Cytokine-induced nitric oxide production inhibits mitochondrial energy production and impairs contractile function in rat cardiac myocytes

Journal of the American College of Cardiology

Volumn 35, Issue 5, 2000, Pages 1338-1346

  Tatsumi, Tetsuya ^a   Matoba, Satoaki ^a   Kawahara, Akira ^a   Keira, Natsuya ^a   Shiraishi, Jun ^a   Akashi, Kazuko ^a   Kobara, Miyuki ^a   Tanaka, Tetsuya ^a   Katamura, Maki ^a   Nakagawa, Chiaki ^a   Ohta, Bon ^a   Shirayama, Takeshi ^a   Takeda, Kazuo ^a   Asayama, Jun ^b   Fliss, Henry ^c   Nakagawa, Masao ^a  

^a KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^b KYOTO PHARMACEUTICAL UNIVERSITY   (Japan)

^c UNIVERSITY OF OTTAWA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

8 BROMO CYCLIC GMP; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CALCIUM; CYCLIC GMP DEPENDENT PROTEIN KINASE INHIBITOR; CYTOKINE; GLUCOSE; IRON SULFUR PROTEIN; KT 5823; LACTIC ACID; N(G) METHYLARGININE; NITRATE; NITRIC OXIDE; NITRIC OXIDE DONOR; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; NITROPRUSSIDE SODIUM; OLIGOMYCIN; RECOMBINANT INTERLEUKIN 1BETA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE);

ANIMAL CELL; ARTICLE; CALCIUM CURRENT; CELL ENERGY; CELL FUNCTION; CONTROLLED STUDY; ENERGY BALANCE; ENERGY METABOLISM; HEART ELECTROPHYSIOLOGY; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; MEMBRANE POTENTIAL; METABOLIC REGULATION; MITOCHONDRIAL RESPIRATION; MUSCLE FIBER CULTURE; NONHUMAN; PRIORITY JOURNAL; RAT;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; CYCLIC GMP; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENERGY METABOLISM; GLUCOSE; GLYCOLYSIS; INFLAMMATION; INTERLEUKIN-1; LACTIC ACID; MITOCHONDRIA, HEART; MYOCARDIAL CONTRACTION; MYOCARDIUM; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITROPRUSSIDE; OMEGA-N-METHYLARGININE; RATS;

EID: 18344413731     PISSN: 07351097     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0735-1097(00)00526-X     Document Type: Article

References (45)

