Abstract
Successful fertilization and early development depend on the quality of the ovulated oocyte. Our knowledge lacks of links between morphological aspects described and the genomic and epigenomic features that work in the backstage. Bringing to light these links would permit the identification of molecular markers of the oocyte developmental competence. In this chapter, we will review our current understanding of the changes that occur to the oocyte epigenetic signature during folliculogenesis and in mature oocytes.
Keywords
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McKenzie LJ, Pangas SA, Carson SA, Kovanci E, Cisneros P, Buster JE, Amato P, Matzuk MM. Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF. Hum Reprod. 2004;19:2869–74.
Zhang X, Jafari N, Barnes RB, Confino E, Milad M, Kazer RR. Studies of gene expression in human cumulus cells indicate pentraxin 3 as a possible marker for oocyte quality. Fertil Steril. 2005;83 Suppl 1:1169–79.
Cillo F, Brevini TA, Antonini S, Paffoni A, Ragni G, Gandolfi F. Association between human oocyte developmental competence and expression levels of some cumulus genes. Reproduction. 2007;134:645–50.
Assou S, Haouzi D, Mahmoud K, Aouacheria A, Guillemin Y, Pantesco V, Rème T, Dechaud H, De Vos J, Hamamah S. A non-invasive test for assessing embryo potential by gene expression profiles of human cumulus cells: a proof of concept study. Mol Hum Reprod. 2008;14:711–9.
van Montfoort AP, Geraedts JP, Dumoulin JC, Stassen AP, Evers JL, Ayoubi TA. Differential gene expression in cumulus cells as a prognostic indicator of embryo viability: a microarray analysis. Mol Hum Reprod. 2008;14:157–68.
Hamel M, Dufort I, Robert C, Gravel C, Leveille MC, Leader A, Sirard MA. Identification of differentially expressed markers in human follicular cells associated with competent oocytes. Hum Reprod. 2008;23:1118–27.
Regassa A, Rings F, Hoelker M, Cinar U, Tholen E, Looft C, Schellander K, Tesfaye D. Transcriptome dynamics and molecular cross-talk between bovine oocyte and its companion cumulus cells. BMC Genomics. 2011;12:57. 1471-2164-12-57.
Chiu TT, Rogers MS, Law EL, Briton-Jones CM, Cheung LP, Haines CJ. Follicular fluid and serum concentrations of myo-inositol in patients undergoing IVF: relationship with oocyte quality. Hum Reprod. 2002;17:1591–6.
Chang CL, Wang TH, Horng SG, Wu HM, Wang HS, Soong YK. The concentration of inhibin B in follicular fluid: relation to oocyte maturation and embryo development. Hum Reprod. 2002;17:1724–8.
Takahashi C, Fujito A, Kazuka M, Sugiyama R, Ito H, Isaka K. Anti-müllerian hormone substance from follicular fluid is positively associated with success in oocyte fertilization during in vitro fertilization. Fertil Steril. 2008;89:586–91.
Hazout A, Bouchard P, Seifer DB, Aussage P, Junca AM, Cohen-Bacrie P. Serum antimüllerian hormone/müllerian-inhibiting substance appears to be a more discriminatory marker of assisted reproductive technology outcome than follicle-stimulating hormone, inhibin B, or estradiol. Fertil Steril. 2004;82:1323–9.
Chenette PE, Sauer MV, Paulson RJ. Very high serum estradiol levels are not detrimental to clinical outcome of in vitro fertilization. Fertil Steril. 1990;54:858–63.
Sharara FI, McClamrock HD. Ratio of oestradiol concentration on the day of human chorionic gonadotrophin administration to mid-luteal oestradiol concentration is predictive of in-vitro fertilization outcome. Hum Reprod. 1999;14:2777–82.
Simón C, Cano F, Valbuena D, Remohí J, Pellicer A. Clinical evidence for a detrimental effect on uterine receptivity of high serum oestradiol concentrations in high and normal responder patients. Hum Reprod. 1995;10:2432–7.
Pellicer A, Valbuena D, Cano F, Remohí J, Simón C. Lower implantation rates in high responders: evidence for an altered endocrine milieu during the preimplantation period. Fertil Steril. 1996;65:1190–5.
