. Molecular mechanisms underlying the activation of mammalian primordial follicles. Endocr. Rev. 2009, 30:438-464.
17. Monniaux D., Clement F., Dalbies-Tran R., Estienne A., Fabre S., Mansanet C., et al. The ovarian reserve of primordial follicles and the dynamic reserve of antral growing follicles: what is the link?. Biol. Reprod. 2014, 90:85.
18. Hayashi K., Ogushi S., Kurimoto K., Shimamoto S., Ohta H., Saitou M. Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice. Science 2012, 338:971-975.
19. Zhang H., Risal S., Gorre N., Busayavalasa K., Li X., Shen Y., et al. Somatic cells initiate primordial follicle activation and govern the development of dormant oocytes in mice. Curr. Biol. 2014, 24:2501-2508.
20. John G.B., Shidler M.J., Besmer P., Castrillon D.H. Kit signaling via PI3K promotes ovarian follicle maturation but is dispensable for primordial follicle activation. Dev. Biol. 2009, 331:292-299.
21. Castrillon D.H., Miao L., Kollipara R., Horner J.W., DePinho R.A. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 2003, 301:215-218.
22. Sánchez F., Smitz J. Molecular control of oogenesis. Biochim. Biophys. Acta 2012, 1822:1896-1912.
23. Sobinoff A.P., Sutherland J.M., Mclaughlin E.A. Intracellular signalling during female gametogenesis. Mol. Hum. Reprod. 2013, 19:265-278.
24. Pan H., O'Brien M.J., Wigglesworth K., Eppig J.J., Schultz R.M. Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. Dev. Biol. 2005, 286:493-506.
25. Ma J.Y., Li M., Luo Y.B., Song S., Tian D., Yang J., et al. Maternal factors required for oocyte developmental competence in mice: transcriptome analysis of non-surrounded nucleolus (NSN) and surrounded nucleolus (SN) oocytes. Cell Cycle 2013, 12:1928-1938.
26. Clarke H. Post-transcriptional control of gene expression during mouse oogenesis. Mouse Development 2012, 1-21. Springer, Berlin/Heidelberg. J.Z. Kubiak (Ed.).
27. Medvedev S., Pan H., Schultz R.M. Absence of MSY2 in mouse oocytes perturbs oocyte growth and maturation, RNA stability, and the transcriptome. Biol. Reprod. 2011, 85:575-583.
28. Flemr M., Ma J., Schultz R.M., Svoboda P. P-body loss is concomitant with formation of a messenger RNA storage domain in mouse oocytes. Biol. Reprod. 2010, 82:1008-1017.
29. Chalupnikova K., Solc P., Sulimenko V., Sedlacek R., Svoboda P. An oocyte-specific ELAVL2 isoform is a translational repressor ablated from meiotically competent antral oocytes. Cell Cycle 2014, 13:1187-1200.
30. Brower P.T., Gizang E., Boreen S.M., Schultz R.M. Biochemical studies of mammalian oogenesis: synthesis and stability of various classes of RNA during growth of the mouse oocyte in vitro. Dev. Biol. 1981, 86:373-383.
31. Bachvarova R. Synthesis, turnover, and stability of heterogeneous RNA in growing mouse oocytes. Dev. Biol. 1981, 86:384-392.
32. Kang M.K., Han S.J. Post-transcriptional post-translational regulation during mouse oocyte maturation. BMB Rep. 2011, 44:147-157.
33. Zuccotti M., Garagna S., Merico V., Monti M., Redi C. Chromatin organisation and nuclear architecture in growing mouse oocytes. Mol. Cell. Endocrinol. 2005, 234:11-17.
34. Tan J.H., Wang H.L., Sun X.S., Liu Y., Sui H.S., Zhang J. Chromatin configurations in the germinal vesicle of mammalian oocytes. Mol. Hum. Reprod. 2009, 15:1-9.
35. Wickramasinghe D., Ebert K., Albertini D. Meiotic competence acquisition is associated with the appearance of M-phase characteristics in growing mouse oocytes. Dev. Biol. 1991, 143:162-172.
36. Debey P., Szollosi M., Szollosi D., Vautier D., Girousse A., Besombes D. Competent mouse oocytes isolated from antral follicles exhibit different chromatin organization and follow different maturation dynamics. Mol. Reprod. Dev. 1993, 36:59-74.
