Effect of follicle size on mRNA expression in cumulus cells and oocytes of Bos indicus: an approach to identify marker genes for developmental competence
Ester Siqueira Caixeta A , Paula Ripamonte C , Maurício Machaim Franco A B , José Buratini Junior C and Margot Alves Nunes Dode A B DA Faculdade de Agronomia e Veterinária, Ciências Animais, Universidade de Brasília, Brasília, DF 70910-970, Brazil.
B Embrapa Recursos Genéticos e Biotecnologia, Brasília, DF 70770-900, Brazil.
C Departamento de Fisiologia, Instituto de Biociências, Universidade Estadual Paulista, Botucatu, SP 18618-000, Brazil.
D Corresponding author. Email: margot@cenargen.embrapa.br
Reproduction, Fertility and Development 21(5) 655-664 https://doi.org/10.1071/RD08201
Submitted: 18 September 2008 Accepted: 8 March 2009 Published: 21 May 2009
Abstract
To identify the genes related to oocyte competence, we quantified transcripts for candidate genes in oocytes (H1Foo, H2A, H3A, GHR, GDF9, BMP15, OOSP1) and cumulus cells (FSHR, EGFR, GHR, PTX3, IGFII) using the follicle size model to select oocytes of better developmental quality. Follicles were dissected and distributed into four groups according to diameter as follows: 1.0–3.0, 3.1–6.0, 6.1–8.0 and ≥8.1 mm. Cumulus–oocyte complexes (COCs) were released, classified morphologically, matured, fertilised and cultured in vitro or denuded for measurement of diameter and determination of gene expression. Denuded germinal vesicle oocytes and their cumulus cells were used for gene expression analysis by reverse transcription–polymerase chain reaction. The blastocyst rate was highest for oocytes recovered from follicles >6 mm in diameter. In the oocyte, expression of the H2A transcript only increased gradually according to follicle size, being greater (P < 0.05) in oocytes from follicles ≥8.1 mm in diameter than in oocytes from follicles <6.0 mm in diameter. In cumulus cells, expression of FSHR, EGFR and GHR mRNA increased with follicular size. In conclusion, we confirmed the importance of H2A for developmental competence and identified important genes in cumulus cells that may be associated with oocyte competence.
Additional keywords: bovine, gene expression.
Acknowledgements
The authors thank Grazieli Marinheiro Machado for helping with in vitro embryo production. This work was supported by Embrapa and CAPES.
Allard, P. , Champigny, M. J. , Skoggard, S. , Erkmann, J. A. , Whitfield, M. L. , Marzluff, W. F. , and Clarke, H. J. (2002). Stem-loop binding protein accumulates during oocyte maturation and is not cell-cycle-regulated in the early mouse embryo. J. Cell Sci. 115, 4577–4586.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Allard, P. , Yang, Q. , Marzluff, W. F. , and Clarke, H. J. (2005). The stem-loop binding protein regulates translation of histone mRNA during mammalian oogenesis. Dev. Biol. 286, 195–206.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Armstrong, D. G. , Baxter, G. , Hogg, C. O. , and Woad, K. J. (2002). Insulin-like growth factor (IGF) system in the oocyte and somatic cells of bovine preantral follicles. Reproduction 123, 789–797.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Arnold, D. R. , Françon, P. , Zhang, J. , Martin, K. , and Clarke, H. J. (2008). Stem-loop binding protein expressed in growing oocytes is required for accumulation of mRNAs encoding histones H3 and H4 and for early embryonic development in the mouse. Dev. Biol. 313, 347–358.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Ashkenazi, H. , Cao, X. , Motola, S. , Popliker, M. , Conti, M. , and Tsafriri, A. (2005). Epidermal growth factor family members: endogenous mediators of the ovulatory response. Endocrinology 146, 77–84.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Assidi, M. , Dufort, I. , Ali, A. , Hamel, M. , Algriany, O. , Dielemann, S. , and Sirard, M. A. (2008). Identification of potential markers of oocyte competence expressed in bovine cumulus cells matured with follicle-stimulating hormone and/or phorbol myristate acetate in vitro. Biol. Reprod. 79, 209–222.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Baran, V. , Pavlok, A. , Bjerregaard, B. , Wrenzycki, C. , Hermann, D. , Philimonenko, V. V. , Lapathitis, G. , Hozak, P. , Niemann, H. , and Motlik, J. (2004). Immunolocalization of upstream binding factor and pocket protein p130 during final stages of bovine oocyte growth. Biol. Reprod. 70, 877–886.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Baruselli, P. S. , Gimenes, L. U. , and Sales, J. N. S. (2007). Fisiologia reprodutiva de fêmeas taurinas e zebuínas. Rev. Bras. Reprod. Anim. 31, 205–211.
