The study of mammalian oocyte competence by transcriptome analysis: progress and challenges.

Various morphological and cytological traits of oocytes and their surrounding cumulus cells may be used to select oocytes for assisted reproduction. However, even with careful selection, successful IVF and subsequent embryo development remain uncertain. The factors that ensure oocyte competence are unclear and other approaches to assessing developmental potential must be explored. With the constant development of the molecular toolbox, genomic/transcriptomic analysis is becoming a more and more interesting approach to understand oocyte quality on the basis of RNA composition. Using bovine and mouse models as well as human oocytes of known developmental potential, various efforts are underway to characterize the mRNA profile of the competent oocyte using microarray technology. The proliferation of gene expression data sets raises new opportunities to identify the mechanisms involved in this complex phenotype, which should lead to improved techniques of assisted reproduction. Although several molecular markers of oocyte quality are known, translating these into cellular functions remains challenging, largely due to the poor correlation between mRNA level and protein synthesis. Unlike most somatic cells, the oocyte can store mRNA for days, with transcriptional activity remaining at a halt during the 4-5 days beginning before ovulation and ending with embryonic genome activation. This review provides an overview of the transcriptomic data obtained from oocytes of different quality as well as interesting avenues to explore in order to improve our understanding of oocyte competence.

[1]  M. Sirard Activation of the embryonic genome. , 2019, Society of Reproduction and Fertility supplement.

[2]  C. Lecellier,et al.  MicroRNAs: new candidates for the regulation of the human cumulus-oocyte complex. , 2013, Human reproduction.

[3]  M. M. Franco,et al.  Transcription profile of candidate genes for the acquisition of competence during oocyte growth in cattle. , 2013, Reproduction in domestic animals = Zuchthygiene.

[4]  Deanne M. Taylor,et al.  Blastocyst biopsy with comprehensive chromosome screening and fresh embryo transfer significantly increases in vitro fertilization implantation and delivery rates: a randomized controlled trial. , 2013, Fertility and sterility.

[5]  J. Opiela,et al.  The utility of Brilliant Cresyl Blue (BCB) staining of mammalian oocytes used for in vitro embryo production (IVP). , 2013, Reproductive biology.

[6]  J. Swain Could time-lapse embryo imaging reduce the need for biopsy and PGS? , 2013, Journal of Assisted Reproduction and Genetics.

[7]  F. Cao,et al.  Age‐associated changes in gene expression and developmental competence of bovine oocytes, and a possible countermeasure against age‐associated events , 2013, Molecular reproduction and development.

[8]  S. Kimber,et al.  Global Gene Expression Profiling of Individual Human Oocytes and Embryos Demonstrates Heterogeneity in Early Development , 2013, PloS one.

[9]  N. Suzuki,et al.  Effects of Maternal Aging on Expression of Sirtuin Genes in Ovulated Oocyte and Cumulus Cells , 2013 .

[10]  Shuhui Song,et al.  Maternal factors required for oocyte developmental competence in mice: Transcriptome analysis of non-surrounded nucleolus (NSN) and surrounded nucleolus (SN) oocytes , 2013, Cell cycle.

[11]  M. Sirard,et al.  Gene Expression Analysis of Bovine Oocytes With High Developmental Competence Obtained From FSH‐Stimulated Animals , 2013, Molecular reproduction and development.

[12]  G. Coticchio,et al.  Oocyte in vitro maturation in normo-ovulatory women. , 2013, Fertility and sterility.

[13]  A. Uyar,et al.  Cumulus and granulosa cell markers of oocyte and embryo quality. , 2013, Fertility and sterility.

[14]  H. Otu,et al.  Identification of a novel gene set in human cumulus cells predictive of an oocyte's pregnancy potential. , 2013, Fertility and sterility.

[15]  J. Mattick,et al.  Structure and function of long noncoding RNAs in epigenetic regulation , 2013, Nature Structural &Molecular Biology.

[16]  L. Rienzi,et al.  Sequential comprehensive chromosome analysis on polar bodies, blastomeres and trophoblast: insights into female meiotic errors and chromosomal segregation in the preimplantation window of embryo development. , 2013, Human reproduction.

[17]  R. Hart,et al.  IVF versus ICSI for the fertilization of in-vitro matured human oocytes. , 2012, Reproductive biomedicine online.

