Effect of follicle size on mRNA expression in cumulus cells and oocytes of Bos indicus: An approach to identify marker genes for developmental competence

Reproduction, Fertility and Development

Volumn 21, Issue 5, 2009, Pages 655-664

  Caixeta, Ester Siqueira ^a   Ripamonte, Paula ^c   Franco, Maurcio MacHaim ^a,b   Junior, Joś Buratini ^c   Dode, Margot Alves Nunes ^a,b  

^a UNIVERSITY OF BRASILIA   (Brazil)

^b EMBRAPA RECURSOS GENÉTICOS E BIOTECNOLOGIA   (Brazil)

^c SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Bovine; Gene expression

Indexed keywords

BONE MORPHOGENETIC PROTEIN 15; CELL PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; FOLLITROPIN RECEPTOR; GROWTH DIFFERENTIATION FACTOR 9; GROWTH HORMONE RECEPTOR; HISTONE H2A; HISTONE H3; HISTONE H3A; MESSENGER RNA; OOCYTE SECRETED PROTEIN 1; PENTRAXIN 3; SOMATOMEDIN B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLASTOCYTE; BOS INDICUS; CATTLE; CELL CULTURE; CELL STRUCTURE; CONTROLLED STUDY; CUMULUS CELL; DEVELOPMENTAL GENE; FEMALE; FERTILIZATION; GENE AMPLIFICATION; GENE EXPRESSION; GENE IDENTIFICATION; GERMINAL VESICLE; H1FOO GENE; IN VITRO STUDY; MALE; NONHUMAN; OOCYTE; OVARY FOLLICLE DEVELOPMENT; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; BLASTOCYST; CATTLE; CELL COMMUNICATION; CELLS, CULTURED; CUMULUS CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC MARKERS; HISTONES; OOCYTES; OVARIAN FOLLICLE; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, FSH; RECEPTORS, SOMATOTROPIN; RNA, MESSENGER;

BOS INDICUS; BOVINAE;

EID: 67649708613     PISSN: 10313613     EISSN: None     Source Type: Journal    
DOI: 10.1071/RD08201     Document Type: Article

References (73)

