Inhibition of endogenous nitric oxide synthase potentiates ischemia- reperfusion-induced myocardial apoptosis via a caspase-3 dependent pathway

Cardiovascular Research

Volumn 45, Issue 3, 2000, Pages 671-678

  Weiland, Ulrike ^a   Haendeler, Judith ^a   Ihling, Christian ^b   Albus, Udo ^c   Scholz, Wolfgang ^c   Ruetten, Hartmut ^c   Zeiher, Andreas M ^a   Dimmeler, Stefanie ^a  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c SANOFI   (France)

Author keywords

Apoptosis; Ischemia; Nitric oxide; Reperfusion

Indexed keywords

CASPASE 3; NITRIC OXIDE SYNTHASE; PROTEIN BAX; PROTEIN BCL 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; ENZYME INHIBITION; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; IMMUNOHISTOCHEMISTRY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; RAT;

ANALYSIS OF VARIANCE; ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BLOTTING, WESTERN; CASPASE 3; CASPASES; CELLS, CULTURED; ENZYME ACTIVATION; IN SITU NICK-END LABELING; MALE; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; NITRIC OXIDE SYNTHASE; OMEGA-N-METHYLARGININE; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION;

EID: 0033980350     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0008-6363(99)00347-8     Document Type: Article

References (39)

