Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
REVIEW

RFD Award Lecture 2009. In vitro maturation of farm animal oocytes: a useful tool for investigating the mechanisms leading to full-term development

Fulvio Gandolfi A B and Tiziana A. L. Brevini A
+ Author Affiliations
- Author Affiliations

A Laboratory of Biomedical Embryology, Department of Animal Sciences, Università degli Studi di Milano, via Celoria, 10-20133, Milano, Italy.

B Corresponding author. Email: fulvio.gandolfi@unimi.it

Reproduction, Fertility and Development 22(3) 495-507 https://doi.org/10.1071/RD09151
Submitted: 25 June 2009  Accepted: 11 September 2009   Published: 12 February 2010

Abstract

Due to logistical and economic reasons, assisted reproduction of domestic animals has been based mostly on the use of oocytes isolated from ovaries collected at the slaughterhouse. In order to propagate valuable or rare genetic material, perform somatic cell nuclear transfer or generate genetically modified animals, it is essential to obtain fully competent oocytes that will allow full-term development of the in vitro-produced embryos. Such a need makes clear the crucial role played by oocyte quality. In fact, it is easy to compromise the oocyte’s developmental potential but it is impossible to restore once it has been lost. Almost three decades after the first cow, sheep, goat, horse and pig in vitro-generated offspring were born, a large body of information has accumulated on the mechanisms regulating oocyte competence and on how the latter may be preserved during all the required manipulations. The amount of knowledge is far from complete and many laboratories are actively working to further expand it. In this review we will highlight the aspects of the ongoing research in which we have been actively involved.

Additional keywords: developmental competence, mitochondria, mRNA polyadenylation, oocyte maturation, parthenogenesis, stem cells.


Acknowledgements

The work of the authors was supported by the Ministry of Education PRIN 2006, 2007, PUR 2007, 2008. We are grateful to Umberto Fascio and Arianna Vanelli for their help with confocal microscopy and computer graphics.


References

Ahn, H. J. , Sohn, I. P. , Kwon, H. C. , Jo, D. H. , Park, Y. D. , and Min, C. K. (2002). Characteristics of the cell membrane fluidity, actin fibers and mitochondrial dysfunctions of frozen–thawed two-cell mouse embryos. Mol. Reprod. Dev. 61, 466–476.
CrossRef | PubMed | CAS |

Akaki, Y. , Yoshioka, K. , Noguchi, M. , Hoshi, H. , and Funahashi, H. (2009). Successful piglet production in a chemically defined system for in vitro production of porcine embryos: dibutyryl cyclic AMP and epidermal growth factor-family peptides support in vitro maturation of oocytes in the absence of gonadotropins. J. Reprod. Dev. 55, 446–453.
CrossRef | PubMed | CAS |

Albertini, D. F. , and Barrett, S. L. (2003). Oocyte–somatic cell communication. Reprod. Suppl. 61, 49–54.
PubMed | |  CAS |

Albertini, D. F. , Combelles, C. M. , Benecchi, E. , and Carabatsos, M. J. (2001). Cellular basis for paracrine regulation of ovarian follicle development. Reproduction 121, 647–653.
CrossRef | PubMed | CAS |

Allen, N. D. , Barton, S. C. , Hilton, K. , Norris, M. L. , and Surani, M. A. (1994). A functional analysis of imprinting in parthenogenetic embryonic stem cells. Development 120, 1473–1482.
PubMed | |  CAS |

Amabile, G. , and Meissner, A. (2009). Induced pluripotent stem cells: current progress and potential for regenerative medicine. Trends Mol. Med. 15, 59–68.
CrossRef | PubMed | CAS |

Arlotto, T. , Schwartz, J. L. , First, N. L. , and Leibfried-Rutledge, M. L. (1996). Aspects of follicle and oocyte stage that affect in vitro maturation and development of bovine oocytes. Theriogenology 45, 943–956.
CrossRef | PubMed | CAS |

Bagg, M. A. , Nottle, M. B. , Grupen, C. G. , and Armstrong, D. T. (2006). Effect of dibutyryl cAMP on the cAMP content, meiotic progression and developmental potential of in vitro-matured pre-pubertal and adult pig oocytes. Mol. Reprod. Dev. 73, 1326–1332.
CrossRef | PubMed | CAS |

