Mechanism of A23187-induced apoptosis in HL-60 cells: Dependency on mitochondrial permeability transition but not on NADPH oxidase

Bioscience, Biotechnology and Biochemistry

Volumn 71, Issue 11, 2007, Pages 2701-2711

  Kajitani, Noriko ^a   Kobuchi, Hirotsugu ^a   Fujita, Hirofumi ^a   Yano, Hiromi ^b   Fujiwara, Takuzo ^c   Yasuda, Tatsuji ^a   Utsumi, Kozo ^a  

^a OKAYAMA UNIVERSITY   (Japan)

^b KAWASAKI UNIVERSITY OF MEDICAL WELFARE   (Japan)

^c Tsuyama Central Hospital   (Japan)

Author keywords

Apoptosis; Calcium; Mitochondrial permeability transition; NADPH oxidase; Reactive oxygen species

Indexed keywords

CALCIUM; ENZYME ACTIVITY; ENZYME INHIBITION; IONS;

CELL-PERMEANT ANTIOXIDANTS; MITOCHONDRIAL PERMEABILITY TRANSITION; NADPH OXIDASE; REACTIVE OXYGEN SPECIES;

CELL DEATH;

CALCIMYCIN; CALCIUM; CYCLOSPORIN; ENZYME INHIBITOR; IONOPHORE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

APOPTOSIS; ARTICLE; CELL STRAIN HL 60; DNA FRAGMENTATION; DRUG ANTAGONISM; DRUG EFFECT; HUMAN; METABOLISM; MITOCHONDRION; PERMEABILITY;

APOPTOSIS; CALCIMYCIN; CALCIUM; CYCLOSPORINE; DNA FRAGMENTATION; ENZYME INHIBITORS; HL-60 CELLS; HUMANS; IONOPHORES; MITOCHONDRIA; NADPH OXIDASE; PERMEABILITY; REACTIVE OXYGEN SPECIES;

EID: 36448952742     PISSN: 09168451     EISSN: 13476947     Source Type: Journal    
DOI: 10.1271/bbb.70304     Document Type: Article

References (42)

