Developmental potential of bovine oocytes following IVM in the presence of glutathione ethyl ester

Reproduction, Fertility and Development

Volumn 22, Issue 4, 2010, Pages 597-605

  Curnow, E C ^a,b   Ryan, J P ^b,c   Saunders, D M ^b   Hayes, E S ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF SYDNEY   (Australia)

^c IVFAustralia   (Australia)

Author keywords

Inner cell mass: trophectoderm cell ratio; Oxygen tension

Indexed keywords

BUTHIONINE SULFOXIMINE; GLUTATHIONE; GLUTATHIONE ETHYL ESTER;

ANIMAL CELL; ARTICLE; BLASTOCYST; CELL COUNT; CELL CULTURE; COMPLEX FORMATION; CONTROLLED STUDY; COW; CUMULUS CELL; EMBRYO DEVELOPMENT; FEMALE; FERTILIZATION IN VITRO; IN VITRO STUDY; NONHUMAN; OOCYTE CLEAVAGE; OOCYTE MATURATION;

ANIMALS; ANTIMETABOLITES; BUTHIONINE SULFOXIMINE; CATTLE; EMBRYONIC DEVELOPMENT; FEMALE; FERTILIZATION IN VITRO; GLUTATHIONE; MALE; MICROSCOPY, FLUORESCENCE; OOCYTES; PREGNANCY;

BOVINAE;

EID: 77950617577     PISSN: 10313613     EISSN: None     Source Type: Journal    
DOI: 10.1071/RD09228     Document Type: Article

References (53)