37. Bouniol-Baly C., Hamraoui L., Guibert J., Beaujean N., Szollosi M., Debey P. Differential transcriptional activity associated to chromatin configuration in fully grown germinal vesicle mouse oocytes. Biol. Reprod. 1999, 60:580-587.
38. De La Fuente R., Viveiros M.M., Burns K.H., Adashi E.Y., Matzuk M.M., Eppig J.J. Major chromatin remodeling in the germinal vesicle (GV) of mammalian oocytes is dispensable for global transcriptional silencing but required for centromeric heterochromatin function. Dev. Biol. 2004, 275:447-458.
39. Andreu-Vieyra C.V., Chen R., Agno J.E., Glaser S., Anastassiadis K., Stewart A.F., et al. MLL2 is required in oocytes for bulk histone 3 lysine 4 trimethylation and transcriptional silencing. PLoS Biol. 2010, 8. pii:e1000453.
40. Burns K.H., Viveiros M.M., Ren Y., Wang P., DeMayo F.J., Frail D.E., et al. Roles of NPM2 in chromatin and nucleolar organization in oocytes and embryos. Science 2003, 300:633-636.
41. Inoue A., Nakajima R., Nagata M., Aoki F. Contribution of the oocyte nucleus and cytoplasm to the determination of meiotic and developmental competence in mice. Hum. Reprod. 2008, 23:1377-1384.
42. Zuccotti M., Giorgi Rossi P., Martinez A., Garagna S., Forabosco A., Redi C. Meiotic and developmental competence of mouse antral oocytes. Biol. Reprod. 1998, 58:700-704.
43. Conti M., Hsieh M., Musa Zamah A., Oh J.S. Novel signaling mechanisms in the ovary during oocyte maturation and ovulation. Mol. Cell. Endocrinol. 2012, 356:65-73.
44. Holt J.E., Lane S.I., Jones K.T. The control of meiotic maturation in mammalian oocytes. Curr. Top. Dev. Biol. 2013, 102:207-226.
45. Liu L., Kong N., Xia G., Zhang M. Molecular control of oocyte meiotic arrest and resumption. Reprod. Fertil. Dev. 2013, 25:463-471.
46. Smallwood S.A., Tomizawa S., Krueger F., Ruf N., Carli N., Segonds-Pichon A., et al. Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat. Genet. 2011, 43:811-814.
47. Kobayashi H., Sakurai T., Imai M., Takahashi N., Fukuda A., Yayoi O., et al. Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS Genet. 2012, 8:e1002440.
48. Shirane K., Toh H., Kobayashi H., Miura F., Chiba H., Ito T., et al. Mouse oocyte methylomes at base resolution reveal genome-wide accumulation of non-CpG methylation and role of DNA methyltransferases. PLoS Genet. 2013, 9:e1003439.
49. Tomizawa S., Nowacka-Woszuk J., Kelsey G. DNA methylation establishment during oocyte growth: mechanisms and significance. Int. J. Dev. Biol. 2012, 56:867-875.
50. Lee H.J., Hore T.A., Reik W. Reprogramming the methylome: erasing memory and creating diversity. Cell Stem Cell 2014, 14:710-719.
51. Guibert S., Forne T., Weber M. Global profiling of DNA methylation erasure in mouse primordial germ cells. Genome Res. 2012, 22:633-641.
52. Popp C., Dean W., Feng S., Cokus S.J., Andrews S., Pellegrini M., et al. Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 2010, 463:1101-1105.
53. Seisenberger S., Andrews S., Krueger F., Arand J., Walter J., Santos F., et al. The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol. Cell 2012, 48:849-862.
54. Hackett J.A., Sengupta R., Zylicz J.J., Murakami K., Lee C., Down T.A., et al. Germline DNA demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine. Science 2013, 339:448-452.
55. Vincent J.J., Huang Y., Chen P.Y., Feng S., Calvopina J.H., Nee K., et al. Stage-specific roles for tet1 and tet2 in DNA demethylation in primordial germ cells. Cell Stem Cell 2013, 12:470-478.
56. Yamaguchi S., Shen L., Liu Y., Sendler D., Zhang Y. Role of Tet1 in erasure of genomic imprinting. Nature 2013, 504:460-464.
57. Hajkova P., Erhardt S., Lane N., Haaf T., El-Maarri O., Reik W., et al. Epigenetic reprogramming in mouse primordial germ cells. Mech. Dev. 2002, 117:15-23.