[18]  D. Tesfaye,et al.  Transcriptome Fingerprint of Bovine 2-Cell Stage Blastomeres Is Directly Correlated with the Individual Developmental Competence of the Corresponding Sister Blastomere1 , 2012, Biology of reproduction.

[19]  R. E. Everts,et al.  Messenger RNAs in metaphase II oocytes correlate with successful embryo development to the blastocyst stage , 2012, Zygote.

[20]  M. Sirard,et al.  Analysis of microRNAs and their precursors in bovine early embryonic development. , 2012, Molecular human reproduction.

[21]  V. Goossens,et al.  Assisted reproductive technology in Europe, 2008: results generated from European registers by ESHRE , 2012 .

[22]  N. Neretti,et al.  Transcriptome variance in single oocytes within, and between, genotypes , 2012, Molecular reproduction and development.

[23]  P. Patrizio,et al.  Alteration of gene expression in human cumulus cells as a potential indicator of oocyte aneuploidy. , 2012, Human reproduction.

[24]  Z. Jiao,et al.  Age-associated alteration of oocyte-specific gene expression in polar bodies: potential markers of oocyte competence. , 2012, Fertility and sterility.

[25]  R. Houlgatte,et al.  Genomic Assessment of Human Cumulus Cell Marker Genes as Predictors of Oocyte Developmental Competence: Impact of Various Experimental Factors , 2012, PloS one.

[26]  P. Haentjens,et al.  Reproductive potential of a metaphase II oocyte retrieved after ovarian stimulation: an analysis of 23 354 ICSI cycles. , 2012, Human reproduction.

[27]  Dorji,et al.  Gene expression differences in oocytes derived from adult and prepubertal Japanese Black cattle during in vitro maturation. , 2012, Reproduction in domestic animals = Zuchthygiene.

[28]  M. Sirard,et al.  Effect of ovarian stimulation on oocyte gene expression in cattle. , 2012, Theriogenology.

[29]  E. De Ponti,et al.  Cumulus cell-oocyte complexes retrieved from antral follicles in IVM cycles: relationship between COCs morphology, gonadotropin priming and clinical outcome , 2012, Journal of Assisted Reproduction and Genetics.

[30]  Xin Tao,et al.  Comprehensive chromosome screening is highly predictive of the reproductive potential of human embryos: a prospective, blinded, nonselection study. , 2012, Fertility and sterility.

[31]  C. Hensey,et al.  Developmental competence in oocytes and cumulus cells: candidate genes and networks , 2012, Systems biology in reproductive medicine.

[32]  V. Goossens,et al.  Assisted reproductive technology in Europe, 2007: results generated from European registers by ESHRE , 2012, Human reproduction.

[33]  L. Gianaroli,et al.  Multiple meiotic errors caused by predivision of chromatids in women of advanced maternal age undergoing in vitro fertilisation , 2012, European Journal of Human Genetics.

[34]  M. Sirard,et al.  FSH withdrawal improves developmental competence of oocytes in the bovine model. , 2012, Reproduction.

[35]  E. Ernst,et al.  Global gene analysis of oocytes from early stages in human folliculogenesis shows high expression of novel genes in reproduction. , 2012, Molecular human reproduction.

[36]  D. Tesfaye,et al.  Expression analysis of regulatory microRNAs in bovine cumulus oocyte complex and preimplantation embryos , 2011, Zygote.

[37]  S. Carson,et al.  The Transcriptome of a Human Polar Body Accurately Reflects Its Sibling Oocyte* , 2011, The Journal of Biological Chemistry.

[38]  Luca Gianaroli,et al.  Polar body array CGH for prediction of the status of the corresponding oocyte. Part I: clinical results , 2011, Human reproduction.

[39]  P. Rigault,et al.  Combining resources to obtain a comprehensive survey of the bovine embryo transcriptome through deep sequencing and microarrays , 2011, Molecular reproduction and development.

[40]  Silvia Garagna,et al.  What does it take to make a developmentally competent mammalian egg? , 2011, Human reproduction update.

[41]  Fang Gu,et al.  Differentially expressed micoRNAs in human oocytes , 2011, Journal of Assisted Reproduction and Genetics.

[42]  D. Griffin,et al.  Array comparative genomic hybridisation on first polar bodies suggests that non-disjunction is not the predominant mechanism leading to aneuploidy in humans , 2011, Journal of Medical Genetics.

