Regulation of mitochondrial function and energetics by reactive nitrogen oxides

Free Radical Biology and Medicine

Volumn 53, Issue 10, 2012, Pages 1919-1928

  Larsen, Filip J ^a   Schiffer, Tomas A ^a   Weitzberg, Eddie ^a   Lundberg, Jon O ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Exercise; Free radicals; Ischemia reperfusion; Nitrate; Nitric oxide; Nitrite; Skeletal muscle

Indexed keywords

CARDIOLIPIN; CYTOCHROME C OXIDASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; MITOGEN ACTIVATED PROTEIN KINASE; NITRATE; NITRIC OXIDE; NITRITE; NITROGEN OXIDE; OXYGEN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TOLL LIKE RECEPTOR 4; TRIACYLGLYCEROL;

ACTIN MYOSIN INTERACTION; BICYCLE ERGOMETER; CELL PROTECTION; DIETARY INTAKE; ENZYME ACTIVITY; EXERCISE; FATIGUE; HUMAN; INTRACELLULAR SIGNALING; METABOLIC REGULATION; MITOCHONDRION; MUSCLE CELL; NITRATION; NONHUMAN; OUTER MEMBRANE; OXYGEN CONSUMPTION; PRIORITY JOURNAL; REPERFUSION INJURY; REVIEW; VASODILATATION;

ANIMALS; ELECTRON TRANSPORT COMPLEX IV; EXERCISE; HUMANS; MITOCHONDRIA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXIDATION-REDUCTION; OXYGEN; REACTIVE NITROGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84867381479     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2012.08.580     Document Type: Review

References (120)