1. Thomas, A. P., Bird, G. S., Hajnoczky, G., Robb-Gaspers, L. D., and Putney, J. W., Jr., Spatial and temporal aspects of cellular calcium signaling. FASEB J., 10, 1505-1517 (1996).
2. Rizzuto, R., Bernardi, P., and Pozzan, T., Mitochondria as all-round players of the calcium game. J. Physiol., 529 (Pt 1), 37-47 (2000).
3. Halestrap, A. P., McStay, G. P., and Clarke, S. J., The permeability transition pore complex: another view. Biochimie, 84, 153-166 (2002).
4. Prehn, J. H., Bindokas, V. P., Marcuccilli, C. J., Krajewski, S., Reed, J. C., and Miller, R. J., Regulation of neuronal Bcl2 protein expression and calcium homeostasis by transforming growth factor type β confers wide-ranging protection on rat hippocampal neurons. Proc. Natl. Acad. Sci. USA, 91, 12599-12603 (1994).
5. Keller, J. N., Guo, Q., Holtsberg, F. W., Bruce-Keller, A. J., and Mattson, M. P., Increased sensitivity to mitochondrial toxin-induced apoptosis in neural cells expressing mutant presenilin-1 is linked to perturbed calcium homeostasis and enhanced oxyradical production. J. Neurosci., 18, 4439-4450 (1998).
6. McPhail, L. C., Clayton, C. C., and Snyderman, R., The NADPH oxidase of human polymorphonuclear leukocytes: evidence for regulation by multiple signals. J. Biol. Chem., 259, 5768-5775 (1984).
7. Zhang, B., Hirahashi, J., Cullere, X., and Mayadas, T. N., Elucidation of molecular events leading to neutrophil apoptosis following phagocytosis: cross-talk between caspase 8, reactive oxygen species, and MAPK/ERK activation. J. Biol. Chem., 278, 28443-28454 (2003).
8. Green, D. R., and Reed, J. C., Mitochondria and apoptosis. Science, 281, 1309-1312 (1998).
9. Kowaltowski, A. J., Castilho, R. F., and Vercesi, A. E., Mitochondrial permeability transition and oxidative stress. FEBS Lett., 495, 12-15 (2001).
10. 2+-induced permeability transition of mitochondria. Free Radic. Res., 38, 27-35 (2004).
11. Qian, T., Herman, B., and Lemasters, J. J., The mitochondrial permeability transition mediates both necrotic and apoptotic death of hepatocytes exposed to Br-A23187. Toxicol. Appl. Pharmacol., 154, 117-125 (1999).
12. Sennvik, K., Benedikz, E., Fastbom, J., Sundstrom, E., Winblad, B., and Ankarcrona, M., Calcium ionophore A23187 specifically decreases the secretion of β-secretase cleaved amyloid precursor protein during apoptosis in primary rat cortical cultures. J. Neurosci. Res., 63, 429-437 (2001).
13. 2+-dependent apoptosis through the mitochondrial pathway. J. Biol. Chem., 279, 25219-25225 (2004).
14. Hamahata, K., Adachi, S., Matsubara, H., Okada, M., Imai, T., Watanabe, K., Toyokuni, S. Y., Ueno, M., Wakabayashi, S., Katanosaka, Y., Akiba, S., Kubota, M., and Nakahata, T., Mitochondrial dysfunction is related to necrosis-like programmed cell death induced by A23187 in CEM cells. Eur. J. Pharmacol., 516, 187-196 (2005).
15. Priceman, S. J., Kirzner, J. D., Nary, L. J., Morris, D., Shankar, D. B., Sakamoto, K. M., and Medh, R. D., Calcium-dependent upregulation of E4BP4 expression correlates with glucocorticoid-evoked apoptosis of human leukemic CEM cells. Biochem. Biophys. Res. Commun., 344, 491-499 (2006).
16. Zhu, H., Gao, W., Jiang, H., Wu, J., Shi, Y. F., and Zhang, X. J., Calcineurin mediates acetylcholinesterase expression during calcium ionophore A23187-induced HeLa cell apoptosis. Biochim. Biophys. Acta, 1773, 593-602 (2007).
17. Goldman, R., Moshonov, S., and Zor, U., Generation of reactive oxygen species in a human keratinocyte cell line: role of calcium. Arch. Biochem. Biophys., 350, 10-18 (1998).
18. Przygodzki, T., Sokal, A., and Bryszewska, M., Calcium ionophore A23187 action on cardiac myocytes is accompanied by enhanced production of reactive oxygen species. Biochim. Biophys. Acta, 1740, 481-488 (2005).
19. Muranaka, S., Fujita, H., Fujiwara, T., Ogino, T., Sato, E. F., Akiyama, J., Imada, I., Inoue, M., and Utsumi, K., Mechanism and characteristics of stimuli-dependent ROS generation in undifferentiated HL-60 cells. Antioxid. Redox Signal., 7, 1367-1376 (2005).
20. Yamamoto, S., Tamai, H., Ishisaka, R., Kanno, T., Arita, K., Kobuchi, H., and Utsumi, K., Mechanism of α-tocopheryl succinate-induced apoptosis of promyelocytic leukemia cells. Free Radic. Res., 33, 407-418 (2000).
21. 2+ with trapped indicators. Kroc. Found. Ser., 17, 147-155 (1984).