Bettegowda, A. , Patel, O. V. , Lee, K. B. , Park, K. E. , Salem, M. , Yao, J. , Ireland, J. J. , and Smith, G. W. (2008). Identification of novel bovine cumulus cell molecular markers predictive of oocyte competence: functional and diagnostic implications. Biol. Reprod. 79, 301–309.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Bevers, M. M. , and Izadyar, F. (2002). Role of growth hormone and growth hormone receptor in oocyte maturation. Mol. Cell. Endocrinol. 197, 173–178.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Brevini-Gandolfi, T. A. , and Gandolfi, F. (2001). The maternal legacy to the embryo: cytoplasmic components and their effects on early development. Theriogenology 55, 1255–1276.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Calder, M. D. , Caveney, A. N. , Smith, L. C. , and Watson, A. J. (2003). Responsiveness of bovine cumulus–oocyte-complexes (COC) to porcine and recombinant human FSH, and the effect of COC quality on gonadotropin receptor and Cx43 marker gene mRNAs during maturation in vitro. Reprod. Biol. Endocrinol. 1, 14.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cillo, F. , Brevini, T. A. L. , Antonini, S. , Paffoni, A. , and Ragni, G. (2007). Association between human oocyte developmental competence and expression levels of some cumulus genes. Reproduction 134, 645–650.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Conti, M. , Hsieh, M. , Park, J. Y. , and Su, Y. Q. (2006). Role of the epidermal growth factor network in ovarian follicles. Mol. Endocrinol. 20, 715–723.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Coticchio, G. , Sereni, E. , Serrao, L. , Mazzone, S. , Iadarola, I. , and Borini, A. (2004). What criteria for the definition of oocyte quality? Ann. N. Y. Acad. Sci. 1034, 132–144.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
de Wit, A. A. C. , Wurth, Y. A. , and Kruip, T. A. M. (2000). Effect of ovarian phase and follicle quality on morphology and developmental capacity of the bovine cumulus–oocyte complex. J. Anim. Sci. 78, 1277–1283.
| PubMed | CAS |
Dode, M. A. N. , Dufort, I. , Massicotte, L. , and Sirard, M. A. (2006). Quantitative expression of candidate genes for developmental competence in bovine two-cell embryos. Mol. Reprod. Dev. 73, 288–297.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Donnison, M. , and Pfeffer, P. L. (2004). Isolation of genes associated with developmentally competent bovine oocytes and quantitation of their levels during development. Biol. Reprod. 71, 1813–1821.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Fair, T. (2003). Follicular oocyte growth and acquisition of developmental competence. Anim. Reprod. Sci. 78, 203–216.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Fair, T. , Hyttel, P. , and Greve, T. (1995). Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol. Reprod. Dev. 42, 437–442.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Fair, T. , Murphy, M. , Rizos, D. , Moss, C. , Martin, F. , Boland, M. P. , and Lonergan, P. (2004). Analysis of differential maternal mRNA expression in developmentally competent and incompetent bovine two-cell embryos. Mol. Reprod. Dev. 67, 136–144.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Feuerstein, P. , Cadoret, V. , Dalbies-Tran, R. , Guerif, F. , Bidault, R. , and Royere, D. (2007). Gene expression in human cumulus cells: one approach to oocyte competence. Hum. Reprod. 22, 3069–3077.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Figueiredo, R. A. , Barros, C. M. , Rocha, G. P. , and Papa, F. O. (1995). Prevalência de duas ondas de crescimento folicular ovariano em vacas da raça Nelore. Rev. Bras. Reprod. Anim. 19, 200–209.