[43]  Elpida Fragouli,et al.  The cytogenetics of polar bodies: insights into female meiosis and the diagnosis of aneuploidy. , 2011, Molecular human reproduction.

[44]  R. Blelloch,et al.  Genome-wide analysis of translation reveals a critical role for deleted in azoospermia-like (Dazl) at the oocyte-to-zygote transition. , 2011, Genes & development.

[45]  Ricardo Azziz,et al.  Polycystic ovary syndrome: etiology, pathogenesis and diagnosis , 2011, Nature Reviews Endocrinology.

[46]  P. Lonergan,et al.  Sequential analysis of global gene expression profiles in immature and in vitro matured bovine oocytes: potential molecular markers of oocyte maturation , 2011, BMC Genomics.

[47]  M. Sirard Follicle environment and quality of in vitro matured oocytes , 2011, Journal of Assisted Reproduction and Genetics.

[48]  Santiago Munné,et al.  Validation of microarray comparative genomic hybridization for comprehensive chromosome analysis of embryos. , 2011, Fertility and sterility.

[49]  M. Sirard Is aneuploidy a defense mechanism to prevent maternity later in a woman’s life , 2011, Journal of Assisted Reproduction and Genetics.

[50]  E. W. Khandjian,et al.  Method to isolate polyribosomal mRNA from scarce samples such as mammalian oocytes and early embryos , 2011, BMC Developmental Biology.

[51]  M. Montag,et al.  Biomarkers of human oocyte developmental competence expressed in cumulus cells before ICSI: a preliminary study , 2011, Journal of Assisted Reproduction and Genetics.

[52]  D. Wells,et al.  Chromosome Abnormalities in the Human Oocyte , 2011, Cytogenetic and Genome Research.

[53]  B. Levy,et al.  Accurate single cell 24 chromosome aneuploidy screening using whole genome amplification and single nucleotide polymorphism microarrays. , 2010, Fertility and sterility.

[54]  P. Patrizio,et al.  Transcriptomic profiling of human oocytes: association of meiotic aneuploidy and altered oocyte gene expression. , 2010, Molecular human reproduction.

[55]  C. Robert,et al.  Identification of follicular marker genes as pregnancy predictors for human IVF: new evidence for the involvement of luteinization process. , 2010, Molecular human reproduction.

[56]  Said Assou,et al.  Human cumulus cells as biomarkers for embryo and pregnancy outcomes. , 2010, Molecular human reproduction.

[57]  D. Tesfaye,et al.  Suppression of the transcription factor MSX1 gene delays bovine preimplantation embryo development in vitro. , 2010, Reproduction.

[58]  J. Bogstad,et al.  Gene expression profiles of single human mature oocytes in relation to age. , 2010, Human reproduction.

[59]  C. Robert,et al.  Genomic assessment of follicular marker genes as pregnancy predictors for human IVF. , 2010, Molecular human reproduction.

[60]  A. Labbe,et al.  Revealing the bovine embryo transcript profiles during early in vivo embryonic development. , 2009, Reproduction.

[61]  M. M. Franco,et al.  Effect of follicle size on mRNA expression in cumulus cells and oocytes of Bos indicus: an approach to identify marker genes for developmental competence. , 2009, Reproduction, fertility, and development.

[62]  D. Gardner,et al.  Transcriptome analysis of in vivo and in vitro matured bovine MII oocytes. , 2009, Theriogenology.

[63]  D. Wells,et al.  Use of comprehensive chromosomal screening for embryo assessment: microarrays and CGH , 2008, Molecular human reproduction.

[64]  M. Matzuk,et al.  Revisiting oocyte–somatic cell interactions: in search of novel intrafollicular predictors and regulators of oocyte developmental competence , 2008, Molecular human reproduction.

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

[66]  L. Gianaroli,et al.  Gene expression profiling of human oocytes following in vivo or in vitro maturation. , 2008, Human reproduction.

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

[68]  T. Hamatani,et al.  What can we learn from gene expression profiling of mouse oocytes? , 2008, Reproduction.

[69]  R. Schultz,et al.  Age-associated increase in aneuploidy and changes in gene expression in mouse eggs. , 2008, Developmental biology.

[70]  Pasquale Patrizio,et al.  Gene expression profiling of human oocytes at different maturational stages and after in vitro maturation. , 2008, American journal of obstetrics and gynecology.

