What does it take to make a developmentally competent mammalian egg?

BACKGROUND A limitation to our ability to distinguish between developmentally competent and incompetent eggs is our still only partial knowledge of the critical features that are needed to make a good egg and when during oogenesis these specific characteristics are acquired. The main objective of this review is to summarize the results of areas of investigation that are contributing to our still inadequate understanding of the molecular aspects of making developmentally competent eggs. METHODS For each area discussed, a systematic search was made using PubMed. The search was without temporal limits but mainly yielded publications between 1982-1999 (23%) and 2000-2011 (77%). RESULTS Taking an oocyte-centred view, we describe throughout folliculogenesis: (i) the factors that regulate oocyte growth; (ii) the role of oocyte-cumulus cell dialogue; (iii) the epigenetic organization of the oocyte genome and (iv) the storage and regulation of maternal RNAs. CONCLUSIONS The multifaceted complex of factors involved in oocyte growth constitutes the backbone on which oocyte developmental competence is built up. Operating behind the expression of these factors is a specific epigenetic signature established during oogenesis, but our knowledge is only approximate and major efforts will be required for more accurate analyses at specific gene loci. The growing research on small silencing RNAs during oogenesis and early oocyte development is revealing these molecules' critical role in mRNA degradation. Our next challenge will be to dissect the complex interactions among the different molecular players identified and to establish the presence of functional links among these factors.

[1]  G. Woude,et al.  The c-mos proto-oncogene product is a cytostatic factor responsible for meiotic arrest in vertebrate eggs , 1989, Nature.

[2]  Michael Q. Zhang,et al.  Critical roles for Dicer in the female germline. , 2007, Genes & development.

[3]  E. Telfer,et al.  How to make a good oocyte: an update on in-vitro models to study follicle regulation. , 2003, Human reproduction update.

[4]  E. Li,et al.  Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting , 2004, Nature.

[5]  J. Juengel,et al.  Growth Differentiation Factor 9 and Bone Morphogenetic Protein 15 Are Essential for Ovarian Follicular Development in Sheep1 , 2002, Biology of reproduction.

[6]  F. Aoki,et al.  Contribution of the oocyte nucleus and cytoplasm to the determination of meiotic and developmental competence in mice. , 2008, Human reproduction.

[7]  T. Bestor,et al.  The DNA methyltransferases of mammals. , 2000, Human molecular genetics.

[8]  C. Sellitto,et al.  Oocyte-granulosa cell heterologous gap junctions are required for the coordination of nuclear and cytoplasmic meiotic competence. , 2000, Developmental biology.

[9]  Shu Liu,et al.  Activation of dormant ovarian follicles to generate mature eggs , 2010, Proceedings of the National Academy of Sciences.

[10]  Lisa M Mehlmann,et al.  Focus on Meiosis Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation , 2005 .

[11]  L. Rienzi,et al.  Morphological selection of gametes. , 2008, Placenta.

[12]  J. M. Thomson,et al.  Argonaute2 Is the Catalytic Engine of Mammalian RNAi , 2004, Science.

[13]  R. Schultz,et al.  The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. , 2002, Human reproduction update.

[14]  Fugaku Aoki,et al.  Degradation of maternal mRNA in mouse embryos: Selective degradation of specific mRNAs after fertilization , 2005, Molecular reproduction and development.

[15]  G. Macchiarelli,et al.  Meiotic spindle configuration is differentially influenced by FSH and epidermal growth factor during in vitro maturation of mouse oocytes. , 2006, Human reproduction.

[16]  F. Sharara,et al.  High estradiol levels and high oocyte yield are not detrimental to in vitro fertilization outcome. , 1999, Fertility and sterility.

[17]  S. Zuckerman,et al.  The growth of the oocyte and follicle in the adult rat. , 1952, The Journal of endocrinology.

[18]  Martin M Matzuk,et al.  Roles of NPM2 in Chromatin and Nucleolar Organization in Oocytes and Embryos , 2003, Science.

[19]  W. Reik Stability and flexibility of epigenetic gene regulation in mammalian development , 2007, Nature.

[20]  R. Gilchrist,et al.  Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice. , 2007, Human reproduction.

[21]  R. Gilchrist,et al.  Role of oocyte-secreted growth differentiation factor 9 in the regulation of mouse cumulus expansion. , 2005, Endocrinology.

[22]  A. C. Perry,et al.  A Restricted Role for Sperm-Borne MicroRNAs in Mammalian Fertilization1 , 2006, Biology of reproduction.

[23]  Thomas Ebner,et al.  Prognosis of oocytes showing aggregation of smooth endoplasmic reticulum. , 2008, Reproductive biomedicine online.