22. Imada, I., Sato, E. F., Miyamoto, M., Ichimori, Y., Minamiyama, Y., Konaka, R., and Inoue, M., Analysis of reactive oxygen species generated by neutrophils using a chemiluminescence probe L-012. Anal. Biochem., 271, 53-58 (1999).
23. Yorimitsu, M., Muranaka, S., Sato, E. F., Fujita, H., Abe, K., Yasuda, T., Inoue, M., and Utsumi, K., Role of α-tocopherol in the regulation of mitochondrial permeability transition. Physiol. Chem. Phys. Med. NMR, 36, 95-107 (2004).
24. Yamada, K., Arita, K., Kobuchi, H., Yamamoto, S., Yoshioka, T., Tamai, H., and Utsumi, K., Cholesterylhemisuccinate-induced apoptosis of promyelocytic leukemia HL-60 cells through a cyclosporin A-insensitive mechanism. Biochem. Pharmacol., 65, 339-348 (2003).
25. Petronilli, V., Penzo, D., Scorrano, L., Bernardi, P., and Di Lisa, F., The mitochondrial permeability transition, release of cytochrome c and cell death: correlation with the duration of pore openings in situ. J. Biol. Chem., 276, 12030-12034 (2001).
26. Burton, K., A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem. J., 62, 315-323 (1956).
27. Miyaguchi, C., Muranaka, S., Kanno, T., Fujita, H., Akiyama, J., Yoshioka, T., and Yasuda, T., 17β-estradiol suppresses ROS-induced apoptosis of CHO cells through inhibition of lipid peroxidation-coupled membrane permeability transition. Physiol. Chem. Phys. Med. NMR, 36, 21-35 (2004).
28. Hogeboom, G. H., Fraction of cell components of animal tissues. In "Methods in Enzymology," ed. Colowick, S., Academic Press, New York, pp. 16-19 (1955).
29. Arita, K., Yamamoto, Y., Takehara, Y., Utsumi, T., Kanno, T., Miyaguchi, C., Akiyama, J., Yoshioka, T., and Utsumi, K., Mechanisms of enhanced apoptosis in HL-60 cells by UV-irradiated n-3 and n-6 polyunsaturated fatty acids. Free Radic. Biol. Med., 35, 189-199 (2003).
30. 2SO-differentiated HL-60 cells: role in phagocytic clearance. J. Biol. Chem., 277, 49965-49975 (2002).
31. Levy, R., Rotrosen, D., Nagauker, O., Leto, T. L., and Malech, H. L., Induction of the respiratory burst in HL-60 cells: correlation of function and protein expression. J. Immunol., 145, 2595-2601 (1990).
32. McLeish, K. R., Klein, J. B., Schepers, T., and Sonnenfeld, G., Modulation of transmembrane signalling in HL-60 granulocytes by tumour necrosis factor-α. Biochem. J., 279 (Pt 2), 455-460 (1991).
33. Crompton, M., Virji, S., and Ward, J. M., Cyclophilin-D binds strongly to complexes of the voltage-dependent anion channel and the adenine nucleotide translocase to form the permeability transition pore. Eur. J. Biochem., 258, 729-735 (1998).
34. Woodfield, K., Ruck, A., Brdiczka, D., and Halestrap, A. P., Direct demonstration of a specific interaction between cyclophilin-D and the adenine nucleotide translocase confirms their role in the mitochondrial permeability transition. Biochem. J., 336 (Pt 2), 287-290 (1998).
35. Harper, M. E., Bevilacqua, L., Hagopian, K., Weindruch, R., and Ramsey, J. J., Ageing, oxidative stress, and mitochondrial uncoupling. Acta Physiol. Scand., 182, 321-331 (2004).
36. Zorov, D. B., Filburn, C. R., Klotz, L. O., Zweier, J. L., and Sollott, S. J., Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J. Exp. Med., 192, 1001-1014 (2000).
37. Leto, T. L., and Geiszt, M., Role of Nox family NADPH oxidases in host defense. Antioxid. Redox Signal., 8, 1549-1561 (2006).
38. Stolk, J., Hiltermann, T. J., Dijkman, J. H., and Verhoeven, A. J., Characteristics of the inhibition of NADPH oxidase activation in neutrophils by apocynin, a methoxy-substituted catechol. Am. J. Respir. Cell Mol. Biol., 11, 95-102 (1994).
39. 2+-induced reactive oxygen species production promotes cytochrome c release from rat liver mitochondria via mitochondrial permeability transition (MPT)-dependent and MPT-independent mechanisms: role of cardiolipin. J. Biol. Chem., 279, 53103-53108 (2004).
40. Fournier, N., Ducet, G., and Crevat, A., Action of cyclosporine on mitochondrial calcium fluxes. J. Bioenerg. Biomembr., 19, 297-303 (1987).
41. Li, Q., Sato, E. F., Kira, Y., Nishikawa, M., Utsumi, K., and Inoue, M., A possible cooperation of SOD1 and cytochrome c in mitochondria-dependent apoptosis. Free Radic. Biol. Med., 40, 173-181 (2006).
42. Gitler, C., Zarmi, B., Kalef, E., Meller, R., Zor, U., and Goldman, R., Calcium-dependent oxidation of thioredoxin during cellular growth initiation. Biochem. Biophys. Res. Commun., 290, 624-628 (2002).