Bagg, M. A. , Nottle, M. B. , Armstrong, D. T. , and Grupen, C. G. (2007). Relationship between follicle size and oocyte developmental competence in prepubertal and adult pigs. Reprod. Fertil. Dev. 19, 797–803.
CrossRef | PubMed | CAS |

Bateman, M. J. , Cornell, R. , d’Alencon, C. , and Sandra, A. (2004). Expression of the zebrafish Staufen gene in the embryo and adult. Gene Expr. Patterns 5, 273–278.
CrossRef | PubMed | CAS |

Bavister, B. D. , and Squirrell, J. M. (2000). Mitochondrial distribution and function in oocytes and early embryos. Hum. Reprod. 15(Suppl. 2), 189–198.
PubMed |

Blondin, P. , and Sirard, M. A. (1995). Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes. Mol. Reprod. Dev. 41, 54–62.
CrossRef | PubMed | CAS |

Blondin, P. , Bousquet, D. , Twagiramungu, H. , Barnes, F. , and Sirard, M. A. (2002). Manipulation of follicular development to produce developmentally competent bovine oocytes. Biol. Reprod. 66, 38–43.
CrossRef | PubMed | CAS |

Brevini, T. A. L. , and Gandolfi, F. (2008). Parthenotes as a source of embryonic stem cells. Cell Prolif. 41(Suppl. 1), 20–30.
PubMed |

Brevini, T. A. L. , Lonergan, P. , Cillo, F. , Francisci, C. , Favetta, L. A. , Fair, T. , and Gandolfi, F. (2002). Evolution of mRNA polyadenylation between oocyte maturation and first embryonic cleavage in cattle and its relation with developmental competence. Mol. Reprod. Dev. 63, 510–517.
CrossRef | PubMed | CAS |

Brevini, T. A. L. , Vassena, R. , Paffoni, A. , Francisci, C. , Fascio, U. , and Gandolfi, F. (2004). Exposure of pig oocytes to PCBs during in vitro maturation: effects on developmental competence, cytoplasmic remodelling and communications with cumulus cells. Eur. J. Histochem. 48, 347–356.
PubMed | |  CAS |

Brevini, T. A. L. , Vassena, R. , Francisci, C. , and Gandolfi, F. (2005). Role of adenosine triphosphate, active mitochondria and microtubules in the acquisition of developmental competence of parthenogenetically activated pig oocytes. Biol. Reprod. 72, 1218–1223.
CrossRef | CAS | PubMed |

Brevini, T. A. L. , Cillo, F. , Antonini, S. , and Gandolfi, F. (2007a). Cytoplasmic remodelling and the acquisition of developmental competence in pig oocytes. Anim. Reprod. Sci. 98, 23–38.
CrossRef | PubMed | CAS |

Brevini, T. A. L. , Tosetti, V. , Crestan, M. , Antonini, S. , and Gandolfi, F. (2007b). Derivation and characterization of pluripotent cell lines from pig embryos of different origins. Theriogenology 67, 54–63.
CrossRef | PubMed |

Brevini, T. A. L. , Pennarossa, G. , Antonini, S. , and Gandolfi, F. (2008). Parthenogenesis as an approach to pluripotency: advantages and limitations involved. Stem Cell Rev. 4, 127–135.
CrossRef | PubMed | CAS |

Brevini-Gandolfi, T. A. L. , and Gandolfi, F. (2001). The maternal legacy to the embryo: cytoplasmic components and their effects on early development. Theriogenology 55, 1255–1276.
CrossRef | PubMed |

Brevini-Gandolfi, T. A. L. , Favetta, L. A. , Mauri, L. , Luciano, A. M. , Cillo, F. , and Gandolfi, F. (1999). Changes in poly(A) tail length of maternal transcripts during in vitro maturation of bovine oocytes and their relation with developmental competence. Mol. Reprod. Dev. 52, 427–433.
CrossRef | PubMed | CAS |

Brison, D. R. , Houghton, F. D. , Falconer, D. , Roberts, S. A. , Hawkhead, J. , Humpherson, P. G. , Lieberman, B. A. , and Leese, H. J. (2004). Identification of viable embryos in IVF by non-invasive measurement of amino acid turnover. Hum. Reprod. 19, 2319–2324.
CrossRef | PubMed | CAS |