[24]  Carolina Perez-Iratxeta,et al.  Oct4 Targets Regulatory Nodes to Modulate Stem Cell Function , 2007, PloS one.

[25]  A. Gansmuller,et al.  Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Bert W O'Malley,et al.  GCNF‐dependent repression of BMP‐15 and GDF‐9 mediates gamete regulation of female fertility , 2003, The EMBO journal.

[27]  U. Vitt,et al.  In vivo treatment with GDF-9 stimulates primordial and primary follicle progression and theca cell marker CYP17 in ovaries of immature rats. , 2000, Endocrinology.

[28]  A. Gougeon,et al.  In vivo changes in oocyte germinal vesicle related to follicular quality and size at mid-follicular phase during stimulated cycles in the cynomolgus monkey. , 1989, Reproduction, nutrition, development.

[29]  Ching-Chien Chang,et al.  A maternal store of macroH2A is removed from pronuclei prior to onset of somatic macroH2A expression in preimplantation embryos. , 2005, Developmental biology.

[30]  H. Schatten,et al.  Mechanisms regulating oocyte meiotic resumption: roles of mitogen-activated protein kinase. , 2007, Molecular endocrinology.

[31]  C. Allis,et al.  Translating the Histone Code , 2001, Science.

[32]  E. Seren,et al.  Maternal chromatin remodeling during maturation and after fertilization in mouse oocytes , 2004, Molecular reproduction and development.

[33]  S. Soyal,et al.  FIGalpha, a germ cell-specific transcription factor required for ovarian follicle formation. , 2000, Development.

[34]  K. Hinrichs,et al.  Relationships among oocyte-cumulus morphology, follicular atresia, initial chromatin configuration, and oocyte meiotic competence in the horse. , 1997, Biology of reproduction.

[35]  T. Tsukamoto,et al.  Sox2 expression in human stomach adenocarcinomas with gastric and gastric‐and‐intestinal‐mixed phenotypes , 2005, Histopathology.

[36]  M. Skinner,et al.  Bone Morphogenetic Protein-4 Acts as an Ovarian Follicle Survival Factor and Promotes Primordial Follicle Development1 , 2003, Biology of reproduction.

[37]  M. Blasco,et al.  Telomere lengthening early in development , 2007, Nature Cell Biology.

[38]  D. Peeper,et al.  KLF4, p21 and context-dependent opposing forces in cancer , 2006, Nature Reviews Cancer.

[39]  M. Matzuk,et al.  Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. , 2001, Molecular endocrinology.

[40]  L. Cantley,et al.  New insights into tumor suppression: PTEN suppresses tumor formation by restraining the phosphoinositide 3-kinase/AKT pathway. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Martin M Matzuk,et al.  NOBOX Deficiency Disrupts Early Folliculogenesis and Oocyte-Specific Gene Expression , 2004, Science.

[42]  Y. Tsunoda,et al.  Role of Histone Acetylation in Reprogramming of Somatic Nuclei Following Nuclear Transfer1 , 2006, Biology of reproduction.

[43]  Oliver H. Tam,et al.  Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes , 2008, Nature.

[44]  C. Migné,et al.  Chromatin configuration and transcriptional control in human and mouse oocytes , 2003, Molecular reproduction and development.

[45]  F. Aoki,et al.  Regulation of histone acetylation during meiotic maturation in mouse oocytes , 2004, Molecular reproduction and development.

[46]  T. Okai,et al.  High concentrations of lactoferrin in the follicular fluid correlate with embryo quality during in vitro fertilization cycles. , 2007, Fertility and sterility.

[47]  W. Reik,et al.  How imprinting centres work , 2006, Cytogenetic and Genome Research.

[48]  M. Matzuk,et al.  The Art and Artifact of GDF9 Activity: Cumulus Expansion and the Cumulus Expansion-Enabling Factor1 , 2005, Biology of reproduction.

[49]  M. Bartolomei,et al.  Gene-specific timing and epigenetic memory in oocyte imprinting. , 2004, Human molecular genetics.

[50]  M. Verlhac,et al.  Interactions between chromosomes, microfilaments and microtubules revealed by the study of small GTPases in a big cell, the vertebrate oocyte , 2008, Molecular and Cellular Endocrinology.

[51]  J. Juengel,et al.  Control of ovarian follicular development to the gonadotrophin-dependent phase: a 2006 perspective. , 2007, Society of Reproduction and Fertility supplement.

[52]  G. Pan,et al.  MicroRNA-145 Regulates OCT4, SOX2, and KLF4 and Represses Pluripotency in Human Embryonic Stem Cells , 2009, Cell.

