Cyclosporine A regulate oxidative stress-induced apoptosis in cardiomyocytes: Mechanisms via ROS generation, iNOS and Hsp70

British Journal of Pharmacology

Volumn 137, Issue 6, 2002, Pages 771-781

  Chen, Huei Wen ^a   Chien, Chiang Ting ^a   Yu, Sung Liang ^a   Lee, Yuan Teh ^a   Chen, Wen Jone ^a  

^a NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

Cardiomyocytes; Cyclosporine A; Free radicals; Membrane potential; Mitochondria

Indexed keywords

ASCORBIC ACID; CYCLOSPORIN A; DNA FRAGMENT; HEAT SHOCK PROTEIN 70; LIPOCORTIN 5; NITRIC OXIDE SYNTHASE; PHOSPHATIDYLSERINE; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL PROTECTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART PROTECTION; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; REOXYGENATION; REPERFUSION INJURY;

ANIMALS; APOPTOSIS; CELL HYPOXIA; CELL LINE; CYCLOSPORINE; DOSE-RESPONSE RELATIONSHIP, DRUG; HSP70 HEAT-SHOCK PROTEINS; HYDROGEN PEROXIDE; INTRACELLULAR MEMBRANES; MEMBRANE POTENTIALS; MITOCHONDRIA; MYOCYTES, CARDIAC; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; OXYGEN; REACTIVE OXYGEN SPECIES;

EID: 0036854528     PISSN: 00071188     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjp.0704908     Document Type: Article

References (67)

1. Arstall, M.A., Sawyer, D.B., Fukazawa, R. & Kelly, R.A. (1999). Cytokine-mediated apoptosis in cardiac myocytes: The role of inducible nitric oxide synthase induction and peroxynitrite generation. Circ. Res., 85, 829-840.
2. Baines, C.P., Goto, M. & Downey, J.M. (1997). Oxygen radicals released during ischemia preconditioning contribute to cardioprotection in rabbit myocardium. J. Mol. Cell. Cardiol., 29, 207-216.
3. Baliga, R., Ueda, N., Walker, P.D. & Shah, S.V. (1997). Oxidant mechanisms in toxic acute renal failure. Am. J. Kidney Disease, 29, 465-477.
4. Ballinger, S.W., Patterson, C., Yan, C.N., Doan, R., Burow, D.L., Young, C.G., Yakes, F.M., Van Houten, B., Ballinger, C.A., Freeman, B.A., & Runge, M.S. (2000). Hydrogen peroxide- and peroxynitrite-induced mitochondrial DNA damage and dysfunction in vascular endothelial and smooth muscle cells. Circ. Res., 86, 960-966.
5. Bernardi, P. (1999). Mitochondria in muscle cell death. Ital. J. Neurol. Sci., 20, 395-400.
6. Boissy, R.E., Trinkle, L.S. & Nordlund, J.J., (1989). Separation of pigmented and albino melanocytes and concomitant evaluation of endogenous peroxide content using flow cytometry. Cytometry, 10, 779-787.
7. Bolli, R. (2001). Cardioprotective function of inducible nitric oxide synthase and role of nitric oxide in myocardial ischemia and preconditioning: An overview of a decade of research. J. Mol. Cell. Cardiol., 33, 1897-1918.
8. Broillet, M., Randin, O. & Chatton, J. (2001). Related articles photoactivation and calcium sensitivity of the fluorescent NO indicator 4,5-diaminofluorescein (DAF-2): Implications for cellular NO imaging. FEBS Lett., 491, 227-232.
9. Buetler, T.M., Cottet-Maire, F., Krauskopf, A., & Ruegg, U.T. (2000). Does cyclosporin A generate free radicals? Trend in Pharmacol. Sci., 21, 288-290.
10. Cai, J., & Jones, D.P. (1998). Superoxide in apoptosis. Mitochondrial generation triggered by cytochrome c loss. J. Biol. Chem., 273, 11401-11404.
11. Calo, L., Semplicini, A., Davis, P.A., Bonvicini, P., Cantaro, S., Rigotti, P., D'Angelo, A., Livi, U. & Antonello, A. (2000). Cyclosporin-induced endothelial dysfunction and hypertension: Are nitric oxide system abnormality and oxidative stress involved? Transpl. Int., 13, S413-S418.
12. Carroll, R. & Yellon, D.M. (1998). Myocardial adaptation to ischaemia - The preconditioning phenomenon. Int. J. Cardiol., 68, S93-S101.
13. Chen, H.W., Hsu MJ, Chien CT, & Huang HC. (2001). Effect of alisol B acetate, a plant triterpene, on apoptosis in vascular smooth muscle cells and lymphocytes. Eur. J. Pharmacol., 419, 127-138
14. Cook, S.A., Sugden, P.H., & Clerk, A. (1999). Regulation of Bcl-2 family proteins during development and in response to oxidative stress in cardiac myocytes: Association with changes in mitochondrial membrane potential. Circ. Res., 85, 940-949.
15. Das, D.K., Engelman, R.M., & Maulik, N. (1999a). Oxygen free radical signaling in ischemic preconditioning. Ann. New York Acad. Sci., 874, 49-65.
16. Das, D.K., Maulik, N., Sato, M., & Ray, P.S. (1999b). Reactive oxygen species function as second messenger during ischemic preconditioning of heart. Mol. Cell. Biochem., 196, 59-67.
17. Denizot, F., & Lang, R. (1986). Rapid colorimetric assay for cell growth and survival: Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J. Immunol. Methods, 89, 271-277.
18. Duranteau, J., Chandel, N.S., Kulisz, A., Shao, Z., & Schumacker, P.T. (1998). Intracellular signaling by reactive oxygen species during hypoxia in cardiomyocytes. J. Biol. Chem., 273, 11619-11624.
19. Esposito, C., Fornoni, A., Cornacchia, F., Bellotti, N., Fasoli, G., Foschi, A., Mazzucchelli, I., Mazzullo, T., Semeraro, L., & Dal Canton, A. (2000). Cyclosporine induces different responses in human epithelial, endothelial and fibroblast cell cultures. Kidney Int., 58, 123-130.
20. Giardino, I., Edelstein, D. & Brownlee, M. (1996). BCL-2 expression or antioxidants prevent hyperglycemia-induced formation of intracellular advanced glycation endproducts in bovine endothelial cells. J. Clin. Invest., 97, 1422-1428.
21. Green, D.R. & Reed, J.C. (1998). Mitochondria and apoptosis. Science, 281, 1309-1312.
22. Griffiths, E.J. & Halestrap, A.P. (1993). Protection by cyclosporine A of ischemia/reperfusion-induced damage in isolated rat hearts. J. Mol. Cell. Cardiol., 25, 1461-1469.
23. 2+-induced large amplitude swelling of liver and heart mitochondria by cyclosporine A is probably caused by the inhibitor binding to mitochondrial matrix peptidyl-prolyl cis-trans isomerase and preventing it interacting with the adenine nucleotide translocase. Biochem. J., 268, 153-160.