Calarco, P. G. (1995). Polarization of mitochondria in the unfertilized mouse oocyte. Dev. Genet. 16, 36–43.
CrossRef | PubMed | CAS |

Camaioni, A. , Hascall, V. C. , Yanagishita, M. , and Salustri, A. (1993). Effects of exogenous hyaluronic acid and serum on matrix organization and stability in the mouse cumulus cell–oocyte complex. J. Biol. Chem. 268, 20 473–20 481.
PubMed | |  CAS |

Chen, L. , Wert, S. E. , Hendrix, E. M. , Russell, P. T. , Cannon, M. , and Larsen, W. J. (1990). Hyaluronic acid synthesis and gap junction endocytosis are necessary for normal expansion of the cumulus mass. Mol. Reprod. Dev. 26, 236–247.
CrossRef | PubMed |

Cillo, F. , Brevini, T. A. , Antonini, S. , Paffoni, A. , Ragni, G. , and Gandolfi, F. (2007). Association between human oocyte developmental competence and expression levels of some cumulus genes. Reproduction 134, 645–650.
CrossRef | PubMed | CAS |

Cohen, R. S. (2002). Oocyte patterning: dynein and kinesin, inc. Curr. Biol. 12, R797–R799.
CrossRef | PubMed | CAS |

Conti, M. , Andersen, C. B. , Richard, F. , Mehats, C. , Chun, S. Y. , Horner, K. , Jin, C. , and Tsafriri, A. (2002). Role of cyclic nucleotide signalling in oocyte maturation. Mol. Cell. Endocrinol. 187, 153–159.
CrossRef | PubMed | CAS |

Craig, J. , Orisaka, M. , Wang, H. , Orisaka, S. , Thompson, W. , Zhu, C. , Kotsuji, F. , and Tsang, B. K. (2007). Gonadotropin and intra-ovarian signals regulating follicle development and atresia: the delicate balance between life and death. Front. Biosci. 12, 3628–3639.
CrossRef | PubMed | CAS |

Cran, D. G. (1985). Qualitative and quantitative structural changes during pig oocyte maturation. J. Reprod. Fertil. 74, 237–245.
CrossRef | PubMed | CAS |

Dekel, N. , Galiani, D. , and Sherizly, I. (1988). Dissociation between the inhibitory and the stimulatory action of cAMP on maturation of rat oocytes. Mol. Cell. Endocrinol. 56, 115–121.
CrossRef | PubMed | CAS |

De Sousa, P. A. , Westhusin, M. E. , and Watson, A. J. (1998). Analysis of variation in relative mRNA abundance for specific gene transcripts in single bovine oocytes and early embryos. Mol. Reprod. Dev. 49, 119–130.
CrossRef | PubMed | CAS |

Eckardt, S. , Leu, N. A. , Bradley, H. L. , Kato, H. , Bunting, K. D. , and McLaughlin, K. J. (2007). Hematopoietic reconstitution with androgenetic and gynogenetic stem cells. Genes Dev. 21, 409–419.
CrossRef | PubMed | CAS |

Edry, I. , Sela-Abramovich, S. , and Dekel, N. (2006). Meiotic arrest of oocytes depends on cell-to-cell communication in the ovarian follicle. Mol. Cell. Endocrinol. 252, 102–106.
CrossRef | PubMed | CAS |

El Shourbagy, S. H. , Spikings, E. C. , Freitas, M. , and St John, J. C. (2006). Mitochondria directly influence fertilisation outcome in the pig. Reproduction 131, 233–245.
CrossRef | PubMed | CAS |

Elvin, J. A. , Clark, A. T. , Wang, P. , Wolfman, N. M. , and Matzuk, M. M. (1999). Paracrine actions of growth differentiation factor-9 in the mammalian ovary. Mol. Endocrinol. 13, 1035–1048.
CrossRef | PubMed | CAS |

Eppig, J. J. (2001). Oocyte control of ovarian follicular development and function in mammals. Reproduction 122, 829–838.
CrossRef | PubMed | CAS |

Fair, T. (2003). Follicular oocyte growth and acquisition of developmental competence. Anim. Reprod. Sci. 78, 203–216.
CrossRef | PubMed | CAS |

