Journal of Embryo Transfer (한국수정란이식학회지)

The Korean Society of Embryo Transfer (한국수정란이식학회)
권호 표지
DOI QR코드

DOI QR Code

Role of $K^+$ Channels in $H_2O_2$- and Cryo-induced Apoptosis of Mouse and Bovine Embryos

과산화수소와 동결에 의해 유도된 생쥐와 소 수정란의 사멸에 있어서 칼륨 통로의 역할

  • Choe, Changyong (National Institute of Animal Science, RDA) ;
  • Kim, Chang-Woon (Department of Physiology and Institute of Health Sciences, Gyeongsang National University School of Medicine) ;
  • Kang, Dawon (Department of Physiology and Institute of Health Sciences, Gyeongsang National University School of Medicine) ;
  • Han, Jaehee (Department of Physiology and Institute of Health Sciences, Gyeongsang National University School of Medicine)
  • 최창용 (국립축산과학원) ;
  • 김창운 (경상대학교 의학전문대학원 생리학교실.건강과학연구원) ;
  • 강다원 (경상대학교 의학전문대학원 생리학교실.건강과학연구원) ;
  • 한재희 (경상대학교 의학전문대학원 생리학교실.건강과학연구원)
  • Received : 2014.09.20
  • Accepted : 2014.09.25
  • Published : 2014.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

Programmed cell death or apoptosis is associated with changes in $K^+$ concentration in many cell types. Recent studies have demonstrated that two-pore domain $K^+$ ($K_{2P}$) channels are involved in mouse embryonic development and apoptotic volume decrease of mammalian cells. In cerebellar granule neurons that normally undergo apoptosis during the early developmental stage, TASK-1 and TASK-3, members of $K_{2P}$ channels, were found to be critical for cell death. This study was performed to identify the role of $K^+$ channels in the $H_2O_2$-induced or cryo-induced cell death of mouse and bovine embryos. Mouse and bovine two-cell stage embryos (2-cells) exposed to $H_2O_2$ for 4 h suffered from apoptosis. The 2-cells showed positive TUNEL staining. Treatment with high concentration of KCl (25mM) inhibited $H_2O_2$-induced apoptosis of 2-cells by 19%. Cryo-induced death in bovine blastocysts showed positive TUNEL staining only in the cells near the plasma membrane. Cryoprotectant supplemented with 25 mM KCl reduced apoptosis slightly compared to cryoprotectant supplemented with 5 mM KCl. However, the combination of antioxidants (${\beta}$-mercaptoethanol) with 25 mM KCl significantly decreased the rate of $H_2O_2$-induced and cryo-induced apoptosis compared to treatments with only antioxidants or 25 mM KCl. These results show that blockage of $K^+$ channel efflux for a short-time reduces $H_2O_2$- and cryo-induced apoptosis in mouse and bovine embryos. Our findings suggest that apoptosis in mouse and bovine embryos might be controlled by modulation of $K^+$ channels which are highly expressed in a given cell type.

