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Melatonin Attenuates Nitric Oxide Induced Oxidative Stress on Viability and Gene Expression in Bovine Oviduct Epithelial Cells, and Subsequently Increases Development of Bovine IVM/IVF Embryos

  • Kim, J.T. (School of Veterinary Medicine, Kangwon National University) ;
  • Jang, H.Y. (College of Animal Life Science, Kangwon National University) ;
  • Park, C.K. (College of Animal Life Science, Kangwon National University) ;
  • Cheong, H.T. (School of Veterinary Medicine, Kangwon National University) ;
  • Park, I.C. (School of Veterinary Medicine, Kangwon National University) ;
  • Yang, B.K. (College of Animal Life Science, Kangwon National University)
  • 투고 : 2010.05.17
  • 심사 : 2010.10.11
  • 발행 : 2011.02.01

초록

The objective of the present study was to elucidate the fundamental mechanism of bovine oviduct epithelial cell (BOEC) co-culture on developmental capacity of bovine IVM/IVF embryos and to determine whether or not melatonin acts as an antioxidant in BOEC culture and subsequent embryo development. These studies examined the effects of melatonin against NO-induced oxidative stress on cell viability, lipid peroxidation (LPO) and the expression of antioxidant genes (CuZnSOD, MnSOD and Catalase) or apoptosis genes (Bcl-2, Caspase-3 and Bax) during BOECs culture. We also evaluated the developmental rates of bovine IVM/IVF embryos with BOEC co-culture, which were pre-treated with melatonin ($1,000\;{\mu}M$) in the presence or absence of sodium nitroprusside (SNP, $1,000\;{\mu}M$) for 24 h. Cell viability in BOECs treated with SNP (50-$2,000\;{\mu}M$) decreased while melatonin addition (1-$1,000\;{\mu}M$) increased viability in a dose-dependent manner. Cell viability in melatonin plus SNP ($1,000\;{\mu}M$) gradually recovered according to increasing melatonin addition (1-$1,000\;{\mu}M$). The LPO products were measured by thiobarbituric acid (TBA) reaction for malondialdehyde (MDA). Addition of melatonin in BOEC culture indicated a dose-dependent decrease of MDA, and in the SNP group among BOECs treated with SNP or melatonin plus SNP groups MDA was significantly increased compared with SNP plus melatonin groups (p<0.05). In expression of apoptosis or antioxidant genes detected by RT-PCR, Bcl-2 and antioxidant genes were detected in melatonin or melatonin plus SNP groups, while Caspase-3 and Bax genes were only found in the SNP group. When bovine IVM/IVF embryos were cultured for 6-7 days under the BOEC co-culture system pre-treated with melatonin in the presence or absence of SNP, the highest developmental ability to blastocysts was obtained in the $1,000\;{\mu}M$ melatonin group. These results suggest that melatonin has an anti-oxidative effect against NO-induced oxidative stress on cell viability of BOECs and on the developmental competence of bovine IVM/IVF embryo co-culture with BOEC.