1. Abeydeera, L. R., Wang, W.-H., Cantley, T. C., Prather, R. S., and Day, B. N. (1999). Glutathione content and embryo development after in vitro fertilisation of pig oocytes matured in the presence of a thiol compound and various concentrations of cysteine. Zygote 7, 203-210. doi:10.1017/ S0967199499000581
2. Bing,Y. Z., Hirao,Y., Iga, K., Che, L. M., Takenouchi, N., Kuwayama, M., Fuchimoto, D., Rodriguez-Martinez, H., and Nagai, T. (2002). In vitro maturation and glutathione synthesis of porcine oocytes in the presence or absence of cysteamine under different oxygen tensions: role of cumulus cells. Reprod. Fertil. Dev. 14, 125-131. doi:10.1071/RD01127
3. Brison, D. R., and Schultz, R. M. (1997). Apoptosis during mouse blastocyst formation: evidence for a role for survival factors including transforming growth factor ?. Biol. Reprod. 56, 1088-1096. doi:10.1095/ BIOLREPROD56.5.1088
4. Byrne, A. T., Southgate, J., Brison, D. R., and Leese, H. J. (1999). Analysis of apoptosis in the preimplantation bovine embryo using TUNEL. J. Reprod. Fertil. 117, 97-105. doi:10.1530/JRF.0.1170097
5. Cetica, P. D., Pintos, L. N., Dalvit, G. C., and Beconi, M. T. (2001). Antioxidant enzyme activity and oxidative stress in bovine oocyte in vitro maturation. IUBMB Life 51, 57-64. doi:10.1080/15216540152035073
6. Chian, R. C., Niwa, K., and Sirard, M. A. (1994). Effects of cumulus cells on male pronuclear formation and subsequent early development of bovine oocytes in vitro. Theriogenology 41, 1499-1508. doi:10.1016/ 0093-691X(94)90201-S
7. Corrêa, G. A., Rumpf, R., Mundim, T. C. D., Franco, M. M., and Dode, M. A. N. (2008). Oxygen tension during in vitro culture of bovine embryos: effect in production and expression of genes related to oxidative stress. Anim. Reprod. Sci. 104, 132-142. doi:10.1016/ J.ANIREPROSCI.2007.02.002
8. Curnow, E. C., Ryan, J., Saunders, D., and Hayes, E. S. (2008). Bovine in vitro oocytes maturation as a model for manipulation of the γ-glutamyl cycle and intraoocyte glutathione. Reprod. Fertil. Dev. 20, 579-588. doi:10.1071/RD08041 (Pubitemid 351776990)
9. de Matos, D. G., and Furnus, C. C. (2000). The importance of having high glutathione (GSH) levels after bovine in vitro maturation on embryo development: effect of β-mercaptoethanol, cysteine and cystine. Theriogenology 53, 761-771. doi:10.1016/S0093-691X(99)00278-2
10. de Matos, D. G., Furnus, C. C., Moses, D. F., and Baldassarre, H. (1995). Effect of cysteamine on glutathione level and developmental capacity of bovine oocyte matured in vitro. Mol. Reprod. Dev. 42, 432-436. doi:10.1002/MRD. 1080420409
11. de Matos, D. G., Furnus, C. C., Moses, D. F., Martinez, A. G., and Matkovic, M. (1996). Stimulation of glutathione synthesis of in vitro matured bovine oocytes and its effect on embryo development and freezability. Mol. Reprod. Dev. 45, 451-457. doi:10.1002/(SICI)1098- 2795(199612)45:43.0.CO;2-Q
12. de Matos,D. G., Furnus, C. C., and Moses,D. F. (1997). Glutathione synthesis during in vitro maturation of bovine oocytes: role of cumulus cells. Biol. Reprod. 57, 1420-1425. doi:10.1095/BIOLREPROD57.6.1420
13. Downs, S. M., Schroeder, A. C., and Eppig, J. J. (1986). Serum maintains the fertilizability of mouse oocytes matured in vitro by preventing hardening of the zona pellucid. Gamete Res. 15, 115-122. doi:10.1002/ MRD.1120150203
14. Du, F., Looney, C. R., and Yang, X. (1996). Evaluation of bovine embryos produced in vitro vs. in vivo by differential staining of inner cell mass and trophectoderm cells. Theriogenology 45, 211. [Abstract] doi:10.1016/0093- 691X(96)84684-X
15. Feugang, J.-M., De Roover, R., Moens, A., Léonard, S., Dessy, F., and Donnay, I. (2004). Addition of β-mercaptoethanol or Trolox® at the morula/blastocyst stage improves the quality of bovine blastocysts and prevents induction of apoptosis and degeneration by prooxidant agents. Theriogenology 61, 71-90. doi:10.1016/S0093-691X(03) 00191-2
16. Furnus, C. C., de Matos, D. G., Picco, S., Peral García, P., Inda, A. M., Mattioli, G., and Errecalde, A. L. (2008). Metabolic requirements associated with GSH synthesis during in vitro maturation of cattle oocytes. Anim. Reprod. Sci. 109, 88-99. doi:10.1016/J.ANIREPROSCI. 2007.12.003
17. Gardiner, C. S., and Reed, D. J. (1994). Status of glutathione during oxidantinduced oxidative stress in the preimplantation mouse embryo. Biol. Reprod. 51, 1307-1314. doi:10.1095/BIOLREPROD51.6.1307 (Pubitemid 24354293)
18. Gardiner, C. S., and Reed, D. J. (1995). Synthesis of glutathione in the preimplantation mouse embryo. Arch. Biochem. Biophys. 318, 30-36. doi:10.1006/ABBI.1995.1200