Gall, L. , Chene, N. , Dahirel, M. , Ruffini, S. , and Boulesteix, C. (2004). Expression of epidermal growth factor receptor in the goat cumulus–oocyte complex. Mol. Reprod. Dev. 67, 439–445.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Gandolfi, F. , Brevini, T. A. L. , 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 |
Gao, S. , Chung, Y. G. , Parseghian, M. H. , King, G. J. , Adashi, E. Y. , and Latham, K. E. (2004). Rapid H1 linker histone transitions following fertilization or somatic cell nuclear transfer: evidence for a uniform developmental program in mice. Dev. Biol. 266, 62–75.
| Crossref | GoogleScholarGoogle Scholar | 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 | GoogleScholarGoogle Scholar |
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 | GoogleScholarGoogle Scholar | PubMed | CAS |
Hastie, P. M. , and Haresign, W. (2006). Expression of mRNAs encoding insulin-like growth factor (IGF) ligands, IGF receptors and IGF binding proteins during follicular growth and atresia in the ovine ovary throughout the oestrous cycle. Anim. Reprod. Sci. 92, 284–299.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Holm, P. , Booth, P. J. , Schmidt, M. H. , Greve, T. , and Callesen, H. (1999). High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum proteins. Theriogenology 52, 683–700.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Izadyar, F. , Hage, W. J. , Colenbrander, B. , and Bevers, M. M. (1998). The promontory effect of growth hormone on the developmental competence of in vitro matured bovine oocytes is due to improved cytoplasmic maturation. Mol. Reprod. Dev. 49, 444–453.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Jamnongjit, M. , Gill, A. , and Hammes, S. R. (2005). Epidermal growth factor receptor signaling is required for normal ovarian steroidogenesis and oocyte maturation. Proc. Natl Acad. Sci. USA 102, 16 257–16 262.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Juengel, J. L. , Bodensteiner, K. J. , Heath, D. A. , Hudson, N. L. , Moeller, C. L. , Smith, P. , Galloway, S. M. , Davis, G. H. , Sawyer, H. R. , and McNatty, K. P. (2004). Physiology of GDF9 and BMP15 signalling molecules. Anim. Reprod. Sci. 82–83, 447–460.
| Crossref | GoogleScholarGoogle Scholar |
Kauffold, J. , Am, H. A. , Bergfeld, U. , Weber, W. , and Sobiraj, A. (2005). The in vitro developmental competence of oocytes from juvenile calves is related to follicular diameter. J. Reprod. Dev. 51, 325–332.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kölle, S. , Sinowatz, F. , Boie, G. , and Lincoln, D. (1998). Developmental changes in the expression of the growth hormone receptor messenger ribonucleic acid and protein in the bovine ovary. Biol. Reprod. 59, 836–842.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kölle, S. , Stojkovic, M. , Boie, G. , Wolf, E. , and Sinowatz, F. (2003). Growth hormone-related effects on apoptosis, mitosis, and expression of Connexin 43 in bovine in vitro maturation cumulus–oocyte complexes. Biol. Reprod. 68, 1584–1589.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Krisher, R. L. (2004). The effect of oocyte quality on development. J. Anim. Sci. 82, 14–23.