58. Tomizawa S-i, Kobayashi H., Watanabe T., Andrews S., Hata K., Kelsey G., et al. Dynamic stage-specific changes in imprinted differentially methylated regions during early mammalian development and prevalence of non-CpG methylation in oocytes. Development 2011, 138:811-820.
59. Lucifero D., Mann M.R., Bartolomei M.S., Trasler J.M. Gene-specific timing and epigenetic memory in oocyte imprinting. Hum. Mol. Genet. 2004, 13:839-849.
60. Hiura H., Obata Y., Komiyama J., Shirai M., Kono T. Oocyte growth-dependent progression of maternal imprinting in mice. Genes Cells 2006, 11:353-361.
61. Obata Y., Kono T. Maternal primary imprinting is established at a specific time for each gene throughout oocyte growth. J. Biol. Chem. 2002, 277:5285-5289.
62. Bourc'his D., Xu G., Lin C., Bollman B., Bestor T. Dnmt3L and the establishment of maternal genomic imprints. Science 2001, 294:2536-2539.
63. Hata K., Okano M., Lei H., Li E. Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 2002, 129:1983-1993.
64. Kaneda M., Okano M., Hata K., Sado T., Tsujimoto N., Li E., et al. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 2004, 429:900-903.
65. Kidder G.M., Vanderhyden B.C. Bidirectional communication between oocytes and follicle cells: ensuring oocyte developmental competence. Can. J. Physiol. Pharmacol. 2010, 88:399-413.
66. Denomme M.M., White C.R., Gillio-Meina C., Macdonald W.A., Deroo B.J., Kidder G.M., et al. Compromised fertility disrupts Peg1 but not Snrpn and Peg3 imprinted methylation acquisition in mouse oocytes. Front. Genet. 2012, 3:129.
67. Smith E.Y., Futtner C.R., Chamberlain S.J., Johnstone K.A., Resnick J.L. Transcription is required to establish maternal imprinting at the Prader-Willi syndrome and Angelman syndrome locus. PLoS Genet. 2011, 7:e1002422.
68. Chotalia M., Smallwood S.A., Ruf N., Dawson C., Lucifero D., Frontera M., et al. Transcription is required for establishment of germline methylation marks at imprinted genes. Genes Dev. 2009, 23:105-117.
69. Kelsey G., Feil R. New insights into establishment and maintenance of DNA methylation imprints in mammals. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2013, 368:20110336.
70. Lucifero D., La Salle S., Bourc'his D., Martel J., Bestor T.H., Trasler J.M. Coordinate regulation of DNA methyltransferase expression during oogenesis. BMC Dev. Biol. 2007, 7:36.
71. Kageyama S.-I., Liu H., Kaneko N., Ooga M., Nagata M., Aoki F. Alterations in epigenetic modifications during oocyte growth in mice. Reproduction 2007, 133:85-94.
72. Kim J.-M., Liu H., Tazaki M., Nagata M., Aoki F. Changes in histone acetylation during mouse oocyte meiosis. J. Cell Biol. 2003, 162:37-46.
73. Akiyama T., Kim J.M., Nagata M., Aoki F. Regulation of histone acetylation during meiotic maturation in mouse oocytes. Mol. Reprod. Dev. 2004, 69:222-227.
74. Shao G.B., Wang J., Zhang L.P., Wu C.Y., Jin J., Sang J.R., et al. Aging alters histone H3 lysine 4 methylation in mouse germinal vesicle stage oocytes. Reprod. Fertil. Dev. 2015, 27:419-426.
75. Ma P., Pan H., Montgomery R.L., Olson E.N., Schultz R.M. Compensatory functions of histone deacetylase 1 (HDAC1) and HDAC2 regulate transcription and apoptosis during mouse oocyte development. Proc. Natl. Acad. Sci. 2012, 109. E481-E9.
76. Stuwe E., Toth K.F., Aravin A.A. Small but sturdy: small RNAs in cellular memory and epigenetics. Genes Dev. 2014, 28:423-431.
77. Siomi M.C., Sato K., Pezic D., Aravin A.A. PIWI-interacting small RNAs: the vanguard of genome defence. Nat. Rev. Mol. Cell Biol. 2011, 12:246-258.
78. Cook M.S., Blelloch R. Small RNAs in germline development. Curr. Top. Dev. Biol. 2013, 102:159-205.
79. Kuramochi-Miyagawa S., Watanabe T., Gotoh K., Totoki Y., Toyoda A., Ikawa M., et al. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev. 2008, 22:908-917.
