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Cobalt Chloride-induced Apoptosis and Extracellular Signal-regulated Protein Kinase 1/2 Activation in Rat C6 Glioma Cells

  • Yang, Seung-Ju (Department of Neurosurgery, Wonju College of Medicine, Yonsei University) ;
  • Pyen, Jhin-Soo (Department of Neurosurgery, Wonju College of Medicine, Yonsei University) ;
  • Lee, In-Soo (Department of Biomedical Laboratory Science, College of Health Science, Yonsei University) ;
  • Lee, Hye-Young (Department of Biomedical Laboratory Science, College of Health Science, Yonsei University) ;
  • Kim, Young-Kwon (Department of Clinical Pathology, Gimcheon College) ;
  • Kim, Tae-Ue (Department of Biomedical Laboratory Science, College of Health Science, Yonsei University)
  • Published : 2004.07.31

Abstract

Brain ischemia brings about hypoxic insults. Hypoxia is one of the major pathological factors inducing neuronal injury and central nervous system infection. We studied the involvement of mitogen-activated protein (MAP) kinase in hypoxia-induced apoptosis using cobalt chloride in C6 glioma cells. In vitro cytotoxicity of cobalt chloride was tested by MTT assay. Its $IC_{50}$ value was $400\;{\mu}M$. The DNA fragment became evident after incubation of the cells with $300\;{\mu}M$ cobalt chloride for 24 h. We also evidenced nuclear cleavage with morphological changes of the cells undergoing apoptosis with electron microscopy. Next, we examined the signal pathway of cobalt chloride-induced apoptosis in C6 cells. The activation of extracellular signal-regulated protein kinase 1/2 (ERK 1/2) started to increase at 1 h and was activated further at 6 h after treatment of 400 M cobalt chloride. In addition, pretreatment of PD98059 inhibited cobalt chloride-induced apoptotic cell morphology in Electron Microscopy. These results suggest that cobalt chloride is able to induce the apoptotic activity in C6 glioma cells, and its apoptotic mechanism may be associated with signal transduction via MAP kinase (ERK 1/2).

Keywords

References

  1. Allen, T. D. (1987) Ultrastructural aspects of cell death in Perspectives on mammalian cell death, Potten, C. S. (ed.), pp. 35-65, Oxford University Press, Oxford, UK.
  2. Arends, M. J. and Wyllie, A. H. (1991) Apoptosis: mechanisms and roles in pathology. Int. Rev. Exp. Pathol. 32, 223-254. https://doi.org/10.1016/B978-0-12-364932-4.50010-1
  3. Bae, S. K., Baek, J. H., Lee, Y. M., Lee, O. H. and Kim, K. W. (1998) Hypoxia-induced apoptosis in human hepatocellular carcinoma cells: a possible involvement of the 6-TG-sensitive protein kinase(s)-dependent signaling pathway. Cancer Lett. 126, 97-104. https://doi.org/10.1016/S0304-3835(97)00538-7
  4. Baek, J. H., Kang, C. M., Chung, H. Y., Park, M. H. and Kim, K. W. (1996) Increased expression of c-jun in the bile acidinduced apoptosis in mouse F9 teratocarcinoma stem cells. J. Biochem. Mol. Biol. 29, 68-72.
  5. Barry, M. A. and Eastman, A. (1992) Endonuclease activation during apoptosis: the role of cytosolic $Ca^{2+}$ and pH. Biochem, Biophys. Res. Commun. 186, 782-789. https://doi.org/10.1016/0006-291X(92)90814-2
  6. Cavigelli, M., Dolfi, F., Claret, F. X. and Karin, M. (1995) Induction of c-fos expression through JNK-mediated TCF/Elk-1 phosphorylation. EMBO J. 14, 5957-5964.
  7. Chandel, N. S., Maltepe, E., Goldwasser, E., Mathieu, C. E., Simon, M. C. and Schumacker, P. T. (1998) Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl. Acad. Sci. USA 95, 11715-11721. https://doi.org/10.1073/pnas.95.20.11715
  8. Chen, R. H., Sharnecki, C. and Blenis, J. (1992) Nuclear localization and regulation of erk- or rsk-encoded protein kinases. Mol. Cell. Biol. 12, 915-927.
  9. Conrad, P. W., Rust, R. T., Han, J., Millhorn, D. E. and Beitner- Johnson, D. (1999) Selective activation of p38 and p38 by hypoxia. J. Biol. Chem. 274, 23570-23576. https://doi.org/10.1074/jbc.274.33.23570
  10. Coso, O. A., Chiariello, M., Yu, J. C., Teramoto, H., Crespo, P., Xu, N., Miki, T. and Gutkind, S. (1995) The small GTPbinding proteins Rac 1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81, 1137-1146.
  11. Davis, R. J. (1993) The mitogen-activated protein kinase signal transduction pathway. J. Biol. Chem. 268, 14553-14556.
  12. Denisenko, M. F., Soldatenkov, V. A., Belovskaya, L. N. and Filippovich, I. V. (1989) Is the NAD-poly(ADP-ribose) polymerase system the trigger in radiation-induced death of mouse thymocytes? Int. J. Radiat. Biol. 56, 277-285. https://doi.org/10.1080/09553008914551441
  13. Forsythe, J. A., Jiang, B. H., Iyer, N. V., Agani, F., Leung, S. W., Koos, R. D. and Semenza, G. L. (1996) Activation of vascular endothelial growth factor gene transcription by hypoxiainducible factor 1. Mol. Cell. Biol. 16, 4604-4613.
  14. Goldberg, M. A., Dunning, S. P. and Burn, H. F. (1988) Regulation of the erythropoietin gene: evidence that the oxygen sensor is a heme protein. Science 242, 1412-1415. https://doi.org/10.1126/science.2849206
  15. Guillemin, K. and Krasnow, M. A. (1997) The hypoxic response: huffing and hifing. Cell 89, 9-12. https://doi.org/10.1016/S0092-8674(00)80176-2
  16. Jimenez, L. A., Zanella, C., Fung, H., Janssen, Y. M., Vacek, P., Charland, C., Goldberg, J. and Mossman, B. T. (1997) Role of extracellular signal-regulated protein kinase in apoptosis by asbestos and $H_{2}O_{2}$. Am. J. Physiol. 273, 1029.
  17. Kerr J. F. R., Wyllie, A. H. and Currie, A. R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26, 239-257. https://doi.org/10.1038/bjc.1972.33
  18. Kerr, J. F. R., Searle, J. and Harmon, B. V. (1987) Apoptosis in Perspectives on mammalian cell death, Potten, C. S. (ed.), p. 93, Oxford University Press, Oxford, UK.
  19. Kim, C. Y., Tsai, M. H., Osmanian, C., Greaber, T. G., Lee, J. E., Giffard, R. G., DiPaolo, J. A., Peehl, D. M. and Giaccia, A. J. (1997) Selection of human cervical epithelial cells that possess reduced apoptotic potential to low-oxygen conditions. Cancer Res. 57, 4200-4204.
  20. Kitazono, M., Takebayashi, Y., Ishitsuka, K., Takao, S., Tani, A., Furukawa, T., Miyadera, K., Yamada, Y., Aikou, T. and Akiyama, S. (1998) Prevention of hypoxia-induced apoptosis by the angiogenic factor thymidine phosphorylase. Biochem. Biophys. Res. Commun. 253, 797-803. https://doi.org/10.1006/bbrc.1998.9852
  21. Koong, A. C., Chen, E. Y., Kim, C. Y. and Giaccia, A. J. (1994) Activators of protein kinase C selectively mediate cellular cytotoxicity to hypoxia cells and not aerobic cells. Int. J. Radiat. Oncol. Biol. Phys. 29, 259-265. https://doi.org/10.1016/0360-3016(94)90272-0
  22. Kyriakis J. M., Banerjee, P., Nikolakaki, E., Dai, T., Rubie, E. A., Ahmad, M. F., Avruch, J. and Woodgett, J. R. (1994) The stress-activated protein kinase subfamily of c-Jun kinase. Nature 369, 156.
  23. Lockshin, R. A. and Zakeri, Z. F. (1990) Programmed cell death: new thoughts and relevance to aging. J. Gerontolt. 45, 135-140.
  24. Marshall, C. J. (1995) Specificity of receptor tyrosine-kinase signaling: transient versus sustained extracellular signalregulated kinase activation. Cell 80, 179-185. https://doi.org/10.1016/0092-8674(95)90401-8
  25. Martin, D. S. and Schwartz, G. K. (1997) Chemotherapeutically induced DNA damage, ATP depletion and the apoptotic biochemical cascade. Oncol. Res. 9, 1-5.
  26. Mazure, N. M., Chen, E. Y., Laderoute, K. R. and Giaccia, A. J. (1997) Induction of vascular endothelial growth factor by hypoxia is modulated by a phosphatidylinositol 3-kinase/Akt signaling pathway in Ha-ras-transformed cells through a hypoxia inducible factor-1 transcriptional element. Blood 90, 3322-3331.
  27. McConkey, D. J., Orrenius, S. and Jondal, M. (1996) Cellular signaling in programmed cell death (apoptosis). Immunol. Today 11, 120-121.
  28. Murray, B., Alessandrini, A., Cole, A. J., Yee, A. G. and Furshpan, E. J. (1998) Inhibition of the p44/42 MAP kinase pathway protects hippocampal neurons in a cell-culture model of seizure activity. Proc. Natl. Acad. Sci. USA 95, 11975-11980. https://doi.org/10.1073/pnas.95.20.11975
  29. Minet, E., Arnould, T., Michel, G., Roland, I., Mottet, D., Raes, M., Remacle, J. and Michiels, C. (2000) ERK activation upon hypoxia: involvement in HIF-1 activation. FEBS Lett. 468, 53-58. https://doi.org/10.1016/S0014-5793(00)01181-9
  30. Molnar, A., Theodoras, A. M., Zon, L. I. and Kyriakis, J. M. (1997) Cdc42Hs, but not Rac1, inhibits serum-stimulated cell cycle progression at G1-S through a mechanism requiring p38/RK. J. Biol. Chem.. 272, 13229-13235. https://doi.org/10.1074/jbc.272.20.13229
  31. Muller, J. M., Krauss, B., Kaltschmidt, C., Baeuerle, P. A. and Rupec, R. A. (1997) Hypoxia induces c-fos transcription via a mitogen-activated protein kinase-dependent pathway. J. Biol. Chem. 272, 23435-23439. https://doi.org/10.1074/jbc.272.37.23435
  32. Raingeaud, J., Gupta, S., Rogers, J. S., Dickens, M., Han, J., Ulevitch, R. J. and Davis, R. J. (1995) Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J. Biol. Chem. 270, 7420-7426. https://doi.org/10.1074/jbc.270.13.7420
  33. Richard, D. E., Berra, E., Gothie, E., Roux, D. and Pouyssegur, J. (1999) p42/p44 Mitogen-activated protein kinases phosphorylate hypoxia-inducible factor 1(HIF-1) and enhance the transcriptional activity of HIF-1. J. Biol. Chem. 274, 32631-32637. https://doi.org/10.1074/jbc.274.46.32631
  34. Rieder, C. L., Schultz, A., Cole, R. and Sluder, G. (1994) Anaphase onset in vertebrate somatic cells is controlled by a checkpoint that monitors sister kinetochore attachment to the spindle. J. Cell. Biol. 127, 1301-1310. https://doi.org/10.1083/jcb.127.5.1301
  35. Risau, W. (1997) Mechanisms of angiogenesis. Nature 386, 671-674. https://doi.org/10.1038/386671a0
  36. Seimiya, H., Tanji, M., Oh-hara, T., Tomida, A., Naasani, I. and Tsuruo, T. (1999) Hypoxia up-regulates telomerase activity via mitogen-activated protein kinase signaling in human solid tumor cells. Biochem. Biophys. Res. Commun. 260, 365-370. https://doi.org/10.1006/bbrc.1999.0910
  37. Sen, S. and D'Incalci, M. (1992) Apoptosis. Biochemical events and relevance to cancer chemotherapy. FEBS Lett. 307, 122-127. https://doi.org/10.1016/0014-5793(92)80914-3
  38. Shtil, A. A., Mandlekar, S., Yu, R., Walter, R. J., Hagen, K., Tan, T. H., Roninson, I. B. and Kong, A. N. T. (1999) Differential regulation of mitogen-activated protein kinases by microtubulebinding agents in human breast cancer cells. Oncogene 18, 377-384. https://doi.org/10.1038/sj.onc.1202305
  39. Shweiki, D., Itin, A., Soffer, D. and Keshet, E. (1992) Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359, 843-845. https://doi.org/10.1038/359843a0
  40. Shweiki, D., Itin, A., Soffer, D. and Keshet, E. (1997) Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 240, 552-556.
  41. Stokoe, D., Macdonald, S., Cadwallader, K., Symons, M. and Hancock, J. (1994) Activation of Ras as a result of recruitment to the plasma membrane. Science 264, 1463-1467.
  42. van Dam, H., Wilhelm, D., Herr, I., Steffen, A., Herrlich, P. and Angel, P. (1995) ATF-2 is preferentially activated by stressactivated protein kinases to mediate c-jun induction in response to genotoxic agents. EMBO J. 14, 1798-1811.
  43. Wang, G., Hazra, T. K., Mitra, S., Lee, H. M. and Englander, E. W. (2000) Mitochondrial DNA damage and hypoxic response are induced by $COCl_{2}$ in rat neuronal PC12 cells. Nucleic Acids Res. 28, 2135-2140. https://doi.org/10.1093/nar/28.10.2135
  44. Wang, G. L. and Semenza, G. L. (1995) Purification and characterization of hypoxia-inducible factor-1. J. Biol. Chem. 270, 1230-1237. https://doi.org/10.1074/jbc.270.3.1230
  45. Wyllie, A. H., Kerr, J. F. R. and Currie, A. R. (1980) Cell death: the significance of apoptosis. Int. Rev. Cytol. 68, 251-306. https://doi.org/10.1016/S0074-7696(08)62312-8
  46. Yao, K. S., Clayton, M. and O'Dwyer, P. J. (1995) Apoptosis in human adenocarcinoma HT29 cells induced by exposure to hypoxia. J. Natl. Cancer. Inst. 87, 117-122. https://doi.org/10.1093/jnci/87.2.117
  47. Yao, K. S., Xanthoudakis, S. and Curran, T. (1994) Activation of AP-1 and of a nuclear redox factor, Ref-1, in the response of HT-29 colon cancer cells to hypoxia. Mol. Cell. Biol. 14, 5997-6003. https://doi.org/10.1128/MCB.14.9.5997
  48. Yoshioka, K., Clejan, S. and Fisher, J. W. (1998) Activation of protein kinase C in human hepatocellular carcinoma (HEP3B) cells increases erythropoietin production. Life Sci. 63, 523-535. https://doi.org/10.1016/S0024-3205(98)00303-8
  49. Yu, R., Shtil, A. A., Tan, T. H., Roninson, I. B. and Kong, A. N. (1996) Adriamycin activates c-jun N-terminal kinase in human leukemia cells: a relevance to apoptosis. Cancer Lett. 107, 73. https://doi.org/10.1016/0304-3835(96)04345-5
  50. Xia, Z., Dickens, M., Raingeaud, J., Davis, R. J. and Greenberg, M. E. (1995) Opposing effects of ERK and JNK-p38 MAP kinases on Apoptosis. Science 270, 1326-1331. https://doi.org/10.1126/science.270.5240.1326

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