[53]  T. Bestor,et al.  Methylation dynamics of imprinted genes in mouse germ cells. , 2002, Genomics.

[54]  H. Schöler,et al.  Differential expression of the Oct-4 transcription factor during mouse germ cell differentiation , 1998, Mechanisms of Development.

[55]  Z. Nagy,et al.  Rapid elimination of the histone variant MacroH2A from somatic cell heterochromatin after nuclear transfer. , 2010, Cellular reprogramming.

[56]  M. Skinner Regulation of primordial follicle assembly and development. , 2005, Human reproduction update.

[57]  R. Gilchrist,et al.  Disruption of Bidirectional Oocyte-Cumulus Paracrine Signaling During In Vitro Maturation Reduces Subsequent Mouse Oocyte Developmental Competence1 , 2009, Biology of reproduction.

[58]  Rabindranath De La Fuente,et al.  Chromatin modifications in the germinal vesicle (GV) of mammalian oocytes , 2006 .

[59]  S. Ying Inhibins, activins, and follistatins: gonadal proteins modulating the secretion of follicle-stimulating hormone. , 1988, Endocrine reviews.

[60]  Jing-He Tan,et al.  Chromatin configurations in the germinal vesicle of mammalian oocytes. , 2009, Molecular human reproduction.

[61]  G. Almouzni,et al.  Mouse centric and pericentric satellite repeats form distinct functional heterochromatin , 2004, The Journal of cell biology.

[62]  D. Levens,et al.  Marking of active genes on mitotic chromosomes , 1997, Nature.

[63]  H. Schatten,et al.  Cyclic adenosine 3',5'-monophosphate-dependent activation of mitogen-activated protein kinase in cumulus cells is essential for germinal vesicle breakdown of porcine cumulus-enclosed oocytes. , 2005, Endocrinology.

[64]  K. Sugiura,et al.  Fibroblast Growth Factors and Epidermal Growth Factor Cooperate with Oocyte-Derived Members of the TGFbeta Superfamily to Regulate Spry2 mRNA Levels in Mouse Cumulus Cells1 , 2009, Biology of reproduction.

[65]  Martin M Matzuk,et al.  Major chromatin remodeling in the germinal vesicle (GV) of mammalian oocytes is dispensable for global transcriptional silencing but required for centromeric heterochromatin function. , 2004, Developmental biology.

[66]  E. Li,et al.  Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. , 2002, Development.

[67]  S. Berger The complex language of chromatin regulation during transcription , 2007, Nature.

[68]  R. Aitken,et al.  CXCR4/SDF1 interaction inhibits the primordial to primary follicle transition in the neonatal mouse ovary. , 2006, Developmental biology.

[69]  M. Matzuk,et al.  Hormonal control of somatic cell oocyte interactions during ovarian follicle development , 2004, Molecular reproduction and development.

[70]  R. Gilchrist,et al.  Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins , 2005, Journal of Cell Science.

[71]  E. McLaughlin,et al.  Kit ligand and c-Kit have diverse roles during mammalian oogenesis and folliculogenesis. , 2006, Molecular human reproduction.

[72]  J. Dumoulin,et al.  Differential gene expression in cumulus cells as a prognostic indicator of embryo viability: a microarray analysis. , 2008, Molecular human reproduction.

[73]  N. Beaujean,et al.  Differential transcriptional activity associated with chromatin configuration in fully grown mouse germinal vesicle oocytes. , 1999, Biology of reproduction.

[74]  W. Gu,et al.  Mammalian male and female germ cells express a germ cell-specific Y-Box protein, MSY2. , 1998, Biology of reproduction.

[75]  X. Chen,et al.  The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells , 2006, Nature Genetics.

[76]  J. Renard,et al.  Differential H4 acetylation of paternal and maternal chromatin precedes DNA replication and differential transcriptional activity in pronuclei of 1-cell mouse embryos. , 1997, Development.

[77]  A. C. Perry,et al.  Second meiotic arrest and exit in frogs and mice , 2008, EMBO reports.

[78]  Y. Sakaki,et al.  Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes , 2008, Nature.

[79]  M. Rogers,et al.  Follicular fluid and serum concentrations of myo-inositol in patients undergoing IVF: relationship with oocyte quality. , 2002, Human reproduction.

[80]  J. D. Vos,et al.  A non-invasive test for assessing embryo potential by gene expression profiles of human cumulus cells: a proof of concept study. , 2008, Molecular human reproduction.

[81]  Jing-He Tan,et al.  Configurations of germinal vesicle (GV) chromatin in the goat differ from those of other species , 2005, Molecular reproduction and development.

