Incidence of apoptosis and transcript abundance in bovine follicular cells is associated with the quality of the enclosed oocyte

Theriogenology

Volumn 78, Issue 3, 2012, Pages 656-669.e5

  Janowski, D ^a   Salilew Wondim, D ^b   Torner, H ^a   Tesfaye, D ^b   Ghanem, N ^c   Tomek, W ^a   El Sayed, A ^c   Schellander, K ^b   Holker M ^b  

^a LEIBNIZ INSTITUTE FOR FARM ANIMAL BIOLOGY FBN   (Germany)

^b UNIVERSITY OF BONN   (Germany)

^c CAIRO UNIVERSITY   (Egypt)

Author keywords

Apoptosis; Bovine; Cumulus; Gene expression; Granulosa; Oocyte

Indexed keywords

BOVINAE;

EID: 84863470269     PISSN: 0093691X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.theriogenology.2012.03.012     Document Type: Article

References (64)

1. Lingenfelter B.M., Dailey R.A., Inskeep E.K., Vernon M.W., Poole D.H., Rhinehart J.D., et al. Microarray analysis of gene expression in granulosa cells from persistent follicles in cattleMicroarray analysis of gene expression in granulosal cells from persistent follicles in cattle. Anim Reprod Sci 2008, 104:405-413.
2. Brower P.T., Schultz R.M. Intercellular communication between granulosa cells and mouse oocytes: existence and possible nutritional role during oocyte growth. Dev Biol 1982, 90:144-153.
3. Larsen W.J., Wert S.E., Brunner G.D. A dramatic loss of cumulus cell gap junctions is correlated with germinal vesicle breakdown in rat oocytes. Dev Biol 1986, 113:517-521.
4. Driancourt M.A., Thuel B. Control of oocyte growth and maturation by follicular cells and molecules present in follicular fluid. A review. Reprod Nutr Dev 1998, 38:345-362.
5. Vozzi C., Formenton A., Chanson A., Senn A., Sahli R., Shaw P., et al. Involvement of connexin 43 in meiotic maturation of bovine oocytes. Reproduction 2001, 122:619-628.
6. Ericsson S.A., Boice M.L., Funahashi H., Day M. Assessment of porcine oocytes using brilliant cresyl blue. Theriogenology 1993, 39:214.
7. Alm H., Torner H., Löhrke B., Viergutz T., Ghoneim I.M., Kanitz W. Bovine blastocyst development rate in vitro is influenced by selection of oocytes by brillant cresyl blue staining before IVM as indicator for glucose-6-phosphate dehydrogenase activity. Theriogenology 2005, 63:2194-2205.
8. Mohammadi-Sangcheshmeh A., Held E., Ghanem N., Rings F., Salilew-Wondim D., Tesfaye D., et al. G6PDH-activity in equine oocytes correlates with morphology, expression of candidate genes for viability, and preimplantative in vitro development. Theriogenology 2011, 76:1215-1226.
9. Wassarman M. The mammalian ovum. The physiology of reproduction 1998, 69-102. Raven Press. E. Knobil, J.D. Neil (Eds.).
10. Opiela J., Katska-Ksiazkiewicz L., Lipiński D., Słomski R., Bzowska M., Ryńska B. Interactions among activity of glucose-6-phosphate dehydrogenase in immature oocytes, expression of apoptosis-related genes Bcl-2 and Bax, and developmental competence following IVP in cattle. Theriogenology 2008, 69:546-555.
11. Hazeleger N.L., Stubbings R.B. Developmental potential of selected bovine oocyte cumulus complexes. Theriogenology 1992, 37:219.
12. Blondin P., Sirard M.A. Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes. Mol Reprod Dev 1995, 41:54-62.
13. De Wit A.A., Kruip T.A. Bovine cumulus-oocyte-complex-quality is reflected in sensitivity for alpha-amanitin, oocyte-diameter and developmental capacity. Anim Reprod Sci 2001, 65:51-65.
14. Bilodeau-Goeseels S., Panich P. Effects of oocyte quality on development and transcriptional activity in early bovine embryos. Anim Reprod Sci 2002, 71:143-155.
15. Hyttel P., Callesen H., Greve T. Ultrastructural features of preovulatory oocyte maturation in superovulated cattle. J Reprod Fertil 1986, 76:645-656.
16. Sirard M.A., Picard L., Dery M., Coenen K., Blondin P. The time interval between FSH administration and ovarian aspiration influences the development of cattle oocytes. Theriogenology 1999, 51:699-708.
17. Hendriksen P.J., Vos P.L., Steenweg W.N., Bevers M.M., Dieleman S.J. Bovine follicular development and its effect on the in vitro competence of oocytes. Theriogenology 2000, 53:11-20.
18. Hsueh A.J., Billig H., Tsafriri A. Ovarian follicle atresia: a hormonally controlled apoptotic process. Endocr Rev 1994, 15:707-724.
