Reproductive and Developmental Biology

  • 제41권1호
  • /
  • Pages.17-23
  • /
  • 2017
  • /
  • 1738-2432(pISSN)
  • /
  • 2288-0151(eISSN)
한국동물번식학회 (The Korean Society of Animal Reproduction)
권호 표지
DOI QR코드

DOI QR Code

돼지 난자의 체외성숙과 배아발달 동안 ROS와 항산화제의 영향

Effects of Reactive Oxygen Species and Antioxidants during In Vitro Maturation Oocytes and Embryo Development in Pigs

  • 이원희 (강원대학교 동물생명과학대학) ;
  • 박지은 (강원대학교 동물생명과학대학) ;
  • 황보용 (강원대학교 동물생명과학대학) ;
  • 김화영 (강원대학교 동물생명과학대학) ;
  • 이지은 (강원대학교 동물생명과학대학) ;
  • 강병범 (강원대학교 동물생명과학대학) ;
  • 정희태 (강원대학교 수의과대학) ;
  • 양부근 (강원대학교 동물생명과학대학) ;
  • 박춘근 (강원대학교 동물생명과학대학)
  • Lee, Won-Hee (College of Animal Life Sciences, Kangwon National University) ;
  • Park, Ji-Eun (College of Animal Life Sciences, Kangwon National University) ;
  • Hwangbo, Yong (College of Animal Life Sciences, Kangwon National University) ;
  • Kim, Hwa-Young (College of Animal Life Sciences, Kangwon National University) ;
  • Lee, Ji-Eun (College of Animal Life Sciences, Kangwon National University) ;
  • Kang, Byeong-Buhm (College of Animal Life Sciences, Kangwon National University) ;
  • Cheong, Hee-Tae (College of Veterinary Medicine, Kangwon National University) ;
  • Yang, Boo-Keun (College of Animal Life Sciences, Kangwon National University) ;
  • Park, Choon-Keun (College of Animal Life Sciences, Kangwon National University)
  • 투고 : 2017.02.22
  • 심사 : 2017.02.28
  • 발행 : 2017.02.28
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

The oocyte undergoes various events during in vitro maturation (IVM) and subsequence development. One of the events is production of reactive oxygen species (ROS) that is a normal process of cell metabolism. But imbalances between ROS production and antioxidant systems induce oxidative stress that negatively affect to mammalian reproductive process. In vitro environments, in vitro matured oocytes have many problems, such as excessive production of ROS and imperfect cytoplasmic maturation. Therefore, in vitro matured oocytes still have lower maturation rates and developmental competence than in vivo matured oocytes. In order to improve the IVM and in vitro culture (IVC) system, antioxidants, vitamins were added to the IVM, IVC medium. Antioxidant supplementation was effective in controlling the production of ROS and it continues to be explored as a potential strategy to overcome mammalian reproductive disorders. Based on these studies, we expect that the use of antioxidants in porcine oocytes could improved maturation and development rates.

키워드

참고문헌

  1. Abeydeera LR, Wang WH, Cantley TC, Rieke A, Prather RS, Day BN (1998): Presence of epidermal growth factor during in vitro maturation of pig oocytes and embryo culture can modulate blastocyst development after in vitro fertilization. Mol Reprod Dev 51(4):395-401. https://doi.org/10.1002/(SICI)1098-2795(199812)51:4<395::AID-MRD6>3.0.CO;2-Y
  2. Agarwal A, Allamaneni SS (2004): Oxidants and antioxidants in human fertility. Middle East Fertil Soc J 9(3):187-197.
  3. Agarwal A, Aponte-Mellado A, Premkumar BJ, Shaman A, Gupta S (2012): The effects of oxidative stress on female reproduction: a review. Reprod Biol Endocrinol 10(1):49. https://doi.org/10.1186/1477-7827-10-49
  4. Alvarez GM, Morado SA, Soto MP, Dalvit GC, Cetica PD (2015): The control of reactive oxygen species influences porcine oocyte in vitro maturation. Reprod Domest Anim 50(2):200-205. https://doi.org/10.1111/rda.12469
  5. Anchordoquy JP, Anchordoquy JM, Picco SJ, Sirini MA, Errecalde AL, Furnus CC (2014): Influence of manganese on apoptosis and glutathione content of cumulus cells during in vitro maturation in bovine oocytes. Cell Biol Int 38(2):246-253. https://doi.org/10.1002/cbin.10195
  6. Appeltant R, Somfai T, Kikuchi K, Maes D, Van Soom A (2015): Influence of co-culture with denuded oocytes during in vitro maturation on fertilization and developmental competence of cumulus-enclosed porcine oocytes in a defined system. Anim Sci J.
  7. Auerbach S, Brinster RL (1968): Effect of oxygen concentration on the development of two-cell mouse embryos. Nature 217:465-466. https://doi.org/10.1038/217465a0
  8. Awda BJ, Mackenzie-Bell M, Buhr MM (2009): Reactive oxygen species and boar sperm function. Biol Reprod 81(3):553-561. https://doi.org/10.1095/biolreprod.109.076471
  9. Balasubramanian S, Son WJ, Kumar BM, Ock SA., Yoo JG, Im GS, Rho GJ (2007): Expression pattern of oxygen and stress-responsive gene transcripts at various developmental stages of in vitro and in vivo preimplantation bovine embryos. Theriogenology 68 (2):265-275. https://doi.org/10.1016/j.theriogenology.2007.05.044
  10. Banwell KM, Lane M, Russell DL, Kind KL, Thompson JG (2007): Oxygen concentration during mouse oocyte in vitro maturation affects embryo and fetal development. Hum Reprod 22(10):2768-2775. https://doi.org/10.1093/humrep/dem203
  11. Batt PA, Gardner DK, Cameron AW (1991): Oxygen concentration and protein source affect the development of preimplantation goat embryos in vitro. Reprod Fertil Dev 3(5):601-607. https://doi.org/10.1071/RD9910601
  12. Bavister BD (1988): Role of oviductal secretions in embryonic growth in vivo and in vitro. Theriogenology 29(1):143-154. https://doi.org/10.1016/0093-691X(88)90037-4
  13. Bayr H (2005): Reactive oxygen species. Crit Care Med 33(12):S498-S501. https://doi.org/10.1097/01.CCM.0000186787.64500.12
  14. Behrman HR, Kodaman PH, Preston SL, Gao S (2001): Oxidative stress and the ovary. J Soc Gynecol Investig 8(1 suppl): S40-S42.
  15. Bertoldo MJ, Nadal-Desbarats L, Gerard N, Dubois A, Holyoake PK, Grupen CG (2013): Differences in the metabolomic signatures of porcine follicular fluid collected from environments associated with good and poor oocyte quality. Reproduction 146(3): 221-231. https://doi.org/10.1530/REP-13-0142
  16. Blondin P, Coenen K, Guilbault LA, Sirard MA (1997): In vitro production of bovine embryos: developmental competence is acquired before maturation. Theriogenology 47(5):1061-1075. https://doi.org/10.1016/S0093-691X(97)00063-0
  17. Cetica PD, Pintos LN, Dalvit GC, Beconi MT (2001): Antioxidant enzyme activity and oxidative stress in bovine oocyte in vitro maturation. IUBMB Life 51 (1):57-64. https://doi.org/10.1080/15216540119253