Hasegawa J, Yanaihara A, Iwasaki S, Otsuka Y, Negishi M, Akahane T, Okai T. Reduction of progesterone receptor expression in human cumulus cells at the time of oocyte collection during IVF is associated with good embryo quality. Hum Reprod. 2005;20:2194–200.
Dumollard R, Duchen M, Carroll J. The role of mitochondrial function in the oocyte and embryo. Curr Top Dev Biol. 2007;77:21–49. S0070-2153(06)77002-8.
Pikó L, Matsumoto L. Number of mitochondria and some properties of mitochondrial DNA in the mouse egg. Dev Biol. 1976;49:1–10. 0012-1606(76)90253-0.
May-Panloup P, Chretien MF, Malthiery Y, Reynier P. Mitochondrial DNA in the oocyte and the developing embryo. Curr Top Dev Biol. 2007;77:51–83. S0070-2153(06)77003-X.
Shoubridge EA, Wai T. Mitochondrial DNA and the mammalian oocyte. Curr Top Dev Biol. 2007;77:87–111. S0070-2153(06)77004-1.
Brenner CA, Kubisch HM, Pierce KE. Role of the mitochondrial genome in assisted reproductive technologies and embryonic stem cell-based therapeutic cloning. Reprod Fertil Dev. 2004;16:743–51. RD04107.
Van Blerkom J, Davis P, Thalhammer V. Regulation of mitochondrial polarity in mouse and human oocytes: the influence of cumulus derived nitric oxide. Mol Hum Reprod. 2008;14:431–44.
Van Blerkom J. Mitochondria in early mammalian development. Semin Cell Dev Biol. 2009;20:354–64. S1084-9521(08)00151-1.
Zeng HT, Ren Z, Yeung WS, Shu YM, Xu YW, Zhuang GL, Liang XY. Low mitochondrial DNA and ATP contents contribute to the absence of birefringent spindle imaged with PolScope in in vitro matured human oocytes. Hum Reprod. 2007;22:1681–6.
Calarco PG. Polarization of mitochondria in the unfertilized mouse oocyte. Dev Genet. 1995;16:36–43.
Dumollard R, Duchen M, Sardet C. Calcium signals and mitochondria at fertilisation. Semin Cell Dev Biol. 2006;17:314–23.
Nagai S, Mabuchi T, Hirata S, Shoda T, Kasai T, Yokota S, Shitara H, Yonekawa H, Hoshi K. Oocyte mitochondria: strategies to improve embryogenesis. Hum Cell. 2004;17:195–201.
Van Blerkom J, Runner MN. Mitochondrial reorganization during resumption of arrested meiosis in the mouse oocyte. Am J Anat. 1984;171:335–55.
Hughes G, Murphy MP, Ledgerwood EC. Mitochondrial reactive oxygen species regulate the temporal activation of nuclear factor kappaB to modulate tumour necrosis factor-induced apoptosis: evidence from mitochondria-targeted antioxidants. Biochem J. 2005;389:83–9.
Nemoto S, Takeda K, Yu ZX, Ferrans VJ, Finkel T. Role for mitochondrial oxidants as regulators of cellular metabolism. Mol Cell Biol. 2000;20:7311–8.
Fratelli M, Goodwin LO, Ørom UA, Lombardi S, Tonelli R, Mengozzi M, Ghezzi P. Gene expression profiling reveals a signaling role of glutathione in redox regulation. Proc Natl Acad Sci USA. 2005;102:13998–4003.
Kim MR, Tilly JL. Current concepts in Bcl-2 family member regulation of female germ cell development and survival. Biochim Biophys Acta. 2004;1644:205–10.
Liu L, Trimarchi JR, Keefe DL. Involvement of mitochondria in oxidative stress-induced cell death in mouse zygotes. Biol Reprod. 2000;62:1745–53.
Ubaldi F, Rienzi L. Morphological selection of gametes. Placenta. 2008;29(Suppl B):115–20.
De Sutter P, Dozortsev D, Qian C, Dhont M. Oocyte morphology does not correlate with fertilization rate and embryo quality after intracytoplasmic sperm injection. Hum Reprod. 1996;11:595–7.