1. J.M. Fukuto Small molecule signaling agents: the integrated chemistry and biochemistry of nitrogen oxides, oxides of carbon, dioxygen, hydrogen sulfide, and their derived species Chem. Res. Toxicol. 25 2012 769 793
2. S. Moncada, and E.A. Higgs Nitric oxide and the vascular endothelium Handb. Exp. Pharmacol 176 Pt 1 2006 213 254
3. G.C. Brown, and C.E. Cooper Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase FEBS Lett 356 1994 295 298
4. J. MacMicking, Q.W. Xie, and C. Nathan Nitric oxide and macrophage function Annu. Rev. Immunol. 15 1997 323 350
5. D.D. Rees, R.M. Palmer, and S. Moncada Role of endothelium-derived nitric oxide in the regulation of blood pressure Proc. Natl. Acad. Sci. USA 86 1989 3375 3378
6. 2 consumption and ATP synthesis in guinea pig hearts Am. J. Physiol. Heart Circ. Physiol 281 2001 H838 H846
7. M.W. Cleeter Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide: implications for neurodegenerative diseases FEBS Lett 345 1994 50 54
8. J.P. Bolanos Nitric oxide-mediated inhibition of the mitochondrial respiratory chain in cultured astrocytes J. Neurochem 63 1994 910 916
9. M.W. Foster, D.T. Hess, and J.S. Stamler Protein S-nitrosylation in health and disease: a current perspective Trends Mol. Med. 15 2009 391 404
10. B.G. Hill What part of NO don't you understand? Some answers to the cardinal questions in nitric oxide biology J. Biol. Chem 285 2010 19699 19704
11. J.O. Lundberg Nitrate, bacteria and human health Nat. Rev. Microbiol. 2 2004 593 602
12. A.R. Butler, and M. Feelisch Therapeutic uses of inorganic nitrite and nitrate: from the past to the future Circulation 117 2008 2151 2159
13. J.D. Roberts Jr. Inhaled nitric oxide and persistent pulmonary hypertension of the newborn. The Inhaled Nitric Oxide Study Group N. Engl. J. Med. 336 1997 605 610
14. K. Alving, E. Weitzberg, and J.M. Lundberg Increased amount of nitric oxide in exhaled air of asthmatics Eur. Respir. J. 6 1993 1368 1370
15. R.A. Dweik An official ATS clinical practice guideline: interpretation of exhaled nitric oxide levels (FENO) for clinical applications Am. J. Respir. Crit. Care Med. 184 2011 602 615
16. W. Shen Role of nitric oxide in the regulation of oxygen consumption in conscious dogs Circ. Res 75 1994 1086 1095
17. Y. Ishibashi ATP-sensitive Kchannels, adenosine, and nitric oxide-mediated mechanisms account for coronary vasodilation during exercise Circ. Res. 82 1998 346 359
18. A.C. Lacerda Evidence that brain nitric oxide inhibition increases metabolic cost of exercise, reducing running performance in rats Neurosci. Lett 393 2006 260 263
19. I. Heinonen Skeletal muscle blood flow and oxygen uptake at rest and during exercise in humans: a PET study with nitric oxide and cyclooxygenase inhibition Am. J. Physiol. Heart Circ. Physiol 300 2011 H1510 15107
20. K.E. Loke Nitric oxide modulates mitochondrial respiration in failing human heart Circulation 100 1999 1291 1297
21. F.A. Recchia Nitric oxide controls cardiac substrate utilization in the conscious dog Cardiovasc. Res. 44 1999 325 332
22. F. Antunes, A. Boveris, and E. Cadenas On the mechanism and biology of cytochrome oxidase inhibition by nitric oxide Proc. Natl. Acad. Sci. USA 101 2004 16774 16779
23. E. Gnaiger Mitochondrial respiration in the low oxygen environment of the cell: effect of ADP on oxygen kinetics Biochim. Biophys. Acta 1365 1998 249 254
24. J.J. Poderoso Nitric oxide inhibits electron transfer and increases superoxide radical production in rat heart mitochondria and submitochondrial particles Arch. Biochem. Biophys 328 1996 85 92
25. R. Rossignol Mitochondrial threshold effects Biochem. J. 370 Pt 3 2003 751 762
26. D.D. Thomas Hypoxic inducible factor 1alpha, extracellular signal-regulated kinase, and p53 are regulated by distinct threshold concentrations of nitric oxide Proc. Natl. Acad. Sci. USA 101 2004 8894 8899
27. A. Boveris Regulation of mitochondrial respiration by oxygen and nitric oxide Ann. N. Y. Acad. Sci 899 2000 121 135
28. P.A. Mole Myoglobin desaturation with exercise intensity in human gastrocnemius muscle Am. J. Physiol. 277 1 Pt 2 1999 R173 180
29. 2 consumption in trained human skeletal muscle J. Appl. Physiol 87 1999 325 331
30. P. Clerc Nitric oxide increases oxidative phosphorylation efficiency J. Bioenerg. Biomembr. 39 2007 158 166
31. M.P. Murphy, and M.D. Brand Variable stoichiometry of proton pumping by the mitochondrial respiratory chain Nature 329 1987 170 172