1. Ramacioti C., Sharkey A., McClellan G., Winegrad S. Endothelial cells regulate cardiac contractility. Proc Natl Acad Sci U S A. 89:1992;33-36.
2. Shah A.M., Spurgeon H.A., Sollott S.J., Talo A., Lakatta E.G. 8-Bromo cGMP reduces the myofilament response to calcium in intact cardiac myocytes. Circ Res. 74:1994;970-978.
3. Brady A.J., Warren J.B., Poole-Wilson P.A., Williams T.J., Harding S.E. Nitric oxide attenuates cardiac myocyte contraction. Am J Physiol. 265:1993;H176-H182.
4. Balligand J.L., Kelly R.A., Marsden P.A., Smith T.W., Michel T. Control of cardiac muscle cell function by an endogenous nitric oxide signalling system. Proc Natl Acad Sci USA. 90:1993;347-351.
5. Pinsky D.J., Cai B., Yang X., Rodriguez C., Sciacca R.R., Cannon P.J. The lethal effects of cytokine-induced nitric oxide on cardiac myocytes are blocked by nitric oxide synthase antagonism or transforming growth factor β J Clin Invest. 95:1995;677-685.
6. Nathan C. Nitric oxide as a secretory product of mammalian cells. FASEB J. 6:1992;3051-3064.
7. Balligand J.L., Ungureanu D., Kelly R.A., et al. Abnormal contractile function due to induction of nitric oxide synthesis in rat cardiac myocytes follows exposure to activated macrophage-conditioned medium. J Clin Invest. 91:1993;2314-2319.
8. Suffredini A.F., Fromm R.E., Parker M.M., et al. The cardiovascular response of normal humans to the administration of endotoxin. N Engl J Med. 321:1989;280-287.
9. Geng Y., Hansson G.K., Holme E. Interferon-gamma and tumor necrosis factor synergize to induce nitric oxide production and inhibit mitochondrial respiration in vascular smooth muscle cells. Circ Res. 71:1992;1268-1276.
10. Stadler J., Billiar T.R., Curran R.D., Stuehr D.J., Ochoa J.B., Simmons R.L. Effect of exogenous and endogenous nitric oxide on mitochondrial respiration of rat hepatocytes. Am J Physiol. 260:1991;C910-C916.
11. Oddis C.V., Finkel M.S. Cytokine-stimulated nitric oxide production inhibits mitochondrial activity in cardiac myocytes. Biochem Biophys Res Commun. 213:1995;1002-1009.
12. Wang D., McMillin J.B., Bick R., Buja L.M. Response of the neonatal rat cardiomyocyte in culture to energy depletion effects of cytokines, nitric oxide, and heat shock proteins . Lab Invest. 75:1996;809-818.
13. Tsujino M., Hirata Y., Imai T., et al. Induction of nitric oxide synthase gene by interleukin-1β in cultured rat cardiocytes. Circulation. 90:1994;375-383.
14. Goshima K. Ouabain-induced arrhythmias of single isolated myocardial cells and cell clusters cultured in vitro and their improvement by quinidine. J Mol Cell Cardiol. 9:1977;7-23.
15. Matoba S., Tatsumi T., Keira N., et al. Cardioprotective effect of angiotensin-converting enzyme inhibition against hypoxia/reoxygenation injury in cultured rat cardiac myocytes. Circulation. 99:1999;817-822.
16. 15N] nitrate in biological fluids. Anal Biochem. 126:1982;131-138.
17. Asayama J., Yamahara Y., Ohta B., et al. Release kinetics of cardiac troponin T in coronary effluent from isolated rat hearts during hypoxia and reoxygenation. Basic Res Cardiol. 87:1992;428-436.
18. Sordahl L.A., Stewart M. Mechanism(s) of altered mitochondrial calcium transport in acutely ischemic canine hearts. Circ Res. 47:1980;814-820.
19. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the folin phenol reagent. J Biol Chem. 193:1951;265-275.
20. Hatefi Y., Rieske J.S. Preparation and properties of DPNH-coenzyme Q reductase (complex I of the respiratory chain). Methods Enzymol. 10:1967;235-239.
21. Ziegler D., Rieske J.S. Preparation and properties of succinate dehydrogenase-coenzyme Q reductase (complex II). Methods Enzymol. 10:1967;231-235.
22. Lowe PN. Methods for studying heart mitochondrial ATPase in native and purified form. In: Dhalla NS, editor. Methods for studying cardiac membranes, Volume 1, Cre Press. 1984;111-31.
23. Hamill O.P., Marty A., Neher E., Sakmann B., Sigworth F.J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch. 391:1981;85-100.