1. 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 andisnot cell-cycle-regulated in the early mouse embryo. J. Cell Sci. 115, 4577-4586. doi:10.1242/ JCS.00132
2. 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. doi:10.1016/ J.YDBIO.2005.07.023
3. Armstrong, D. G., Baxter, G., Hogg, C. O., and Woad, K. J. (2002). Insulinlike growth factor (IGF) system in the oocyte and somatic cells of bovine preantral follicles. Reproduction 123, 789-797. doi:10.1530/ REP.0.1230789
4. 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. doi:10.1016/J.YDBIO.2007.10.032
5. 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. doi:10.1210/ EN.2004-0588
6. 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. doi:10.1095/BIOLREPROD.108.067686
7. Baran, V., Pavlok, A., Bjerregaard, B., Wrenzycki, C., Hermann, D., Philimo-nenko,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. doi:10.1095/BIOLREPROD.103.018408
8. Baruselli, P. S., Gimenes, L. U., and Sales, J. N. S. (2007). Fisiologia reprodutiva de femeas taurinas e zebuínas. Rev. Bras. Reprod. Anim. 31, 205-211.
9. 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. doi:10.1095/BIOLREPROD.107.067223
10. Bevers, M. M., and Izadyar, F. (2002). Role of growth hormone and growth hormone receptor in oocyte maturation. Mol. Cell. Endocrinol. 197, 173-178. doi:10.1016/S0303-7207(02)00270-8
11. Brevini-Gandolfi, T. A., and Gandolfi, F. (2001). The maternal legacy to the embryo: cytoplasmic components and their effectsonearly development. Theriogenology 55, 1255-1276. doi:10.1016/S0093-691X(01)00481-2
12. Calder,M.D., Caveney,A.N., Smith,L.C., andWatson,A.J.(2003). Responsiveness of bovine cumulus-oocyte-complexes (COC) to porcine and recombinant human FSH, and the effect of COC quality ongonadotropin receptor and Cx43 marker gene mRNAs during maturation in vitro. Reprod. Biol. Endocrinol. 1, 14. doi:10.1186/1477-7827-1-14
13. 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. doi:10.1530/REP-07-0182
14. Conti, M., Hsieh, M., Park, J.Y., and Su,Y. Q. (2006). Role of the epidermal growthfactor networkinovarian follicles. Mol. Endocrinol. 20, 715-723. doi:10.1210/ME.2005-0185
15. Coticchio, G., Sereni, E., Serrao, L., Mazzone, S., Iadarola, I., and Borini,A. (2004). What criteria for the definition ofoocyte quality?Ann. N. Y.Acad. Sci. 1034, 132-144. doi:10.1196/ANNALS.1335.016
16. 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.
17. 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. doi:10.1002/MRD.20427
18. 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. doi:10.1095/BIOLREPROD.104.032367
19. Fair, T. (2003). Follicular oocyte growth and acquisition of developmental competence. Anim. Reprod. Sci. 78, 203-216. doi:10.1016/S0378-4320(03)00091-5
20. Fair,T., Hyttel, P., and Greve,T. (1995). Bovine oocyte diameter inrelation to maturational competence and transcriptional activity. Mol. Reprod. Dev. 42, 437-442. doi:10.1002/MRD.1080420410
21. 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. doi:10.1002/MRD.10385
22. 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. doi:10.1093/HUMREP/DEM336
23. Figueiredo, R. A., Barros, C. M., Rocha, G. P., and Papa, F. O. (1995). Prevalencia de duas ondas de crescimento folicular ovariano em vacas da raça Nelore. Rev. Bras. Reprod. Anim. 19, 200-209.
24. 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. doi:10.1002/ MRD.20040
25. 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.
26. 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. doi:10.1016/J.YDBIO.2003.10.003
27. 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. doi:10.1016/J.ANIREPROSCI.2004.05.017
28. 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. doi:10.1002/(SICI)1098-2795(199908)53:4451::AID-MRD11>3. 0.CO;2-3
29. 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. doi:10.1016/J.ANIREPROSCI. 2005.05.022
30. 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. doi:10.1016/J.ANIREPROSCI.2005.05.022
31. 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. doi:10.1002/(SICI)1098-2795(199804) 49:4<444::AID-MRD12>3.0.CO;2-U
32. 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. doi:10.1073/PNAS.0508521102
33. 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. doi:10.1016/ J.ANIREPROSCI.2004.04.021
34. 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. doi:10.1262/ JRD.17002
35. 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. doi:10.1095/BIOLREPROD59.4.836
36. 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. doi:10.1095/BIOLREPROD.102.010264
37. Krisher, R. L. (2004). The effect of oocyte quality on development. J. Anim. Sci. 82, 14-23.
38. 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. doi:10.1016/ J.THERIOGENOLOGY.2004.05.015
39. 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. doi:10.1002/MRD.1080370107
40. 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. doi:10.1046/J.1439-0531.2003.00437.X
41. 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. doi:10.1016/S0093-691X(03)00216-4
42. Maddox-Hyttel, P., Bjerregaard, B., and Laurincik, J. (2005). Meiosis and embryo technology: renaissance of the nucleolus. Reprod. Fertil. Dev. 17, 3-14. doi:10.1071/RD04108
43. 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. doi:10.1002/MRD.20448
44. 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. doi:10.1017/ S0967199400000861
45. 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. doi:10.1002/MRD.20585
46. a in Boran and Boran × Friesian cross-breed heifers. J. Agric. Sci. 120, 103-106. doi:10.1017/S0021859600073652
47. 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. doi:10.1016/J.MOLCEL.2007.04.011
48. 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. doi:10.1016/ J.DOMANIEND.2004.03.003
49. 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. doi:10.1017/S0967199404002710
50. 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. doi:10.1095/BIOLREPROD.105.042127
51. 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.
52. 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. doi:10.1016/0093-691X(95)00271-9
53. 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. doi:10.1530/REP.1.01123
54. 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. doi:10.1002/ MRD.1080310111
55. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45. doi:10.1093/ NAR/29.9.E45
56. Racedo, S.E., Wrenzycki, C., Herrmann, D., Salamone, D., and Niemann, H. (2008). Effectsof follicle size and stagesofmaturationonmRNA expression in bovine in vitro matured oocytes. Mol. Reprod. Dev. 75, 17-25. doi:10.1002/MRD.20770
57. 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. doi:10.1016/S0304-3940(02) 01423-4
58. 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. doi:10.1002/1098- 2795(200010)57:2<167::AID-MRD8>3.0.CO;2-P
59. Sirard, M. A., Richard, F., Blondin, P., and Robert, C. (2006). Contribution of the oocyte to embryo quality. Theriogenology 65, 126-136. doi:10.1016/J.THERIOGENOLOGY.2005.09.020
60. Song, J. L., and Wessel, G. M. (2005). How to make an egg: transcriptional regulation in oocytes. Differentiation 73, 1-17. doi:10.1111/J.1432-0436.2005.07301005.X
61. Stojkovic, M., Machado, S. A., Stojkovic, P., Zakhartchenko, V., Hutzler, P., Gonçalves, P. B., and Wolf, E. (2001). Mitochondrial distribution and adenosine triphosphate contentofbovine 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. doi:10.1095/BIOLREPROD64.3.904
62. 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. doi:10.1093/NAR/16.17.8571
63. 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. doi:10.1016/J.YDBIO.2004.08.020
64. Tanaka, M., Kihara, M., Meczekalski, B., King, G. J., and Adashi, E. Y. (2003). HIoo: a pre-embryonic H1 linker histone in search of a function. Mol. Cell. Endocrinol. 202, 5-9.
65. Tanaka, M., Kihara, M., Hennebold, J. D., Eppig, J. J., Viveiros, M. M., et al. (2005). H1FOO is coupled to the initiation of oocytic growth. Biol. Reprod. 72, 135-142. doi:10.1095/BIOLREPROD.104.032474
66. 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. doi:10.1002/MRD.10102
67. 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. doi:10.1016/ J.GENE.2006.02.006
68. Vandesompele, J., Preter, K. D., Pattyn, F., Poppe, B., Roy, N. V., Paepe, A. D., and Speleman, F. (2002). Accurate normalization of realtime quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, research0034.1-research0034.11. doi:10.1186/GB-2002-3-7-RESEARCH0034
69. Wu, X., and Matzuk, M. M. (2002). GDF-9 and BMP-15: oocyte organizers. Rev. Endocr. Metab. Disord. 3, 27-32. doi:10.1023/A:1012796601311
70. 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. doi:10.1530/REP.0. 1220601
71. Yuan, W., Lucy, M. C., and Smith, M. F. (1996). Messenger ribonu-cleic acid for insulin-like growth factors-I and -II, insulin-like growth factor-binding protein-2, gonadotropin receptors, and steroido-genic enzymes in porcine follicles. Biol. Reprod. 55, 1045-1054. doi:10.1095/BIOLREPROD55.5.1045
72. 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. doi:10.1016/J.FERTNSTERT.2004.11.030
73. 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. doi:10.1016/J.ANIREPROSCI.2007.02.011