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Korean Society for Biochemistry and Molecular Biology (생화학분자생물학회)
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Endoplasmic Reticulum Mediated Necrosis-like Apoptosis of HeLa Cells Induced by Ca2+ Oscillation

  • Hu, Qingliu (Medical School, Tsinghua University) ;
  • Chang, Junlei (Medical School, Tsinghua University) ;
  • Tao, Litao (Department of Biological Sciences and Biotechnology, Tsinghua University) ;
  • Yan, Guoliang (Department of Biological Sciences and Biotechnology, Tsinghua University) ;
  • Xie, Mingchao (Medical School, Tsinghua University) ;
  • Wang, Zhao (Medical School, Tsinghua University)
  • Published : 2005.11.30
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Abstract

Apoptosis and necrosis are distinguished by modality primarily. Here we show an apoptosis occurred instantly, induced by $300\;{\mu}M$ W-7 ((N-(6-aminohexyl)-5-chloro-1-naphthalenesulfonamide hydrochloride), inhibitor of calmodulin), which demonstrated necrotic modality. As early as 30 min after W-7 addition, apoptotic (sub-diploid) peak could be detected by fluorescence-activated cell sorter (FACS), “DNA ladders” began to emerge also at this time point, activity of caspase-3 elevated obviously within this period. Absence of mitochondrial membrane potential (MMP) reduction and cytochrome c, AIF (apoptosis inducing factor) release, verified that this rapid apoptosis did not proceed through mitochondria pathway. Activation of caspase-12 and changes of other endoplasmic reticulum (ER) located proteins ascertained that ER pathway mediated this necrosis-like apoptosis. Our findings suggest that it is not credible to judge apoptosis by modality. Elucidation of ER pathway is helpful to comprehend the pathology of diseases associated with ER stress, and may offer a new approach to the therapy of cancer and neurodegenerative diseases.