80. Carmell M.A., Girard A., van de Kant H.J., Bourc'his D., Bestor T.H., de Rooij D.G., et al. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev. Cell 2007, 12:503-514.
81. Deng W., Lin H. Miwi, a murine homolog of Piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev. Cell 2002, 2:819-830.
82. Murchison E.P., Stein P., Xuan Z., Pan H., Zhang M.Q., Schultz R.M., et al. Critical roles for Dicer in the female germline. Genes Dev. 2007, 21:682-693.
83. Tang F., Kaneda M., O'Carroll D., Hajkova P., Barton S.C., Sun Y.A., et al. Maternal microRNAs are essential for mouse zygotic development. Genes Dev. 2007, 21:644-648.
84. Kaneda M., Tang F., O'Carroll D., Lao K., Surani M.A. Essential role for Argonaute2 protein in mouse oogenesis. Epigenet. Chrom. 2009, 2:9.
85. Stein P., Rozhkov N.V., Li F., Cardenas F.L., Davydenk O., Vandivier L.E., et al. Essential Role for endogenous siRNAs during meiosis in mouse oocytes. PLoS Genet. 2015, 11:e1005013.
86. Suh N., Baehner L., Moltzahn F., Melton C., Shenoy A., Chen J., et al. MicroRNA function Is globally suppressed in mouse oocytes and early embryos. Curr. Biol. 2010, 20:271-277.
87. Yuan S., Ortogero N., Wu Q., Zheng H., Yan W. Murine follicular development requires oocyte DICER, but not DROSHA. Biol. Reprod. 2014, 91:39.
88. Ma J., Flemr M., Stein P., Berninger P., Malik R., Zavolan M., et al. MicroRNA activity is suppressed in mouse oocytes. Curr. Biol. 2010, 20:265-270.
89. Flemr M., Malik R., Franke V., Nejepinska J., Sedlacek R., Vlahovicek K., et al. A retrotransposon-driven dicer isoform directs endogenous small interfering RNA production in mouse oocytes. Cell 2013, 155:807-816.
90. Tam O.H., Aravin A.A., Stein P., Girard A., Murchison E.P., Cheloufi S., et al. Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 2008, 453:534-538.
91. Watanabe T., Totoki Y., Toyoda A., Kaneda M., Kuramochi-Miyagawa S., Obata Y., et al. Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 2008, 453:539-543.
92. Martos S.N., Tang W.Y., Wang Z. Elusive inheritance: transgenerational effects and epigenetic inheritance in human environmental disease. Prog. Biophys. Mol. Biol. 2015, 118:44-54.
93. Heard E., Martienssen R.A. Transgenerational epigenetic inheritance: myths and mechanisms. Cell 2014, 157:95-109.
94. Daxinger L., Whitelaw E. Understanding transgenerational epigenetic inheritance via the gametes in mammals. Nat. Rev. Genet. 2012, 13:153-162.
95. McCarrey J.R. Distinctions between transgenerational and non-transgenerational epimutations. Mol. Cell. Endocrinol. 2014, 398:13-23.
96. Lane M., Robker R.L., Robertson S.A. Parenting from before conception. Science 2014, 345:756-760.
97. Gu L., Liu H., Gu X., Boots C., Moley K.H., Wang Q. Metabolic control of oocyte development: linking maternal nutrition and reproductive outcomes. Cell. Mol. Life Sci. 2015, 72:251-271.
98. Grindler N.M., Moley K.H. Maternal obesity, infertility and mitochondrial dysfunction: potential mechanisms emerging from mouse model systems. Mol. Hum. Reprod. 2013, 19:486-494.
99. Lane M., Zander-Fox D.L., Robker R.L., McPherson N.O. Peri-conception parental obesity, reproductive health, and transgenerational impacts. Trends Endocrinol. Metab. 2015, 26:84-90.
100. Wu L.L., Russell D.L., Wong S.L., Chen M., Tsai T.S., St John J.C., et al. Mitochondrial dysfunction in oocytes of obese mothers: transmission to offspring and reversal by pharmacological endoplasmic reticulum stress inhibitors. Development 2015, 142:681-691.
101. Wang Q., Ratchford A.M., Chi M.M., Schoeller E., Frolova A., Schedl T., et al. Maternal diabetes causes mitochondrial dysfunction and meiotic defects in murine oocytes. Mol. Endocrinol. 2009, 23:1603-1612.
