Mitochondria and nitric oxide: Chemistry and pathophysiology

Advances in Experimental Medicine and Biology

Volumn 942, Issue , 2012, Pages 75-92

  Sarti, Paolo ^a   Arese, Marzia ^a   Forte, Elena ^a   Giuffrè, Alessandro ^a   Mastronicola, Daniela ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Bioenergetics; Cell respiration; Cytochromes; Mitochondria; Nitrosative stress; ROS

Indexed keywords

CYTOCHROME C OXIDASE; MYOGLOBIN; NITRIC OXIDE; NITRITE; OXYMYOGLOBIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UNCLASSIFIED DRUG;

ARTICLE; CELL FUNCTION; CELL PROTECTION; DISSOCIATION; ENZYME ACTIVE SITE; ENZYME INHIBITION; ENZYME METABOLISM; HUMAN; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL RESPIRATION; MOLECULAR INTERACTION; NITROSATION; NITROSATIVE STRESS; NITROSYLATION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXYGEN TENSION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY CHAIN; STEADY STATE;

ANIMALS; HUMANS; MITOCHONDRIA; NITRIC OXIDE;

EID: 84859917863     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-94-007-2869-1_4     Document Type: Article

References (107)

1. Almeida A, Almeida J, Bolanos JP, Moncada S (2001) Different responses of astrocytes and neurons to nitric oxide: the role of glycolytically generated ATP in astrocyte protection. Proc Natl Acad Sci USA 98:15294-15299
2. Almeida A, Moncada S, Bolanos JP (2004) Nitric oxide switches on glycolysis through the AMP protein kinase and 6-phosphofructo-2-kinase pathway. Nat Cell Biol 6:45-51
3. Antonini E, Brunori M, Colosimo A, Greenwood C, Wilson MT (1977) Oxygen "pulsed" cytochrome c oxidase: functional properties and catalytic relevance. Proc Natl Acad Sci USA 74:3128-3132
4. Antunes F, Boveris A, Cadenas E (2007) On the biologic role of the reaction of NO with oxidized cytochrome c oxidase. Antioxid Redox Signal 9:1569-1579
5. Babcock GT (1999) How oxygen is activated and reduced in respiration. Proc Natl Acad Sci USA 96:12971-12973
6. Basu S, Azarova NA, Font MD, King SB, Hogg N, Gladwin MT, Shiva S, Kim-Shapiro DB (2008) Nitrite reductase activity of cytochrome c. J Biol Chem 283:32590-32597
7. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 87:1620-1624
8. Blackmore RS, Greenwood C, Gibson QH (1991) Studies of the primary oxygen intermediate in the reaction of fully reduced cytochrome oxidase. J Biol Chem 266:19245-19249
9. Blandini F, Braunewell KH, Manahan-Vaughan D, Orzi F, Sarti P (2004) Neurodegeneration and energy metabolism: from chemistry to clinics. Cell Death Differ 11:479-484
10. Bolanos JP, Peuchen S, Heales SJ, Land JM, Clark JB (1994) Nitric oxide-mediated inhibition of the mitochondrial respiratory chain in cultured astrocytes. J Neurochem 63:910-916
11. Borisov VB, Forte E, Konstantinov AA, Poole RK, Sarti P, Giuffrè A (2004) Interaction of the bacterial terminal oxidase cytochrome bd with nitric oxide. FEBS Lett 576:201-204
12. Borisov VB, Forte E, Sarti P, Brunori M, Konstantinov AA, Giuffrè A (2006) Nitric oxide reacts with the ferryl-oxo catalytic intermediate of the CuB-lacking cytochrome bd terminal oxidase. FEBS Lett 580:4823-4826
13. Borisov VB, Forte E, Sarti P, Brunori M, Konstantinov AA, Giuffrè A (2007) Redox control of fast ligand dissociation from Escherichiacoli cytochrome bd. Biochem Biophys Res Commun 355:97-102