Lequarre, A. S. , Vigneron, C. , Ribaucour, F. , Holm, P. , Donnay, I. , Dalbiès-Tran, R. , Callesen, H. , and Mermillod, P. (2005). Influence of antral follicle size on oocyte characteristics and embryo development in the bovine. Theriogenology 63, 841–859.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lonergan, P. , Monaghan, P. , Rizos, D. , Boland, M. P. , and Gordon, I. (1994). Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro. Mol. Reprod. Dev. 37, 48–53.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
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 | GoogleScholarGoogle Scholar | PubMed | CAS |
Machatkova, M. , Krausova, K. , Jokesova, E. , and Tomanek, M. (2004). Developmental competence of bovine oocytes: effects of follicle size and the phase of follicular wave on in vitro embryo production. Theriogenology 61, 329–335.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Maddox-Hyttel, P. , Bjerregaard, B. , and Laurincik, J. (2005). Meiosis and embryo technology: renaissance of the nucleolus. Reprod. Fertil. Dev. 17, 3–14.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
McGraw, S. , Vigneault, C. , Tremblay, K. , and Sirard, M. A. (2006). Characterization of linker histone H1FOO during bovine in vitro embryo development. Mol. Reprod. Dev. 73, 692–699.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Memili, E. , and First, N. L. (2000). Zygotic and embryonic gene expression in cow: a review of timimng and mechanism of early gene expression as compared with others species. Zygote 8, 87–96.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Mourot, M. , Dufort, I. , Gravel, C. , Algriany, O. , Dieleman, S. , and Sirard, M. A. (2006). The influence of follicle size, FSH-enriched maturation medium, and early cleavage on bovine oocyte maternal mRNA levels. Mol. Reprod. Dev. 73, 1367–1379.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Mutiga, E. R. , Mukasa-Mugerwa, E. , and Azag, T. (1993). Luteolytic effect of PGF2α in Boran and Boran × Friesian cross-breed heifers. J. Agric. Sci. 120, 103–106.
| Crossref | GoogleScholarGoogle Scholar | CAS |
Narita, T. , Yung, T. M. C. , Yamamoto, J. , Tsuboi, Y. , Tanabe, H. , Tanaka, K. , Yamaguchi, Y. , and Handa, H. (2007). NELF interacts with CBC and participates in 3′ end processing of replication-dependent histone mRNAs. Mol. Cell 26, 349–365.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Nuttinck, F. , Charpigny, G. , Mermillod, P. , Loosfelt, H. , Meduri, G. , Freret, S. , Grimard, B. , and Heyman, Y. (2004). Expression of components of the insulin-like growth factor system and gonadotropin receptors in bovine cumulus–oocyte complexes during oocyte maturation. Domest. Anim. Endocrinol. 27, 179–195.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Oyamada, T. , Iwayama, H. , and Fukui, Y. (2004). Additional effect of epidermal growth factor during in vitro maturation for individual bovine oocytes using a chemically defined medium. Zygote 12, 143–150.
| Crossref | GoogleScholarGoogle Scholar | 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 | GoogleScholarGoogle Scholar | PubMed | CAS |
Parrish, J. J. , Susjo-Parrish, J. L. , Winer, M. A. , and First, N. L. (1988). Capacitation of bovine sperm by heparin. Biol. Reprod. 38, 1171–1180.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Parrish, J. J. , Krogenaes, A. , and Susko-Parrish, J. L. (1995). Effect of bovine sperm separation by either swim-up or Percoll method on success of in vitro fertilization and early embryonic development. Theriogenology 44, 859–869.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Patel, O. V. , Bettegowda, A. , Ireland, J. J. , Coussens, P. M. , Lonergan, P. , and Smith, G. W. (2007). Functional genomics studies of oocyte competence: evidence that reduced transcript abundance for follistatin is associated with poor development competence of bovine oocytes. Reproduction 133, 95–106.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Pavlok, A. , Lucas-Hahn, A. , and Niemann, H. (1992). Fertilization and developmental competence of bovine oocytes derived from different categories of antral follicles. Mol. Reprod. Dev. 31, 63–67.