Journal of Animal Reproduction and Biotechnology (한국동물생명공학회지)

The Korean Society of Animal Reproduction and Biotechnology (한국동물생명공학회)
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Correlation between Sestrin-2 and PERK Signaling in Matured Porcine Oocytes according to ER-stress during In Vitro Maturation

  • Park, Hyo-Jin (Department of Biotechnology, College of Engineering, Daegu University) ;
  • Kim, In-Su (Department of Biotechnology, College of Engineering, Daegu University) ;
  • Kim, Jin-Woo (Department of Biotechnology, College of Engineering, Daegu University) ;
  • Yang, Seul-Gi (Department of Biotechnology, College of Engineering, Daegu University) ;
  • Kim, Min-Ji (Department of Biotechnology, College of Engineering, Daegu University) ;
  • Koo, Deog-Bon (Department of Biotechnology, College of Engineering, Daegu University)
  • Received : 2019.09.11
  • Accepted : 2019.09.24
  • Published : 2019.09.30
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Abstract

Sestrin-2 (SESN2) as a stress-metabolic protein is known for its anti-oxidative effects as a downstream factor of PERK pathways in mammalian cells. However, the expression patterns of SESN2 in conjunction with the UPR signaling against to ER stress on porcine oocyte maturation in vitro, have not been reported. Therefore, we confirmed the expression pattern of SESN2 protein, for which to examine the relationship between PERK signaling and SESN2 in porcine oocyte during IVM. We investigated the SESN2 expression patterns using Western blot analysis in denuded oocytes (DOs), cumulus cells (CCs), and cumulus-oocyte complexes (COCs) at 22 and 44 h of IVM. As expected, the SESN2 protein level significantly increased (p < 0.01) in porcine COCs during 44 h of IVM. We investigated the meiotic maturation after applying ER stress inhibitor in various concentration (50, 100 and 200 μM) of tauroursodeoxycholic acid (TUDCA). We confirmed significant increase (p < 0.05) of meiotic maturation rate in TUDCA 200 μM treated COCs for 44 h of IVM. Finally, we confirmed the protein level of SESN2 and meiotic maturation via regulating ER-stress by only tunicamycin (Tm), only TUDCA, and Tm + TUDCA treatment in porcine COCs. As a result, treatment of the TUDCA following Tm pre-treatment reduced SESN2 protein level in porcine COCs. In addition, SESN2 protein level significantly reduced in only TUDCA treated porcine COCs. Our results suggest that the SESN2 expression is related to the stress mediator response to ER stress through the PERK signaling pathways in porcine oocyte maturation.