[82]  T. Bestor,et al.  Dnmt3L and the Establishment of Maternal Genomic Imprints , 2001, Science.

[83]  Thomas Ebner,et al.  Is oocyte morphology prognostic of embryo developmental potential after ICSI? , 2006, Reproductive biomedicine online.

[84]  N. Crozet Effects of actinomycin D and cycloheximide on the nucleolar ultrastructure of porcine oocytes , 1983, Biology of the cell.

[85]  F. Longo,et al.  Development of cortical polarity in mouse eggs: involvement of the meiotic apparatus. , 1985, Developmental biology.

[86]  L. Fanti,et al.  HP1: a functionally multifaceted protein. , 2008, Current opinion in genetics & development.

[87]  G. Reimer,et al.  Heterochromatin protein HP1Hsbeta (p25beta) and its localization with centromeres in mitosis. , 1997, Chromosoma.

[88]  Benjamin A. Garcia,et al.  Regulation of HP1–chromatin binding by histone H3 methylation and phosphorylation , 2005, Nature.

[89]  Qing-Yuan Sun,et al.  Involvement of Mitogen-Activated Protein Kinase Cascade During Oocyte Maturation and Fertilization in Mammals1 , 2004, Biology of reproduction.

[90]  P. Mermillod,et al.  Differential regulation of abundance and deadenylation of maternal transcripts during bovine oocyte maturation in vitro and in vivo , 2007, BMC Developmental Biology.

[91]  H. Peters,et al.  RNA SYNTHESIS IN THE MOUSE OOCYTE , 1974, The Journal of cell biology.

[92]  M. Skinner,et al.  Kit-ligand/stem cell factor induces primordial follicle development and initiates folliculogenesis. , 1999, Endocrinology.

[93]  R. Gatti,et al.  Nuclear localization of NORs and centromeres in mouse oocytes during folliculogenesis , 2003, Molecular reproduction and development.

[94]  K. Luger,et al.  Structural Characterization of the Histone Variant macroH2A , 2005, Molecular and Cellular Biology.

[95]  T. Bestor,et al.  Coordinate regulation of DNA methyltransferase expression during oogenesis , 2007, BMC Developmental Biology.

[96]  C. Allis,et al.  Dynamic alterations of specific histone modifications during early murine development , 2004, Journal of Cell Science.

[97]  R. Rempel,et al.  Changes in state of adenylation and time course of degradation of maternal mRNAs during oocyte maturation and early embryonic development in the mouse. , 1988, Developmental biology.

[98]  S. Cecconi,et al.  Mouse antral oocytes regulate preantral granulosa cell ability to stimulate oocyte growth in vitro. , 2001, Developmental biology.

[99]  M. Matzuk,et al.  Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility , 1997, Nature Genetics.

[100]  Y. Allory,et al.  Localization and phosphorylation of HP1 proteins during the cell cycle in mammalian cells , 1999, Chromosoma.

[101]  M. Matzuk,et al.  Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition , 2003, Nature Genetics.

[102]  B M Turner,et al.  Histone acetylation and an epigenetic code. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[103]  G. Montgomery,et al.  Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner , 2000, Nature Genetics.

[104]  M. Matzuk,et al.  Paracrine actions of growth differentiation factor-9 in the mammalian ovary. , 1999, Molecular endocrinology.

[105]  C B Harley,et al.  Telomere length predicts replicative capacity of human fibroblasts. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[106]  K. Sugiura,et al.  Regulation of Pcsk6 Expression During the Preantral to Antral Follicle Transition in Mice: Opposing Roles of FSH and Oocytes1 , 2008, Biology of reproduction.

[107]  B. Hogan,et al.  The mouse forkhead gene Foxc1 is required for primordial germ cell migration and antral follicle development. , 2006, Developmental biology.

[108]  A. C. Perry Induced pluripotency and cellular alchemy , 2006, Nature Biotechnology.

[109]  Petr Svoboda,et al.  Maternal BRG1 regulates zygotic genome activation in the mouse. , 2006, Genes & development.

[110]  M. Matzuk,et al.  Anti-Müllerian Hormone Attenuates the Effects of FSH on Follicle Development in the Mouse Ovary. , 2001, Endocrinology.

[111]  Guocheng Lan,et al.  Coculture with cumulus cells improves maturation of mouse oocytes denuded of the cumulus oophorus: observations of nuclear and cytoplasmic events. , 2008, Fertility and sterility.

[112]  Y. Obata,et al.  Maternal Primary Imprinting Is Established at a Specific Time for Each Gene throughout Oocyte Growth* , 2002, The Journal of Biological Chemistry.