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Racedo, S. E. , Wrenzycki, C. , Herrmann, D. , Salamone, D. , and Niemann, H. (2008). Effects of follicle size and stages of maturation on mRNA expression in bovine in vitro matured oocytes. Mol. Reprod. Dev. 75, 17–25.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ramakers, C. , Ruijter, J. M. , Deprez, R. H. , and Moorman, A. F. (2003). Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339, 62–66.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Robert, C. , Barnes, F. L. , Hue, I. , and Sirard, M. A. (2000). Subtractive hybridization used to identify mRNA associated with the maturation of bovine oocytes. Mol. Reprod. Dev. 57, 167–175.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Sirard, M. A. , Richard, F. , Blondin, P. , and Robert, C. (2006). Contribution of the oocyte to embryo quality. Theriogenology 65, 126–136.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Song, J. L. , and Wessel, G. M. (2005). How to make an egg: transcriptional regulation in oocytes. Differentiation 73, 1–17.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Stojkovic, M. , Machado, S. A. , Stojkovic, P. , Zakhartchenko, V. , Hutzler, P. , Gonçalves, 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 | GoogleScholarGoogle Scholar | PubMed | CAS |
Sturm, R. A. , Dalton, S. , and Wells, J. R. E. (1988). Conservation of histone H2A/HB intergene regions: a role for the H2B specific element in divergent transcription. Nucleic Acids Res. 16, 8571–8586.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Su, Y. Q. , Wu, X. , Brien, M. J. O. , Pendola, F. L. , Denegre, J. N. , Matzuk, M. M. , and Eppig, J. J. (2004). Synergistic roles of BMP15 and GDF9 in the development and function of the oocyte–cumulus cell complex in mice: genetic evidence for an oocyte–granulosa cell regulatory loop. Dev. Biol. 276, 64–73.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Tanaka, M. , Kihara, M. , Meczekalski, B. , King, G. J. , and Adashi, E. Y. (2003). H1oo: a pre-embryonic H1 linker histone in search of a function. Mol. Cell. Endocrinol. 202, 5–9.
| PubMed | CAS |
Tanaka, M. , Kihara, M. , Hennebold, J. D. , Eppig, J. J. , and Viveiros, M. M. , et al. (2005). H1FOO is coupled to the initiation of oocytic growth. Biol. Reprod. 72, 135–142.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Tanghe, S. , Van Soom, A. , Nauwynck, H. , Coryn, M. , and de Kruif, A. (2002). Minireview: functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol. Reprod. Dev. 61, 414–424.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Tremblay, K. , Vigneault, C. , McGraw, S. , Morin, G. , and Sirard, M. A. (2006). Identification and characterization of a novel bovine oocyte-specific secreted protein gene. Gene 375, 44–53.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Vandesompele, J. , Preter, K. D. , Pattyn, F. , Poppe, B. , Roy, N. V. , Paepe, A. D. , and Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, research0034.1–research0034.11.
| Crossref | GoogleScholarGoogle Scholar |
Wu, X. , and Matzuk, M. M. (2002). GDF-9 and BMP-15: oocyte organizers. Rev. Endocr. Metab. Disord. 3, 27–32.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Yaseen, M. A. , Wrenzycki, C. , Herrmann, D. , Carnwath, J. W. , and Niemann, H. (2001). Changes in the relative abundance of mRNA transcripts for insulin-like growth factor (IGF-I and IGF-II) ligands and their receptors (IGF-IR/IGF-IIR) in preimplantation bovine embryos derived from different in vitro systems. Reproduction 122, 601–610.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Yuan, W. , Lucy, M. C. , and Smith, M. F. (1996). Messenger ribonucleic acid for insulin-like growth factors-I and -II, insulin-like growth factor-binding protein-2, gonadotropin receptors, and steroidogenic enzymes in porcine follicles. Biol. Reprod. 55, 1045–1054.
| Crossref | GoogleScholarGoogle Scholar | 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, 1169–1179.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |
Zhu, G. , Guo, B. , Pan, D. , Mu, Y. , and Feng, S. (2008). Expression of bone morphogenetic proteins and receptors in porcine cumulus–oocyte complexes during in vitro maturation. Anim. Reprod. Sci. 104, 275–283.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |