DOI QR코드

DOI QR Code

Nitric Oxide-induced Protein S-nitrosylation Causes Mitochondrial Dysfunction and Accelerates Post-ovulatory Aging of Oocytes in Cattle

  • Niu, Ying-Jie (Department of Animal Science, Chungbuk National University) ;
  • Zhou, Dongjie (Department of Animal Science, Chungbuk National University) ;
  • Zhou, Wenjun (Department of Animal Science, Chungbuk National University) ;
  • Nie, Zheng-Wen (Department of Animal Science, Chungbuk National University) ;
  • Kim, Ju-Yeon (Department of Animal Science, Chungbuk National University) ;
  • Oh, YoungJin (Chung Cheong Buk-Do Institute of Livestock and Veterinary Research) ;
  • Lee, So-Rim (Chung Cheong Buk-Do Institute of Livestock and Veterinary Research) ;
  • Cui, Xiang-Shun (Department of Animal Science, Chungbuk National University)
  • 투고 : 2020.03.17
  • 심사 : 2020.03.24
  • 발행 : 2020.03.31

초록

Nitric oxide (NO)-induced protein S-nitrosylation triggers mitochondrial dysfunction and was related to cell senescence. However, the exact mechanism of these damages is not clear. In the present study, to investigate the relationship between in vitro aging and NO-induced protein S-nitrosylation, oocytes were treated with sodium nitroprusside dihydrate (SNP), and the resultant S-nitrosylated proteins were detected through biotin-switch assay. The results showed that levels of protein S-nitroso thiols (SNO)s and expression of S-nitrosoglutathione reductase (GSNOR) increased, while activity and function of mitochondria were impaired during oocyte aging. Addition of SNP, a NO donor, to the oocyte culture led to accelerated oocyte aging, increased mitochondrial dysfunction and damage, apoptosis, ATP deficiency, and enhanced ROS production. These results suggested that the increased NO signal during oocyte aging in vitro, accelerated oocyte degradation due to increased protein S-nitrosylation, and ROS-related redox signaling.