14. Borisov VB, Forte E, Giuffrè A, Konstantinov A, Sarti P (2009) Reaction of nitric oxide with the oxidized di-heme and heme-copper oxygen-reducing centers of terminal oxidases: different reaction pathways and end-products. J Inorg Biochem 103:1185-1187
15. Borutaite V, Brown GC (1996) Rapid reduction of nitric oxide by mitochondria, and reversible inhibition of mitochondrial respiration by nitric oxide. Biochem J 315(Pt 1):295-299
16. Borutaite V, Brown GC (2003) Nitric oxide induces apoptosis viahydrogen peroxide, but necrosis viaenergy and thiol depletion. Free Radic Biol Med 35:1457-1468
17. Borutaite V, Budriunaite A, Brown GC (2000) Reversal of nitric oxide-, peroxynitrite-and S-nitrosothiol-induced inhibition of mitochondrial respiration or complex I activity by light and thiols. Biochim Biophys Acta 1459:405-412
18. Brookes P, Darley-Usmar VM (2002) Hypothesis: the mitochondrial NO(*) signaling pathway, and the transduction of nitrosative to oxidative cell signals: an alternative function for cytochrome C oxidase. Free Radic Biol Med 32: 370-374
19. Brookes PS, Levonen AL, Shiva S, Sarti P, Darley-Usmar VM (2002) Mitochondria: regulators of signal transduction by reactive oxygen and nitrogen species. Free Radic Biol Med 33:755-764
20. Brookes PS, Kraus DW, Shiva S, Doeller JE, Barone MC, Patel RP, Lancaster JR Jr, Darley-Usmar V (2003) Control of mitochondrial respiration by NO*, effects of low oxygen and respiratory state. J Biol Chem 278:31603-31609
21. Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS (2004) Calcium, ATP, and ROS: amitochondrial love-hate triangle. Am J Physiol Cell Physiol 287:C817-C833
22. Brown GC, Cooper CE (1994) Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. FEBS Lett 356:295-298
23. Brown GC, Bolanos JP, Heales SJ, Clark JB (1995) Nitric oxide produced by activated astrocytes rapidly and reversibly inhibits cellular respiration. Neurosci Lett 193:201-204
24. Brudvig GW, Stevens TH, Chan SI (1980) Reactions of nitric oxide with cytochrome c oxidase. Biochemistry 19:5275-5285
25. Brunori M, Giuffrè A, Sarti P, Stubauer G, Wilson MT (1999) Nitric oxide and cellular respiration. Cell Mol Life Sci 56:549-557
26. Brunori M, Giuffrè A, Forte E, Mastronicola D, Barone MC, Sarti P (2004) Control of cytochrome c oxidase activity by nitric oxide. Biochim Biophys Acta 1655:365-371
27. Brunori M, Forte E, Arese M, Mastronicola D, Giuffrè A, Sarti P (2006) Nitric oxide and the respiratory enzyme. Biochim Biophys Acta 1757:1144-1154
28. Bryan NS, Calvert JW, Elrod JW, Gundewar S, Ji SY, Lefer DJ (2007) Dietary nitrite supplementation protects against myocardial ischemia-reperfusion injury. Proc Natl Acad Sci USA 104:19144-19149
29. Carr GJ, Ferguson SJ (1990) Nitric oxide formed by nitrite reductase of Paracoccus denitrificans is sufficiently stable to inhibit cytochrome oxidase activity and is reduced by its reductase under aerobic conditions. Biochim Biophys Acta 1017:57-62
30. Castello PR, David PS, McClure T, Crook Z, Poyton RO (2006) Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: implications for oxygen sensing and hypoxic signaling in eukaryotes. Cell Metab 3:277-287
31. Castello PR, Woo DK, Ball K, Wojcik J, Liu L, Poyton RO (2008) Oxygen-regulated isoforms of cytochrome c oxidase have differential effects on its nitric oxide production and on hypoxic signaling. Proc Natl Acad Sci USA 105:8203-8208