32. - stoichiometry of mitochondrial cytochrome complexes reconstituted in liposomes: rate-dependent changes of the stoichiometry in the cytochrome c oxidase vesicles FEBS Lett 288 1991 179 182
33. B. Kadenbach Mitochondrial energy metabolism is regulated via nuclear-coded subunits of cytochrome c oxidase Free Radic. Biol. Med 29 2000 211 221
34. J.D. Erusalimsky, and S. Moncada Nitric oxide and mitochondrial signaling: from physiology to pathophysiology Arterioscler. Thromb. Vasc. Biol. 27 2007 2524 2531
35. J.O. Lundberg, E. Weitzberg, and M.T. Gladwin. The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics Nat. Rev. Drug Discovery 7 2008 156 167
36. J.O. Lundberg Nitrate and nitrite in biology, nutrition and therapeutics Nat. Chem. Biol. 5 2009 865 869
37. N.G. Hord, Y. Tang, and N.S. Bryan Food sources of nitrates and nitrites: the physiologic context for potential health benefits Am. J. Clin. Nutr. 90 2009 1 10
38. B. Spiegelhalder, G. Eisenbrand, and R. Preussmann Influence of dietary nitrate on nitrite content of human saliva: possible relevance to in vivo formation of N-nitroso compounds Food Cosmet. Toxicol 14 1976 545 548
39. J.O. Lundberg, and M. Govoni Inorganic nitrate is a possible source for systemic generation of nitric oxide Free Radic. Biol. Med. 37 2004 395 400
40. C. Duncan Chemical generation of nitric oxide in the mouth from the enterosalivary circulation of dietary nitrate Nat. Med 1 1995 546 551
41. J.O. Lundberg Intragastric nitric oxide production in humans: measurements in expelled air Gut 35 1994 1543 1546
42. N. Benjamin Stomach NO synthesis Nature 368 1994 502
43. A.J. Webb Acute blood pressure lowering, vasoprotective, and antiplatelet properties of dietary nitrate via bioconversion to nitrite Hypertension 51 2008 784 790
44. K. Cosby Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation Nat. Med 9 2003 1498 1505
45. V.P. Reutov, and E.G. Sorokina NO-synthase and nitrite-reductase components of nitric oxide cycle Biochemistry (Moscow) 63 1998 874 884
46. E. Nagababu Active nitric oxide produced in the red cell under hypoxic conditions by deoxyhemoglobin-mediated nitrite reduction J. Biol. Chem 278 2003 46349 46356
47. S. Shiva Deoxymyoglobin is a nitrite reductase that generates nitric oxide and regulates mitochondrial respiration Circ. Res 100 2007 654 661
48. M.G. Petersen, S. Dewilde, and A. Fago Reactions of ferrous neuroglobin and cytoglobin with nitrite under anaerobic conditions J. Inorg. Biochem. 102 2008 1777 1782
49. P.R. Castello Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: implications for oxygen sensing and hypoxic signaling in eukaryotes Cell Metab 3 2006 277 287
50. A.J. Webb Mechanisms underlying erythrocyte and endothelial nitrite reduction to nitric oxide in hypoxia: role for xanthine oxidoreductase and endothelial nitric oxide synthase Circ. Res 103 2008 957 964
51. H. Li Nitric oxide production from nitrite occurs primarily in tissues not in the blood: critical role of xanthine oxidase and aldehyde oxidase J. Biol. Chem 283 2008 17855 17863
52. R. Aamand Generation of nitric oxide from nitrite by carbonic anhydrase: a possible link between metabolic activity and vasodilation Am. J. Physiol. Heart Circ. Physiol 297 2009 H2068 H2074
53. S. Carlsson Effects of pH, nitrite, and ascorbic acid on nonenzymatic nitric oxide generation and bacterial growth in urine Nitric Oxide 5 2001 580 586
54. B. Gago Red wine-dependent reduction of nitrite to nitric oxide in the stomach Free Radic. Biol. Med 43 2007 1233 1242
55. E.A. Jansson A mammalian functional nitrate reductase that regulates nitrite and nitric oxide homeostasis Nat. Chem. Biol. 4 2008 411 417
56. D.J. Stuehr Update on mechanism and catalytic regulation in the NO synthases J. Biol. Chem. 279 2004 36167 36170
57. E.E. van Faassen Nitrite as regulator of hypoxic signaling in mammalian physiology Med. Res. Rev. 29 2009 683 741
58. C.L. Walters, and A.M. Taylor. The reduction of nitrite by skeletal-muscle mitochondria Biochim. Biophys. Acta 96 1965 522 524
59. S. Basu Nitrite reductase activity of cytochrome c J. Biol. Chem. 283 2008 32590 32597
60. A.V. Kozlov, K. Staniek, and H. Nohl Nitrite reductase activity is a novel function of mammalian mitochondria FEBS Lett 454 1999 127 130
61. L. Castro Cytochrome c: a catalyst and target of nitrite-hydrogen peroxide-dependent protein nitration Arch. Biochem. Biophys. 421 2004 99 107