키워드

참고문헌

  1. Allegra, M., R. J. Reiter, D. X. Tan, C. Gentile, L. Tesoriere and M. A. Livrea. 2003. The chemistry of melatonin's interaction with reactive species. J. Pineal Res. 34:1-10. https://doi.org/10.1034/j.1600-079X.2003.02112.x
  2. Ashok, B. T., L. David, Y. G. Chen, V. P. Garikapaty, B. Chander, D. Kanduc, A. Mittrlman and R. K. Tiwari. 2003. Peptide mitmotopes of on oncoproteins as therapeutic agents in breast cancer. Int. J. Mol. Med. 11:465-471.
  3. Bavister, B. D. 1995. Culture of preimplantation embryos: facts and artifacts. Hum. Reprod. Update, 1 91-148. https://doi.org/10.1093/humupd/1.2.91
  4. Chomczynski, P. and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
  5. Exley, G. E., C. Tang, A. S. McElhinny and C. M. Warner. 1999. Expression of caspase and Bcl-2 apoptotic family members in mice preimplantation embryos. Biol. Reprod. 61:231-239. https://doi.org/10.1095/biolreprod61.1.231
  6. Flood, L. P. and B. Shirley. 1991. Reduction of embryotoxicity by protein in embryo culture media. Reprod. Dev. 30:226-231. https://doi.org/10.1002/mrd.1080300310
  7. Galli, C., R. Duchi, G. Crotti, P. Turini, N. Ponderato, S. Colleoni, I. Lagutina and G. Lazzari. 2003. Bovine embryo technologies. Theriogenology 59:599-616. https://doi.org/10.1016/S0093-691X(02)01243-8
  8. Gardner, P. R., D. D. Nguyen and C. W. White. 1994. Aconitase is a sensitive and critical target of oxygen poisoning in cultured mammalian cells and in rat lungs. Proc. Natl. Acad. Sci. USA. 91:12248-12252. https://doi.org/10.1073/pnas.91.25.12248
  9. Griveau, J. F., E. Dumont, B. Renard, J. P. Callegari and D. L. Lannou. 1995. Reactive oxygen species, lipid peroxidation and enzymatic defense systems in human spermatozoa. J. Reprod. Fertil. 103:17-26. https://doi.org/10.1530/jrf.0.1030017
  10. Guerin, P., S. El Mouatassim and Y. Menezo. 2001. Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update., 7:175-189. https://doi.org/10.1093/humupd/7.2.175
  11. Hailliwell, B. 2000. The antioxidant paradox. Lancet 355:1179-1180. https://doi.org/10.1016/S0140-6736(00)02075-4
  12. Hancock, J. T., R. Desikan and S. J. Neill. 2001. Role of reactive oxygen species in cell signaling pathways. Biochem. Soc. Trans. 29:345-350. https://doi.org/10.1042/BST0290345
  13. Hardy, K. 1999. Apoptosis in human embryo. Rev. Reprod. 4:125-134. https://doi.org/10.1530/ror.0.0040125
  14. Haunstter, A. and S. Izumo. 1998. Apoptosis; basic mechanisms and implications for cardiovascular diease. Cir. Res. 82:1111-1129. https://doi.org/10.1161/01.RES.82.11.1111
  15. Ishizuka, B., Y. Kuribayashi, K. Murai, A. Amemiya and M. T. Itoh. 2000. The effect of melatonin on in vitro fertilization and embryo development in mice. J. Pineal Res. 28:48-51. https://doi.org/10.1034/j.1600-079x.2000.280107.x
  16. Jeon, K., E. Y. Kim, J. C. Tae, C. H. Lee, K. S. Lee, Y. O. Kim, D. K. Jeong, S. K. Cho, J. H. Kim, H. Y. Lee, K. Z. Riu, S. G. Cho and S. P. Park. 2008. Survivin protein expression in bovine follicular oocytes and their in vitro developmental competence. Anim. Reprod. Sci. 108:319-333. https://doi.org/10.1016/j.anireprosci.2007.09.003
  17. Juknat, A. A., M. V.Mendez, A. Quaglino, C. I. Fameli, M. Mena and M. L. Kotler. 2005. Melatonin prevents hydrogen peroxide-induced Bax expression in cultured rat astrocytes. J. Pineal Res. 38:84-92. https://doi.org/10.1111/j.1600-079X.2004.00166.x
  18. Kim, H. J. and J. S. Kwon. 1999. Effects of placing microimplants of melatonin in striatum on oxidative stress and neuronal damage mediated by N-methyl-D-aspartate (NMDA) and non-NMDA receptors. Arch. Pharm. Res. 22:35-43. https://doi.org/10.1007/BF02976433
  19. de Lamirande, E. and C. O'Flaherty. 2008. Sperm activation: Role of reactive oxygen species and kinases. Biochim. Biophys. Acta. 1784:106-115. https://doi.org/10.1016/j.bbapap.2007.08.024