  18. Chan AC (1993): Partners in defense, vitamin E and vitamin C. Can J Physiol Pharmacol 71(9):725-731. https://doi.org/10.1139/y93-109
  19. Combelles CM, Gupta S, Agarwal A (2009): Could oxidative stress influence the in-vitro maturation of oocytes? Reprod Biomed Online 18(6): 864-880. https://doi.org/10.1016/S1472-6483(10)60038-7
  20. De Matos DG, Furnus CC (2000): The importance of having high glutathione (GSH) level after bovine in vitro maturation on embryo development: effect of ${\beta}$-mercaptoethanol, cysteine and cystine. Theriogenology 53(3):761-771. https://doi.org/10.1016/S0093-691X(99)00278-2
  21. De Matos DG, Furnus CC, Moses DF, Martinez AG, 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(4):451-457. https://doi.org/10.1002/(SICI)1098-2795(199612)45:4<451::AID-MRD7>3.0.CO;2-Q
  22. Ealy AD, Drost M, Barros CM, Hansen PJ (1992): Thermoprotection of preimplantation bovine embryos from heat shock by glutathione and taurine. Cell Biol Int Rep 16(2):125-131. https://doi.org/10.1016/S0309-1651(06)80106-2
  23. Fujii J, Iuchi Y, Matsuki S, Ishii T (2003): Cooperative function of antioxidant and redox systems against oxidative stress in male reproductive tissues. Asian J Androl 5(3):231-242.
  24. Fujii J, Iuchi Y, Okada F (2005): Fundamental roles of reactive oxygen species and protective mechanisms in the female reproductive system. Reprod Biol Endocrinol 3(1):43. https://doi.org/10.1186/1477-7827-3-43
  25. Gille JJ, Joenje H (1991): Biological significance of oxygen toxicity: an introduction. Membrane Lipid Oxidation 3:1-32.
  26. Goodsell DS (2004): Catalase. Molecule of the Mon th. RCSB Protein Data Bank. doi 10:2210.
  27. Goto Y, Noda Y, Narimoto K, Umaoka Y, Mori T (1992): Oxidative stress on mouse embryo development in vitro. Free Radic Biol Med 13(1):47-53. https://doi.org/10.1016/0891-5849(92)90165-D
  28. Guerin P, El Mouatassim S, Menezo Y (2001): Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum Reprod Update 7(2):175-189. https://doi.org/10.1093/humupd/7.2.175
  29. Halliwell B, Gutteridge JMC (1988): Free radicals and antioxidant protection: mechanisms and significance in toxicology and disease. Hum Toxicol 7:7-13. https://doi.org/10.1177/096032718800700102
  30. Hu J, Cheng D, Gao X, Bao J, Ma X and Wang H (2012): Vitamin C enhances the In vitro development of porcine pre-implantation embryos by reducing oxidative stress. Reprod Domest Anim 47(6): 873-879. https://doi.org/10.1111/j.1439-0531.2011.01982.x
  31. Jeon Y, Yoon JD, Cai L, Hwang SU, Kim E, Zheng Z, Lee E, Kim DY, Hyun SH (2014): Supplementation of zinc on oocyte in vitro maturation improves preimplatation embryonic development in pigs. Theriogenology 82(6):866-874. https://doi.org/10.1016/j.theriogenology.2014.06.021
  32. Kehrer JP (2000): The Haber-Weiss reaction and mechanisms of toxicity. Toxicology 149(1):43-50. https://doi.org/10.1016/S0300-483X(00)00231-6
  33. Kitagawa Y, Suzuki K, Yoneda A, 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(7):1186-1197. https://doi.org/10.1016/j.theriogenology.2004.01.011
  34. Koerber S, Santos AN, Tetens F, Kuchenhoff A, Fischer B (1998): Increased expression of NADH-ubiquinone oxidoreductase chain 2 (ND2) in preimplantation rabbit embryos cultured with 20% oxygen concentration. Mol Reprod Dev 49(4):394-399. https://doi.org/10.1002/(SICI)1098-2795(199804)49:4<394::AID-MRD6>3.0.CO;2-I
  35. Krisher RL, Bavister BD (1998): Responses of oocytes and embryos to the culture environment. Theriogenology 49(1):103-114. https://doi.org/10.1016/S0093-691X(97)00405-6
