Hypoxia accelerates nitric oxide-dependent inhibition of mitochondrial complex I in activated macrophages

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 288, Issue 2 57-2, 2005, Pages

  Frost, Matthew T ^a   Wang, Qi ^a   Moncada, Salvador ^a   Singer, Mervyn ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Nitration; Oxygen; Respiration; S nitrosylation; Sepsis

Indexed keywords

ENDOTOXIN; GAMMA INTERFERON; GLUTATHIONE ETHYL ESTER; N5 (1 IMINOETHYL)ORNITHINE; NITRIC OXIDE; OXYGEN; PEROXYNITRITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); TYROSINE;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL CULTURE; CELL FRACTIONATION; CELL VIABILITY; CONTROLLED STUDY; DRUG INHIBITION; DRUG MECHANISM; HYPOXIA; MACROPHAGE; MITOCHONDRIAL RESPIRATION; MOUSE; NITRATION; NITROSYLATION; NONHUMAN; OXYGEN CONSUMPTION; PATHOPHYSIOLOGY; PRIORITY JOURNAL;

ANIMALS; CELL HYPOXIA; CELL LINE; ELECTRON TRANSPORT COMPLEX I; MACROPHAGE ACTIVATION; MACROPHAGES; MITOCHONDRIA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXYGEN; TIME FACTORS;

EID: 12344335535     PISSN: 03636119     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpregu.00504.2004     Document Type: Article

References (46)