[71]  R. Guigó,et al.  A Combinatorial Code for CPE-Mediated Translational Control , 2008, Cell.

[72]  D. Tesfaye,et al.  Molecular and subcellular characterisation of oocytes screened for their developmental competence based on glucose-6-phosphate dehydrogenase activity. , 2008, Reproduction.

[73]  C. Wrenzycki,et al.  Effects of follicle size and stages of maturation on mRNA expression in bovine in vitro matured oocytes , 2008, Molecular reproduction and development.

[74]  G. Adams,et al.  Oocyte developmental competence in a bovine model of reproductive aging. , 2007, Reproduction.

[75]  D. Tesfaye,et al.  Alterations in transcript abundance of bovine oocytes recovered at growth and dominance phases of the first follicular wave , 2007, BMC Developmental Biology.

[76]  F. Franciosi,et al.  Large‐scale chromatin remodeling in germinal vesicle bovine oocytes: Interplay with gap junction functionality and developmental competence , 2007, Molecular reproduction and development.

[77]  D. Tesfaye,et al.  Dielectrophoretic behavior of in vitro-derived bovine metaphase II oocytes and zygotes and its relation to in vitro embryonic developmental competence and mRNA expression pattern. , 2007, Reproduction.

[78]  Y. Murakami,et al.  Analysis of transcription factor expression during oogenesis and preimplantation development in mice , 2007, Zygote.

[79]  J. Yao,et al.  Changes of maternal transcripts in oocytes from persistent follicles in cattle , 2007, Molecular reproduction and development.

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

[81]  J. Wood,et al.  Molecular abnormalities in oocytes from women with polycystic ovary syndrome revealed by microarray analysis. , 2007, The Journal of clinical endocrinology and metabolism.

[82]  Gang Wu,et al.  Integrative Analysis of Transcriptomic and Proteomic Data: Challenges, Solutions and Applications , 2007, Critical reviews in biotechnology.

[83]  D. Loutradis,et al.  Oocyte Maturation in Assisted Reproductive Techniques , 2006, Annals of the New York Academy of Sciences.

[84]  M. Sirard,et al.  The influence of follicle size, FSH‐enriched maturation medium, and early cleavage on bovine oocyte maternal mRNA levels , 2006, Molecular reproduction and development.

[85]  K. Latham,et al.  Analysis of polysomal mRNA populations of mouse oocytes and zygotes: dynamic changes in maternal mRNA utilization and function. , 2006, Developmental biology.

[86]  M. Matzuk,et al.  Mining the oocyte transcriptome , 2006, Trends in Endocrinology & Metabolism.

[87]  F. Richard,et al.  Contribution of the oocyte to embryo quality. , 2006, Theriogenology.

[88]  M. Kimura,et al.  Diverse patterns of poly(A) tail elongation and shortening of murine maternal mRNAs from fully grown oocyte to 2-cell embryo stages. , 2005, Biochemical and biophysical research communications.

[89]  R. Schultz,et al.  Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. , 2005, Developmental biology.

[90]  P. Devroey,et al.  Blastocyst formation in in vitro fertilization versus intracytoplasmic sperm injection cycles: influence of the fertilization procedure. , 2005, Fertility and sterility.

[91]  K. Tremblay,et al.  Expression of Cyclin B1 Messenger RNA Isoforms and Initiation of Cytoplasmic Polyadenylation in the Bovine Oocyte1 , 2005, Biology of reproduction.

[92]  C. Robert,et al.  RNA interference as a tool to study gene function in bovine oocytes , 2005, Molecular reproduction and development.

[93]  P. Mermillod,et al.  Influence of antral follicle size on oocyte characteristics and embryo development in the bovine. , 2005, Theriogenology.

[94]  G. Coticchio,et al.  What Criteria for the Definition of Oocyte Quality? , 2004, Annals of the New York Academy of Sciences.

[95]  P. Pfeffer,et al.  Isolation of Genes Associated with Developmentally Competent Bovine Oocytes and Quantitation of Their Levels During Development1 , 2004, Biology of reproduction.

[96]  A. Sharov,et al.  Age-associated alteration of gene expression patterns in mouse oocytes. , 2004, Human molecular genetics.

[97]  Fanyi Zeng,et al.  Transcript profiling during preimplantation mouse development. , 2004, Developmental biology.