102. Wu L.L., Dunning K.R., Yang X., Russell D.L., Lane M., Norman R.J., et al. High-fat diet causes lipotoxicity responses in cumulus-oocyte complexes and decreased fertilization rates. Endocrinology 2010, 151:5438-5445.
103. Wang Q., Chi M.M., Moley K.H. Live imaging reveals the link between decreased glucose uptake in ovarian cumulus cells and impaired oocyte quality in female diabetic mice. Endocrinology 2012, 153:1984-1989.
104. Igosheva N., Abramov A.Y., Poston L., Eckert J.J., Fleming T.P., Duchen M.R., et al. Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS ONE 2010, 5:e10074.
105. Luzzo K.M., Wang Q., Purcell S.H., Chi M., Jimenez P.T., Grindler N., et al. High fat diet induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation/brain defects. PLoS ONE 2012, 7:e49217.
106. Ge Z.J., Liang X.W., Guo L., Liang Q.X., Luo S.M., Wang Y.P., et al. Maternal diabetes causes alterations of DNA methylation statuses of some imprinted genes in murine oocytes. Biol. Reprod. 2013, 88:117.
107. Ratchford A.M., Esguerra C.R., Moley K.H. Decreased oocyte-granulosa cell gap junction communication and connexin expression in a type 1 diabetic mouse model. Mol. Endocrinol. 2008, 22:2643-2654.
108. Li R., Albertini D.F. The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat. Rev. Mol. Cell Biol. 2013, 14:141-152.
109. Bernhardt M.L., Kong B.Y., Kim A.M., O'Halloran T.V., Woodruff T.K. A zinc-dependent mechanism regulates meiotic progression in mammalian oocytes. Biol. Reprod. 2012, 86:114.
110. Kim A.M., Vogt S., O'Halloran T.V., Woodruff T.K. Zinc availability regulates exit from meiosis in maturing mammalian oocytes. Nat. Chem. Biol. 2010, 6:674-681.
111. Tian X., Diaz F.J. Zinc depletion causes multiple defects in ovarian function during the periovulatory period in mice. Endocrinology 2012, 153:873-886.
112. Tian X., Diaz F.J. Acute dietary zinc deficiency before conception compromises oocyte epigenetic programming and disrupts embryonic development. Dev. Biol. 2012, 376:51-61.
113. Chaffin C.L., Latham K.E., Mtango N.R., Midic U., VandeVoort C.A. Dietary sugar in healthy female primates perturbs oocyte maturation and in vitro preimplantation embryo development. Endocrinology 2014, 155:2688-2695.
114. VandeVoort C.A., Grimsrud K.N., Midic U., Mtango N., Latham K.E. Transgenerational effects of binge drinking in a primate model: implications for human health. Fertil. Steril. 2015, 103:560-569.
115. Morgan H.D., Sutherland H.G., Martin D.I., Whitelaw E. Epigenetic inheritance at the agouti locus in the mouse. Nat. Genet. 1999, 23:314-318.
116. Rakyan V.K., Chong S., Champ M.E., Cuthbert P.C., Morgan H.D., Luu K.V., et al. Transgenerational inheritance of epigenetic states at the murine Axin(Fu) allele occurs after maternal and paternal transmission. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:2538-2543.
117. Rassoulzadegan M., Grandjean V., Gounon P., Vincent S., Gillot I., Cuzin F. RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse. Nature 2006, 441:469-474.
118. Yuan S., Oliver D., Schuster A., Zheng H., Yan W. Breeding scheme and maternal small RNAs affect the efficiency of transgenerational inheritance of a paramutation in mice. Sci. Rep. 2015, 5:9266.
119. Nilsson E., Larsen G., Manikkam M., Guerrero-Bosagna C., Savenkova M.I., Skinner M.K. Environmentally induced epigenetic transgenerational inheritance of ovarian disease. PLoS ONE 2012, 7:e36129.
120. Manikkam M., Haque M.M., Guerrero-Bosagna C., Nilsson E.E., Skinner M.K. Pesticide methoxychlor promotes the epigenetic transgenerational inheritance of adult-onset disease through the female germline. PLoS ONE 2014, 9:e102091.
121. Skinner M.K. Endocrine disruptor induction of epigenetic transgenerational inheritance of disease. Mol. Cell. Endocrinol. 2014, 398:4-12.