Xia P. Intracytoplasmic sperm injection: correlation of oocyte grade based on polar body, perivitelline space and cytoplasmic inclusions with fertilization rate and embryo quality. Hum Reprod. 1997;12:1750–5.
Balaban B, Urman B, Sertac A, Alatas C, Aksoy S, Mercan R. Oocyte morphology does not affect fertilization rate, embryo quality and implantation rate after intracytoplasmic sperm injection. Hum Reprod. 1998;13:3431–3.
Balaban B, Urman B. Effect of oocyte morphology on embryo development and implantation. Reprod Biomed Online. 2006;12:608–15.
Ebner T, Moser M, Tews G. Is oocyte morphology prognostic of embryo developmental potential after ICSI? Reprod Biomed Online. 2006;12:507–12.
Ebner T, Moser M, Shebl O, Sommerguber M, Tews G. Prognosis of oocytes showing aggregation of smooth endoplasmic reticulum. Reprod Biomed Online. 2008;16:113–8.
Mattson BA, Albertini DF. Oogenesis: chromatin and microtubule dynamics during meiotic prophase. Mol Reprod Dev. 1990;25:374–83.
Lefèvre B, Gougeon A, Nomé F, Testart J. In vivo changes in oocyte germinal vesicle related to follicular quality and size at mid-follicular phase during stimulated cycles in the cynomolgus monkey. Reprod Nutr Dev. 1989;29:523–31.
Mandl AM, Zuckerman S. The growth of the oocyte and follicle in the adult rat. J Endocrinol. 1952;8:126–32.
Crozet N. Effects of actinomycin D and cycloheximide on the nucleolar ultrastructure of porcine oocytes. Biol Cell. 1983;48:25–9.
Parfenov V, Potchukalina G, Dudina L, Kostyuchek D, Gruzova M. Human antral follicles: oocyte nucleus and the karyosphere formation (electron microscopic and autoradiographic data). Gamete Res. 1989;22:219–31.
Sui HS, Liu Y, Miao DQ, Yuan JH, Qiao TW, Luo MJ, Tan JH. Configurations of germinal vesicle (GV) chromatin in the goat differ from those of other species. Mol Reprod Dev. 2005;71:227–36.
Hinrichs K, Williams KA. Relationships among oocyte-cumulus morphology, follicular atresia, initial chromatin configuration, and oocyte meiotic competence in the horse. Biol Reprod. 1997;57:377–84.
Zuccotti M, Piccinelli A, Giorgi Rossi P, Garagna S, Redi CA. Chromatin organization during mouse oocyte growth. Mol Reprod Dev. 1995;41:479–85.
Zuccotti M, Giorgi Rossi P, Martinez A, Garagna S, Forabosco A, Redi CA. Meiotic and developmental competence of mouse antral oocytes. Biol Reprod. 1998;58:700–4.
Zuccotti M, Boiani M, Ponce R, Guizzardi S, Scandroglio R, Garagna S, Redi CA. Mouse Xist expression begins at zygotic genome activation and is timed by a zygotic clock. Mol Reprod Dev. 2002;61:14–20.
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;23:1377–84.
Pan GJ, Chang ZY, Schöler HR, Pei D. Stem cell pluripotency and transcription factor Oct4. Cell Res. 2002;12:321–9.
Adjaye J, Huntriss J, Herwig R, BenKahla A, Brink TC, Wierling C, Hultschig C, Groth D, Yaspo ML, Picton HM, Gosden RG, Lehrach H. Primary differentiation in the human blastocyst: comparative molecular portraits of inner cell mass and trophectoderm cells. Stem Cells. 2005;23:1514–25.
Babaie Y, Herwig R, Greber B, Brink TC, Wruck W, Groth D, Lehrach H, Burdon T, Adjaye J. Analysis of Oct4-dependent transcriptional networks regulating self-renewal and pluripotency in human embryonic stem cells. Stem Cells. 2007;25:500–10.
Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663–76.
