Heat shock at the germinal vesicle breakdown stage induces apoptosis in surrounding cumulus cells and reduces maturation rates of porcine oocytes in vitro

Theriogenology

Volumn 70, Issue 2, 2008, Pages 168-178

  Yuan, Y ^a   Hao, Z D ^a   Liu, J ^a   Wu, Y ^a   Yang, L ^a   Liu, G S ^a   Tian, J H ^a   Zhu, S E ^a   Zeng, S M ^a  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

Apoptosis; Cumulus cells; Heat shock; Oocyte; Pig

Indexed keywords

DNA;

ANIMAL; APOPTOSIS; ARTICLE; CELL CULTURE; CUMULUS CELL; CYTOLOGY; DNA DAMAGE; FEMALE; GROWTH, DEVELOPMENT AND AGING; HEAT; METABOLISM; OOCYTE; PHYSIOLOGY; SWINE;

ANIMALS; APOPTOSIS; CELLS, CULTURED; CUMULUS CELLS; DNA; DNA DAMAGE; FEMALE; HEAT; OOCYTES; SWINE;

SUIDAE; SUS;

EID: 44949149971     PISSN: 0093691X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.theriogenology.2008.03.005     Document Type: Article

References (55)

1. Monty Jr. D.E., and Racowsky C. In vitro evaluation of early embryo viability and development in summer heat-stressed, superovulated dairy cows. Theriogenology 28 (1987) 451-465
2. Al-Katanani Y.M., Paula-Lopes F.F., and Hansen P.J. Effect of season and exposure to heat stress on oocyte competence in Holstein cows. J Dairy Sci 85 (2002) 390-396
3. Omtvedt I.T., Nelson R.E., Edwards R.L., Stephens D.F., and Turman E.J. Influence of heat stress during early, mid, and late pregnancy of gilts. J Anim Sci 32 (1971) 312-317
4. Dutt R.H. Critical period for early embryo mortality in ewes exposed to high ambient temperature. J Anim Sci 22 (1963) 713-719
5. Badinga L., Collier R.J., Thatcher W.W., and Wilcox C.J. Effects of climatic and management factors on conception rate of dairy cattle in subtropical environment. J Dairy Sci 68 (1985) 78-85
6. Cavestany D., El-Wishy A.B., and Foote R.H. Effect of season and high environmental temperature on fertility of Holstein cattle. J Dairy Sci 68 (1985) 1471-1478
7. Wolfenson D., ThatcherWW, Badinag L., Savio J.D., Meidan R., Lew B.J., et al. Effect of heat stress on follicular development during the estrous cycle in lactating dairy cattle. Biol Reprod 52 (1995) 1106-1113
8. Wolfenson D., Roth Z., and Meidan R. Impaired reproduction in heat-stressed cattle: basic and applied aspects. Anim Reprod Sci 60 (2000) 535-547
9. Putney D.J., Malayer J.R., Gross T.S., Thatcher W.W., Hansen P.J., and Drost M. Heat stress-induced alterations in the synthesis and secretion of proteins and prostaglandins by cultured bovine conceptuses and uterine endometrium. Biol Reprod 39 (1988) 717-728
10. Edwards J.L., and Hansen P.J. Differential responses of bovine oocytes and preimplantation embryos to heat shock. Mol Reprod Dev 46 (1997) 138-145
11. Rivera R.M., and Hansen P.J. Development of cultured bovine embryos after exposure to high temperatures in the physiological range. Reproduction 121 (2001) 107-115
12. Tseng J.K., Chen C.H., Chou P.C., Yeh S.P., and Ju J.C. Influences of follicular size on parthenogenetic activation and in vitro heat shock on the cytoskeleton in cattle oocytes. Reprod Domest Anim 39 (2004) 146-153
13. Roth Z., and Hansen P.J. Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reproduction 129 (2005) 235-244
14. Roth Z., and Hansen P.J. Involvement of apoptosis in disruption of developmental competence of bovine oocytes by heat shock during maturation. Biol Reprod 71 (2004) 1898-1906
15. Tseng J.K., Tang P.C., and Ju J.C. In vitro thermal stress induces apoptosis and reduces development of porcine parthenotes. Theriogenology 66 (2006) 1073-1082