  36. Kwak SS, Cheong SA, Jeon Y, Lee E, Choi KC, Jeung EB, Hyun SH (2012): The effects of resveratrol on porcine oocyte in vitro maturation and subsequent embryonic development after parthenogenetic activation and in vitro fertilization. Theriogenology 78(1):86-101. https://doi.org/10.1016/j.theriogenology.2012.01.024
  37. Lee H, Bae JH, Lee SR (2004): Protective effect of green tea polyphenol EGCG against neuronal damage and brain edema after unilateral cerebral ischemia in gerbils. J Neurosci Res 77(6):892-900. https://doi.org/10.1002/jnr.20193
  38. Lee S, Park EJ, Moon JH, Kim SJ, Song K, Lee BC (2015): Sequential treatment with resveratrol-trolox improves development of porcine embryos derived from parthenogenetic activation and somatic cell nuclear transfer. Theriogenology 84(1):145-154. https://doi.org/10.1016/j.theriogenology.2015.02.021
  39. Lim JM, Liou SS, Hansel W (1996): Intracytoplasmic glutathione concentration and the role of ${\beta}$-mercaptoethanol in preimplantation development of bovine embryos. Theriogenology 46(3):429-439. https://doi.org/10.1016/0093-691X(96)00165-3
  40. Liu Z, Foote RH (1995): Development of bovine embryos in KSOM with added superoxide dismutase and taurine and with five and twenty percent $O_2$. Biol Reprod 53(4):786-790. https://doi.org/10.1095/biolreprod53.4.786
  41. Manes C, Lai MC (1995): Nonmitochondrial oxygen utilization by rabbit blastocysts and surface production of superoxide radicals. J Reprod Fertil 104: 69-75. https://doi.org/10.1530/jrf.0.1040069
  42. McCord JM, Fridovich I (1969): Superoxide dismutase an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244(22):6049-6055.
  43. Meister A, Tate SS (1976): Glutathione and related $\gamma$-glutamyl compounds: biosynthesis and utilization. Annu Rev Biochem 45(1):559-604. https://doi.org/10.1146/annurev.bi.45.070176.003015
  44. Moyer RA, Hummer KE, Finn CE, Frei B, Wrolstad RE (2002): Anthocyanins, phenolics, and antioxidant capacity in diverse small fruits: Vaccinium, Rubus, and Ribes. J Agric Food Chem 50(3):519-525. https://doi.org/10.1021/jf011062r
  45. Munne S, Estop A (1991): Superoxide anion increases after sperm storage and produces chromosome abnormalities. Biol Reprod 44(Suppl 1):74.
  46. Nagashima H, Nagai T, Yamakawa H (1993): In vitro development of in vivo and in vitro fertilized porcine zygotes. J Reprod Dev 39(2):163-168. https://doi.org/10.1262/jrd.39.163
  47. Nasr-Esfahani MH, Aitken JR, Johnson MH (1990): Hydrogen peroxide levels in mouse oocytes and early cleavage stage embryos developed in vitro or in vivo. Development 109(2):501-507.
  48. Nasr-Esfahani MH, Johnson MH (1991): The origin of reactive oxygen species in mouse embryo cultured in vitro. Development 113:551-560.
  49. Noda Y, Goto Y, Umaoka Y, Shiotani M, Nakayama T, Mori T (1994): Culture of human embryos in alpha modification of Eagle's medium under low oxygen tension and low illumination. Fertil Steril 62(5):1022-1027. https://doi.org/10.1016/S0015-0282(16)57068-X
  50. Nonogaki T, Noda Y, Narimoto K, Umaoka Y, Mori T (1992): Effects of superoxide dismutase on mouse in vitro fertilization and embryo culture system. J Assist Reprod Genet 9(3):274-280. https://doi.org/10.1007/BF01203828
  51. Olson SE, Seidel GE (2000): Culture of in vitro-produced bovine embryos with vitamin E improves development in vitro and after transfer to recipients. Biol Reprod 62(2):248-252. https://doi.org/10.1095/biolreprod62.2.248
  52. Orsi NM, Gopichandran N, Leese HJ, Picton HM, Harris SE (2005): Fluctuations in bovine ovarian follicular fluid composition throughout the oestrous cycle. Reproduction 129(2):219-228. https://doi.org/10.1530/rep.1.00460