24. Haunstetter, A., & Izumo, S. (1998). Apoptosis: Basic mechanisms and implications for cardiovascular disease. Circ. Res., 82, 1111-1129.
25. Hutcheson, A.E., Rao, M.R., Olinde, K.D. & Markov, A.K. (1995). Myocardial toxicity of cyclosporin A: Inhibition of calcium ATPase and nitric oxide synthase activities and attenuation by fructose-1,6-diphosphate in vitro. Res. Commun. Mol. Pathol. Pharmacol., 89, 17-26.
26. Kahan, B.D. (1989). Cyclosporine. N. Engl. J. Med., 321, 1725-1738.
27. Kang, P.M., Haunstetter, A., Aoki, H., Usheva, A., & Izumo, S. (2000). Morphological and molecular characterization of adult cardiomyocyte apoptosis during hypoxia and reoxygenation. Circ. Res., 87, 118-125.
28. Kimes, B.W. & Brandt, B.L. (1976). Properties of a clonal muscle cell line from rat heart. Exp. Cell. Res., 98, 367-381.
29. Kloner, R.A. (1998). Medical and cellular implication of stunning, hibernation and preconditioning. An NHLBI workshop. Circulation, 97, 1848-1867.
30. Kojima, H., Nakatsubo, N., Kikuchi, K., Kawahara, S., Kirino, Y., Nagoshi, H., Hirata, Y. & Nagano, T. (1998). Detection and imaging of nitric oxide with novel fluorescent indicators: Diaminofluoresceins. Anal. Biochem., 70, 2446-2453.
31. Kroemer, G., Zamzami, N., & Susin, S.A. (1997). Mitochondrial control of apoptosis. Immun. Today, 18, 44-51.
32. Lopez-Ongil, S., Hernandez-Perera, O., Navarro-Antolin, J., Perez De Lema, G., Rodriguez-Puyol, M., Lamas, S., & Rodriguez-Puyol, D. (1998). Role of reactive oxygen species in the signalling cascade of cyclosporine A-mediated up-regulation of eNOS in vascular endothelial cells. Br. J. Pharmacol., 124, 447-454.
33. Marber, M.S. (2000). Ischemic preonditioning in isolated cells. Circ. Res., 86, 926-931.
34. Massoudy, P., Zahler, S., Kupatt, C., Reder, E., Mecker, B.F. & Gerlach, E. (1997). Cardioprotection by cyclosporine A in experimental ischemia and reperfusion-evidence for a nitric oxide-dependent mechanism mediated by endothelin. J. Mol. Cell. Cardiol., 29, 535-544.
35. Mathony, M., Hong, Y., Kemp, B.K., Barrientos, A.A., & Erusalimsky, J.D. (2000). Evaluation of fluorescent dyes for the detection of mitochondrial membrane potential changes in cultured cardiomyocytes. Cardiovas. Res., 46, 126-138.
36. Minners J. Van Den Bos EJ. Yellon DM. Schwalb H. Opie LH. & Sack MN. (2000). Dinitrophenol, cyclosporin A, and trimetazidine modulate preconditioning in the isolated rat heart: Support for a mitochondrial role in cardioprotection. Cardiovasc. Res., 47, 68-73.
37. Mosmann, T. (1983). Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods, 65, 55-63.
38. Navarro-Antolin, J. & Lamas, S. (2001). Nitrosative stress by cyclosporin A in the endothelium: Studies with the NO-sensitive probe diaminofluorescein-2/diacetate using flow cytometry. Nephrol. Dial. Transplant., 16, S6-S9.
39. Navarro-Antolin, J., Lopez-Munoz, M.J., Soria, J. & Lamas, S. (2002). Superoxide limits cyclosporine-A-induced formation of peroxynitrite in endothelial cells. Free Radic. Biol. Med., 32, 702-711.
40. O'Rourke, B. (1999). Apoptosis: Rekindling the mitochondrial fire. Circ. Res., 85, 880-883.
41. Paslaru, L., Rallu, M., Manuel, M., Davidson, S., & Morange, M. (2000). Cyclosporine A induces an atypical heat shock response. Biochem. Biophys. Res. Commun., 269, 464-469.
42. Ping, P. (1999). Isoform-selective activation of protein kinase C by nitric oxide in the heart of conscious rat: A signaling mechanism for both nitric oxide-induced and ischemia-induced preconditioning. Circ. Res., 84, 587-604.
43. Pinsky, D.J., Aji, W., Szabolcs, M., Athan, E.S., Liu, Y., Yang, Y.M., Kline, R.P., Olson, K.E. & Cannon, P.J. (1999). Nitric oxide triggers programmed cell death (apoptosis) of adult rat ventricular myocytes in culture. Am. J. Physiol., 277, H1189-H1199.
44. Rao, M.R., Hutcheson, A.E., & Markov, A.K. (1998). Changes in the cardiovascular nitric oxide pathway in cyclosporin-A treated rats. Drug & Chem. Toxicol., 21, 27-34.
45. Rubino, A., & Yellon, D.M. (2000). Ischaemic preconditioning of the vasculature: An overlooked phenomenon for protecting the heart? Trend in Pharmacol. Sci., 21, 225-230.
46. Saikumar, P., Dong, Z., Weinberg, J.M., & Venkatachalam, M.A. (1998). Mechanisms of cell death in hypoxia/reoxygenation injury. Oncogene, 17, 3341-3349.