16. Ju J.C., and Tseng J.K. Nuclear and cytoskeletal alterations of in vitro matured porcine oocytes under hyperthermia. Mol Reprod Dev 68 (2004) 125-133
17. Moor R.M., Smith M.W., and Dawson M.C. Measurement of intercellular coupling between oocytes and cumulus cells using intracellular markers. Exp Cell Res 126 (1980) 15-29
18. Larsen W.J., and Wert S.E. Role of cell junctions in gametogenesis and in early embryonic development. Tissue Cell 20 (1988) 809-848
19. Warnes G.M., Moor R.M., and Johnson M.H. Changes in protein synthesis during maturation of sheep oocytes in vivo and in vitro. J Reprod Fertil 49 (1977) 331-335
20. Binor Z., and Wolf D.P. In vitro maturation and penetration of mouse primary oocytes after removal of zona pellucida. J Reprod Fertil 56 (1979) 309-314
21. Magnusson C. Role of cumulus cells for rat oocyte maturation and metabolism. Gamete Res 3 (1980) 133-140
22. Staigmiller R.G., and Moor R.M. Effect of follicle cells on the maturation and developmental competence of ovine oocytes matured outside the follicle. Gamete Res 9 (1984) 221-229
23. Chian R.C., Niwa K., and Sirard M.A. Effect of cumulus cells on the male pronuclear formation and subsequent early development of bovine oocytes in vitro. Theriogenology 41 (1994) 1499-1508
24. Yamauchi N., and Nagai T. Male pronuclear formation in denuded porcine oocytes after in vitro maturation in the presence of cysteamine. Biol Reprod 61 (1999) 828-833
25. Kim S.K., Minami N., Yamada M., and Utsumi K. Functional role of cumulus cells during maturation in development of in vitro matured and fertilized bovine oocytes. Theriogenology 45 (1996) 278
26. Tanghe S., Van Soom A., Nauwynck H., Coryn M., and de Kruif A. Minireview: functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol Reprod Dev 61 (2002) 414-424
27. Tatemoto H., Sakurai N., and Muto N. Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation: role of cumulus cells. Biol Reprod 63 (2000) 805-810
28. Bavister B.D., Leibfried M.L., and Lieberman G. Development of preimplantation embryos of the golden hamster in a defined culture medium. Biol Reprod 28 (1983) 235-247
29. Wang W.H., Abeydeera L.R., Han Y.M., Prather R.S., and Day B.N. Morphologic evaluation and actin filament distribution in porcine embryos produced in vitro and in vivo. Biol Reprod 60 (1999) 1020-1028
30. Petters R.M., and Wells K.D. Culture of pig embryos. J Reprod Fertil Suppl 48 (1993) 61-73
31. Singh N.P., McCoy M.T., Tice R.R., and Schneider E.L. A simple technique for quantitation of low level of DNA damage in individual cells. Exp Cell Res 175 (1988) 184-191
32. Bernardini C., Fantinati P., Zannoni A., Forni M., Tamanini C., and Bacci M.L. Expression of HSP70/HSC70 in swine blastocysts: effects of oxidative and thermal stress. Mol Reprod Dev 69 (2004) 303-307
33. Wu D., Cheung Q.C., Wen L., and Li J. A growth-maturation system that enhances the meiotic and developmental competence of porcine oocytes isolated from small follicles. Biol Reprod 75 (2006) 547-554
34. Funahashi H., Cantley T.C., and Day B.N. Preincubation of cumulus-oocyte complexes before exposure to gonadotropins improves the developmental competence of porcine embryos matured and fertilized in vitro. Theriogenology 47 (1997) 679-686
35. Edwards J.L., Saxton A.M., Lawrence J.L., Payton R.R., and Dunlap J.R. Exposure to a physiologically relevant elevated temperature hastens in vitro maturation in bovine oocytes. J Dairy Sci 88 (2005) 4326-4333