19. Ge, L., Sui, H.-S., Lan, G.-C., Na Liu, N., Wang, J.-Z., and Tan, J.-H. (2008). Coculture with cumulus cells improves maturation of mouse oocytes denuded of the cumulus oophorus: observations of nuclear and cytoplasmic events. Fertil. Steril. 90, 2376-2388. doi:10.1016/J.FERTNSTERT.2007.10.054
20. Geshi, M., Takenouchi, N.,Yaamauchi, N., and Nagai, T. (2000). Effects of sodium pyruvate in nonserum maturation medium on maturation, fertilization, and subsequent development of bovine oocytes with or without cumulus cells. Biol. Reprod. 63, 1730-1734. doi:10.1095/ BIOLREPROD63.6.1730
21. Goto,Y., Noda,Y.,Mori,T., and Nakano, M. (1993). Increased generation of reactive oxygen species in embryos cultured in vitro. Free Radic. Biol. Med. 15, 69-75. doi:10.1016/0891-5849(93)90126-F (Pubitemid 23171444)
22. Guérin, P., El Mouatassim, S., and Ménézo,Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update 7, 175-189. doi:10.1093/ HUMUPD/7.2.175
23. Khurana, N. K., and Niemann, H. (2000). Effects of oocyte quality, oxygen tension, embryo density, cumulus cells and energy substrates on cleavage and morula/blastocyst formation of bovine embryos. Theriogenology 54, 741-756. doi:10.1016/S0093-691X(00)00387-3
24. Kitagawa, Y., Suzuki, K., Yoneda, A., and Watanabe, T. (2004). Effects of oxygen concentration and antioxidants on the in vitro developmental ability, production of reactive oxygen species (ROS), and DNA fragmentation in porcine embryos. Theriogenology 62, 1186-1197. doi:10.1016/J.THERIOGENOLOGY.2004.01.011 (Pubitemid 39123698)
25. Knijn, H. M., Gjørret, J. O., Vos, P. L. A. M., Hendriksen, P. J. M., van der Weijden, B. C., Maddox-Hytell, P., and Dieleman, S. J. (2003). Consequences of in vivo development and subsequent culture on apoptosis, cell number, and blastocyst formation in bovine embryos. Biol. Reprod. 69, 1371-1378. doi:10.1095/BIOLREPROD.103.017251 (Pubitemid 37173874)
26. Lim, J. M., Reggio, B. C., Godke, R. A., and Hansel, W. (1999). Development of in-vitro-derived bovine embryos cultured in 5% CO2 in air or in 5% O2, 5% CO2 and 90% N2. Hum. Reprod. 14, 458-464. doi:10.1093/HUMREP/14.2.458
27. Luciano, A. M., Lodde, V., Beretta, M. S., Colleoni, S., Lauria, A., and Modina, S. (2005). Developmental capability of denuded bovine oocyte in a co-culture system with intact cumulus-oocyte complexes: role of cumulus cells, cyclic adenosine 3′,5′-monophosphate, and glutathione. Mol. Reprod. Dev. 71, 389-397. doi:10.1002/MRD.20304 (Pubitemid 40770393)
28. Maedomari, N., Kikuchi, K., Ozawa, M., Noguchi, M., Kaneko, H., Ohnuma, K., Nakai, M., Shino, M., Nagai, T., and Kashiwazaki, N. (2007). Cytoplasmic glutathione regulated by cumulus cells during porcine oocytes maturation affects fertilization and embryonic development in vitro. Theriogenology 67, 983-993. doi:10.1016/ J.THERIOGENOLOGY.2006.11.012
29. Meister, A. (1985). Methods for the selective modification of glutathione metabolism and study of glutathione transport. Methods Enzymol. 113, 571-585. doi:10.1016/S0076-6879(85)13077-6
30. Meister, A., and Anderson, M. E. (1983). Glutathione. Annu. Rev. Biochem. 52, 711-760. doi:10.1146/ANNUREV.BI.52.070183.003431
31. Mizushima, S., and Fukui,Y. (2001). Fertilizability and developmental capacity of bovine oocytes cultured individually in a chemically defined maturation medium. Theriogenology 55, 1431-1445. doi:10.1016/ S0093-691X(01)00492-497
32. Mori, T., Amano, T., and Shimizu, H. (2000). Roles of gap junctional communication of cumulus cells in cytoplasmic maturation of porcine oocytes cultured in vitro. Biol. Reprod. 62, 913-919. doi:10.1095/ BIOLREPROD62.4.913
33. Ozawa, M., Nagai, T., Fahrudin, M., Karja, N. W. K., Kaneko, H., Noguchi, J., Ohnuma, K., and Kikuchi, K. (2006). Addition of glutathione or thioredoxin to culture medium reduces intracellular redox status of porcine IVM/IVF embryos, resulting in improved development to the blastocyst stage. Mol. Reprod. Dev. 73, 998-1007. doi:10.1002/ MRD.20533
34. Perreault, S. D., Barbee, R. R., and Slott, V. L. (1988). Importance of glutathione in the acquisition and maintenance of sperm nuclear decondensing activity in maturing hamster oocytes. Dev. Biol. 125, 181-186. doi:10.1016/0012-1606(88)90070-X
35. Pierce, G. B., Parchment, R. E., and Lewellyn, A. L. (1991). Hydrogen peroxide as a mediator of programmed cell death in the blastocyst. Differentiation 46, 181-186. doi:10.1111/J.1432-0436.1991.TB00880.X