Fair, T. , Hulshof, S. C. , Hyttel, P. , Greve, T. , and Boland, M. (1997). Nucleus ultrastructure and transcriptional activity of bovine oocytes in preantral and early antral follicles. Mol. Reprod. Dev. 46, 208–215.
CrossRef | PubMed | CAS |

Fang, Z. F. , Gai, H. , Huang, Y. Z. , Li, S. G. , Chen, X. J. , Shi, J. J. , Wu, L. , Liu, A. , Xu, P. , and Sheng, H. Z. (2006). Rabbit embryonic stem cell lines derived from fertilized, parthenogenetic or somatic cell nuclear transfer embryos. Exp. Cell Res. 312, 3669–3682.
CrossRef | PubMed | CAS |

Feng, B. , Jiang, J. , Kraus, P. , Ng, J. H. , and Heng, J. C. , et al. (2009). Reprogramming of fibroblasts into induced pluripotent stem cells with orphan nuclear receptor Esrrb. Nat. Cell Biol. 11, 197–203.
CrossRef | PubMed | CAS |

Galli, C. , and Lazzari, G. (1996). Practical aspects of IVM/IVF in cattle. Anim. Reprod. Sci. 42, 371–379.
CrossRef |

Galli, C. , Lagutina, I. , Duchi, R. , Colleoni, S. , and Lazzari, G. (2008). Somatic cell nuclear transfer in horses. Reprod. Domest. Anim. 43(Suppl. 2), 331–337.
CrossRef | PubMed |

Gandolfi, F. , Milanesi, E. , Pocar, P. , Luciano, A. M. , Brevini, T. A. , Acocella, F. , Lauria, A. , and Armstrong, D. T. (1998). Comparative analysis of calf and cow oocytes during in vitro maturation. Mol. Reprod. Dev. 49, 168–175.
CrossRef | PubMed | CAS |

Gandolfi, F. , Brevini, T. A. , Cillo, F. , and Antonini, S. (2005). Cellular and molecular mechanisms regulating oocyte quality and the relevance for farm animal reproductive efficiency. Rev. Sci. Tech. 24, 413–423.
PubMed | |  CAS |

Gavis, E. R. , and Lehmann, R. (1992). Localization of nano RNA controls embryonic polarity. Cell 71, 301–313.
CrossRef | PubMed | CAS |

Gil, M. A. , Alminana, C. , Roca, J. , Vazquez, J. M. , and Martinez, E. A. (2008). Boar semen variability and its effects on IVF efficiency. Theriogenology 70, 1260–1268.
CrossRef | PubMed | CAS |

Gilchrist, R. B. , Ritter, L. J. , and Armstrong, D. T. (2004). Oocyte–somatic cell interactions during follicle development in mammals. Anim. Reprod. Sci. 82–83, 431–446.
CrossRef |

Gilchrist, R. B. , Lane, M. , and Thompson, J. G. (2008). Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum. Reprod. Update 14, 159–177.
CrossRef | PubMed | CAS |

Giraldez, A. J. , Mishima, Y. , Rihel, J. , Grocock, R. J. , Van Dongen, S. , Inoue, K. , Enright, A. J. , and Schier, A. F. (2006). Zebrafish MiR-430 promotes de-adenylation and clearance of maternal mRNAs. Science 312, 75–79.
CrossRef | PubMed | CAS |

Hachet, O. , and Ephrussi, A. (2004). Splicing of oskar RNA in the nucleus is coupled to its cytoplasmic localization. Nature 428, 959–963.
CrossRef | PubMed | CAS |

Hagemann, L. J. , Beaumont, S. E. , Berg, M. , Donnison, M. J. , Ledgard, A. , Peterson, A. J. , Schurmann, A. , and Tervit, H. R. (1999). Development during single IVP of bovine oocytes from dissected follicles: interactive effects of estrous cycle stage, follicle size and atresia. Mol. Reprod. Dev. 53, 451–458.
CrossRef | PubMed | CAS |

Hasler, J. F. , Henderson, W. B. , Hurtgen, P. J. , Jin, Z. Q. , McCauley, A. D. , Mower, S. A. , Neely, B. , Shuey, L. S. , Stokes, J. E. , and Trimmer, S. A. (1995). Production, freezing and transfer of bovine IVF embryos and subsequent calving results. Theriogenology 43, 141–152.
CrossRef |