[113]  M. Surani,et al.  stella Is a Maternal Effect Gene Required for Normal Early Development in Mice , 2003, Current Biology.

[114]  G. Zielhuis,et al.  Antimüllerian hormone predicts ovarian responsiveness, but not embryo quality or pregnancy, after in vitro fertilization or intracyoplasmic sperm injection. , 2007, Fertility and sterility.

[115]  R. Bellazzi,et al.  Reproductive biology Oct4 regulates the expression of Stella and Foxj 2 at the Nanog locus : implications for the developmental competence of mouse oocytes , 2009 .

[116]  C. Redi,et al.  Chromatin organization during mouse oocyte growth , 1995, Molecular reproduction and development.

[117]  Koji Sugiura,et al.  Mouse Oocyte Control of Granulosa Cell Development and Function: Paracrine Regulation of Cumulus Cell Metabolism , 2009, Seminars in reproductive medicine.

[118]  R. Sullivan,et al.  Regulation of gap junctions in porcine cumulus-oocyte complexes: contributions of granulosa cell contact, gonadotropins, and lipid rafts. , 2009, Molecular endocrinology.

[119]  Seang Tan,et al.  Current perspective on primordial follicle cryopreservation and culture for reproductive medicine. , 2002, Human reproduction update.

[120]  A. Sharov,et al.  Dynamics of global gene expression changes during mouse preimplantation development. , 2004, Developmental cell.

[121]  R. Gatti,et al.  Three-dimensional localization and dynamics of centromeres in mouse oocytes during folliculogenesis , 2004, Journal of Molecular Histology.

[122]  M. Blasco,et al.  Telomere length predicts embryo fragmentation after in vitro fertilization in women--toward a telomere theory of reproductive aging in women. , 2005, American journal of obstetrics and gynecology.

[123]  J. Juengel,et al.  The cooperative effect of growth and differentiation factor-9 and bone morphogenetic protein (BMP)-15 on granulosa cell function is modulated primarily through BMP receptor II. , 2008, Endocrinology.

[124]  David F. Albertini,et al.  Growth differentiation factor-9 is required during early ovarian folliculogenesis , 1996, Nature.

[125]  R. Gilchrist,et al.  Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. , 2008, Human reproduction update.

[126]  R. Bellazzi,et al.  Maternal Oct-4 is a potential key regulator of the developmental competence of mouse oocytes , 2008, BMC Developmental Biology.

[127]  Maciej Meglicki,et al.  Constitutive heterochromatin during mouse oogenesis: The pattern of histone H3 modifications and localization of HP1α and HP1β proteins , 2008 .

[128]  B. Balaban,et al.  Oocyte morphology does not affect fertilization rate, embryo quality and implantation rate after intracytoplasmic sperm injection. , 1998, Human reproduction.

[129]  E. Miska,et al.  Maternal Argonaute 2 is essential for early mouse development at the maternal-zygotic transition. , 2008, Molecular biology of the cell.

[130]  J. Eppig,et al.  Oocyte control of ovarian follicular development and function in mammals. , 2001, Reproduction.

[131]  K. Song,et al.  Human Ku70 Interacts with Heterochromatin Protein 1α* , 2001, The Journal of Biological Chemistry.

[132]  S. Yamanaka,et al.  Induction of Pluripotent Stem Cells from Mouse Embryonic and Adult Fibroblast Cultures by Defined Factors , 2006, Cell.

[133]  Laura Fanti,et al.  Heterochromatin protein 1 (HP1) is associated with induced gene expression in Drosophila euchromatin , 2003, The Journal of cell biology.

[134]  J. Richards,et al.  New Signaling Pathways for Hormones and Cyclic Adenosine 3؅,5؅-monophosphate Action in Endocrine Cells , 2022 .

[135]  Maurizio Zuccotti,et al.  Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei , 1998, Nature.

[136]  P. Zhou,et al.  Factors affecting the in vitro action of cumulus cells on the maturing mouse oocytes , 2008, Molecular reproduction and development.

[137]  C. Robert,et al.  Identification of differentially expressed markers in human follicular cells associated with competent oocytes. , 2008, Human reproduction.

[138]  K. Sugiura,et al.  Mouse oocytes enable LH-induced maturation of the cumulus-oocyte complex via promoting EGF receptor-dependent signaling. , 2010, Molecular endocrinology.

[139]  T. Rana,et al.  Illuminating the silence: understanding the structure and function of small RNAs , 2007, Nature Reviews Molecular Cell Biology.

[140]  Z. Polański,et al.  Meiotic maturation of the mouse oocyte requires an equilibrium between cyclin B synthesis and degradation. , 2001, Developmental biology.