Payer B, Saitou M, Barton SC, Thresher R, Dixon JP, Zahn D, Colledge WH, Carlton MB, Nakano T, Surani MA. Stella is a maternal effect gene required for normal early development in mice. Curr Biol. 2003;13:2110–7.
Wu X, Viveiros MM, Eppig JJ, Bai Y, Fitzpatrick SL, Matzuk MM. Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat Genet. 2003;33:187–91.
Burns KH, Viveiros MM, Ren Y, Wang P, DeMayo FJ, Frail DE, Eppig JJ, Matzuk MM. Roles of NPM2 in chromatin and nucleolar organization in oocytes and embryos. Science. 2003;300:633–6.
Bultman SJ, Gebuhr TC, Pan H, Svoboda P, Schultz RM, Magnuson T. Maternal BRG1 regulates zygotic genome activation in the mouse. Genes Dev. 2006;20:1744–54.
Foygel K, Choi B, Jun S, Leong DE, Lee A, Wong CC, Zuo E, Eckart M, Reijo Pera RA, Wong WH, Yao MW. A novel and critical role for Oct4 as a regulator of the maternal-embryonic transition. PLoS One. 2008;3:e4109.
Li L, Zheng P, Dean J. Maternal control of early mouse development. Development. 2010;137:859–70.
Zuccotti M, Merico V, Sacchi L, Bellone M, Brink TC, Bellazzi R, Stefanelli M, Redi CA, Garagna S, Adjaye J. Maternal Oct-4 is a potential key regulator of the developmental competence of mouse oocytes. BMC Dev Biol. 2008;8:97.
Zuccotti M, Merico V, Redi CA, Bellazzi R, Adjaye J, Garagna S. Role of Oct-4 during acquisition of developmental competence in mouse oocyte. Reprod Biomed Online. 2009;19 Suppl 3:57–62.
Martín-de-Lara F, Sánchez-Aparicio P, Arias de la Fuente C, Rey-Campos J. Biological effects of FoxJ2 over-expression. Transgenic Res. 2008;17:1131–41.
Levasseur DN, Wang J, Dorschner MO, Stamatoyannopoulos JA, Orkin SH. Oct4 dependence of chromatin structure within the extended Nanog locus in ES cells. Genes Dev. 2008;22:575–80.
Campbell PA, Perez-Iratxeta C, Andrade-Navarro MA, Rudnicki MA. Oct4 targets regulatory nodes to modulate stem cell function. PLoS One. 2007;2:e553.
Zuccotti M, Merico V, Bellone M, Mulas F, Sacchi L, Rebuzzini P, Prigione A, Redi CA, Bellazzi R, Adjaye J, Garagna S. Gatekeeper of pluripotency: a common Oct4 transcriptional network operates in mouse eggs and embryonic stem cells. BMC Genomics. 2011;12:1–13.
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;129:1983–93.
Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, Li E, Sasaki H. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature. 2004;429:900–3.
Kageyama S, Liu H, Kaneko N, Ooga M, Nagata M, Aoki F. Alterations in epigenetic modifications during oocyte growth in mice. Reproduction. 2007;133:85–94.
Smallwood SA, Tomizawa S, Krueger F, Ruf N, Carli N, Segonds-Pichon A, Sato S, Hata K, Andrews SR, Kelsey G. Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat Genet. 2011;43:811–4.
Obata Y, Kono T. Maternal primary imprinting is established at a specific time for each gene throughout oocyte growth. J Biol Chem. 2002;277:5285–9.
Lucifero D, Mann MR, Bartolomei MS, Trasler JM. Gene-specific timing and epigenetic memory in oocyte imprinting. Hum Mol Genet. 2004;13:839–49.
Lucifero D, La Salle S, Bourc’his D, Martel J, Bestor TH, Trasler JM. Coordinate regulation of DNA methyltransferase expression during oogenesis. BMC Dev Biol. 2007;7:36.
Bourc’his D, Xu GL, Lin CS, Bollman B, Bestor TH. Dnmt3L and the establishment of maternal genomic imprints. Science. 2001;294:2536–9.
Kim JM, Liu H, Tazaki M, Nagata M, Aoki F. Changes in histone acetylation during mouse oocyte meiosis. J Cell Biol. 2003;162:37–46.