Keywords

References

  1. Bortner CD, Hughes FM Jr. and Cidlowski JA. 1997. A primary role for$K^+$ and $Na^+$ efflux in the activation of apoptosis. J. Biol. Chem. 272:32436-32442. https://doi.org/10.1074/jbc.272.51.32436
  2. Bortner CD and Cidlowski JA. 1999. Caspase independent/dependent regulation of K+, cell shrinkage, and mitochondrial membrane potential during lymphocyte apoptosis. J. Biol. Chem. 274:21953-21962. https://doi.org/10.1074/jbc.274.31.21953
  3. Caamano JN, Ryoo ZY, Thomas JA and Youngs CR. 1996. beta-Mercaptoethanol enhances blastocyst formation rate of bovine in vitro-matured/in vitro-fertilized embryos. Biol. Reprod. 55: 1179-1184. https://doi.org/10.1095/biolreprod55.5.1179
  4. Choe C, Shin YW, Kim EJ, Cho SR, Kim HJ, Choi SH, Han MH, Han J, Son DS and Kang D. 2010. Synergistic effects of glutathione and beta-mercaptoethanol treatment during in vitro maturation of porcine oocytes on early embryonic development in a culture system supplemented with L-cysteine. J. Reprod. Dev. 56:575-582. https://doi.org/10.1262/jrd.09-214H
  5. Ekhterae D, Platoshyn O, Zhang S, Remillard CV and Yuan JX. 2003. Apoptosis repressor with caspase domain inhibits cardiomyocyte apoptosis by reducing $K^+$ currents. Am. J. Physiol. Cell Physiol. 284:C1405-1410. https://doi.org/10.1152/ajpcell.00279.2002
  6. Han J, Truell J, Gnatenco C and Kim D. 2002. Characterization of four types of background potassium channels in rat cerebellar granule neurons. J. Physiol. 542:431-444. https://doi.org/10.1113/jphysiol.2002.017590
  7. Hur CG, Choe C, Kim GT, Cho SK, Park JY, Hong SG, Han J and Kang D. 2009. Expression and localization of two-pore domain $K^+$ channels in bovine germ cells. Reproduction 137:237-244. https://doi.org/10.1530/REP-08-0035
  8. Hur CG, Kim EJ, Cho SK, Cho YW, Yoon SY, Tak HM, Kim CW, Choe C, Han J and Kang D. 2012.$K^+$ efflux through two-pore domain $K^+$ channels is required for mouse embryonic development. Reproduction 143:625-636. https://doi.org/10.1530/REP-11-0225
  9. Kim CW, Choe C, Kim EJ, Lee JI, Yoon SY, Cho YW, Han S, Tak HM, Han J and Kang D. 2012. Dual effects of fluoxetine on mouse early embryonic development. Toxicol. Appl. Pharmacol. 265:61-72. https://doi.org/10.1016/j.taap.2012.09.020
  10. Lang F, Busch GL, Ritter M, Volkl H, Waldegger S, Gulbins E and Haussinger D. 1998. Functional significance of cell volume regulatory mechanisms. Physiol. Rev. 78:247-306. https://doi.org/10.1152/physrev.1998.78.1.247
  11. Lauritzen I, Zanzouri M, Honore E, Duprat F, Ehrengruber MU, Lazdunski M and Patel AJ. 2003. $K^+$-dependent cerebellar granule neuron apoptosis. Role of task leak $K^+$ channels. J. Biol. Chem. 278:32068-32076. https://doi.org/10.1074/jbc.M302631200
  12. Maeno E, Ishizaki Y, Kanaseki T, Hazama A and Okada Y. 2000. Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis. Proc. Natl. Acad. Sci. U.S.A. 97:9487-92. https://doi.org/10.1073/pnas.140216197
  13. Martin G, Sabido O, Durand P and Levy R. 2004. Cryopreservation induces an apoptosis-like mechanism in bull sperm. Biol. Reprod. 71:28-37. https://doi.org/10.1095/biolreprod.103.024281
  14. Said TM, Gaglani A and Agarwal A. 2010. Implication of apoptosis in sperm cryoinjury. Reprod. Biomed. Online 21:456-462. https://doi.org/10.1016/j.rbmo.2010.05.011
  15. Simon HU, Haj-Yehia A and Levi-Schaffer F. 2000. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5:415-418. https://doi.org/10.1023/A:1009616228304
  16. Thomson LK, Fleming SD, Aitken RJ, De Iuliis GN, Zieschang JA and Clark AM. 2009. Cryopreservation-induced human sperm DNA damage is predominantly mediated by oxidative stress rather than apoptosis. Hum. Reprod. 24: 2061-2070. https://doi.org/10.1093/humrep/dep214
  17. Trimarchi JR, Liu L, Smith PJ and Keefe DL. 2002. Apoptosis recruits two-pore domain potassium channels used for homeostatic volume regulation. Am. J. Physiol. Cell Physiol. 282:C588-594. https://doi.org/10.1152/ajpcell.00365.2001
  18. Wang AW, Zhang H, Ikemoto I, Anderson DJ and Loughlin KR. 1997. Reactive oxygen species generation by seminal cells during cryopreservation. Urology 49:921-925. https://doi.org/10.1016/S0090-4295(97)00070-8
  19. Xu X, Cowley S, Flaim CJ, James W, Seymour L and Cui Z. 2010. The roles of apoptotic pathways in the low recovery rate after cryopreservation of dissociated human embryonic stem cells. Biotechnol. Prog. 26:827-837. https://doi.org/10.1002/btpr.368
  20. Yu SP and Choi DW. 2000. Ions, cell volume, and apoptosis. Proc. Natl. Acad. Sci. U S A. 97:9360-9362. https://doi.org/10.1073/pnas.97.17.9360