Horii, T. , Kimura, M. , Morita, S. , Nagao, Y. , and Hatada, I. (2008). Loss of genomic imprinting in mouse parthenogenetic embryonic stem cells. Stem Cells 26, 79–88.
CrossRef | PubMed | CAS |

Hyttel, P. , Callesen, H. , and Greve, T. (1989). A comparative ultrastructural study of in vivo versus in vitro fertilization of bovine oocytes. Anat. Embryol. (Berl.) 179, 435–442.
CrossRef | PubMed | CAS |

Hyttel, P. , Fair, T. , Callesen, H. , and Greve, T. (1997). Oocyte growth, capacitation and final maturation in cattle. Theriogenology 47, 23–32.
CrossRef |

Ju, J. C. , Tsay, C. , and Ruan, C. W. (2003). Alterations and reversibility in the chromatin, cytoskeleton and development of pig oocytes treated with roscovitine. Mol. Reprod. Dev. 64, 482–491.
CrossRef | PubMed | CAS |

Kim, N. H. , Funahashi, H. , Abeydeera, L. R. , Moon, S. J. , Prather, R. S. , and Day, B. N. (1996). Effects of oviductal fluid on sperm penetration and cortical granule exocytosis during fertilization of pig oocytes in vitro. J. Reprod. Fertil. 107, 79–86.
CrossRef | PubMed | CAS |

Kim, N. H. , Cho, S. K. , Choi, S. H. , Kim, E. Y. , Park, S. P. , and Lim, J. H. (2000). The distribution and requirements of microtubules and microfilaments in bovine oocytes during in vitro maturation. Zygote 8, 25–32.
CrossRef | PubMed | CAS |

Kim, V. N. , and Nam, J. W. (2006). Genomics of microRNA. Trends Genet. 22, 165–173.
CrossRef | PubMed | CAS |

Krisher, R. L. , and Bavister, B. D. (1999). Enhanced glycolysis after maturation of bovine oocytes in vitro is associated with increased developmental competence. Mol. Reprod. Dev. 53, 19–26.
CrossRef | PubMed | CAS |

Latham, K. E. , and Schultz, R. M. (2001). Embryonic genome activation. Front. Biosci. 6, D748–D759.
CrossRef | PubMed | CAS |

Lee, J. , Miyano, T. , and Moor, R. M. (2000). Spindle formation and dynamics of gamma-tubulin and nuclear mitotic apparatus protein distribution during meiosis in pig and mouse oocytes. Biol. Reprod. 62, 1184–1192.
CrossRef | PubMed | CAS |

Lee, K. S. , Joo, B. S. , Na, Y. J. , Yoon, M. S. , Choi, O. H. , and Kim, W. W. (2001). Cumulus cells apoptosis as an indicator to predict the quality of oocytes and the outcome of IVF-ET. J. Assist. Reprod. Genet. 18, 490–498.
CrossRef | PubMed | CAS |

Leoni, G. G. , Bebbere, D. , Succu, S. , Berlinguer, F. , Mossa, F. , Galioto, M. , Bogliolo, L. , Ledda, S. , and Naitana, S. (2007). Relations between relative mRNA abundance and developmental competence of ovine oocytes. Mol. Reprod. Dev. 74, 249–257.
CrossRef | PubMed | CAS |

Lin, D. P. , Huang, C. C. , Wu, H. M. , Cheng, T. C. , Chen, C. I. , and Lee, M. S. (2004). Comparison of mitochondrial DNA contents in human embryos with good or poor morphology at the 8-cell stage. Fertil. Steril. 81, 73–79.
CrossRef | PubMed | CAS |

Lin, G. , OuYang, Q. , Zhou, X. , Gu, Y. , Yuan, D. , Li, W. , Liu, G. , Liu, T. , and Lu, G. (2007). A highly homozygous and parthenogenetic human embryonic stem cell line derived from a one-pronuclear oocyte following in vitro fertilization procedure. Cell Res. 17, 999–1007.
CrossRef | PubMed | CAS |

Liu, L. , Hammar, K. , Smith, P. J. , Inoue, S. , and Keefe, D. L. (2001). Mitochondrial modulation of calcium signalling at the initiation of development. Cell Calcium 30, 423–433.
CrossRef | PubMed | CAS |