  20. Lawlor, S. M. and N. M. O'Brien. 1995. Modulation of oxidative stress by beta-carotene in chicken embryo fibroblasts. Br. J. Nutr. 73:841-850. https://doi.org/10.1079/BJN19950089
  21. Liu, L. P. S., S. T. H. Chan, P. C. Ho and W. S. B. Yeung. 1998. Partial purification of embryotrophic factors from human oviductal cells. Hum. Reprod. 13:1613-1619. https://doi.org/10.1093/humrep/13.6.1613
  22. Papis, K., O. Poleszczuk, E. Wenta-Muchalska and J. A. Modlinski. 2007. Melatonin effect on bovine embryo development in vitro in relation to oxygen concentration. J. Pineal Res. 43:321-326. https://doi.org/10.1111/j.1600-079X.2007.00479.x
  23. Rief, S., F. Sinowatz, M. Stojkovic, R. Einspanier, E. Wolf and K. Prelle. 2002. Effects of novel co-culture system on development, metabolism and gene expression of bovine embryos produced in vitro. Reproduction 124:543-556. https://doi.org/10.1530/rep.0.1240543
  24. Reiter, R. J., D. X. Tan, C. Osuna and E. Gitto. 2000. Actions of melatonin in the reduction of oxidative stress. J. Biomed. Sci. 7:444-448. https://doi.org/10.1007/BF02253360
  25. Rodriguez-Osorio, N., I. J. Kim, H. Wang, A.Kaya and E. Memili. 2007. Melatonin increases cleavage rate of porcine preimplantation embryos in vitro. J. Pineal Res. 43:283-288. https://doi.org/10.1111/j.1600-079X.2007.00475.x
  26. Siu, A. W., M. Maldonado, M. Sanchez-Hidalgo, D. X. Tan and R. J. Reiter. 2006. Protective effects of melatonin in experimental free radical-related ocular diseases. J. Pineal Res. 40:101-109. https://doi.org/10.1111/j.1600-079X.2005.00304.x
  27. Sonmez, M., A. Yuce and G. Turk. 2007. The protective effects of melatonin and vitamin E on antioxidant enzyme activities and epididymal sperm characteristics of homocysteine treated male rats. Reprod. Toxicol. 23:226-231. https://doi.org/10.1016/j.reprotox.2006.11.003
  28. Tamura, H., A. Takasaki, I. Miwa, K. Taniguchi, R. Maekawa, H. Asada, T. Taketani, A. Matsuoka, Y. Yamagata, K. Shimamura, H.. Morioka, H. Ishikawa, R. J. Reiter and N. Sugino, 2008. Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate. J. Pineal Res. 44:280-287. https://doi.org/10.1111/j.1600-079X.2007.00524.x
  29. Tanaka, H., I. Matsumura, S. Ezoe, Y. Satoh, T. Sakamaki, C. Albanese, T. Machii, R. G. Pestell and Y. Kanakura. 2002. E2F1 and c-Myc potentiate apoptosis through inhibition of NF-kappaB activity that facilitates MnSOD-mediated ROS elimination. Mol. Cell 9:1017-1029. https://doi.org/10.1016/S1097-2765(02)00522-1
  30. Tranguch, S., N. Steuerwald and Y. M. Huet-Hudson. 2003. Nitric oxide synthase production and nitric oxide regulation of preimplantation embryo development. Biol. Reprod. 68:1538-1544.
  31. Viana, K. S., M. C. Caldas-Bussiere, S. G. C. Matta, M. R. Faes, C. S. P. Carvalho and C. R Quirino, 2007. Effect of sodium nitroprusside, a nitric oxide donor, on the in vitro maturation of bovine oocytes. Anim. Reprod. Sci. 102: 217-227. https://doi.org/10.1016/j.anireprosci.2006.11.004
  32. Yang, B. K., X. Yang and R. H. Foote. 1993. Effect of growth factors on morula and blastocyst development of in vitro matured and in vitro fertilized bovine oocytes. Theriogenology 40:521-530. https://doi.org/10.1016/0093-691X(93)90405-T
  33. Yang, J., X. Liu, K. Bhalla, C. N. Kim, A. M. Ibrado, J. Cai, T. I. Peng, D. P. Jones and X. Wang. 1997. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275:1129-1132. https://doi.org/10.1126/science.275.5303.1129
  34. Yang, M. Y. and R. Rajamahendran. 2002. Expression of Bcl-2 and Bax proteins in relation to quality of bovine embryos produced in vitro. Anim. Reprod. Sci. 70:159-169. https://doi.org/10.1016/S0378-4320(01)00186-5

피인용 문헌

  1. Does Melatonin Exert Its Effect on Ram Sperm Capacitation Through Nitric Oxide Synthase Regulation? vol.21, pp.6, 2020, https://doi.org/10.3390/ijms21062093