36. Ramana, K. V., Bhatnagar, A., Srivastava, S., Yadav, U. C., Awasthi, S., Awasthi, Y. C., and Srivastava, S. K. (2006). Mitogenic responses of vascular smooth muscle cells to lipid peroxidation-derived aldehyde 4-hydroxy-trans-2- nonenal (HNE). J. Biol. Chem. 281, 17 652-17 660. doi:10.1074/JBC.M600270200 (Pubitemid 44043077)
37. Richman, P. G., and Meister, A. (1975). Regulation of γ-glutamyl-cysteine synthetase by nonallosteric feedback inhibition by glutathione. J. Biol. Chem. 250, 1422-1426.
38. Stover, S. K., Gushansky, G. A., Salmen, J. J., and Gardiner, C. S. (2000). Regulation of ?-glutamate-cysteine ligase expression by oxidative stress in the mouse preimplantation embryo. Toxicol. Appl. Pharmacol. 168, 153-159. doi:10.1006/TAAP.2000.9030
39. Sutovsky, P., and Schatten, G. (1997). Depletion of glutathione during bovine oocyte maturation reversibly blocks the decondensation of the male pronucleus and pronuclear apposition during fertilization. Biol. Reprod. 56, 1503-1512. doi:10.1095/BIOLREPROD56.6.1503 (Pubitemid 27215459)
40. Takahashi, M., Nagai, T., Hamano, S., Kuwayama, M., Okamura, N., and Okano, A. (1993). Effect of thiol compounds on in vitro development and intracellular glutathione content of bovine embryos. Biol. Reprod. 49, 228-232. doi:10.1095/BIOLREPROD49.2.228
41. Takahashi, M., Keicho, K., Takahashi, H., Ogawa, H., Schultz, R. M., and Okano, A. (2000). Effect of oxidative stress on development and DNA damage in in-vitro cultured bovine embryos by COMET assay. Theriogenology 54, 137-145. doi:10.1016/S0093-691X(00)00332-0
42. Takahashi, M., Nagai,T., Okamura,N.,Takahashi, H., and Okano, A. (2002). Promoting effect of β-mercaptoethanol on in vitro development under oxidative stress and cystine uptake of bovine embryos. Biol. Reprod. 66, 562-567. doi:10.1095/BIOLREPROD66.3.562
43. Tatemoto, H., Sakurai, N., and Muto, N. (2000). Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation: role of cumulus cells. Biol. Reprod. 63, 805-810. doi:10.1095/BIOLREPROD63.3.805
44. Thouas, G. A., Korfiatis, N. A., French, A. J., Jones, G. M., and Trounson, A. O. (2001). Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts. Reprod. BioMed. Online 3, 25-29.
45. Vanderhyden, B. C., and Armstrong, D. T. (1989). Role of cumulus cells and serum on the in vitro maturation, fertilization, and subsequent development of rat oocytes. Biol. Reprod. 40, 720-728.
46. Van Soom, A., Yuan, Y. Q., Peelman, L. J., de Matos, D. G., Dewulf, J., Laevens, H., and de Kruif, A. (2002). Prevalence of apoptosis and inner cell allocation in bovine embryos cultured under different oxygen tensions with or without cysteine addition. Theriogenology 57, 1453-1465. doi:10.1016/S0093- 691X(01)00726-9 (Pubitemid 34534315)
47. Walker, S. K., Hartwich, K. M., and Seamark, R. F. (1996). The production of unusually large offspring following embryo manipulation: concepts and challenges. Theriogenology 45, 111-120. doi:10.1016/0093-691X (95)00360-K
48. Yamauchi, N., and Nagai, T. (1999). Male pronuclear formation in denuded porcine oocytes after in vitro maturation in the presence of cysteamine. Biol. Reprod. 61, 828-833. doi:10.1095/BIOLREPROD61.3.828 (Pubitemid 29402647)
49. Yang, H., Magilnick, N., Xia, M., and Lu, S. C. (2008). Effects of hepatocyte growth factor on glutathione synthesis, growth, and apoptosis is cell density-dependent. Exp. Cell Res. 314, 398-412. doi:10.1016/ J.YEXCR.2007.09.015
50. Yuan, Y. Q., Van Soom, A., Coopman, F. O. J., Mintiens, K., Boerjan, M. L., Van Zeveren, A., de Kruif, A., and Peelman, L. J. (2003). Influence of oxygen tension on apoptosis and hatching in bovine embryos cultured in vitro. Theriogenology 59, 1585-1596. doi:10.1016/S0093- 691X(02)01204-1209
51. Zhang, L., Jiang, S., Wazniak, P. J., Yang, X., and Godke, R. A. (1995). Cumulus cell function during oocyte maturation, fertilization, http://www.publish.csiro.au/journals/rfd and embryo development in vitro. Mol. Reprod. Dev. 40, 338-344. doi:10.1002/MRD.1080400310
52. Zhou, P., Wu, Y.-G., Li, Q., Lan, G.-C., Wang, G., Gao, D., and Tan, J.-H. (2008). The interactions between cysteamine, cystine and cumulus cells increase the intracellular glutathione level and developmental capacity of goat cumulus-denuded oocytes. Reproduction 135, 605-611. doi:10.1530/REP-08-0003 (Pubitemid 351676445)
53. Zuelke, K. A., Jeffay, S. C., Zucker, R. M., and Perreault, S. D. (2003). Glutathione (GSH) concentrations vary with the cell cycle in maturing hamster oocytes, zygotes, and pre-implantation stage embryos. Mol. Reprod. Dev. 64, 106-112.