Lonergan, P. , Rizos, D. , Ward, F. , and Boland, M. P. (2001). Factors influencing oocyte and embryo quality in cattle. Reprod. Nutr. Dev. 41, 427–437.
CrossRef | CAS | PubMed |

Lonergan, P. , Rizos, D. , Gutierrez-Adan, A. , Fair, T. , and Boland, M. P. (2003). Oocyte and embryo quality: effect of origin, culture conditions and gene expression patterns. Reprod. Domest. Anim. 38, 259–267.
CrossRef | PubMed | CAS |

Luciano, A. M. , Pocar, P. , Milanesi, E. , Modina, S. , Rieger, D. , Lauria, A. , and Gandolfi, F. (1999). Effect of different levels of intracellular cAMP on the in vitro maturation of cattle oocytes and their subsequent development following in vitro fertilization. Mol. Reprod. Dev. 54, 86–91.
CrossRef | PubMed | CAS |

Luciano, A. M. , Modina, S. , Vassena, R. , Milanesi, E. , Lauria, A. , and Gandolfi, F. (2004). Role of intracellular cyclic adenosine 3′,5′-monophosphate concentration and oocyte–cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocytes. Biol. Reprod. 70, 465–472.
CrossRef | PubMed | CAS |

Mai, Q. , Yu, Y. , Li, T. , Wang, L. , Chen, M. J. , Huang, S. Z. , Zhou, C. , and Zhou, Q. (2007). Derivation of human embryonic stem cell lines from parthenogenetic blastocysts. Cell Res. 17, 1008–1019.
CrossRef | PubMed | CAS |

Maro, B. , Howlett, S. K. , and Webb, M. (1985). Non-spindle microtubule organizing centers in metaphase II-arrested mouse oocytes. J. Cell Biol. 101, 1665–1672.
CrossRef | PubMed | CAS |

McKenzie, L. J. , Pangas, S. A. , Carson, S. A. , Kovanci, E. , Cisneros, P. , Buster, J. E. , Amato, P. , and Matzuk, M. M. (2004). Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF. Hum. Reprod. 19, 2869–2874.
CrossRef | PubMed | CAS |

Mehlmann, L. M. (2005). Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction 130, 791–799.
CrossRef | PubMed | CAS |

Moor, R. M. , and Gandolfi, F. (1987). Molecular and cellular changes associated with maturation and early development of sheep eggs. J. Reprod. Fertil. Suppl. 34, 55–69.
PubMed | |  CAS |

Muggleton-Harris, A. L. , and Brown, J. J. (1988). Cytoplasmic factors influence mitochondrial reorganization and resumption of cleavage during culture of early mouse embryos. Hum. Reprod. 3, 1020–1028.
PubMed | |  CAS |

Pangas, S. A. , and Matzuk, M. M. (2005). The art and artifact of GDF9 activity: cumulus expansion and the cumulus expansion-enabling factor. Biol. Reprod. 73, 582–585.
CrossRef | CAS | PubMed |

Park, J. Y. , Su, Y. Q. , Ariga, M. , Law, E. , Jin, S. L. , and Conti, M. (2004). EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303, 682–684.
CrossRef | PubMed | CAS |

Pisani, L. F. , Antonini, S. , Pocar, P. , Ferrari, S. , Brevini, T. A. , Rhind, S. M. , and Gandolfi, F. (2008). Effects of pre-mating nutrition on mRNA levels of developmentally relevant genes in sheep oocytes and granulosa cells. Reproduction 136, 303–312.
CrossRef | PubMed | CAS |

Pocar, P. , Brevini, T. A. , Perazzoli, F. , Cillo, F. , Modina, S. , and Gandolfi, F. (2001). Cellular and molecular mechanisms mediating the effects of polychlorinated biphenyls on oocyte developmental competence in cattle. Mol. Reprod. Dev. 60, 535–541.
CrossRef | PubMed | CAS |

Racki, W. J. , and Richter, J. D. (2006). CPEB controls oocyte growth and follicle development in the mouse. Development 133, 4527–4537.
CrossRef | PubMed | CAS |

Ragni, G. , Allegra, A. , Anserini, P. , Causio, F. , Ferraretti, A. P. , Greco, E. , Palermo, R. , and Somigliana, E. (2005). The 2004 Italian legislation regulating assisted reproduction technology: a multicentre survey on the results of IVF cycles. Hum. Reprod. 20, 2224–2228.
CrossRef | PubMed | CAS |