[98]  M. Machatkova,et al.  Developmental competence of bovine oocytes: effects of follicle size and the phase of follicular wave on in vitro embryo production. , 2004, Theriogenology.

[99]  A. Gutiérrez-Adán,et al.  Relative messenger RNA abundance in bovine oocytes collected in vitro or in vivo before and 20 hr after the preovulatory luteinizing hormone surge , 2003, Molecular reproduction and development.

[100]  Juan F Medrano,et al.  Development and testing of a high-density cDNA microarray resource for cattle. , 2003, Physiological genomics.

[101]  G. Adams,et al.  Morphology and developmental competence of bovine oocytes relative to follicular status. , 2003, Theriogenology.

[102]  Dawood B Dudekula,et al.  In situ-synthesized novel microarray optimized for mouse stem cell and early developmental expression profiling. , 2003, Genome research.

[103]  J. Geraedts,et al.  Conception to ongoing pregnancy: the 'black box' of early pregnancy loss. , 2002, Human reproduction update.

[104]  P. Lonergan,et al.  Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: Implications for blastocyst yield and blastocyst quality , 2002, Molecular reproduction and development.

[105]  M. Sauer,et al.  Assessing fertility in women of advanced reproductive age. , 2001, American journal of obstetrics and gynecology.

[106]  V. Duranthon,et al.  The developmental competence of mammalian oocytes: a convenient but biologically fuzzy concept. , 2001, Theriogenology.

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

[108]  D. Armstrong Effects of maternal age on oocyte developmental competence. , 2001, Theriogenology.

[109]  C. Robert,et al.  Subtractive hybridization used to identify mRNA associated with the maturation of bovine oocytes , 2000, Molecular reproduction and development.

[110]  N. Steuerwald,et al.  Association between spindle assembly checkpoint expression and maternal age in human oocytes. , 2000, Molecular human reproduction.

[111]  O. Hovatta,et al.  Luteal phase start of low-dose FSH priming of follicles results in an efficient recovery, maturation and fertilization of immature human oocytes. , 2000, Human reproduction.

[112]  P. Lonergan,et al.  Effect of time interval from insemination to first cleavage on the developmental characteristics, sex ratio and pregnancy rate after transfer of bovine embryos. , 1999, Journal of reproduction and fertility.

[113]  H. R. Tervit,et al.  Development during single IVP of bovine oocytes from dissected follicles: Interactive effects of estrous cycle stage, follicle size and atresia , 1999, Molecular reproduction and development.

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

[115]  L. J. Hagemann Influence of the dominant follicle on oocytes from subordinate follicles. , 1999, Theriogenology.

[116]  G. Vajta,et al.  Developmental kinetics of the first cell cycles of bovine in vitro produced embryos in relation to their in vitro viability and sex. , 1998, Theriogenology.

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

[118]  M. Wiltbank,et al.  Emergence and deviation of follicles during the development of follicular waves in cattle. , 1997, Theriogenology.

[119]  M. Soules,et al.  Influence of maternal age on meiotic spindle assembly in oocytes from naturally cycling women. , 1996, Human reproduction.

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

[121]  M. Sirard,et al.  Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes , 1995, Molecular reproduction and development.

[122]  N. Ahmad,et al.  Effect of persistent follicles on early embryonic losses in beef cows. , 1995, Biology of reproduction.

[123]  H. D. de Boer,et al.  Kinetics of first polar body extrusion and the effect of time of stripping of the cumulus and time of insemination on developmental competence of bovine oocytes. , 1994, Theriogenology.

[124]  B. Grisart,et al.  Cinematographic analysis of bovine embryo development in serum-free oviduct-conditioned medium. , 1994, Journal of reproduction and fertility.

[125]  R. Schultz,et al.  Relationship between the developmental programs controlling nuclear and cytoplasmic maturation of mouse oocytes. , 1994, Developmental biology.

[126]  P. Lonergan,et al.  Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro , 1994, Molecular reproduction and development.

[127]  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.

[128]  A. Lucas-Hahn,et al.  Fertilization and developmental competence of bovine oocytes derived from different categories of antral follicles , 1992, Molecular reproduction and development.

[129]  Mary-Anne Williams,et al.  Poor oocyte quality rather than implantation failure as a cause of age-related decline in female fertility , 1991, The Lancet.