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References

  1. Basar M, Bozkurt I, Guzeloglu-Kayisli O, Sozen B, Tekmen I, Schatz F, Arici A, Lockwood CJ and Kayisli UA. 2014. Unfolded protein response prevents blastocyst formation during preimplantation embryo development in vitro. Fertil Steril. 102(6):1777-1784. https://doi.org/10.1016/j.fertnstert.2014.09.004
  2. Bravo R, Parra V, Gatica D, Rodriguez AE, Torrealba N, Paredes F and Quest AF. 2013. Endoplasmic reticulum and the unfolded protein response: dynamics and metabolic integration. Int Rev Cell Mol Biol. 301:215-290. https://doi.org/10.1016/B978-0-12-407704-1.00005-1
  3. Brewer JW and Diehl JA. 2000. PERK mediates cell-cycle exit during the mammalian unfolded protein response. Proc Nati Acad Sci U S A. 97(23):12625-12630. https://doi.org/10.1073/pnas.220247197
  4. Ding B, Parmigiani A, Divakaruni AS, Archer K, Murphy AN and Budanov AV. 2016. Sestrin2 is induced by glucose starvation via the unfolded protein response and protects cells from non-canonical necroptotic cell death. Sci Rep. 6:22538. https://doi.org/10.1038/srep22538
  5. Harding HP, Zeng H, Zhang Y, Jungries R, Chung P, Plesken H, Sabatini DD and Ron D. 2001. Diabetes mellitus and exocrine pancreatic dysfunction in perk-/- mice reveals a role for translational control in secretory cell survival. Mol Cell. 7(6):1153-1163. https://doi.org/10.1016/S1097-2765(01)00264-7
  6. Jin HR, Du CH, Wang CZ, Yuan CS and Du W. 2019. Ginseng metabolite Protopanaxadiol induces Sestrin2 expression and AMPK activation through GCN2 and PERK. Cell Death Dis. 10(4):311. https://doi.org/10.1038/s41419-019-1548-7
  7. Kaufman RJ. 1999. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 13(10):1211-1233. https://doi.org/10.1101/gad.13.10.1211
  8. Kim GT, Lee SH, Kim JI and Kim YM. 2014. Quercetin regulates the sestrin 2-AMPK-p38 MAPK signaling pathway and induces apoptosis by increasing the generation of intracellular ROS in a p53-independent manner. Int J Mol Med. 33(4): 863-869. https://doi.org/10.3892/ijmm.2014.1658
  9. Kim H, An S, Ro SH, Teixeira F, Park GJ, Kim C, Cho CS, Kim JS, Jakob U, Lee JH and Cho US. 2015. Janus-faced Sestrin2 controls ROS and mTOR signalling through two separate functional domains. Nat Commun. 27(6):10025.
  10. Kim JS, Song BS, Lee KS, Kim DH, Kim SU, Choo YK, Chang KT and Koo DB. 2012. Tauroursodeoxycholic acid enhances the pre-implantation embryo development by reducing apoptosis in pigs. Reprod Domest Anim. 47(5):791-798. https://doi.org/10.1111/j.1439-0531.2011.01969.x
  11. 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(7):1186-1197. https://doi.org/10.1016/j.theriogenology.2004.01.011
  12. Latham KE. 2016. Stress signaling in mammalian oocytes and embryos: a basis for intervention and improvement of outcomes. Cell Tissue Res. 363(1):159-167. https://doi.org/10.1007/s00441-015-2124-9
  13. Lin T, Diao YF, Choi HS, Oqani RK, Kang JW, Lee JE and Jin DI. 2015. Procedure used for denuding pig oocytes influences oocyte damage, and development of in vitro and nuclear transfer embryos. Anim Reprod Sci. 152:65-76. https://doi.org/10.1016/j.anireprosci.2014.11.009
  14. Lin T, Lee JE, Kang JW, Shin HY, Lee JB and Jin DI. 2019. Endoplasmic Reticulum (ER) Stress and Unfolded Protein Response (UPR) in Mammalian Oocyte Maturation and Preimplantation Embryo Development. Int J Mol Sci. 20(2):409. https://doi.org/10.3390/ijms20020409
  15. Luo S, Mao C, Lee B and Lee AS. 2006. GRP78/BiP is required for cell proliferation and protecting the inner cell mass from apoptosis during early mouse embryonic development. Mol Cell Biol. 26(15):5688-5697. https://doi.org/10.1128/MCB.00779-06
  16. Marciniak SJ, Yun CY, Oyadomari S, Novoa I, Zhang Y, Jungreis R, Nagata K, Harding HP and Ron D. 2004. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 18(24):3066-3077. https://doi.org/10.1101/gad.1250704
  17. Park HJ, Park JY, Kim JW, Yang SG, Jung JM, Kim MJ, Kang MJ, Cho YH, Wee G, Yang HY, Song BS, Kim SU and Koo DB. 2018. Melatonin improves the meiotic maturation of porcine oocytes by reducing endoplasmic reticulum stress during in vitro maturation. J. Pineal Res. 64(2):E12458. https://doi.org/10.1111/jpi.12458
  18. Park HJ, Park SY, Kim JW, Yang SG, Kim MJ, Kang MJ, Jegal HG, Kim IS, Choo YK and Koo DB. 2018. Melatonin Improves Oocyte Maturation and Mitochondrial Functions by Reducing Bisphenol A-Derived Superoxide in Porcine Oocytes In Vitro. Int J Mol Sci. 19(11):3422. https://doi.org/10.3390/ijms19113422
  19. Park HW, Park H, Ro SH, Jang I, Semple IA, Kim DN, Kim M, Nam M, Zhang D, Yin L and Lee JH. 2014. Hepatoprotective role of Sestrin2 against chronic ER stress. Nat Commun. 5:4233. https://doi.org/10.1038/ncomms5233
  20. Rasheva VI and Domingos PM. 2009. Cellular responses to endoplasmic reticulum stress and apoptosis. Apoptosis. 14(8):996-1007. https://doi.org/10.1007/s10495-009-0341-y
  21. Rodrigues CM, Linehan-Stieers C, Keene CD, Ma X, Kren BT, Low WC and Steer CJ. 2000. Tauroursodeoxycholic acid partially prevents apoptosis induced by 3-nitropropionic acid. J Neurochem. 75(6):2368-2379. https://doi.org/10.1046/j.1471-4159.2000.0752368.x
  22. Schroder M. 2008. Endoplasmic reticulum stress responses. Cell Mol Life Sci. 65(6):862-894. https://doi.org/10.1007/s00018-007-7383-5
  23. Shin BY, Jin SH, Cho IJ and Ki SH. 2012. Nrf2-ARE pathway regulates induction of Sestrin-2 expression. Free Radic Biol Med. 53(4):834-841. https://doi.org/10.1016/j.freeradbiomed.2012.06.026
  24. Walter P and Ron D. 2011. The unfolded protein response: from stress pathway to homeostatic regulation. Science. 334(6059):1081-1086. https://doi.org/10.1126/science.1209038
  25. Wang M, Xu Y, Liu J, Ye J, Yuan W, Jiang H, Wang Z, Jiang H and Wan J. 2017. Recent insights into the biological functions of sestrins in health and disease. Cell Physiol Biochem. 43(5):1731-1741. https://doi.org/10.1159/000484060
  26. Yang SG, Park HJ, Lee SM, Kim JW, Kim MJ, Kim IS, Jegal HG and Koo DB. 2019. Reduction of mitochondrial derived superoxide by Mito-TEMPO improves porcine oocyte maturation in vitro. Journal of Animal Reproduction & Biotechnology. 34(1):10-19. https://doi.org/10.12750/JARB.34.1.10
  27. Yang Y, Pei X, Jin Y, Wang Yand Zhang C. 2016. The roles of endoplasmic reticulum stress response in female mammalian reproduction. Cell Tissue Res. 363(3):589-597. https://doi.org/10.1007/s00441-015-2212-x
  28. Ye J, Palm W, Peng M, King B, Lindsten T, Li MO, Koumenis C and Thompson CB. 2015. GCN2 sustains mTORC1 suppression upon amino acid deprivation by inducing Sestrin2. Genes Dev. 29(22):2331-2336. https://doi.org/10.1101/gad.269324.115
  29. Zeeshan H, Lee G, Kim HR and Chae HJ. 2016. Endoplasmic reticulum stress and associated ROS. Int J Mol Sci. 17(3):327. https://doi.org/10.3390/ijms17030327
  30. Zhang J, Morris Jr MW, Dorsett-Martin WA, Drake LC and Anderson CD. 2013. Autophagy is involved in endoplasmic reticulum stress-induced cell death of rat hepatocytes. J Surg Res. 183(2):929-935. https://doi.org/10.1016/j.jss.2013.02.043
  31. Zhang JY, Diao YF, Oqani RK, Han RX and Jin DI. 2012. Effect of endoplasmic reticulum stress on porcine oocyte maturation and parthenogenetic embryonic development in vitro. Biol Reprod. 86(4):128. https://doi.org/10.1095/biolreprod.111.095059
  32. Zhao N, Liu XJ, Li JT, Zhang L, Fu Y, Zhang YJ, Chen RX, Wei XQ, Wang R and Wang Y. 2015. Endoplasmic reticulum stress inhibition is a valid therapeutic strategy in vitrifying oocytes. Cryobiology. 70(1):48-52. https://doi.org/10.1016/j.cryobiol.2014.12.001