32. Chance B (1965) Reaction of oxygen with the respiratory chain in cells and tissues. J Gen Physiol 49(Suppl):163-195
33. Cleeter MW, Cooper JM, Darley-Usmar VM, Moncada S, Schapira AH (1994) Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. Implications for neurodegenerative diseases. FEBS Lett 345:50-54
34. Clementi E, Brown GC, Feelisch M, Moncada S (1998) 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 USA 95:7631-7636
35. Clementi E, Brown GC, Foxwell N, Moncada S (1999) On the mechanism by which vascular endothelial cells regulate their oxygen consumption. Proc Natl Acad Sci USA 96:1559-1562
36. Cooper CE (2002) Nitric oxide and cytochrome oxidase: substrate, inhibitor or effector? Trends Biochem Sci 27:33-39
37. Cooper CE, Giulivi C (2007) Nitric oxide regulation of mitochondrial oxygen consumption II: molecular mechanism and tissue physiology. Am J Physiol Cell Physiol 292:C1993-C2003
38. Cooper CE, Torres J, Sharpe MA, Wilson MT (1997) Nitric oxide ejects electrons from the binuclear centre of cytochrome c oxidase by reacting with oxidised copper: ageneral mechanism for the interaction of copper proteins with nitric oxide? FEBS Lett 414:281-284
39. Cooper CE, Mason MG, Nicholls P (2008) A dynamic model of nitric oxide inhibition of mitochondrial cytochrome c oxidase. Biochim Biophys Acta 1777:867-876
40. Dawson TM, Dawson VL (2003) Molecular pathways of neurodegeneration in Parkinsons disease. Science 302:819-822
41. Dezfulian C et al (2009) Nitrite therapy after cardiac arrest reduces reactive oxygen species generation, improves cardiac and neurological function, and enhances survival viareversible inhibition of mitochondrial complex I. Circulation 120:897-905
42. Di Lisa F, Bernardi P (2006) Mitochondriaand ischemia-reperfusion injury of the heart: fixing ahole. Cardiovasc Res 70:191-199
43. Erusalimsky JD, Moncada S (2007) Nitric oxide and mitochondrial signaling: from physiology to pathophysiology. Arterioscler Thromb Vasc Biol 27:2524-2531
44. Fabian M, Wong WW, Gennis RB, Palmer G (1999) Mass spectrometric determination of dioxygen bond splitting in the "peroxy" intermediate of cytochrome c oxidase. Proc Natl Acad Sci USA 96:13114-13117
45. Forte E, Urbani A, Saraste M, Sarti P, Brunori M, Giuffrè A (2001) The cytochrome cbb3 from Pseudomonas stutzeri displays nitric oxide reductase activity. Eur J Biochem 268:6486-6491
46. Foster KA, Galeffi F, Gerich FJ, Turner DA, Muller M (2006) Optical and pharmacological tools to investigate the role of mitochondriaduring oxidative stress and neurodegeneration. Prog Neurobiol 79:136-171
47. Galkin A, Moncada S (2007) S-nitrosation of mitochondrial complex I depends on its structural conformation. J Biol Chem 282:37448-37453
48. Galkin A, Abramov AY, Frakich N, Duchen MR, Moncada S (2009) Lack of oxygen deactivates mitochondrial complex I: implications for ischemic injury? J Biol Chem 284(52):36055-36061
49. Gavrikova EV, Vinogradov AD (1999) Active/de-active state transition of the mitochondrial complex I as revealed by specific sulfhydryl group labeling. FEBS Lett 455:36-40
50. Gibson Q, Greenwood C (1963) Reactions of cytochrome oxidase with oxygen and carbon monoxide. Biochem J 86:541-555
51. Giuffrè A, Stubauer G, Brunori M, Sarti P, Torres J, Wilson MT (1998) Chloride bound to oxidized cytochrome c oxidase controls the reaction with nitric oxide. J Biol Chem 273:32475-32478