Renard, J. P. (1998). Chromatin remodelling and nuclear reprogramming at the onset of embryonic development in mammals. Reprod. Fertil. Dev. 10, 573–580.
CrossRef | PubMed | CAS |

Revazova, E. S. , Turovets, N. A. , Kochetkova, O. D. , Kindarova, L. B. , Kuzmichev, L. N. , Janus, J. D. , and Pryzhkova, M. V. (2007). Patient-specific stem cell lines derived from human parthenogenetic blastocysts. Cloning Stem Cells 9, 432–449.
CrossRef | PubMed | CAS |

Schliwa, M. , and Woehlke, G. (2003). Molecular motors. Nature 422, 759–765.
CrossRef | PubMed | CAS |

Scott, L. (2003). The biological basis of non-invasive strategies for selection of human oocytes and embryos. Hum. Reprod. Update 9, 237–249.
CrossRef | PubMed |

Sirard, M. A. (2001). Resumption of meiosis: mechanism involved in meiotic progression and its relation with developmental competence. Theriogenology 55, 1241–1254.
CrossRef | CAS | PubMed |

Sritanaudomchai, H. , Pavasuthipaisit, K. , Kitiyanant, Y. , Kupradinun, P. , Mitalipov, S. , and Kusamran, T. (2007). Characterization and multilineage differentiation of embryonic stem cells derived from a buffalo parthenogenetic embryo. Mol. Reprod. Dev. 74, 1295–1302.
CrossRef | PubMed | CAS |

Stojkovic, M. , Machado, S. A. , Stojkovic, P. , Zakhartchenko, V. , Hutzler, P. , Goncalves, P. B. , and Wolf, E. (2001). Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biol. Reprod. 64, 904–909.
CrossRef | PubMed | CAS |

Sun, Q. Y. , Lai, L. , Wu, G. M. , Park, K. W. , Day, B. N. , Prather, R. S. , and Schatten, H. (2001a). Microtubule assembly after treatment of pig oocytes with taxol: correlation with chromosomes, gamma-tubulin and MAP kinase. Mol. Reprod. Dev. 60, 481–490.
CrossRef | PubMed | CAS |

Sun, Q. Y. , Wu, G. M. , Lai, L. , Park, K. W. , Cabot, R. , Cheong, H. T. , Day, B. N. , Prather, R. S. , and Schatten, H. (2001b). Translocation of active mitochondria during pig oocyte maturation, fertilization and early embryo development in vitro. Reproduction 122, 155–163.
CrossRef | PubMed | CAS |

Szabo, P. , and Mann, J. R. (1994). Expression and methylation of imprinted genes during in vitro differentiation of mouse parthenogenetic and androgenetic embryonic stem cell lines. Development 120, 1651–1660.
PubMed | |  CAS |

Talbot, N. C. , Caperna, T. J. , Powell, A. M. , Garrett, W. M. , and Ealy, A. D. (2004). Isolation and characterization of a bovine trophectoderm cell line derived from a parthenogenetic blastocyst. Mol. Reprod. Dev. 69, 164–173.
CrossRef | PubMed | CAS |

Talbot, N. C. , Caperna, T. J. , Powell, A. M. , Ealy, A. D. , Blomberg, L. A. , and Garrett, W. M. (2005). Isolation and characterization of a bovine visceral endoderm cell line derived from a parthenogenetic blastocyst. In Vitro Cell. Dev. Biol. Anim. 41, 130–141.
CrossRef | PubMed | CAS |

Tan, J. H. , Wang, H. L. , Sun, X. S. , Liu, Y. , Sui, H. S. , and Zhang, J. (2009). Chromatin configurations in the germinal vesicle of mammalian oocytes. Mol. Hum. Reprod. 15, 1–9.
CrossRef | PubMed | CAS |

Tang, F. , Kaneda, M. , O’Carroll, D. , Hajkova, P. , Barton, S. C. , Sun, Y. A. , Lee, C. , Tarakhovsky, A. , Lao, K. , and Surani, M. A. (2007). Maternal microRNAs are essential for mouse zygotic development. Genes Dev. 21, 644–648.
CrossRef | PubMed | CAS |

Telford, N. A. , Watson, A. J. , and Schultz, G. A. (1990). Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol. Reprod. Dev. 26, 90–100.
CrossRef | PubMed | CAS |