19. Goodman A.L., Hodgen G.D. The ovarian triad of the primate menstrual cycle. Recent Prog Horm Res 1983, 39:1-73.
20. Alm H., Torner H., Heleil B., Srsen V., Kuzmina T. Apoptosis and pyknosis in cumulus cells from bovine cumulus-oocyte complexes before and after maturation in vitro. Theriogenology 2000, 53:447.
21. Isobe N., Yoshimura Y. Localization of apoptotic cells in the cystic ovarian follicles of cows: A DNA-end labeling histochemical study. Theriogenology 2000, 53:897-904.
22. Feranil J., Isobe N., Nakao T. Apoptosis in the antral follicles of swamp buffalo and cattle ovary: TUNEL and caspase-3 histochemistry. Reprod Domest Anim 2005, 40:111-116.
23. Boone D.L., Tsang B.K. Caspase-3 in the rat ovary: localization and possible role in follicular atresia and luteal regression. Biol Reprod 1998, 58:1533-1539.
24. Fenwick M.A., Hurst P.R. Immunohistochemical localization of active caspase-3 in the mouse ovary: growth and atresia of small follicles. Reproduction 2002, 124:659-665.
25. Nicholas B., Alberio R., Fouladi-Nashta A.A., Webb R. Relationship between low-molecular-weight insulin-like growth factor-binding proteins, caspase-3 activity, and oocyte quality. Biol Reprod 2005, 72:796-804.
26. Filali M., Frydman N., Belot M.P., Hesters L., Gaudin F., Tachdjian G., et al. Oocyte in-vitro maturation: BCL2 mRNA content in cumulus cells reflects oocyte competency. Reprod Biomed Online 2009, 19:71-84.
27. Bhojwani S., Alm H., Torner H., Kanitz W., Poehland R. Selection of developmentally competent oocytes through brilliant cresyl blue stain enhances blastocyst development rate after bovine nuclear transfer. Theriogenology 2007, 67:341-345.
28. Alm H., Choi Y.H., Love L., Heleil B., Torner H., Hinrichs K. Holding bovine oocytes in the absence of maturation inhibitors: kinetics of in vitro maturation and effect on blastocyst development after in vitro fertilization. Theriogenology 2008, 70:1024-1029.
29. Wu Z.J., Irizarry R.A. Preprocessing of oligonucleotide array data. Nat Biotechnol 2004, 22:656-658.
30. Smyth G.K., Michaud J., Scott H.S. Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 2005, 21:2067-2075.
31. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Statist Soc B 1995, 57:289-300.
32. Torner H., Ghanem N., Ambros C., Hölker M., Tomek W., Phatsara C., et al. Molecular and subcellular characterisation of oocytes screened for their developmental competence based on glucose-6-phosphate dehydrogenase activity. Reproduction 2008, 135:197-212.
33. Machatkova M., Krausova K., Jokesova E., Tomanek M. Developmental competence of bovine oocytes: effects of follicle size and the phase of follicular wave on in vitro embryo production. Theriogenology 2004, 61:329-335.
34. Motlík J., Kubelka M. Cell-cycle aspects of growth and maturation of mammalian oocytes. Mol Reprod Dev 1990, 27:366-375.
35. Fair T., Hyttel P., Greve T. Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol Reprod Dev 1995, 42:437-442.
36. Zeuner A., Müller K., Reguszynski K., Jewgenow K. Apoptosis within bovine follicular cells and its effect on oocyte development during in vitro maturation. Theriogenology 2003, 59:1421-1433.
37. Yang M.Y., Rajamahendran R. Involvement of apoptosis in the atresia of nonovulatory dominant follicle during the bovine estrous cycle. Biol Reprod 2000, 63:1313-1321.
38. Hagemann L.J., Beaumont S.E., Berg M., Donnison M.J., Ledgard A., Peterson A.J., et al. Development during single IVP of bovine oocytes from dissected follicles: interactive effects of estrous cycle stage, follicle size and atresia. Mol Reprod Dev 1999, 53:451-458.
39. Van Wezel I.L., Dharmarajan A.M., Lavranos T.C., Rodgers R.J. Evidence for alternative pathways of granulosa cell death in healthy and slightly atretic bovine antral follicles. Endocrinology 1999, 140:2602-2612.
40. Cohen G.M. Caspases: the executioners of apoptosis. Biochem J 1997, 326:1-16.
41. Hirata H., Takahashi A., Kobayashi S., Yonehara S., Sawai H., Okazaki T., et al. Caspases are activated in a branched protease cascade and control distinct downstream processes in Fas-induced apoptosis. J Exp Med 1998, 187:587-600.