1. Buja L.M., Eigenbrodt M.L., Eigenbrodt E.H. Apoptosis and necrosis. Basic types and mechanisms of cell death. Arch Pathol Lab Med. 117:1993;1208-1214.
2. Kerr J.F.R., Wyllie A.H., Currie A.R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 26:1972;239-257.
3. Searle J., Kerr J.F.R., Bishop C.J. Necrosis and apoptosis: distinct modes of cell death with fundamentally different significance. Pathol Annu. 17:1982;229-259.
4. Narula J., Haider N., Virmani R., et al. Apoptosis in myocytes in end-stage heart failure. New Engl J Med. 335:1996;1182-1189.
5. Gottlieb R.A., Burleson K.O., Kloner R.A., et al. Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J Clin Invest. 94:1994;1621-1628.
6. Kajstura J., Cheng W., Reiss K., et al. Apoptotic and necrotic myocyte cell deaths are independent contributing variables of infarct size in rats. Lab Invest. 74:1996;86-107.
7. Bialik, S, Geenen, DL, Sasson, IE, et al., Myocyte apoptosis during myocardial infarction in the mouse localizes to hypoxic regions but occurs independently of p53. J Clin Invest 1997;100.
8. Hengartner M.O., Horvitz H.R. Programmed cell death in Caenorhabditis elegans. Curr Opin Genet Dev. 4:1994;581-586.
9. Thornberry N.A., Lazebnik Y. Caspases: enemies within. Science. 281:1998;1312-1316.
10. Reed J.C. Double identity for proteins of the Bcl-2 family. Nature. 387:1997;773-776.
11. Kroemer G. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nature Med. 3:1997;614-620.
12. Kumar S. ICE-like proteases in apoptosis. Trends Biochem Sci. 20:1995;198-202.
13. Nicholson D.W., Ali A., Thornberry N.A., et al. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature. 376:1995;37-43.
14. Enari M., Sakahira H., Yokoyama H., Okawa K., Iwamatsu A., Nagata S. A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature. 391:1998;43-50.
15. Moncada S., Higgs A. The L-arginine-nitric oxide pathway. New Engl J Med. 329:1993;2002-2012.
16. Drexler H. Nitric oxide synthases in the failing human heart: A doubled-edged sword? Circulation. 99:1999;2972-2975.
17. Nathan C. Inducible nitric oxide synthase: what difference does it make ? J Clin Invest. 100:1997;2417-2423.
18. Suzuki H., Wildhirt S.M., Dudek R.R., Narayan K.S., Bailey A.H., Bing R.J. Induction of apoptosis in myocardial infarction and its possible relationship to nitric oxide synthase in macrophages. Tissue Cell. 28:1996;89-97.
19. Kawaguchi H., Shin W.S., Wang Y., et al. In vivo gene transfection of human endothelial cell nitric oxide synthase in cardiomyocytes causes apoptosis-like cell death. Identification using Sendai virus-coated liposomes. Circulation. 95:1997;2441-2447.
20. Albina J., Cui S., Mateo R., Reichner J. Nitric oxide-mediated apoptosis in murine peritoneal macrophages. J Immunol. 150:1993;5080-5085.
21. Dimmeler S., Haendeler J., Nehls M., Zeiher A.M. Suppression of apoptosis by nitric oxide via inhibition of ICE-like and CPP32-like proteases. J. Exp. Med. 185:1997;601-608.
22. Cheng W., Li B., Kajustra J., Li P., Wolin M.S., Sonnenblick E.H., Hintze T.H., Olivetti G., Anversa P. Stretch-induced programmed myocyte cell death. J Clin Invest. 96:1995;2247-2259.
23. Nonami Y., Rao V., Shiono N., Ogoshi S. Quenching the effects of L-Arginine on free radical injury in cultured cardiomyocytes. Surg Today. 28:1998;379-384.
24. Gorbunov N.V., Tyurina Y.Y., Salama G., Day B.W., Claycamp H.G., Argyros H.G., Elsayed N.M. Nitric oxide protects cardiomyocytes against tert.-butyl hyperoxide-induced formation of alkoxyl and peroxyl radicals and peroxidation of phosphatidylserine. Biochem Biophys Res Commun. 244:1998;647-651.
25. Rössig L., Fichtlscherer B., Breitschopf K., Haendeler J., Zeiher A.M., Mülsch A., Dimmeler S. Nitric oxide inhibits caspase-3 by S-nitrosation in vivo. J Biol Chem. 274:1999;6823-6826.
26. Li J., Billiar T.R., Talanian R.V., Kim Y.M. Nitric oxide reversibly inhibits seven members of the caspase family via S-nitrosylation. Biochem Biophys Res Commun. 240:1997;419-424.
27. Gavrieli Y., Sherman Y.S.A. B.-S. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol. 119:1992;493-501.
28. Kockx M.M., De Meyer G.R., Muhring J., Jacob W., Bult H., Herman A.G. Apoptosis and related proteins in different stages of human atherosclerotic plaques. Circulation. 97:1998;2307-2315.
29. Haendeler J., Meßmer U.K., Brüne B., Neugebauer E., Dimmeler S. Endotoxic shock leads to apoptosis in vivo and reduces Bcl-2. Shock. 6:1996;405-409.
30. Misao J., Hayakawa Y., Ohno M., Kato S., Fujiwara T., Fujiwara H. Expression of Bcl-2, an inhibitor of apoptosis, and Bax, an accelerator of apoptosis, in ventricular myocytes of human hearts with myocardial infarction. Circulation. 94:1996;1506-1512.
31. Isenmann S., Stoll G., Schroeter M., Krajewski S., Reed J.C., Bahr M. Differential regulation of Bax, Bcl-2, and Bcl-X proteins in focal cortical ischemia in the rat. Brain Pathol. 8:1998;49-62.
32. Antonawich F.J., Krajewski S., Reed J.C., Davis J.N. Bcl-x(l) Bax interaction after transient global ischemia. J Cereb Blood Flow Metab. 18:1998;882-886.
33. Chakrabarti S., Hoque A.N., Karmazyn M. A rapid ischemia-induced apoptosis in isolated rat hearts and its attenuation by the sodium-hydrogen exchange inhibitor HOE 642 (cariporide). J Moll Cell Cardiol. 29:1997;3169-3174.
34. Ferrer I., Lopez E., Blanco R., et al. Bcl-2, Bax, and Bcl-x expression in the CA1 area of the hippocampus following transient forebrain ischemia in the adult gerbil. Exp Brain Res. 121:1998;167-173.
35. Yaoita H., Ogawa K., Maehara K., Maruyama Y. Attenuation of ischemia-reperfusion injury in rats by a caspase inhibitor. Circulation. 97:1998;276-281.
36. Ravelli S., Albala A., Ming M., et al. Inducible nitric oxide synthase expression in smooth muscle cells and macrophages of human transplant coronary artery disease. Circulation. 97:1998;2338-2345.
37. Wildhirt S.M., Dudek R.R., Suzuki H., Bing R.H. Involvement of inducible nitric oxide synthase in the inflammatory process of myocardial infarction. Int J Cardiol. 50:1995;253-261.
38. Yasmin W., Strynadka K.D., Schulz R. Generation of peroxynitrite contributes to ischemia-reperfusion injury in isolated rat hearts. Cardiovasc Res. 33:1997;422-432.
39. Szabolcs M., Michler R.E., Yang X., et al. Apoptosis of cardiac myocytes during cardiac allograft rejection. Relation to induction of nitric oxide synthase. Circulation. 94:1996;1665-1673.