Tesfaye, D. , Worku, D. , Rings, F. , Phatsara, C. , Tholen, E. , Schellander, K. , and Hoelker, M. (2009). Identification and expression profiling of microRNAs during bovine oocyte maturation using heterologous approach. Mol. Reprod. Dev. 76, 665–677.
CrossRef | PubMed | CAS |

Thomas, F. H. , Walters, K. A. , and Telfer, E. E. (2003). How to make a good oocyte: an update on in vitro models to study follicle regulation. Hum. Reprod. Update 9, 541–555.
CrossRef | PubMed |

Tokuyama, O. , Nakamura, Y. , Musoh, A. , Honda, K. , Ozaki, K. , and Ishiko, O. (2003). Expression and distribution of cyclooxygenase-2 in human ovary during follicular development. Osaka City Med. J. 49, 39–47.
PubMed | |  CAS |

Torner, H. , Brussow, K. P. , Alm, H. , Ratky, J. , Pohland, R. , Tuchscherer, A. , and Kanitz, W. (2004). Mitochondrial aggregation patterns and activity in porcine oocytes and apoptosis in surrounding cumulus cells depend on the stage of pre-ovulatory maturation. Theriogenology 61, 1675–1689.
CrossRef | PubMed | CAS |

Tremoleda, J. L. , Schoevers, E. J. , Stout, T. A. , Colenbrander, B. , and Bevers, M. M. (2001). Organisation of the cytoskeleton during in vitro maturation of horse oocytes. Mol. Reprod. Dev. 60, 260–269.
CrossRef | PubMed | CAS |

van Wagtendonk-de Leeuw, A. M. , Mullaart, E. , de Roos, A. P. W. , Merton, J. S. , den Daas, J. H. G. , Kemp, B. , and Ruígh, L. (2000). Effects of different reproduction techniques: AI, MOET or IVP, on health and welfare of bovine offspring. Theriogenology 53, 575–597.
CrossRef | PubMed | CAS |

Veeck L. L. (1999). ‘An Atlas of Human Gametes and Conceptuses: An Illustrated Reference for Assisted Reproductive Technology.’ (The Parthenon Publishing Group: New York.)

Vrana, K. E. , Hipp, J. D. , Goss, A. M. , McCool, B. A. , and Riddle, D. R. , et al. (2003). Nonhuman primate parthenogenetic stem cells. Proc. Natl. Acad. Sci. USA 100(Suppl. 1), 11 911–11 916.
CrossRef | PubMed | CAS |

Wang, S. , Tang, X. , Niu, Y. , Chen, H. , Li, B. , Li, T. , Zhang, X. , Hu, Z. , and Ji, W. (2007). Generation and characterization of rabbit embryonic stem cells. Stem Cells 25, 481–489.
CrossRef | PubMed | CAS |

Watson, A. J. , Westhusin, M. E. , De Sousa, P. A. , Betts, D. H. , and Barcroft, L. C. (1999). Gene expression regulating blastocyst formation. Theriogenology 51, 117–133.
CrossRef | PubMed | CAS |

Wickham, L. , Duchaine, T. , Luo, M. , Nabi, I. R. , and DesGroseillers, L. (1999). Mammalian staufen is a double-stranded RNA- and tubulin-binding protein which localizes to the rough endoplasmic reticulum. Mol. Cell. Biol. 19, 2220–2230.
PubMed | |  CAS |

Ye, X. , Hama, K. , Contos, J. J. , Anliker, B. , and Inoue, A. , et al. (2005). LPA3-mediated lysophosphatidic acid signalling in embryo implantation and spacing. Nature 435, 104–108.
CrossRef | PubMed | CAS |

Yoon, Y. J. , and Mowry, K. L. (2004). Xenopus Staufen is a component of a ribonucleoprotein complex containing Vg1 RNA and kinesin. Development 131, 3035–3045.
CrossRef | PubMed | CAS |

Zhang, X. , Jafari, N. , Barnes, R. B. , Confino, E. , Milad, M. , and Kazer, R. R. (2005). Studies of gene expression in human cumulus cells indicate pentraxin 3 as a possible marker for oocyte quality. Fertil. Steril. 83(Suppl. 1), 1169–1179.
CrossRef | PubMed | CAS |



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