키워드

참고문헌

  1. Choi BH, Park BY, Kong R, Son MJ, Park CS, Shin NH, Cheon HY, Yang YR, Lee JW, Jin JI, Kong IK. 2019. Effect of serum and serum free media on the developmental competence of OPU derived bovine IVP embryo. J. Anim. Reprod. Biotechnol. 34:305-310. https://doi.org/10.12750/JARB.34.4.305
  2. Choudhury SM, Bhuiyan MMU, Rahman MM, Rahman MM, Sharif MN, Bhattacharjee J, Bari FY, Juyena NS. 2017. Comparison between two cryo-devices for vitrification of immature oocytes of indigenous zebu cows in Bangladesh. J. Emb. Trans. 32:311-317. https://doi.org/10.12750/JET.2017.32.4.311
  3. Dodson MG, Minhas BS, Curtis SK, Palmer TV, Robertson JL. 1989. Spontaneous zona reaction in the mouse as a limiting factor for the time in which an oocyte may be fertilized. J. In Vitro Fert. Embryo Transf. 6:101-106. https://doi.org/10.1007/BF01130735
  4. Ducibella T, Duffy P, Reindollar R, Su B. 1990. Changes in the distribution of mouse oocyte cortical granules and ability to undergo the cortical reaction during gonadotropin-stimulated meiotic maturation and aging in vivo. Biol. Reprod. 43:870-876. https://doi.org/10.1095/biolreprod43.5.870
  5. Fang X, Qamar AY, Yoon KY, Cho J. 2018. Improved preimplantation development of porcine cloned embryos by flavone supplement as antioxidant. J. Emb. Trans. 33:255-264. https://doi.org/10.12750/JET.2018.33.4.255
  6. Guerin P, El Mouatassim S, Menezo Y. 2001. Oxidative stress and protection against reactive oxygen species in the preimplantation embryo and its surroundings. Hum. Reprod. Update 7:175-189. https://doi.org/10.1093/humupd/7.2.175
  7. Hassan BMS, Fang X, Roy PK, Shin ST, Cho JK. 2017. Effect of alpha lipoic acid as an antioxidant supplement during in Vitro maturation medium on bovine embryonic development. J. Emb. Trans. 32:123-130. https://doi.org/10.12750/JET.2017.32.3.123
  8. Haun F, Nakamura T, Shiu AD, Cho DH, Tsunemi T, Holland EA, La Spada AR, Lipton SA. 2013. S-nitrosylation of dynamin-related protein 1 mediates mutant huntingtin-induced mitochondrial fragmentation and neuronal injury in Huntington's disease. Antioxid. Redox Signal. 19:1173-1184. https://doi.org/10.1089/ars.2012.4928
  9. Hess DT and Stamler JS. 2012. Regulation by S-nitrosylation of protein post-translational modification. J. Biol. Chem. 287:4411-4418. https://doi.org/10.1074/jbc.R111.285742
  10. Hwang IS, Kwon DJ, Kwak TU, Lee JY, Hyung NW, Yang H, Oh KB, Ock SA, Park EW, Im GS, Hwang S. 2016. Effect of a short-term in vitro exposure time on the production of in vitro produced piglets. J. Emb. Trans. 31:117-121. https://doi.org/10.12750/JET.2016.31.2.117
  11. Iyer AK, Rojanasakul Y, Azad N. 2014. Nitrosothiol signaling and protein nitrosation in cell death. Nitric Oxide. 42:9-18. https://doi.org/10.1016/j.niox.2014.07.002
  12. Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH. 2001. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat. Cell Biol. 3:193-197. https://doi.org/10.1038/35055104
  13. Jeon YE, Hwangbo Y, Cheong HT, Park CK. 2019. Effects of hyaluronidase during in vitro maturation on maturation and developmental competence in porcine oocytes. J. Anim. Reprod. Biotechnol. 34:86-92. https://doi.org/10.12750/JARB.34.2.86
  14. Kikuchi K, Naito K, Noguchi J, Kaneko H, Tojo H. 2002. Maturation/M-phase promoting factor regulates aging of porcine oocytes matured in vitro. Cloning Stem Cells 4:211-222. https://doi.org/10.1089/15362300260339494
  15. Kim SY, Lin T, Lee JB, Lee JE, Shin HY, Jin DI. 2019. Expression pattern of early transcription factors in porcine oocytes and embryos. J. Anim. Reprod. Biotechnol. 34:123-129. https://doi.org/10.12750/JARB.34.2.123
  16. Lee HJ, Park BJ, Jeon RH, Jang SJ, Son YB, Lee SL, Rho GJ, Kim SJ, Lee WJ. 2019a. Alteration of apoptosis during differentiation in human dental pulp-derived mesenchymal stem cell. J. Anim. Reprod. Biotechnol. 34:2-9. https://doi.org/10.12750/jarb.34.1.2
  17. Lee SY, Park CJ, Nam YK. 2019b. Assessment of suitable reference genes for RT-qPCR normalization with developmental samples in pacific abalone Haliotis discus hannai. J. Anim. Reprod. Biotechnol. 34:280-291. https://doi.org/10.12750/JARB.34.4.280
  18. Lee TH, Lee MS, Huang CC, Tsao HM, Lin PM, Ho HN, Shew JY, Yang YS. 2013. Nitric oxide modulates mitochondrial activity and apoptosis through protein S-nitrosylation for preimplantation embryo development. J. Assist. Reprod. Genet. 30:1063-1072. https://doi.org/10.1007/s10815-013-0045-7
  19. Li Q and Cui LB. 2016. Combined inhibitory effects of low temperature and N-acetyl-l-cysteine on the postovulatory aging of mouse oocytes. Zygote 24:195-205. https://doi.org/10.1017/S0967199415000039
  20. Liang QX, Lin YH, Zhang CH, Sun HM, Zhou L, Schatten H, Sun QY, Qian WP. 2018. Resveratrol increases resistance of mouse oocytes to postovulatory aging in vivo. Aging (Albany NY) 10:1586-1596. https://doi.org/10.18632/aging.101494