62. A.M. Cassina Cytochrome c nitration by peroxynitrite J. Biol. Chem. 275 2000 21409 21415
63. N.S. Bryan Cellular targets and mechanisms of nitros(yl)ation: an insight into their nature and kinetics in vivo Proc. Natl. Acad. Sci. USA 101 2004 4308 43013
64. H.K. Eltzschig, and T. Eckle Ischemia and reperfusion - from mechanism to translation Nat. Med 17 2011 1391 1401
65. K.A. Powers Oxidative stress generated by hemorrhagic shock recruits Toll-like receptor 4 to the plasma membrane in macrophages J. Exp. Med 203 2006 1951 1961
66. G.Y. Chen, and G. Nunez Sterile inflammation: sensing and reacting to damage Nat. Rev. Immunol. 10 2010 826 837
67. P. Weerateerangkul, S. Chattipakorn, and N. Chattipakorn Roles of the nitric oxide signaling pathway in cardiac ischemic preconditioning against myocardial ischemia-reperfusion injury Med. Sci. Monit 17 2011 RA44 RA52
68. J.D. Lang Jr. Inhaled NO accelerates restoration of liver function in adults following orthotopic liver transplantation J. Clin. Invest. 117 2007 2583 2591
69. D. Murillo Nitrite as a mediator of ischemic preconditioning and cytoprotection Nitric Oxide 25 2011 70 80
70. S. Shiva Nitrite augments tolerance to ischemia/reperfusion injury via the modulation of mitochondrial electron transfer J. Exp. Med. 204 2007 2089 2102
71. S.G. Zhu Dietary nitrate supplementation protects against doxorubicin-induced cardiomyopathy by improving mitochondrial function J. Am. Coll. Cardiol. 57 2011 2181 2189
72. V. Borutaite, A. Budriunaite, and G.C. Brown 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
73. G.J. Grover Excessive ATP hydrolysis in ischemic myocardium by mitochondrial F1F0-ATPase: effect of selective pharmacological inhibition of mitochondrial ATPase hydrolase activity Am. J. Physiol. Heart Circ. Physiol 287 2004 H1747 H1755
74. B. Liu Proteomic analysis of protein tyrosine nitration after ischemia reperfusion injury: mitochondria as the major target Biochim. Biophys. Acta 1794 2009 476 485
75. J. Sun Preconditioning results in S-nitrosylation of proteins involved in regulation of mitochondrial energetics and calcium transport Circ. Res 101 2007 1155 1163
76. R.M. Bell, H.L. Maddock, and D.M. Yellon. The cardioprotective and mitochondrial depolarising properties of exogenous nitric oxide in mouse heart Cardiovasc. Res. 57 2003 405 415
77. A.D. Costa Protein kinase G transmits the cardioprotective signal from cytosol to mitochondria Circ. Res 97 2005 329 336
78. G. Paradies Reactive oxygen species affect mitochondrial electron transport complex I activity through oxidative cardiolipin damage Gene 286 2002 135 141
79. I.I. Vlasova Nitric oxide inhibits peroxidase activity of cytochrome c·cardiolipin complex and blocks cardiolipin oxidation J. Biol. Chem 281 2006 14554 14562
80. M. Garcia Fernandez Early changes in intramitochondrial cardiolipin distribution during apoptosis Cell Growth Differ 13 2002 449 455
81. C. Jadert Decreased leukocyte recruitment by inorganic nitrate and nitrite in microvascular inflammation and NSAID-induced intestinal injury Free Radic. Biol. Med 52 2011 683 692
82. F.J. Larsen Effects of dietary nitrate on oxygen cost during exercise Acta Physiol. (Oxford) 191 2007 59 66
83. F.J. Larsen Dietary inorganic nitrate improves mitochondrial efficiency in humans Cell Metab. 13 2011 149 159
84. J.P. Little Skeletal muscle and beyond: the role of exercise as a mediator of systemic mitochondrial biogenesis Appl. Physiol. Nutr. Metab. 36 2011 598 607
85. R.C. Scarpulla Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network Biochim. Biophys. Acta 1813 2011 1269 1278
86. T.R. Koves Peroxisome proliferator-activated receptor-gamma co-activator 1alpha-mediated metabolic remodeling of skeletal myocytes mimics exercise training and reverses lipid-induced mitochondrial inefficiency J. Biol. Chem 280 2005 33588 33598
87. J.O. Holloszy, and E.F. Coyle Adaptations of skeletal muscle to endurance exercise and their metabolic consequences J. Appl. Physiol. 56 1984 831 838
88. M. Tonkonogi Mitochondrial function and antioxidative defence in human muscle: effects of endurance training and oxidative stress J. Physiol 528 Pt 2 2000 379 388
89. D. Pesta Similar qualitative and quantitative changes of mitochondrial respiration following strength and endurance training in normoxia and hypoxia in sedentary humans Am. J. Physiol. Regul. Integr. Comp. Physiol 301 2011 R1078 R1087
90. M. Tonkonogi Mitochondrial function in human skeletal muscle is not impaired by high intensity exercise Pflugers Arch 437 1999 562 568