[141]  G. Kaplan,et al.  rRNA accumulation and protein synthetic patterns in growing mouse oocytes. , 1982, The Journal of experimental zoology.

[142]  M. Sairam,et al.  Dynamics of Ovarian Development in the FORKO Immature Mouse: Structural and Functional Implications for Ovarian Reserve1 , 2003, Biology of reproduction.

[143]  D. Belin,et al.  Transient translational silencing by reversible mRNA deadenylation , 1992, Cell.

[144]  S. Roy,et al.  Requirement for follicle-stimulating hormone action in the formation of primordial follicles during perinatal ovarian development in the hamster. , 2000, Endocrinology.

[145]  Andrew J. Bannister,et al.  Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain , 2001, Nature.

[146]  A. Mauro,et al.  Meiotic maturation of incompetent prepubertal sheep oocytes is induced by paracrine factor(s) released by gonadotropin-stimulated oocyte-cumulus cell complexes and involves mitogen-activated protein kinase activation. , 2008, Endocrinology.

[147]  D. Albertini,et al.  Oogenesis: Chromatin and microtubule dynamics during meiotic prophase , 1990, Molecular reproduction and development.

[148]  Basak Balaban,et al.  Effect of oocyte morphology on embryo development and implantation. , 2006, Reproductive biomedicine online.

[149]  F. Aoki,et al.  Changes in histone modifications during in vitro maturation of porcine oocytes , 2005, Molecular reproduction and development.

[150]  M. Skinner,et al.  Platelet-derived growth factor modulates the primordial to primary follicle transition. , 2006, Reproduction.

[151]  M. Kirsch‐Volders,et al.  Spindle formation, chromosome segregation and the spindle checkpoint in mammalian oocytes and susceptibility to meiotic error. , 2008, Mutation research.

[152]  J. Affourtit,et al.  Selective degradation of transcripts during meiotic maturation of mouse oocytes. , 2007, Developmental biology.

[153]  Kuang-Hung Cheng,et al.  Histone Deacetylases: Unique Players in Shaping the Epigenetic Histone Code , 2003, Annals of the New York Academy of Sciences.

[154]  R. Gilchrist,et al.  Simulated physiological oocyte maturation (SPOM): a novel in vitro maturation system that substantially improves embryo yield and pregnancy outcomes. , 2010, Human reproduction.

[155]  B. Vanderhyden,et al.  Interplay between paracrine signaling and gap junctional communication in ovarian follicles , 2005, Journal of Cell Science.

[156]  M. Skinner,et al.  Keratinocyte Growth Factor Acts as a Mesenchymal Factor That Promotes Ovarian Primordial to Primary Follicle Transition , 2005, Biology of reproduction.

[157]  H. Leese,et al.  The effect of glucose metabolism on murine follicle development and steroidogenesis in vitro. , 1994, Human reproduction.

[158]  S. Weitsman,et al.  Insulin-like growth factor-I regulation of luteinizing hormone (LH) receptor messenger ribonucleic acid expression and LH-stimulated signal transduction in rat ovarian theca-interstitial cells. , 1994, Biology of reproduction.

[159]  T. Kawai,et al.  LH-induced neuregulin 1 (NRG1) type III transcripts control granulosa cell differentiation and oocyte maturation. , 2011, Molecular endocrinology.

[160]  P. Chenette,et al.  Very high serum estradiol levels are not detrimental to clinical outcome of in vitro fertilization , 1991, Fertility and sterility.

[161]  Potential local regulatory functions of inhibins, activins and follistatin in the ovary. , 2001, Reproduction.

[162]  S. Lowe,et al.  A microRNA polycistron as a potential human oncogene , 2005, Nature.

[163]  R. Méndez,et al.  Translational control by CPEB: a means to the end , 2001, Nature Reviews Molecular Cell Biology.

[164]  Michael O. Dorschner,et al.  Oct4 dependence of chromatin structure within the extended Nanog locus in ES cells. , 2008, Genes & development.

[165]  S. Kageyama,et al.  Alterations in epigenetic modifications during oocyte growth in mice. , 2007, Reproduction.

[166]  Y. Soong,et al.  The concentration of inhibin B in follicular fluid: relation to oocyte maturation and embryo development. , 2002, Human reproduction.

[167]  G. Kidder,et al.  Differential contributions of connexin37 and connexin43 to oogenesis revealed in chimeric reaggregated mouse ovaries , 2005, Journal of Cell Science.

[168]  C. Combelles,et al.  Cellular basis for paracrine regulation of ovarian follicle development. , 2001, Reproduction.