  21. Liu J, Liu M, Ye X, Liu K, Huang J, Wang L, Ji G, Liu N, Tang X, Baltz JM, Keefe DL, Liu L. 2012. Delay in oocyte aging in mice by the antioxidant N-acetyl-L-cysteine (NAC). Hum. Reprod. 27:1411-1420. https://doi.org/10.1093/humrep/des019
  22. Lord T and Aitken RJ. 2013. Oxidative stress and ageing of the post-ovulatory oocyte. Reproduction 146:R217-R227. https://doi.org/10.1530/REP-13-0111
  23. Lord T, Nixon B, Jones KT, Aitken RJ. 2013. Melatonin prevents postovulatory oocyte aging in the mouse and extends the window for optimal fertilization in vitro. Biol. Reprod. 88:67. https://doi.org/10.1095/biolreprod.112.106450
  24. Nakamura T and Lipton SA. 2011. Redox modulation by S-nitrosylation contributes to protein misfolding, mitochondrial dynamics, and neuronal synaptic damage in neurodegenerative diseases. Cell Death Differ. 18:1478-1486. https://doi.org/10.1038/cdd.2011.65
  25. 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 109:501-507. https://doi.org/10.1242/dev.109.2.501
  26. Park SH, Jeon Y, Yu IJ. 2017. Effects of antioxidants supplement in porcine sperm freezing on in vitro fertilization and the glutathione and reactive oxygen species level of presumptive zygotes. J. Emb. Trans. 32:337-342. https://doi.org/10.12750/JET.2017.32.4.337
  27. Pendergrass W, Wolf N, Poot M. 2004. Efficacy of MitoTracker GreenTM and CMXRosamine to measure changes in mitochondrial membrane potentials in living cells and tissues. Cytometry A 61:162-169. https://doi.org/10.1002/cyto.a.20033
  28. Premkumar KV and Chaube SK. 2015. Nitric oxide signals postovulatory aging-induced abortive spontaneous egg activation in rats. Redox Rep. 20:184-192. https://doi.org/10.1179/1351000215Y.0000000003
  29. Raju K, Doulias PT, Evans P, Krizman EN, Jackson JG, Horyn O, Daikhin Y, Nissim I, Yudkoff M, Nissim I, Sharp KA, Robinson MB, Ischiropoulos H. 2015. Regulation of brain glutamate metabolism by nitric oxide and S-nitrosylation. Sci. Signal. 8:ra68. https://doi.org/10.1126/scisignal.aaa4312
  30. Rizza S, Cardaci S, Montagna C, Di Giacomo G, De Zio D, Bordi M, Maiani E, Campello S, Borreca A, Puca AA, Stamler JS, Cecconi F, Filomeni G. 2018. S-nitrosylation drives cell senescence and aging in mammals by controlling mitochondrial dynamics and mitophagy. Proc. Natl. Acad. Sci. U. S. A. 115:E3388-E3397. https://doi.org/10.1073/pnas.1722452115
  31. Seth D, Hess DT, Hausladen A, Wang L, Wang YJ, Stamler JS. 2018. A multiplex enzymatic machinery for cellular protein S-nitrosylation. Mol. Cell 69:451-464.e456. https://doi.org/10.1016/j.molcel.2017.12.025
  32. Sun J, Morgan M, Shen RF, Steenbergen C, Murphy E. 2007. Preconditioning results in S-nitrosylation of proteins involved in regulation of mitochondrial energetics and calcium transport. Circ. Res. 101:1155-1163. https://doi.org/10.1161/CIRCRESAHA.107.155879
  33. Tatone C, Di Emidio G, Barbaro R, Vento M, Ciriminna R, Artini PG. 2011. Effects of reproductive aging and postovulatory aging on the maintenance of biological competence after oocyte vitrification: insights from the mouse model. Theriogenology 76:864-873. https://doi.org/10.1016/j.theriogenology.2011.04.017
  34. Wakayama S, Thuan NV, Kishigami S, Ohta H, Mizutani E, Hikichi T, Miyake M, Wakayama T. 2004. Production of offspring from one-day-old oocytes stored at room temperature. J. Reprod. Dev. 50:627-637. https://doi.org/10.1262/jrd.50.627
  35. Wang T, Gao YY, Chen L, Nie ZW, Cheng W, Liu X, Schatten H, Zhang X, Miao YL. 2017. Melatonin prevents postovulatory oocyte aging and promotes subsequent embryonic development in the pig. Aging (Albany NY) 9:1552-1564. https://doi.org/10.18632/aging.101252
  36. Wang Y, Li L, Fan LH, Jing Y, Li J, Ouyang YC, Wang ZB, Hou Y, Sun QY. 2019. N-acetyl-L-cysteine (NAC) delays post-ovulatory oocyte aging in mouse. Aging (Albany NY) 11:2020-2030. https://doi.org/10.18632/aging.101898
  37. Xu Z, Abbott A, Kopf GS, Schultz RM, Ducibella T. 1997. Spontaneous activation of ovulated mouse eggs: time-dependent effects on M-phase exit, cortical granule exocytosis, maternal messenger ribonucleic acid recruitment, and inositol 1,4,5-trisphosphate sensitivity. Biol. Reprod. 57:743-750. https://doi.org/10.1095/biolreprod57.4.743
  38. Zhang M, ShiYang X, Zhang Y, Miao Y, Chen Y, Cui Z, Xiong B. 2019. Coenzyme Q10 ameliorates the quality of postovulatory aged oocytes by suppressing DNA damage and apoptosis. Free Radic. Biol. Med. 143:84-94. https://doi.org/10.1016/j.freeradbiomed.2019.08.002
  39. Zhang N, Wakai T, Fissore RA. 2011. Caffeine alleviates the deterioration of Ca(2+) release mechanisms and fragmentation of in vitro-aged mouse eggs. Mol. Reprod. Dev. 78:684-701. https://doi.org/10.1002/mrd.21366