91. D.E. Befroy Increased substrate oxidation and mitochondrial uncoupling in skeletal muscle of endurance-trained individuals Proc. Natl. Acad. Sci. USA 105 2008 16701 16706
92. L. Moseley No differences in cycling efficiency between world-class and recreational cyclists Int. J. Sports Med 25 2004 374 379
93. 2 cost of low-intensity exercise and enhances tolerance to high-intensity exercise in humans J. Appl. Physiol 107 2009 1144 1155
94. F.J. Larsen Dietary nitrate reduces maximal oxygen consumption while maintaining work performance in maximal exercise Free Radic. Biol. Med 48 2010 342 347
95. S.J. Bailey Dietary nitrate supplementation enhances muscle contractile efficiency during knee-extensor exercise in humans J. Appl. Physiol 109 2010 135 148
96. A. Vanhatalo Acute and chronic effects of dietary nitrate supplementation on blood pressure and the physiological responses to moderate-intensity and incremental exercise Am. J. Physiol. Regul. Integr. Comp. Physiol 299 2010 R1121 R1131
97. 2 cost of walking and running: a placebo-controlled study J. Appl. Physiol 110 2011 591 600
98. 2peak in endurance athletes Med. Sci. Sports Exerc 43 2011 1979 1986
99. A.A. Kenjale Dietary nitrate supplementation enhances exercise performance in peripheral arterial disease J. Appl. Physiol. 110 2011 1582 1591
100. K.E. Lansley Acute dietary nitrate supplementation improves cycling time trial performance Med. Sci. Sports Exerc. 43 2011 1125 1131
101. A. Vanhatalo Dietary nitrate reduces muscle metabolic perturbation and improves exercise tolerance in hypoxia J. Physiol 589 Pt 22 2011 5517 5528
102. N.M. Cermak, M.J. Gibala, and L.J. van Loon Nitrate supplementation's improvement of 10-km time-trial performance in trained cyclists Int. J. Sport Nutr. Exerc. Metab. 22 2012 64 71
103. L.J. Toime, and M.D. Brand Uncoupling protein-3 lowers reactive oxygen species production in isolated mitochondria Free Radic. Biol. Med. 49 2010 606 611
104. G. Gouspillou Alteration of mitochondrial oxidative phosphorylation in aged skeletal muscle involves modification of adenine nucleotide translocator Biochim. Biophys. Acta 1797 2010 143 151
105. P.A. Mole Impact of energy intake and exercise on resting metabolic rate Sports Med 10 1990 72 87
106. C.J. Gore Live high: train low increases muscle buffer capacity and submaximal cycling efficiency Acta Physiol. Scand. 173 2001 275 286
107. C. Marconi Economy of locomotion in high-altitude Tibetan migrants exposed to normoxia J. Physiol 569 Pt 2 2005 667 675
108. P.W. Hochachka Metabolic and work efficiencies during exercise in Andean natives J. Appl. Physiol. 70 1991 1720 1730
109. D.Z. Levett Acclimatization of skeletal muscle mitochondria to high-altitude hypoxia during an ascent of Everest FASEB J. 26 2012 1431 1441
110. J.W. Kim HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia Cell Metab 3 2006 177 185
111. F.J. Larsen Mitochondrial oxygen affinity predicts basal metabolic rate in humans FASEB J. 25 2011 2843 2852
112. S. Arnold The power of life - cytochrome c oxidase takes center stage in metabolic control, cell signalling and survival Mitochondrion 12 2011 46 56
113. M.H. Ward Workgroup report: drinking-water nitrate and health - recent findings and research needs Environ. Health Perspect. 113 2005 1607 1614
114. T.T. Mensinga, G.J. Speijers, and J. Meulenbelt Health implications of exposure to environmental nitrogenous compounds Toxicol. Rev 22 2003 41 51
115. C. Dezfulian Role of the anion nitrite in ischemia-reperfusion cytoprotection and therapeutics Cardiovasc. Res 75 2007 327 338
116. A. Dejam Nitrite infusion in humans and nonhuman primates: endocrine effects, pharmacokinetics, and tolerance formation Circulation 116 2007 1821 1831
117. M. Carlstrom Dietary nitrate attenuates oxidative stress, prevents cardiac and renal injuries, and reduces blood pressure in salt-induced hypertension Cardiovasc. Res 89 2011 574 585
118. L. Wang Normoxic cyclic GMP-independent oxidative signaling by nitrite enhances airway epithelial cell proliferation and wound healing Nitric Oxide 26 2012 203 210
119. B.S. Rocha Intragastric nitration by dietary nitrite: implications for modulation of protein and lipid signaling Free Radic. Biol. Med. 52 2012 693 698
120. J.F. Horowitz, L.S. Sidossis, and E.F. Coyle High efficiency of type I muscle fibers improves performance Int. J. Sports Med 15 1994 152 157