Inhibition of mitochondrial respiratory complex I by nitric oxide, peroxynitrite and S-nitrosothiols

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1658, Issue 1-2, 2004, Pages 44-49

  Brown, Guy C ^a   Borutaite, Vilmante ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Complex I; electron paramagnetic resonance; endothelial inducible and neuronal nitric oxide synthases; eNOS, iNOS and nNOS; EPR; GSH; Mitochondria; NADH ubiquinone oxidoreductase; Nitric oxide; Parkinson's disease; reduced glutathione; Respiration; RNS

Indexed keywords

IRON; NITRIC OXIDE; OXIDIZING AGENT; PEROXYNITRITE; REACTIVE NITROGEN SPECIES; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); S NITROSOTHIOL; SULFUR; THIOL DERIVATIVE; TYROSINE;

BIOCHEMISTRY; CELL; CELL MEMBRANE PERMEABILITY; CONCENTRATION (PARAMETERS); CYTOSTASIS; CYTOTOXICITY; ELECTRON TRANSPORT; EMOTIONAL STRESS; ENZYME ACTIVATION; ENZYME ACTIVITY; GLYCOLYSIS; HUMAN; INFLAMMATION; LIGHT; LIPID PEROXIDATION; MACROPHAGE; MACROPHAGE ACTIVATION; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NITRATION; NITROSATION; NITROSYLATION; NONHUMAN; OXIDATION; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SEPTIC SHOCK; TISSUE; TUMOR CELL;

ADENOSINE TRIPHOSPHATE; ANIMALS; ELECTRON TRANSPORT COMPLEX I; HUMANS; IRON-SULFUR PROTEINS; MACROPHAGES; MITOCHONDRIA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; NITROSATION; NITROSO COMPOUNDS; PARKINSON DISEASE; PEROXYNITROUS ACID; REACTIVE NITROGEN SPECIES; TYROSINE;

EID: 3543008400     PISSN: 00052728     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbabio.2004.03.016     Document Type: Review

References (52)