52. Giuffrè A, Stubauer G, Sarti P, Brunori M, Zumft WG, Buse G, Soulimane T (1999) The heme-copper oxidases of Thermus thermophilus catalyze the reduction of nitric oxide: evolutionary implications. Proc Natl Acad Sci USA 96:14718-14723
53. Giuffrè A, Barone MC, Mastronicola D, DItri E, Sarti P, Brunori M (2000) Reaction of nitric oxide with the turnover intermediates of cytochrome c oxidase: reaction pathway and functional effects. Biochemistry 39:15446-15453
54. Giuffrè A, Barone MC, Brunori M, DItri E, Ludwig B, Malatesta F, Muller HW, Sarti P (2002) Nitric oxide reacts with the single-electron reduced active site of cytochrome c oxidase. J Biol Chem 277:22402-22406
55. Giuffrè A, Forte E, Brunori M, Sarti P (2005) Nitric oxide, cytochrome c oxidase and myoglobin: competition and reaction pathways. FEBS Lett 579:2528-2532
56. Giuffrè A, Sarti P, DItri E, Buse G, Soulimane T, Brunori M (1996) On the mechanism of inhibition of cytochrome c oxidase by nitric oxide. J Biol Chem 271:33404-33408
57. Giulivi C (2003) Characterization and function of mitochondrial nitric-oxide synthase. Free Radic Biol Med 34:397-408
58. Gladwin MT, Shelhamer JH, Schechter AN, Pease-Fye ME, Waclawiw MA, Panza JA, Ognibene FP, Cannon RO 3rd (2000) Role of circulating nitrite and S-nitrosohemoglobin in the regulation of regional blood flow in humans. Proc Natl Acad Sci USA 97:11482-11487
59. Hagen T, Taylor CT, Lam F, Moncada S (2003) Redistribution of intracellular oxygen in hypoxiaby nitric oxide: effect on HIF1alpha. Science 302:1975-1978
60. Hare JM, Keaney JF Jr, Balligand JL, Loscalzo J, Smith TW, Colucci WS (1995) Role of nitric oxide in parasympathetic modulation of beta-adrenergic myocardial contractility in normal dogs. J Clin Invest 95:360-366
61. Hendgen-Cotta UB et al (2008) Nitrite reductase activity of myoglobin regulates respiration and cellular viability in myocardial ischemia-reperfusion injury. Proc Natl Acad Sci USA 105:10256-10261
62. Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS (2005) Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6:150-166
63. Jenkins RR (1993) Exercise, oxidative stress, and antioxidants: areview. Int J Sport Nutr 3:356-375
64. Keynes RG, Garthwaite J (2004) Nitric oxide and its role in ischaemic brain injury. Curr Mol Med 4:179-191
65. Lundberg JO, Weitzberg E, Gladwin MT (2008) The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discov 7:156-167
66. Masci A, Mastronicola D, Arese M, Piane M, De Amicis A, Blanck TJ, Chessa L, Sarti P (2008) Control of cell respiration by nitric oxide in AtaxiaTelangiectasialymphoblastoid cells. Biochim Biophys Acta 1777:66-73
67. Mason MG, Nicholls P, Wilson MT, Cooper CE (2006) Nitric oxide inhibition of respiration involves both competitive (heme) and noncompetitive (copper) binding to cytochrome c oxidase. Proc Natl Acad Sci USA 103:708-713
68. Mason MG, Shepherd M, Nicholls P, Dobbin PS, Dodsworth KS, Poole RK, Cooper CE (2009a) Cytochrome bd confers nitric oxide resistance to Escherichiacoli. Nat Chem Biol 5:94-96
69. Mason MG, Nicholls P, Cooper CE (2009b) The steady-state mechanism of cytochrome c oxidase: redox interactions between metal centres. Biochem J 422:237-246
70. Mastronicola D et al (2003) Control of respiration by nitric oxide in Keilin-Hartree particles, mitochondriaand SH-SY5Y neuroblastomacells. Cell Mol Life Sci 60:1752-1759