De La Fuente R, Viveiros MM, Burns KH, Adashi EY, Matzuk MM, Eppig JJ. 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;275:447–58.
Zuccotti M, Bellone M, Longo F, Redi CA, Garagna S. Fully-mature antral mouse oocytes are transcriptionally silent but their heterochromatin maintains a transcriptional permissive histone acetylation profile. J Assist Reprod Genet. 2011;28(12):1193–6.
Probst AV, Okamoto I, Casanova M, El Marjou F, Le Baccon P, Almouzni G. A strand-specific burst in transcription of pericentric satellites is required for chromocenter formation and early mouse development. Dev Cell. 2010;19:625–38.
Andreu-Vieyra CV, Chen R, Agno JE, Glaser S, Anastassiadis K, Stewart AF, Matzuk MM. MLL2 is required in oocytes for bulk histone 3 lysine 4 trimethylation and transcriptional silencing. PLoS Biol. 2010;8:e1000453.
Schultz RM. The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Hum Reprod Update. 2002;8:323–31.
Huarte J, Stutz A, O’Connell ML, Gubler P, Belin D, Darrow AL, Strickland S, Vassalli JD. Transient translational silencing by reversible mRNA deadenylation. Cell. 1992;69:1021–30.
Gu W, Tekur S, Reinbold R, Eppig JJ, Choi YC, Zheng JZ, Murray MT, Hecht NB. Mammalian male and female germ cells express a germ cell-specific Y-Box protein, MSY2. Biol Reprod. 1998;59:1266–74.
Davies HG, Giorgini F, Fajardo MA, Braun RE. A sequence-specific RNA binding complex expressed in murine germ cells contains MSY2 and MSY4. Dev Biol. 2000;221:87–100.
Rana TM. Illuminating the silence: understanding the structure and function of small RNAs. Nat Rev Mol Cell Biol. 2007;8:23–36.
Tang F, Kaneda M, O’Carroll D, Hajkova P, Barton SC, Sun YA, Lee C, Tarakhovsky A, Lao K, Surani MA. Maternal microRNAs are essential for mouse zygotic development. Genes Dev. 2007;21:644–8.
Amanai M, Brahmajosyula M, Perry AC. A restricted role for sperm-borne microRNAs in mammalian fertilization. Biol Reprod. 2006;75:877–84.
He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, Powers S, Cordon-Cardo C, Lowe SW, Hannon GJ, Hammond SM. A microRNA polycistron as a potential human oncogene. Nature. 2005;435:828–33.
O’Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Myc-regulated microRNAs modulate E2F1 expression. Nature. 2005;435:839–43.
Hamatani T, Carter MG, Sharov AA, Ko MS. Dynamics of global gene expression changes during mouse preimplantation development. Dev Cell. 2004;6:117–31.
Gangaraju VK, Lin H. MicroRNAs: key regulators of stem cells. Nat Rev Mol Cell Biol. 2009;10:116–25.
Xu N, Papagiannakopoulos T, Pan G, Thomson JA, Kosik KS. MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell. 2009;137:647–58.
Wassarman PM. The mammalian ovum. In: Knobil E, Neill J, Challis JRG, De Kretser DM, Pfaff DW, Richards JS, Plant TM, Wasserman PM, editors. The physiology of reproduction. New York: Raven Press, Ltd; 1988. p. 69.
Jaffe LA, Norris RP, Freudzon M, Ratzan WJ, Mehlmann LM. Microinjection of follicle-enclosed mouse oocytes. Methods Mol Biol. 2009;518:157–73.
Acknowledgments
We thank the following organizations for support: UNIPV-Regione Lombardia, Fondazione Alma Mater Ticinensis, Fondazione I.R.C.C.S. Policlinico San Matteo, and “Bando Giovani Ricercatori 2007” to C.A.R.
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Zuccotti, M., Merico, V., Redi, C.A., Garagna, S. (2013). An Epigenomic Biography of the Mammalian Oocyte. In: Coticchio, G., Albertini, D., De Santis, L. (eds) Oogenesis. Springer, London. https://doi.org/10.1007/978-0-85729-826-3_10
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