36. Ju J.C., Parks J.E., and Yang X. Thermotolerance of IVM-derived bovine oocytes and embryos after short-term heat shock. Mol Reprod Dev 53 (1999) 336-340
37. Ryan D.P., Blakewood E.G., Lynn J.W., Munyakazi L., and Godke R.A. Effect of heat-stress on bovine embryo development in vitro. J Anim Sci 70 (1992) 3490-3497
38. Rocha A., Randel R.D., Broussard J.R., Lim J.M., Blair R.M., Roussel J.D., et al. High environmental temperature and humidity decrease oocyte quality in Bos taurus but not in Bos indicus cows. Theriogenology 49 (1998) 657-665
39. Gavrieli Y., Sherman Y., and Ben-Sasson S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119 (1992) 493-501
40. Ostling O., and Johanson K.J. Microelectrophoretic study of radiation-induced DNA damages in individual mammalian cells. Biochem Biophys Res Commun 123 (1984) 291-298
41. Collins A.R. Comet assay: principles, applications, and limitations. Methods Mol Biol 203 (2002) 163-177
42. Choucroun P., Gillet D., Dorange G., Sawicki B., and Dewitte J.D. Comet assay and early apoptosis. Mutat Res 478 (2001) 89-96
43. Lévesque J.T., and Sirard M.A. Resumption of meiosis is initiated by the accumulation of cyclin B in bovine oocytes. Biol Reprod 55 (1996) 1427-1436
44. Mitra J., and Schultz R.M. Regulation of the acquisition of meiotic competence in the mouse: changes in the subcellular localization of cdc2, cyclin B1, cdc25C and wee1, and in the concentration of these proteins and their transcripts. J Cell Sci 109 (1996) 2407-2415
45. De Sousa P.A., Caveney A., Westhusin M.E., and Watson A.J. Temporal patterns of embryonic gene expression and their dependence on oogenetic factors. Theriogenology 49 (1998) 115-128
46. De Sousa P.A., Watson A.J., Schultz G.A., and Bilodeau-Goeseels S. Oogenetic and zygotic gene expression directing early bovine embryogenesis: a review. Mol Reprod Dev 51 (1998) 112-121
47. Gandolfi T.A., and Gandolfi F. The maternal legacy to the embryo: cytoplasmic components and their effects on early development. Theriogenology 55 (2001) 1255-1276
48. Collins A.R., Dobson V.L., Dusinská M., Kennedy G., and Stětina R. The comet assay: what can it really tell us?. Mutat Res 375 (1997) 183-193
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 63 (2005) 2147-2163
50. Godard T., Deslandes E., Lebailly P., Vigreux C., Sichel F., Poul J.M., et al. Early detection of staurosporine-induced apoptosis by comet and annexin V assays. Histochem Cell Biol 112 (1999) 155-161
51. Yasuhara S., Zhu Y., Matsui T., Tipirneni N., Yasuhara Y., Kaneki M., et al. Comparison of comet assay, electron microscopy, and flow cytometry for detection of apoptosis. J Histochem Cytochem 51 (2003) 873-885
52. Host E., Mikkelsen A.L., Lindenberg S., and Smidt-Jensen S. Apoptosis in human cumulus cells in relation to maturation stage and cleavage of the corresponding oocyte. Acta Obstet Gynecol Scand 79 (2000) 936-940
53. Saito H., Saito T., Kaneko T., Sasagawa I., Kuramoto T., and Hiroi M. Relatively poor oocyte quality is an indication for intracytoplasmic sperm injection. Fertil Steril 73 (2000) 465-469
54. Raman R.S., Chan P.J., Corselli J.U., Patton W.C., Jacobson J.D., Chan S.R., et al. Comet assay of cumulus cell DNA status and the relationship to oocyte fertilization via intracytoplasmic sperm injection. Hum Reprod 16 (2001) 831-835
55. Iwata H., Ohota M., Hashimoto S., and Nagai Y. Free oxygen radicals are generated at the time of aspiration of oocytes from ovaries that have been stored for a long time. Zygote 11 (2003) 1-5