71. Moncada S, Erusalimsky JD (2002) Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nat Rev Mol Cell Biol 3:214-220
72. Nadtochiy SM, Burwell LS, Brookes PS (2007) Cardioprotection and mitochondrial S-nitrosation: effects of S-nitroso-2-mercaptopropionyl glycine (SNO-MPG) in cardiac ischemia-reperfusion injury. J Mol Cell Cardiol 42:812-825
73. Palacios-Callender M, Quintero M, Hollis VS, Springett RJ, Moncada S (2004) Endogenous NO regulates superoxide production at low oxygen concentrations by modifying the redox state of cytochrome c oxidase. Proc Natl Acad Sci USA 101:7630-7635
74. Palacios-Callender M, Hollis V, Mitchison M, Frakich N, Unitt D, Moncada S (2007a) Cytochrome c oxidase regulates endogenous nitric oxide availability in respiring cells: apossible explanation for hypoxic vasodilation. Proc Natl Acad Sci USA 104:18508-18513
75. Palacios-Callender M, Hollis V, Frakich N, Mateo J, Moncada S (2007b) Cytochrome c oxidase maintains mitochondrial respiration during partial inhibition by nitric oxide. J Cell Sci 120:160-165
76. Pearce LL, Kanai AJ, Birder LA, Pitt BR, Peterson J (2002) The catabolic fate of nitric oxide: the nitric oxide oxidase and peroxynitrite reductase activities of cytochrome oxidase. J Biol Chem 277:13556-13562
77. Poderoso JJ, Carreras MC, Lisdero C, Riobo N, Schopfer F, Boveris A (1996) Nitric oxide inhibits electron transfer and increases superoxide radical production in rat heart mitochondriaand submitochondrial particles. Arch Biochem Biophys 328:85-92
78. Poyton RO, Castello PR, Ball KA, Woo DK, Pan N (2009) Mitochondriaand hypoxic signaling: anew view. Ann N Y Acad Sci 1177:48-56
79. Prime TA et al (2009) A mitochondria-targeted S-nitrosothiol modulates respiration, nitrosates thiols, and protects against ischemia-reperfusion injury. Proc Natl Acad Sci USA 106:10764-10769
80. Rassaf T, Flogel U, Drexhage C, Hendgen-Cotta U, Kelm M, Schrader J (2007) Nitrite reductase function of deoxymyoglobin: oxygen sensor and regulator of cardiac energetics and function. Circ Res 100:1749-1754
81. Sarti P, Lendaro E, Ippoliti R, Bellelli A, Benedetti PA, Brunori M (1999) Modulation of mitochondrial respiration by nitric oxide: investigation by single cell fluorescence microscopy. FASEB J 13:191-197
82. Sarti P, Giuffrè A, Forte E, Mastronicola D, Barone MC, Brunori M (2000) Nitric oxide and cytochrome c oxidase: mechanisms of inhibition and NO degradation. Biochem Biophys Res Commun 274:183-187
83. Sarti P, Giuffrè A, Barone MC, Forte E, Mastronicola D, Brunori M (2003) Nitric oxide and cytochrome oxidase: reaction mechanisms from the enzyme to the cell. Free Radic Biol Med 34:509-520
84. Schapira AH (1998) Human complex I defects in neurodegenerative diseases. Biochim Biophys Acta 1364:261-270
85. Schapira AH (2010) Complex I: inhibitors, inhibition and neurodegeneration. Exp Neurol 224(2):331-335
86. Schweizer M, Richter C (1994) Nitric oxide potently and reversibly deenergizes mitochondriaat low oxygen tension. Biochem Biophys Res Commun 204:169-175
87. Shen W, Hintze TH, Wolin MS (1995) Nitric oxide. An important signaling mechanism between vascular endothelium and parenchymal cells in the regulation of oxygen consumption. Circulation 92:3505-3512
88. Shiva S, Gladwin MT (2009) Nitrite mediates cytoprotection after ischemia/reperfusion by modulating mitochondrial function. Basic Res Cardiol 104:113-119