[169]  B. Vanderhyden,et al.  Follicle-stimulating hormone regulates oocyte growth by modulation of expression of oocyte and granulosa cell factors. , 2005, Endocrinology.

[170]  S. E. Harris,et al.  The in vitro growth and maturation of follicles. , 2008, Reproduction.

[171]  Chie Takahashi,et al.  Anti-Müllerian hormone substance from follicular fluid is positively associated with success in oocyte fertilization during in vitro fertilization. , 2008, Fertility and sterility.

[172]  P. Donovan,et al.  Long-term proliferation of mouse primordial germ cells in culture , 1992, Nature.

[173]  M. Boiani,et al.  Gene expression and chromatin organization during mouse oocyte growth. , 1999, Developmental biology.

[174]  C. Redi,et al.  Chromatin organisation and nuclear architecture in growing mouse oocytes , 2005, Molecular and Cellular Endocrinology.

[175]  V. Liakopoulos,et al.  Estradiol and leptin as conditional prognostic IVF markers. , 2005, Reproduction.

[176]  N. Jafari,et al.  Studies of gene expression in human cumulus cells indicate pentraxin 3 as a possible marker for oocyte quality. , 2005, Fertility and sterility.

[177]  V. Parfenov,et al.  Human antral follicles: oocyte nucleus and the karyosphere formation (electron microscopic and autoradiographic data). , 1989, Gamete research.

[178]  W. S. Lee,et al.  Effect of Bone Morphogenetic Protein-7 on Folliculogenesis and Ovulation in the Rat1 , 2001, Biology of reproduction.

[179]  M. Matzuk,et al.  Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF. , 2004, Human reproduction.

[180]  R. Webb,et al.  Relationship Between Low-Molecular-Weight Insulin-Like Growth Factor-Binding Proteins, Caspase-3 Activity, and Oocyte Quality1 , 2005, Biology of reproduction.

[181]  Martin M Matzuk,et al.  Oogenesis requires germ cell-specific transcriptional regulators Sohlh1 and Lhx8. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[182]  Kathryn A. O’Donnell,et al.  c-Myc-regulated microRNAs modulate E2F1 expression , 2005, Nature.

[183]  J. Richter,et al.  CPEB controls oocyte growth and follicle development in the mouse , 2006, Development.

[184]  F. Otsuka,et al.  A negative feedback system between oocyte bone morphogenetic protein 15 and granulosa cell kit ligand: Its role in regulating granulosa cell mitosis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[185]  K. Wigglesworth,et al.  Printed in U.S.A. Copyright © 2002 by The Endocrine Society Mitogen-Activated Protein Kinase Activity in Cumulus Cells Is Essential for Gonadotropin-Induced Oocyte Meiotic Resumption and Cumulus Expansion in the Mouse , 2022 .

[186]  K. Sugiura,et al.  Estrogen promotes the development of mouse cumulus cells in coordination with oocyte-derived GDF9 and BMP15. , 2010, Molecular endocrinology.

[187]  Megan F. Cole,et al.  Core Transcriptional Regulatory Circuitry in Human Embryonic Stem Cells , 2005, Cell.

[188]  P. Patrizio,et al.  Molecular methods for selection of the ideal oocyte. , 2007, Reproductive biomedicine online.

[189]  J. Rey-Campos,et al.  Biological effects of FoxJ2 over-expression , 2008, Transgenic Research.

[190]  R. Braun,et al.  A sequence-specific RNA binding complex expressed in murine germ cells contains MSY2 and MSY4. , 2000, Developmental biology.

[191]  D. Vautier,et al.  Competent mouse oocytes isolated from antral follicles exhibit different chromatin organization and follow different maturation dynamics , 1993, Molecular reproduction and development.

[192]  R. Gilchrist,et al.  Oocyte-Secreted Factor Activation of SMAD 2/3 Signaling Enables Initiation of Mouse Cumulus Cell Expansion1 , 2007, Biology of reproduction.

[193]  P. Hunt,et al.  To err (meiotically) is human: the genesis of human aneuploidy , 2001, Nature Reviews Genetics.

[194]  P. Giorgi Rossi,et al.  Meiotic and developmental competence of mouse antral oocytes. , 1998, Biology of reproduction.

[195]  Karl Mechtler,et al.  Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins , 2001, Nature.

[196]  F. Aoki,et al.  Changes in histone acetylation during mouse oocyte meiosis , 2003, The Journal of cell biology.

[197]  K. Wigglesworth,et al.  Oocyte regulation of kit ligand expression in mouse ovarian follicles. , 1999, Developmental biology.