42. Porter A.G., Jänicke R.U. Emerging roles of caspase-3 in apoptosis. Cell Death Differ 1999, 6:99-104.
43. Martin S.J., Reutelingsperger C.P., Mcgahon A.J., Rader J.A., van Schie R.C., Laface D.M., et al. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J Exp Med 1995, 182:1545-1556.
44. Han Z.B., Lan G.C., Wu Y.G., Han D., Feng W.G., Wang J.Z., et al. Interactive effects of granulosa cell apoptosis, follicle size, cumulus-oocyte complex morphology, and cumulus expansion on the developmental competence of goat oocytes: a study using the well-in-drop culture system. Reproduction 2006, 132:749-758.
45. Feng W.G., Sui H.S., Han Z.B., Chang Z.L., Zhou P., Liu D.J., et al. Effects of follicular atresia and size on the developmental competence of bovine oocytes: A study using the well-in-drop culture system. Theriogenology 2007, 67:1339-1350.
46. Anguita B., Paramio M.T., Morató R., Romaguera R., Jiménez-Macedo A.R., Mogas T., et al. Effect of the apoptosis rate observed in oocytes and cumulus cells on embryo development in prepubertal goats. Anim Reprod Sci 2009, 116:95-106.
47. Høst E., Mikkelsen A.L., Lindenberg S., Smidt-Jensen S. Apoptosis in human cumulus cells in relation to maturation stage and cleavage of the corresponding oocyte. Acta Obstet Gynecol Scand 2000, 79:936-940.
48. Alisch A., Rüping K., Köster F., Schöpper B., Baum M., Finas D., et al. [Cumulus cell apoptosis as a predictor for oocyte quality in artificial reproduction technique]. Zentralbl Gynakol 2003, 125:452-457.
49. Yuan Y.Q., Van Soom A., Leroy J.L., Dewulf J., Van Zeveren A., de Kruif A., et al. Apoptosis in cumulus cells, but not in oocytes, may influence bovine embryonic developmental competence. Theriogenology 2005, 63:2147-2163.
50. Irving-Rodgers H.F., van Wezel I.L., Mussard M.L., Kinder J.E., Rodgers R.J. Atresia revisited: two basic patterns of atresia of bovine antral follicles. Reproduction 2001, 122:761-775.
51. Manabe N., Goto Y., Matsuda-Minehata F., Inoue N., Maeda A., Sakamaki K., et al. Regulation mechanism of selective atresia in porcine follicles: regulation of granulosa cell apoptosis during atresia. J Reprod Dev 2004, 50:493-514.
52. Hussein T.S., Froiland D.A., Amato F., Thompson J.G., Gilchrist R.B. Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J Cell Sci 2005, 118:5257-5268.
53. D'haeseleer M., Cocquyt G., Van Cruchten S., Simoens P., Van Den Broeck W. Cell-specific localisation of apoptosis in the bovine ovary at different stages of the oestrous cycle. Theriogenology 2006, 65:757-772.
54. Nagata S. Apoptotic DNA fragmentation. Exp Cell Res 2000, 256:12-18.
55. Choudhuri A., Evans T., Maitra U. Non-core subunit eIF3h of translation initiation factor eIF3 regulates zebra fish embryonic development. Dev Dynam 2010, 239:1632-1644.
56. Ghanem N., Hölker M., Rings F., Jennen D., Tholen E., Sirard M.A., et al. Alterations in transcript abundance of bovine oocytes recovered at growth and dominance phases of the first follicular wave. BMC Dev Biol 2007, 7:90.
57. El Mouatassim S., Guérin P., Ménézo Y. Expression of genes encoding antioxidant enzymes in human and mouse oocytes during the final stages of maturation. Mol Hum Reprod 1999, 5:720-725.
58. Salilew Wondim R.F., Hölker M., Hölker M., Jennen D., Tholen E., Havlicek V., 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. Reproduction 2007, 133:931-946.
59. Eliyahu E., Tsaadon A., Shtraizent N., Shalgi R. The involvement of protein kinase C and actin filaments in cortical granule exocytosis in the rat. Reproduction 2005, 129:161-170.
60. Sutovský P., Fléchon J.E., Pavlok A. F-actin is involved in control of bovine cumulus expansion. Mol Reprod Dev 1995, 41:521-529.
61. Green D.R. Apoptotic pathways: the roads to ruin. Cell 1998, 94:695-698.
62. Thornberry N.A., Lazebnik Y. Caspases: enemies within. Science 1998, 281:1312-1316.
63. Adams J.M., Cory S. Life-or-death decisions by the Bcl-2 protein family. Trends Biochem Sci 2001, 26:61-66.
64. Vandaele L., Goossens K., Peelman L., Van Soom A. mRNA expression of Bcl-2, Bax, caspase-3 and -7 cannot be used as a marker for apoptosis in bovine blastocysts. Anim Reprod Sci 2008, 106:168-173.