89. Shiva S, Brookes PS, Patel RP, Anderson PG, Darley-Usmar VM (2001) Nitric oxide partitioning into mitochondrial membranes and the control of respiration at cytochrome c oxidase. Proc Natl Acad Sci USA 98:7212-7217
90. Shiva S, Oh JY, Landar AL, Ulasova E, Venkatraman A, Bailey SM, Darley-Usmar VM (2005) Nitroxia: the pathological consequence of dysfunction in the nitric oxide-cytochrome c oxidase signaling pathway. Free Radic Biol Med 38:297-306
91. Shiva S et al (2007a) Nitrite augments tolerance to ischemia/reperfusion injury viathe modulation of mitochondrial electron transfer. J Exp Med 204:2089-2102
92. Shiva S et al (2007b) Deoxymyoglobin is anitrite reductase that generates nitric oxide and regulates mitochondrial respiration. Circ Res 100:654-661
93. Stamler JS et al (1992) Nitric oxide circulates in mammalian plasmaprimarily as an S-nitroso adduct of serum albumin. Proc Natl Acad Sci USA 89:7674-7677
94. Stubauer G, Giuffrè A, Brunori M, Sarti P (1998) Cytochrome c oxidase does not catalyze the anaerobic reduction of NO. Biochem Biophys Res Commun 245:459-465
95. Stuehr DJ, Nathan CF (1989) Nitric oxide. A macrophage product responsible for cytostasis and respiratory inhibition in tumor target cells. J Exp Med 169:1543-1555
96. Thomas DD, Liu X, Kantrow SP, Lancaster JR Jr (2001) The biological lifetime of nitric oxide: implications for the perivascular dynamics of NO and O2. Proc Natl Acad Sci USA 98:355-360
97. Torres J, Darley-Usmar V, Wilson MT (1995) Inhibition of cytochrome c oxidase in turnover by nitric oxide: mechanism and implications for control of respiration. Biochem J 312:169-173
98. Torres J, Cooper CE, Wilson MT (1998) A common mechanism for the interaction of nitric oxide with the oxidized binuclear centre and oxygen intermediates of cytochrome c oxidase. J Biol Chem 273:8756-8766
99. Torres J, Sharpe MA, Rosquist A, Cooper CE, Wilson MT (2000) Cytochrome c oxidase rapidly metabolises nitric oxide to nitrite. FEBS Lett 475:263-266
100. Trimmer BA, Aprille JR, Dudzinski DM, Lagace CJ, Lewis SM, Michel T, Qazi S, Zayas RM (2001) Nitric oxide and the control of firefly flashing. Science 292:2486-2488
101. Vinogradov AD (1998) Catalytic properties of the mitochondrial NADH-ubiquinone oxidoreductase (complex I) and the pseudo-reversible active/inactive enzyme transition. Biochim Biophys Acta 1364:169-185
102. Webb A, Bond R, McLean P, Uppal R, Benjamin N, Ahluwalia A (2004) Reduction of nitrite to nitric oxide during ischemiaprotects against myocardial ischemia-reperfusion damage. Proc Natl Acad Sci USA 101:13683-13688
103. Weitzberg E, Lundberg JO (1998) Nonenzymatic nitric oxide production in humans. Nitric Oxide 2:1-7
104. Weng L, Baker GM (1991) Reaction of hydrogen peroxide with the rapid form of resting cytochrome oxidase. Biochemistry 30:5727-5733
105. Xie YW, Shen W, Zhao G, Xu X, Wolin MS, Hintze TH (1996) Role of endothelium-derived nitric oxide in the modulation of canine myocardial mitochondrial respiration in vitro. Implications for the development of heart failure. Circ Res 79:381-387
106. Zhao G, Bernstein RD, Hintze TH (1999) Nitric oxide and oxygen utilization: exercise, heart failure and diabetes. Coron Artery Dis 10:315-320
107. Zweier JL, Samouilov A, Kuppusamy P (1999) Non-enzymatic nitric oxide synthesis in biological systems. Biochim Biophys Acta 1411:250-262