1. Carroll J., Fearnley R.J., Shannon J., Hirst J.E., Walker J.E. Analysis of the subunit composition of complex I from bovine heart mitochondria. Mol. Cell. Proteomics. 2:2003;117-126
2. Hirst J., Carroll J., Fearnley I.M., Shannon R.J., Walker J.E. The nuclear encoded subunits of complex I from bovine heart mitochondria. Biochim. Biophys. Acta. 1604:2003;135-150
3. Runswick M.J., Fearnley I.M., Skehel J.M., Walker J.E. Presence of an acyl carrier protein in NADH:ubiquinone oxidoreductase from bovine heart mitochondria. FEBS Lett. 286:1991;121-124
4. Turrens J.F., Boveris A. Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem. J. 191:1980;421-427
5. St-Pierre J., Buckingham J.A., Roebuck S.J., Brand M.D. Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 277:2002;44784-44790
6. Liu Y., Fiskum G., Schubert D. Generation of reactive oxygen species by the mitochondrial electron transport chain. J. Neurochem. 80:2002;780-787
7. Chauvin C., De Oliveira F., Ronot X., Mousseau M., Leverve X., Fontain E. Rotenone inhibits the mitochondrial permeability transition-induced cell death in U937 and KB cells. J. Biol. Chem. 276:2001;41394-41398
8. Fearnley I.M., Carroll J., Shannon R.J., Runswick M.J., Walker J.E., Hirst J.E. GRIM-19, a cell death regulatory gene product, is a subunit of bovine mitochondrial NADH:ubiquinone oxidoreductase (complex I). J. Biol. Chem. 276:2001;38345-38348
9. Gavrikova E.V., Vinogradov A.D. Active/de-active state transition of the mitochondrial complex I as revealed by specific sulfhydryl group labeling. FEBS Lett. 455:1999;36-40
10. Vinogradov A.D. Catalytic properties of the mitochondrial NADH-ubiquinone oxidoreductase (complex I) and the pseudo-reversible active/inactive enzyme transition. Biochim. Biophys. Acta. 1364:1998;169-185
11. Papa S., Sardanelli A.M., Scacco S., Petruzzella V., Technikova-Dobrova Z., Vergari R., Signorile A. The NADH:ubiquinone oxidoreductase (complex I) of the mammalian respiratory chain and the cAMP cascade. J. Bioenerg. Biomembranes. 34:2002;1-10
12. Ignarro L.J. Nitric Oxide: Biology and Pathobiology. 2000;Academic Press, San Diego
13. Giulivi C., Poderoso J.J., Boveris A. Production of NO by mitochondria. J. Biol. Chem. 273:1998;11038-11043
14. Ghafourifar P., Schenk U., Klein S.D., Richter C. Mitochondrial nitric-oxide synthase stimulation causes cytochrome c release from isolated mitochondria - evidence for intramitochondrial peroxynitrite formation. J. Biol. Chem. 274:1999;31185-31188
15. Zweier J.L., Samouilov A., Kuppusamy P. Non-enzymatic nitric oxide synthesis in biological systems. Biochim. Biophys. Acta. 1411:1999;250-262
16. Brown G.C. Nitric oxide and mitochondrial respiration. Biochim. Biophys. Acta. 1411:1999;351-369
17. Brown G.C. Regulation of mitochondrial respiration by nitric oxide inhibition of cytochrome oxidase. Biochim. Biophys. Acta. 1504:2001;46-57
18. Cassina A., Radi R. Different inhibitory actions of NO and peroxynitrite on mitochondrial electron transport. Arch. Biochem. Biophys. 328:1996;309-316
19. Cleeter M.W.J., Cooper J.M., Darley-Usmar V.M., Moncada S., Schapira A.H.V. Reversible inhibition of cytochrome oxidase, the terminal enzyme of the mitochondrial respiratory chain by NO. FEBS Lett. 345:1994;50-54
20. Brown G.C., Cooper C.E. Nanomolar concentrations of NO reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. FEBS Lett. 356:1994;295-298
21. Schweizer M., Richter C. NO potently and reversibly deenergizes mitochondria at low oxygen tension. Biochim. Biophys. Acta. 204:1994;169-175
22. Brown G.C., Borutaite V. Nitric oxide, mitochondria, and cell death. IUBMB Life. 52:2001;189-195
23. Clementi E., Brown G.C., Feelisch M., Moncada S. Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione. Proc. Natl. Acad. Sci. U. S. A. 95:1998;7631-7636
24. Gadelha F.R., Thomson L., Fagian M.M., Costa A.D.T., Radi R., Vercesi A.E. Calcium-independent permeabilization of the inner mitochondrial membrane by peroxynitrite is mediated by membrane protein thiol cross-linking and lipid peroxidation. Arch. Biochem. Biophys. 345:1997;243-250
25. Poderoso J.J., Carreras M.C., Lisdero C., Riobo N., Schopfer F., Boveris A. NO inhibits electron transfer and increases superoxide radical production in rat heart mitochondria and submitochondrial particles. Arch. Biochem. Biophys. 328:1996;85-92
26. Packer M.A., Murphy M.P. Peroxynitrite causes calcium efflux from mitochondria which is prevented by cyclosporin A. FEBS Lett. 345:1994;237-240
27. Borutaite V., Morkuniene R., Brown G.C. Release of cytochrome c from heart mitochondria is induced by high calcium and peroxynitrite and is responsible for calcium-induced inhibition of substrate oxidation. Biochim. Biophys. Acta. 1453:1999;41-48