47. Sanchez, H., Zoll, J., Bigard, X., Veksler, V., Mettauer, B., Lampert, E., Lonsdorfer, J. & Ventura-Clapier, R. (2001). Effect of cyclosporin A and its vehicle on cardiac and skeletal muscle mitochondria: Relationship to efficacy of the respiratory chain. Br. J. Pharmacol., 133, 781-788.
48. Seko, Y., Tobe, K., Ueki, K., Kadowaki, T. & Yazaki, Y. (1996). Hypoxia and hypoxia/reoxygenation activate Raf-1, mitogen-activated protein kinase kinase, mitogen-activated protein kinases, and S6 kinase in cultured rat cardiac myocytes. Circ. Res., 78, 82-90.
49. Schreiber, S.L. & Carbtree, G.R. (1992). The mechanism of action of cyclosporine and FK506. Immunol. Today, 13, 136-142.
50. Semenza, G.L. (2000). Cellular and molecular dissection of reperfusion injury-ROS within and without. Circ. Res., 86, 117-118.
51. 2 for platelet-derived growth factor signal transduction. Science, 270, 296-299.
52. Suzuki, K., Sawa, Y., Kagisaki, K., Taketani, S., Ichikawa, H., Kaneda, Y., & Matsuda, H. (2000). Reduction in myocardial apoptosis associated with overexpression of heat shock protein 70. Basic Res. Cardiol., 95, 397-403.
53. Szigeti, G., Banyasz, T., Magyar, J., Kortvely, A., Szigigeti, P., Kovacs, L., Jednakovits, A. & Nanasi, P.P. (2000). Effects of bimoclomol, the novel heat shock protein coinducer, in dog ventricular myocardium. Life Sci., 67, 73-79.
54. Vanden Hoek, T.L., Becker, L.B., Shao, Z., LI, C., & Schumacker, P.T. (1998). Reactive oxygen species released from mitochondria during brief hypoxia induce preconditioning in cardiomyocytes. J. Biol. Chem., 273, 18092-18098.
55. Vigh, L., Literati, P.N., Horvath, I., Torok, Z., Balogh, G., Glatz, A., Kovacs, E., Boros, I., Ferdinandy, P., Farkas, B., Jaszlits, L., Jednakovits, A., Koranyi, L. & Maresca, B. (1997). Biomoclomol: A nontoxic, hydroxylamine derive with stress protein-inducing activity and cytoprotective effects. Nat. Med., 3, 1150-1154.
56. Von Harsdorf, R., Li, P.F., & Dietz, R. (1999). Signaling pathways in reactive oxygen species-induced cardiomyocyte apoptosis. Circulation, 99, 2934-2941.
57. Walter, D.H., Haendeler, J., Galle, J., Zeiher, A.M., & Dimmeler, S. (1998). Cyclosporine A inhibit apoptosis of human endothelial cells by preventing release of cytochrome C from mitochondria. Circulation, 98, 1153-1157.
58. Webster, K.A., Discher, D.J., Kaiser, S., Hernandez, O., Sato, B., & Bishopric, N.H. (1999). Hypoxia-activated apoptosis of cardiac myocytes requires reoxygenation or a pH shift and is independent of p53. J. Clin. Invest., 104, 239-252.
59. Weinbrenner, C., Liu, G.S., Downey, J.M., & Cohen, M.V. (1998). Cyclosporine A limits myocardial infarct size even when administered after onset of ischemia. Cardiovasc. Res., 38, 678-684.
60. Williams, R.S. (1997). Heat shock proteins and ischemic injury to the myocardium. Circulation, 96, 4138-4140.
61. Wolf, A., Trendelenburg, C.F., Diez-Fernandez, C., Prieto, P., Houy, S., Trommer, W.E., & Cordier, A. (1997). Cyclosporine A-induced oxidative stress in rat hepatocytes. J. Pharmacol. Exp. Ther., 280, 1328-1334.
62. Yuan, C.M., Bohen, E.M., Musio, F., & Carome, M.A. (1996). Sublethal heat shock and cyclosporine exposure produce tolerance against subsequent cyclosporine toxicity. Am. J. Physiol., 271, F571-F578.
63. Zamai, L., Falcieri, E., Marhejka, G., & Vitale, M. (1996). Supravital exposure to propidium iodide identifies apoptotic cells in the absence of nucleosomal DNA fragmentation. Cytometry, 23, 303-311.
64. Zamzami, N., Marchetti, P., Castedo, M., Hirsch, T., Susin, S.A., Masse, B., & Kroemer, G. (1996). Inhibitors of permeability transition interfere with the disruption of the mitochondrial transmembrane potential during apoptosis. FEBS Lett., 384, 53-57.
65. Zhao, T., Xi, L., Chelliah, J., Levasseur, J.E., & Kukreja, R.C. (2000). Inducible nitric oxide synthase mediates delayed myocardial protection induced by activation of adenosine A1 receptors evidence from gene-knockout mice. Circulation, 102, 902-907.
66. Zhong, Z., Arteel, G.E., Connor, H.D., Yin, M., Frankenberg, M.V., Stachlewitz, R.F., Raleigh, J.A., Mason, R.P., & Thurman, R.G. (1998). Cyclosporine A increases hypoxia and free radical production in rat kidneys: Prevention by dietary glycine. Am. J. Physiol., 275, F595-F604.
67. Zhong, Z., Connor, H.D., Yin, M., Moss, N., Mason, R.P., Bunzendahl, H., Forman, D.T., & Thurman, R.G. (1999). Dietary glycine and renal denervation prevents cyclosporine A-induced hydroxyl radical production in rat kidney. Mol. Pharmacol., 56, 455-463.