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References

  1. Arnaudeau, S., Frieden, M., Nakamura, K., Castelbou, C., Michalak, M. and Demaurex, N. (2002) Calreticulin differentially modulates calcium uptake and release in the endoplasmic reticulum and mitochondria. J. Biol. Chem. 277, 46696-46705 https://doi.org/10.1074/jbc.M202395200
  2. Berridge, M. J., Bootman, M. D. and Lipp, P. (1998) Calcium–a life and death signal. Nature 395, 645-648 https://doi.org/10.1038/27094
  3. Berridge, M. J., Lipp, P. and Bootman, M. D. (2000) The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell. Biol. 1, 11-21 https://doi.org/10.1038/35036035
  4. Chen, Y., Douglass, T., Jeffes, E. W., Xu, Q., Williams, C. C., Arpajirakul, N., Delgado, C., Kleinman, M., Sanchez, R., Dan, Q., Kim, R. C., Wepsic, H. T. and Jadus, M. R. (2002) Living T9 glioma cells expressing membrane macrophage colonystimulating factor produce immediate tumor destruction by polymorphonuclear leukocytes and macrophages via a 'paraptosis'-induced pathway that promotes systemic immunity against intracranial T9 gliomas. Blood 100, 1373-1380 https://doi.org/10.1182/blood-2002-01-0174
  5. Groner, M. and Malchow, D. (1996) Calmodulin-antagonists inhibit vesicular $Ca^{2+}$ uptake in Dictyostelium. Cell Calcium 19, 105-111 https://doi.org/10.1016/S0143-4160(96)90079-2
  6. Hitomi, J., Katayama, T., Taniguchi, M., Honda, A., Imaizumi, K. and Tohyama, M. (2004) Apoptosis induced by endoplasmic reticulum stress depends on activation of caspase-3 via caspase-12. Neurosci. Lett. 357, 127-130 https://doi.org/10.1016/j.neulet.2003.12.080
  7. Ito, M., Tanaka, T., Nunoki, K., Hidaka, H. and Suzuki, K. (1987) The $Ca^{2+}$ -activated protease (calpain) modulates $Ca^{2+}$ / calmodulin dependent activity of smooth muscle myosin light chain kinase. Biochem. Biophys. Res. Commun. 145, 1321- 1328 https://doi.org/10.1016/0006-291X(87)91582-8
  8. Jan, C. R. and Tseng, C. J. (2000) W-7 induces [$Ca^{2+}$ ]i increases in Madin-Darby canine kidney (MDCK) cells. J. Pharmcol. Exp. Ther. 292, 358-365
  9. Kijima, Y., Ogunbunmi, E. and Fleischer, S. (1991) Drug action of thapsigargin on the $Ca^{2+}$ pump protein of sarcoplasmic reticulum. J. Biol. Chem. 266, 22912-22918
  10. Liu, M. J., Wang, Z., Li, H. X., Wu, R. C., Liu, Y. Z. and Wu Q. Y. (2004) Mitochondrial dysfunction as an early event in the process of apoptosis induced by woodfordin I in human leukemia K562 cells. Toxicol. Appl. Pharmacol. 194, 141-155 https://doi.org/10.1016/j.taap.2003.08.017
  11. Liu, X. and Schnellmann, R. G. (2003) Calpain mediates progressive plasma membrane permeability and proteolysis of cytoskeleton-associated paxillin, talin, and vinculin during renal cell death. J. Pharmacol. Exp. Ther. 304, 63-70 https://doi.org/10.1124/jpet.102.043406
  12. Liu, X., Kim, C. N., Yang, J. and Jemmerson, R. (1996) Induction of apoptotic program in cell-free extracts: Requirement for dATP and cytochrome c. Cell 86, 147-157 https://doi.org/10.1016/S0092-8674(00)80085-9
  13. Lytton, J., Westlin, M. and Hanley, M. R. (1991) Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps. J. Biol. Chem. 266, 17067-17071
  14. Mene, P., Pugliese, F. and Cinotti, G. A. (1996) Regulation of capacitative calcium influx in cultured human mesangial cells: roles of protein kinase C and calmodulin. J. Am. Soc. Nephrol. 7, 983-990
  15. Michalak, M., Corbett, E. F., Mesaeli, N., Nakamura, K. and Opas, M. (1999) Calreticulin: one protein, one gene, many functions. Biochem. J. 344, 281-292 https://doi.org/10.1042/0264-6021:3440281
  16. Morishima, N., Nakanishi, K., Takenouchi, H., Shibata, T. and Yasuhiko, Y. (2002) An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J. Biol. Chem. 277, 34287-34294 https://doi.org/10.1074/jbc.M204973200
  17. Nakagawa, T., Zhu, H., Morishima, N., Li, E., Xu, J. and Yankner, B. A. (2000) Caspase-12 mediates endoplasmicreticulum- specific apoptosis and cytotoxicity by amyloid-beta. Nature 403, 98-103 https://doi.org/10.1038/47513
  18. Nishikawa, M., Tanaka, T. and Hidaka, H. (1980) $Ca^{2+}$- calmodulin-dependent phosphorylation and platelet secretion. Nature 287, 863-865 https://doi.org/10.1038/287863a0
  19. Paschen, W. (2003) Endoplasmic reticulum: a primary target in various acute disorders and degenerative diseases of the brain. Cell Calcium 34, 365-383 https://doi.org/10.1016/S0143-4160(03)00139-8
  20. Reddy, R., Buckley, S., Doerken, M., Barsky, L., Weinberg, K., Anderson, K. D., Warburton, D. and Driscoll, B. (2004) Isolation of a putative progenitor subpopulation of alveolar epithelial type 2 cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 286, 658-667 https://doi.org/10.1152/ajplung.00159.2003
  21. Rizzuto, R., Pinton, P., Carrington, W., Fay, F. S., Fogarty, K. E. and Lifshitz, L. M. (1998) Close contacts with the endoplasmic reticulum as determinants of mitochondrial $Ca^{2+}$ responses. Science 280, 1763-1766 https://doi.org/10.1126/science.280.5370.1763
  22. Single, B., Leist, M. and Nicotera, P. (1998) Simultaneous release of adenylate kinase and cytochrome c in cell death. Cell Death Differ. 5, 1001-1003 https://doi.org/10.1038/sj.cdd.4400462
  23. Stout, M. A. and Silver, P. J. (1992) Calcium transport by sarcoplasmic reticulum of vascular smooth muscle: II. Effects of calmodulin and calmodulin inhibitors. J. Cell Physiol. 153, 169-175 https://doi.org/10.1002/jcp.1041530121
  24. Thastrup, O., Cullen, P. J., Drobak, B. K., Hanley, M. R. and Dawson, A. P. (1990) Thapsigargin, a tumor promoter, discharges intracellular $Ca^{2+}$ stores by specific inhibition of the endoplasmic reticulum $Ca^{2+}$ -ATPase. Proc. Natl. Acad. Sci. USA 87, 2466-2470
  25. Tornquist, K. (1993) Activation of calcium entry by cyclopiazonic acid in thyroid FRTL-5 cells. Cell Calcium 14, 411-417 https://doi.org/10.1016/0143-4160(93)90045-8
  26. Van, C. S. and Van, D. B. W. (2002) Morphological and biochemical aspects of apoptosis, oncosis and necrosis. Anat. Histol. Embryol. 31, 214-223 https://doi.org/10.1046/j.1439-0264.2002.00398.x
  27. Veselska, R., Zitterbart, K., Jelinkova, S., Neradil, J. and Svoboda, A. (2003) Specific cytoskeleton changes during apoptosis accompanying induced differentiation of HL-60 myeloid leukemia cells. Oncol. Rep. 10, 1049-1058

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