[130]  O. Destrée,et al.  The effects of α‐amanitin and cycloheximide on nuclear progression, protein synthesis, and phosphorylation during bovine oocyte maturation in vitro , 1991, Molecular reproduction and development.

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

[132]  J. Lussier,et al.  Growth rates of follicles in the ovary of the cow. , 1987, Journal of reproduction and fertility.

[133]  R. Moor,et al.  Stage-dependent effects of inhibiting ribonucleic acids and protein synthesis on meiotic maturation of bovine oocytes in vitro. , 1987, Journal of dairy science.

[134]  A. Gougeon Dynamics of follicular growth in the human: a model from preliminary results. , 1986, Human reproduction.

[135]  R. Schultz,et al.  Biochemical studies of mammalian oogenesis: synthesis and stability of various classes of RNA during growth of the mouse oocyte in vitro. , 1981, Developmental biology.

[136]  T. Rodman,et al.  RNA synthesis in preovulatory mouse oocytes , 1976, The Journal of cell biology.

[137]  P. Wassarman,et al.  Relationship between growth and meiotic maturation of the mouse oocyte. , 1976, Developmental biology.

[138]  P. Wassarman,et al.  RNA synthesis in fully-grown mouse oocytes , 1976, Nature.

[139]  V. Lodde,et al.  Changes of Large-Scale Chromatin Configuration During Mammalian Oocyte Differentiation , 2013 .

[140]  M. Ko,et al.  Developmental Arrest and Mouse Antral Not-Surrounded Nucleolus Oocytes1 , 2013, Biology of reproduction.

[141]  L. Rienzi,et al.  Study Selection , 2013 .

[142]  R. Bellazzi,et al.  Knowledge-based bioinformatics for the study of mammalian oocytes. , 2012, The International journal of developmental biology.

[143]  H. Clarke Post-transcriptional control of gene expression during mouse oogenesis. , 2012, Results and problems in cell differentiation.

[144]  M. Sirard,et al.  Improving oocyte quality in cows and heifers - What have we learned so far? , 2012 .

[145]  A. Kuliev,et al.  Meiosis errors in over 20,000 oocytes studied in the practice of preimplantation aneuploidy testing. , 2011, Reproductive biomedicine online.

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

[147]  E. De Ponti,et al.  Effect of different gonadotrophin priming on IVM of oocytes from women with normal ovaries: a prospective randomized study. , 2009, Reproductive biomedicine online.

[148]  Qing-Yuan Sun,et al.  Evaluation of oocyte quality: morphological, cellular and molecular predictors. , 2007, Reproduction, fertility, and development.

[149]  P. Coussens,et al.  Functional genomics studies of oocyte competence: evidence that reduced transcript abundance for follistatin is associated with poor developmental competence of bovine oocytes. , 2007, Reproduction.

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

[151]  Jacques Cohen,et al.  Maternal age-related differential global expression profiles observed in human oocytes. , 2007, Reproductive biomedicine online.

[152]  C. Robert,et al.  Potential and limitations of bovine-specific arrays for the analysis of mRNA levels in early development: preliminary analysis using a bovine embryonic array. , 2005, Reproduction, fertility, and development.

[153]  S. Lindenberg,et al.  Time interval between FSH priming and aspiration of immature human oocytes for in-vitro maturation: a prospective randomized study. , 2003, Reproductive biomedicine online.

[154]  M. Sirard,et al.  Manipulation of Follicular Development to Produce Developmentally Competent Bovine Oocytes1 , 2002, Biology of reproduction.

[155]  D. Lockhart,et al.  Functional Genomics , 2002, Springer Netherlands.

[156]  J. Eppig,et al.  Transcriptional activity of the mouse oocyte genome: companion granulosa cells modulate transcription and chromatin remodeling. , 2001, Developmental biology.

[157]  J. Hasler The Current Status of Oocyte Recovery, In Vitro Embryo Production, and Embryo Transfer in Domestic Animals, with an Emphasis on the Bovine , 1998 .

[158]  I. Lewis,et al.  Current status of IVM/IVF and embryo culture in humans and farm animals , 1994 .

[159]  P. Mermillod,et al.  Bmc Developmental Biology Differential Regulation of Abundance and Deadenylation of Maternal Transcripts during Bovine Oocyte Maturation in Vitro and in Vivo , 2022 .