28. Granger D.L., Lehninger A.L. Sites of inhibition of mitochondrial electron transport in macrophage-injured neoplastic cells. J. Cell Biol. 95:1982;527-535
29. Drapier J.C., Hibbs J.B. Jr. Differentiation of murine macrophages to express non-specific cytotoxicity for tumour cells results in L-arginine-dependent inhibition of mitochondrial iron-sulfur in the macrophage effector cells. J. Immunol. 140:1988;2829-2838
30. Stuehr D.J., Nathan C.F. NO: a macrophage product responsible for cytostasis and respiratory inhibition in tumour target cells. J. Exp. Med. 169:1989;1543-1555
31. Hibbs J.B. Jr., Taintor R.R., Vavrin Z., Rachlin E.M. Nitric oxide: a cytotoxic activated macrophage effector molecule. Biochem. Biophys. Res. Commun. 157:1988;87-94
32. Lancaster J.R., Hibbs J.B. EPR demonstration of iron-nitrosyl complex formation by cytotoxic activated macrophages. Proc. Natl. Acad. Sci. U. S. A. 87:1990;1223-1227
33. Welter R., Yu L., Yu C.A. The effects of NO on electron transport complexes. Arch. Biochem. Biophys. 331:1996;9-14
34. Rogers P.A., Eide L., Klungland A., Ding H. Reversible inactivation of E. coli endonuclease III via modification of its [4Fe-4S] cluster by nitric oxide. DNA Repair. 2:2003;809-817
35. Gardner P.R., Costantino G., Szabo C., Salzman A.L. Nitric oxide sensitivity of the aconitases. J. Biol. Chem. 272:1997;25071-25076
36. Castro L.A., Robalinho R.L., Cayota A., Meneghini R., Radi R. Nitric oxide and peroxynitrite-dependent aconitase inactivation and iron-regulatory protein-1 activation in mammalian fibroblasts. Arch. Biochem. Biophys. 359:1998;215-224
37. Beltran B., Orsi A., Clementi E., Moncada S. Oxidative stress and S-nitrosylation of proteins in cells. Br. J. Pharmacol. 129:2000;953-960
38. Borutaite V., Budriunaite A., Brown G.C. Reversal of nitric oxide-, peroxynitrite-, and S-nitrosothiol-induced inhibition of mitochondrial respiration or complex I activity by light and thiols. Biochim. Biophys. Acta. 1459:2000;405-412
39. Jekabsone A., Ivanoviene L., Brown G.C., Borutaite V. Nitric oxide and calcium together inactivate mitochondrial complex I and induce cytochrome c release. J. Mol. Cell. Cardiol. 35:2003;803-809
40. Riobo N.A., Clementi E., Melani M., Boveris A., Cadenas E., Moncada S., Poderoso J.J. Nitric oxide inhibits mitochondrial NADH: ubiquinone reductase activity through peroxynitrite formation. Biochem. J. 359:2001;139-145
41. Yamamoto T., Maruyama W., Kato Y., Yi H., Shamoto-Nagai M., Tanaka M., Sato Y., Naoi M. Selective nitration of mitochondrial complex I by peroxynitrite: involvement in mitochondria dysfunction and cell death of dopaminergic SH-SY5Y cells. J. Neural Transm. 109:2002;1-13
42. Murray J., Taylor S.W., Zhang B., Ghosh S.S., Capaldi R.A. Oxidative damage to mitochondrial complex I due to peroxynitrite. Identification of reactive tyrosines by mass spectrometry. J. Biol. Chem. 278:2003;37223-37230
43. Radi R., Rodriguez M., Castro L., Telleri R. Inhibition of mitochondrial electron transport by peroxynitrite. Arch. Biochem. Biophys. 308:1994;89-95
44. Brookes P.S., Land J.M., Clark J.B., Heales S.J. Peroxynitrite and brain mitochondria: evidence for increased proton leak. J. Neurochem. 70:1998;2195-2202
45. Taylor E.R., Hurrell F., Shannon R.J., Lin T.-K., Hirst J., Murphy M.P. Reversible glutathionylation of complex I increases mitochondrial superoxide formation. J. Biol. Chem. 278:2003;19603-19610
46. Brealey D., Brand M., Hargreaves I., Heales S., Land J., Smolenski R., Davies N.A., Cooper C.E., Singer M. Association between mitochondrial dysfunction and severity and outcome of septic shock. Lancet. 360:2002;219-223
47. Brealey D., Karyampudi S., Jaques T.S., Novelli M., Stidwill R., Taylor V., Smolenski R.T., Singer M. Mitochondrial dysfunction in a long-term rodent model of sepsis and organ failure. Am. J. Physiol. 286:2004;R491-R497
48. Orth M., Schapira A.H. Mitochondrial involvement in Parkinson's disease. Neurochem. Int. 40:2002;533-541
49. Chenais B., Morjani H., Drapier J.C. Impact of endogenous nitric oxide on microglial cell energy metabolism and labile iron pool. J. Neurochem. 81:2002;615-623
50. Heales S.J., Bolanos J.P., Stewart V.C., Brookes P.S., Land J.M., Clark J.B. Nitric oxide, mitochondria and neurological disease. Biochim. Biophys. Acta. 1410:1999;215-228
51. Antunes F., Han D., Rettori D., Cadenas E. Mitochondrial damage by nitric oxide is potentiated by dopamine in PC12 cells. Biochim. Biophys. Acta. 1556:2002;233-238
52. Madrigal J.L., Olivenza R., Moro M.A., Lizasoain I., Lorenzo P., Rodrigo J., Leza J.C. Glutathione depletion, lipid peroxidation and mitochondrial dysfunction are induced by chronic stress in rat brain. Neuropsychopharmacology. 24:2001;420-429