  53. Perkins AV (2006): Endogenous anti-oxidants in pregnancy and preeclampsia. Aust NZ J Obstet Gynaecol 46(2):77-83. https://doi.org/10.1111/j.1479-828X.2006.00532.x
  54. Perreault SD (1999, January): Regulation of sperm nuclear reactivation during fertilization in: Bavister Cummins J, Roldon Ers (eds), Fertilization. Proceeding of International Symposium on Mammals.
  55. Rinaudo PF, Giritharan G, Talbi S, Dobson AT, Schultz RM (2006): Effects of oxygen tension on gene expression in preimplantation mouse embryos. Fertil Steril 86(4):1265-e1.
  56. Sawai K, Funahashi H, Niwa K (1997): Stage-specific requirement of cysteine during in vitro maturation of porcine oocytes for glutathione synthesis associated with male pronuclear formation. Biol Reprod 57(1):1-6. https://doi.org/10.1095/biolreprod57.1.1
  57. Sharma RK, Agarwal A (2004): Role of reactive oxygen species in gynecologic diseases. Reprod Med Biol 3(4):177-199. https://doi.org/10.1111/j.1447-0578.2004.00068.x
  58. Sies H, Stahl W (1995): Vitamins E and C, beta-carotene, and other carotenoids as antioxidants. The Am J Clin Nutr 62(6):1315S-1321S. https://doi.org/10.1093/ajcn/62.6.1315S
  59. Spinaci M, Volpe S, De Ambrogi M, Tamanini C, and Galeati G (2008): Effects of epigallocatechin-3-gallate (EGCG) on in vitro maturation and fertilization of porcine oocytes. Theriogenology 69(7):877-885. https://doi.org/10.1016/j.theriogenology.2008.01.005
  60. Takahashi M (2012): Oxidative stress and redox regulation on in vitro development of mammalian embryos. J Reprod Dev 58(1):1-9. https://doi.org/10.1262/jrd.11-138N
  61. Tareq KMA, Akter QS, Khandoker MY, Tsujii H (2012): Selenium and vitamin E improve the in vitro maturation, fertilization and culture to blastocyst of porcine oocytes. J Reprod Dev 58(6):621-628. https://doi.org/10.1262/jrd.2012-064
  62. Tarin JJ, Vendrell FJ, Ten J, Blanes R, Van Blerkom J, Cano A (1996): The oxidizing agent tertiary butyl hydroperoxide induces disturbances in spindle organization, c-meiosis, and aneuploidy in mouse oocytes. Mol Hum Reprod 2(12):895-901. https://doi.org/10.1093/molehr/2.12.895
  63. Tatemoto H, Muto N, Sunagawa I, Shinjo A, Nakada T (2004): Protection of porcine oocytes against cell damage caused by oxidative stress during in vitro maturation: role of superoxide dismutase activity in porcine follicular fluid. Biol Reprod 71(4):1150. https://doi.org/10.1095/biolreprod.104.029264
  64. Tatemoto H, Sakurai N, 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(3):805-810. https://doi.org/10.1095/biolreprod63.3.805
  65. Thompson JGE, Simpson AC, Pugh PA, Donnelly PE, Tervit HR (1990): Effect of oxygen concentration on in-vitro development of preimplantation sheep and cattle embryos. J Reprod Fertil 89(2):573-578. https://doi.org/10.1530/jrf.0.0890573
  66. Wright RW (1977): Successful culture of swine embryos to the blastocyst stage. J Anim Sci 44(5):854-858. https://doi.org/10.2527/jas1977.445854x
  67. Yamauchi N, Nagai T (1999): Male pronuclear formation in denuded porcine oocytes after in vitro maturation in the presence of cysteamine. Biol Reprod 61(3):828-833. https://doi.org/10.1095/biolreprod61.3.828
  68. Yang HW, Hwang KJ, Kwon HC, Kim HS, Choi KW, Oh KS (1998): Detection of reactive oxygen species (ROS) and apoptosis in human fragmented embryos. Hum Reprod 13(4):998-1002. https://doi.org/10.1093/humrep/13.4.998
  69. Yoshida M (1993): Role of glutathione in the maturation and fertilization of pig oocytes in vitro. Mol Reprod Dev 35(1):76-81. https://doi.org/10.1002/mrd.1080350113