24. Fliss H., Gattinger D. Apoptosis in ischemic and reperfused rat myocardium. Circ Res. 79:1996;949-956.
25. Shen W., Hintze T.H., Wolin M.S. Nitric oxide. An important signaling mechanism between vascular endothelium and parenchymal cells in the regulation of oxygen consumption. Circulation. 92:1995;3505-3512.
26. Sheng Z., Knowlton K., Chen J., Hoshijima M., Brown J.H., Chien K.R. Cardiotrophin 1 (CT-1) inhibition of cardiac myocyte apoptosis via a mitogen-activated protein kinase-dependent pathway. J Biol Chem. 272:1997;5783-5791.
27. Drapier J.C., Hibbs J.B.J. Differentiation of murine macrophages to express non-specific cytotoxicity for tumor cells results in L-arginine-dependent inhibition of mitochondrial iron-sulfur enzymes in the macrophage effector cells. J Immunol. 140:1988;2829-2838.
28. Drapier J.C., Bouton C. Modulation by nitric oxide of metalloprotein regulatory activities. Bioassays. 18:1996;549-556.
29. Lancaster J.R.J., Hibbs J.B.J. EPR demonstration of iron-nitrosyl complex formation by cytotoxic-activated macrophages. Proc Natl Acad Sci USA. 87:1990;1223-1227.
30. Lancaster J.R.J., Langehr J.M., Bergonia H.A., Murase N., Simmons R.L., Hoffman R.A. EPR detection of heme and non-heme iron-containing protein nitrosylation by nitric oxide during rejection of rat heart allograft. J Biol Chem. 267:1992;10994-10998.
31. 2+ current is regulated by cyclic GMP-dependent protein kinase in mammalian cardiac myocytes. Proc Natl Acad Sci USA. 88:1991;1197-1201.
32. Stefanovic-Racic M., Stadler J., Georgescu H.I., Evans C.H. Nitric oxide and energy production in articular chondrocytes. J Cell Physiol. 159:1994;274-280.
33. Gevers W. Generation of protons by metabolic processes in heart cells. J Mol Cell Cardiol. 9:1977;867-874.
34. Elliott A.C., Smith G.L., Allen D.G. The metabolic consequences of an increase in the frequency of stimulation in isolated ferret hearts. J Physiol (Lond). 474:1994;147-159.
35. Mitchell M.R., Powell T., Terran D.A., Twist V.W. Electrical activity and contraction in cells isolated from rat and guinea-pig ventricular muscle a comparative study . J Physiol (Lond). 391:1987;527-544.
36. Shirayama T., Pappano A.J. Biphasic effects of intrapipette cyclic guanosine monophosphate on L-type calcium current and contraction of guinea pig ventricular myocytes. J Pharmacol Exp Ther. 279:1996;1274-1281.
37. Kase H., Iwahashi K., Nakanishi S., et al. K-252 Compounds, novel and potent inhibitors of protein kinase C and cyclic nucleotide-dependent protein kinases. Biochem Biophys Res Commun. 142:1987;436-440.
38. 2+ transients and adenylate cyclase activity. Am J Physiol. 272:1997;H1937-H1944.
39. 2+/calmodulin-dependent formation of hydrogen peroxide by brain nitric oxide synthase. Biochem J. 281:1992;627-630.
40. Pou S., Pou W.S., Bredt D.S., et al. Generation of superoxide by purified brain nitric oxide synthase. J Biol Chem. 267:1992;24173-24176.
41. Radi R., Beckman J.S., Bush K.M., Freeman B.A. Peroxynitrite oxidation of sulfhydryls the cytotoxic potential of superoxide and nitric oxide . J Biol Chem. 266:1991;4244-4250.
42. Dimmeler S., Ankarcrona M., Nicotera P., Brune B. Exogenous nitric oxide (NO) generation of IL-1-beta-induced intracellular NO production stimulates inhibitory auto-ADP-ribosylation of glyceraldehyde-3-phosphate dehydrogenase in RINm5F cells. J Immunol. 150:1993;2964-2971.
43. Kwon N.S., Stuehr D.J., Nathan C.F. Inhibition of tumor cell ribonucleotide reductase by macrophage-derived nitric oxide. J Exp Med. 174:1991;761-767.
44. Zhang J., Dawson V.L., Danson T.M. Nitric oxide activation of poly (ADP-ribose) synthetase in neurotoxicity. Science. 263:1994;687-689.
45. Welsh N., Sandler S. Interleukin-1-beta induces nitric oxide production and inhibits the activity of aconitase without decreasing glucose oxidation rates in isolated pancreatic islets. Biochem Biophys Res Commun. 182:1992;333-340.