[198]  I. Wilmut,et al.  Viable offspring derived from fetal and adult mammalian cells , 1997, Nature.

[199]  M. Blasco,et al.  Irregular telomeres impair meiotic synapsis and recombination in mice. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[200]  S. Antonini,et al.  Association between human oocyte developmental competence and expression levels of some cumulus genes. , 2007, Reproduction.

[201]  C. Redi,et al.  Oogenesis specific genes (Nobox, Oct4, Bmp15, Gdf9, Oogenesin1 and Oogenesin2) are differentially expressed during natural and gonadotropin‐induced mouse follicular development , 2009, Molecular reproduction and development.

[202]  P. De Sutter,et al.  Oocyte morphology does not correlate with fertilization rate and embryo quality after intracytoplasmic sperm injection. , 1996, Human reproduction.

[203]  K. Wigglesworth,et al.  The mammalian oocyte orchestrates the rate of ovarian follicular development , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[204]  D. Angelov,et al.  The histone variant macroH2A interferes with transcription factor binding and SWI/SNF nucleosome remodeling. , 2003, Molecular cell.

[205]  J. E. Fortune,et al.  Follicular development: the role of the follicular microenvironment in selection of the dominant follicle. , 2004, Animal reproduction science.

[206]  S. Gaines,et al.  The Mouse , 2011 .

[207]  F. Tang,et al.  Maternal microRNAs are essential for mouse zygotic development. , 2007, Genes & development.

[208]  M. Matzuk,et al.  Insulin-like growth factor I regulates gonadotropin responsiveness in the murine ovary. , 1997, Molecular endocrinology.

[209]  F. Ding,et al.  Genomic Imprinting Disrupted by a Maternal Effect Mutation in the Dnmt1 Gene , 2001, Cell.

[210]  M. Poutanen,et al.  Normal prenatal but arrested postnatal sexual development of luteinizing hormone receptor knockout (LuRKO) mice. , 2001, Molecular endocrinology.

[211]  P. Govoni,et al.  The analysis of chromatin organisation allows selection of mouse antral oocytes competent for development to blastocyst , 2002, Zygote.

[212]  G. Macchiarelli,et al.  Granulosa cell-oocyte interactions. , 2004, European journal of obstetrics, gynecology, and reproductive biology.

[213]  J. Juengel,et al.  Effects of Immunization Against Bone Morphogenetic Protein 15 and Growth Differentiation Factor 9 on Ovulation Rate, Fertilization, and Pregnancy in Ewes1 , 2004, Biology of reproduction.

[214]  P Xia,et al.  Intracytoplasmic sperm injection: correlation of oocyte grade based on polar body, perivitelline space and cytoplasmic inclusions with fertilization rate and embryo quality. , 1997, Human reproduction.

[215]  D. Valbuena,et al.  Lower implantation rates in high responders: evidence for an altered endocrine milieu during the preimplantation period. , 1996, Fertility and sterility.

[216]  J. Visser,et al.  Regulation of ovarian function: the role of anti-Müllerian hormone. , 2002, Reproduction.

[217]  M. Matzuk,et al.  Interrelationship of growth differentiation factor 9 and inhibin in early folliculogenesis and ovarian tumorigenesis in mice. , 2004, Molecular endocrinology.

[218]  K. Song,et al.  Human Ku70 interacts with heterochromatin protein 1alpha. , 2001, The Journal of biological chemistry.

[219]  Satoshi Tanaka,et al.  PGC7/Stella protects against DNA demethylation in early embryogenesis , 2007, Nature Cell Biology.

[220]  D. Albertini,et al.  Meiotic competence acquisition is associated with the appearance of M-phase characteristics in growing mouse oocytes. , 1991, Developmental biology.

[221]  G. Brem,et al.  Secretion of cumulus expansion‐enabling factor (CEEF) in porcine follicles , 1998, Molecular reproduction and development.

[222]  F. Aoki,et al.  Transcriptional activity associated with meiotic competence in fully grown mouse GV oocytes , 2002, Zygote.

[223]  D. Seifer,et al.  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. , 2004, Fertility and sterility.

[224]  S. Clark,et al.  Bisulfite sequencing in preimplantation embryos: DNA methylation profile of the upstream region of the mouse imprinted H19 gene. , 1998, Genomics.

[225]  T. Okai,et al.  Reduction of progesterone receptor expression in human cumulus cells at the time of oocyte collection during IVF is associated with good embryo quality. , 2005, Human reproduction.

[226]  Wing H. Wong,et al.  A Novel and Critical Role for Oct4 as a Regulator of the Maternal-Embryonic Transition , 2008, PloS one.