1. Abu-Soud HM, Ichimori K, Nakazawa H, and Stuehr DJ. Regulation of inducible nitric oxide synthase by self-generated NO. Biochemistry 40: 6876-6881, 2001.
2. Alvarez S, Valdez LB, Tamara Zaobornyj T, and Boveris A. Oxygen dependence of mitochondrial nitric oxide synthase activity. Biochem Biophys Res Commun 305: 771-775, 2003.
3. Angele MK, Schwacha MG, Smail N, Catania RA, Ayala A, Cioffi WG, and Chaudry IH. Hypoxemia in the absence of blood loss upregulates iNOS expression and activity in macrophages. Am J Physiol Cell Physiol 276: C285-C290, 1999.
4. Assreuy J, Cunha FQ, Liew FY, and Moncada S. Feedback inhibition of nitric oxide synthase activity by nitric oxide. Br J Pharmacol 108: 833-837, 1993.
5. Aulak KS, Koeck T, Crabb JW, and Stuehr DJ. Dynamics of protein nitration in cells and mitochondria. Am J Physiol Heart Circ Physiol 286: H30-H38, 2004.
6. Barreiro E, Comtois AS, Gea J, Laubach VE, and Hussain SN. Protein tyrosine nitration in the ventilatory muscles: role of nitric oxide synthases. Am J Respir Cell Mol Biol 26: 438-446, 2002.
7. Beltran B, Orsi A, Clementi E, and Moncada S. Oxidative stress and S-nitrosylation of proteins in cells. Br J Pharmacol 129: 953-960, 2000.
8. Bolanos JP, Heales SJ, Land JM, and Clark JB. Effect of peroxynitrite on the mitochondrial respiratory chain: differential susceptibility of neurones and astrocytes in primary culture. J Neurochem 64: 1965-1972, 1995.
9. Borutaite V, Budriunaite A, and Brown GC. 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, 2000.
10. Brealey D, Brand M, Hargreaves I, Heales S, Land J, Smolenski R, Davies NA, Cooper CE, and Singer M. Association between mitochondrial dysfunction and severity and outcome of septic shock. Lancet 360: 219-223, 2002.
11. Brealey D and Singer M. Mitochondrial dysfunction in sepsis. Curr Infect Dis Rep 5: 365-371, 2003.
12. Brealey D, Karyampudi S, Jacques T, Noveilli M, Stidwill R, Taylor V, Smolenski R, and Singer M. Mitochondrial dysfunction in a long-term rodent model of sepsis and organ failure. Am J Physiol Regul Integr Comp Physiol 286: R491-R497, 2004.
13. Brennan ML, Wu W, Fu X, Shen Z, Song W, Frost H, Vadseth C, Narine L, Lenkiewicz E, Borchers MT, Lusis AJ, Lee JJ, Lee NA, Abu-Soud HM, Ischiropoulos H, and Hazen SL. A tale of two controversies: defining both the role of peroxidases in nitrotyrosine formation in vivo using eosinophil peroxidase and myeloperoxidase-deficient mice, and the nature of peroxidase-generated reactive nitrogen species. J Biol Chem 277: 17415-17427, 2002.
14. Castro L, Eiserich JP, Sweeney S, Radi R, and Freeman BA. Cytochrome c: a catalyst and target of nitrite-hydrogen peroxide-dependent protein nitration. Arch Biochem Biophys 421: 99-107, 2004.
15. Clementi E, Brown GC, Feelisch M, and 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 USA 95: 7631-7636, 1998.
16. Connelly L, Palacios-Callender M, Ameixa C, Moncada S, and Hobbs AJ. Biphasic regulation of NF-κB activity underlies the pro- and anti-inflammatory actions of nitric oxide. J Immunol 166: 3873-3881, 2001.
17. m for oxygen of mitochondrial cytochrome oxidase: in vitro and in vivo studies. Biochim Biophys Acta 1607: 27-34, 2003.
18. Dada LA, Chandel NS, Ridge KM, Pedemonte C, Bertorello AM, and Sznajder JI. Hypoxia-induced endocytosis of Na,K-ATPase in alveolar epithelial cells is mediated by mitochondrial reactive oxygen species and PKC-zeta. J Clin Invest 111: 1057-1064, 2003.
19. Daniliuc S, Bitterman H, Rahat MA, Kinarty A, Rosenzweig D, Lahat N, and Nitza L. Hypoxia inactivates inducible nitric oxide synthase in mouse macrophages by disrupting its interaction with α-actinin 4. J Immunol 171: 3225-3232, 2003.
20. Elfering SL, Haynes VL, Traaseth NJ, Ettl A, and Giulivi C. Aspects, mechanism, and biological relevance of mitochondrial protein nitration sustained by mitochondrial nitric oxide synthase. Am J Physiol Heart Circ Physiol 286: H22-H29, 2004.
21. Frost MT, Halliwell B, and Moore KP. Analysis of free and protein-bound nitrotyrosine in human plasma by a gas chromatography/mass spectrometry method that avoids nitration artifacts. Biochem J 345: 453-458, 2000.
22. Gow AJ, Duran D, Malcolm S, and Ischiropoulos H. Effects of peroxynitrite-induced protein modifications on tyrosine phosphorylation and degradation. FEBS Lett 385: 63-66, 1996.
23. Griscavage JM, Hobbs AJ, and Ignarro LJ. Negative modulation of nitric oxide synthase by nitric oxide and nitroso compounds. Adv Pharmacol 34: 215-34, 1995.
24. Hollis VS, Palacios-Callender M, Springett RJ, Delpy DT, and Moncada S. Monitoring cytochrome redox changes in the mitochondria of intact cells using multi-wavelength visible light spectroscopy. Biochim Biophys Acta 1607: 191-202, 2003.
25. Ischiropoulos H. Biological tyrosine nitration: a pathophysiological function of nitric oxide and reactive oxygen species. Arch Biochem Biophys 356: 1-11, 1998.
26. Ischiropoulos H. Biological selectivity and functional aspects of protein tyrosine nitration. Biochem Biophys Res Commun 305: 776-783, 2003.
27. Kamisaki Y, Wada K, Bian K, Balabanli B, Davis K, Martin E, Behbod F, Lee YC, and Murad F. An activity in rat tissues that modifies nitrotyrosine- containing proteins. Proc Natl Acad Sci USA 95: 11584-11589, 1998.
28. Lee VY, McClintock DS, Santore MT, Budinger GR, and Chandel NS. Hypoxia sensitizes cells to nitric oxide-induced apoptosis. J Biol Chem 277: 16067-16074, 2002.
29. Li C, Jackson RM. Reactive species mechanisms of cellular hypoxia-reoxygenation injury. Am J Physiol Cell Physiol 282: C227-C241, 2002.
30. Liu L, Yan Y, Zeng M, Zhang J, Hanes MA, Ahearn G, McMahon TJ, Dickfeld T, Marshall HE, Que LG, and Stamler JS. Essential roles of S-nitrosothiols in vascular homeostasis and endotoxic shock. Cell 116: 617-628, 2004.
31. Lopez A, Lorente JA, Steingrub J, Bakker J, McLuckie A, Willatts S, Brockway M, Anzueto A, Holzapfel L, Breen D, Silverman MS, Takala J, Donaldson J, Arneson C, Grove G, Grossman S, and Grover R. Multiple-center, randomized, placebo-controlled, double-blind study of the nitric oxide synthase inhibitor 546C88: effect on survival in patients with septic shock. Crit Care Med 32: 21-30, 2004.
32. McCormick CC, Li WP, and Calero M. Oxygen tension limits nitric oxide synthesis by activated macrophages. Biochem J 350: 709-716, 2000.
33. Melillo G, Taylor LS, Brooks A, Cox GW, and Varesio L. Regulation of inducible nitric oxide synthase expression in IFN-γ-treated murine macrophages cultured under hypoxic conditions. J Immunol 157: 2638-2644, 1996.
34. Monzani E, Roncone R, Galliano M, Koppenol WH, and Casella L. Mechanistic insight into the peroxidase-catalyzed nitration of tyrosine derivatives by nitrite and hydrogen peroxide. Eur J Biochem 271: 895-906, 2004.
35. Moss DW, Wei X, Liew FY, Moncada S, and Charles IG. Enzymatic characterisation of recombinant murine inducible nitric oxide synthase. Eur J Pharmacol 289: 41-48, 1995.
36. Moss DW and Bates TE. Activation of murine microglial cell lines by lipopolysaccharide and interferon-γ causes NO-mediated decreases in mitochondrial and cellular function. Eur J Neurosci 13: 529-538, 2001.
37. Murray J, Taylor SW, Zhang B, Ghosh SS, and Capaldi RA. Oxidative damage to mitochondrial complex I due to peroxynitrite: identification of reactive tyrosines by mass spectrometry. J Biol Chem 278: 37223-37230, 2003.
38. Orsi A, Rees DD, Beltran B, and Moncada S. Physiological regulation and pathological inhibition of tissue respiration by nitric oxide in vivo (Abstract). Biol Nitric Oxide 7: 35, 2004.
39. Palacios-Callender M, Quintero M, Hollis VS, Springett RJ, and Moncada S. 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, 2004.
40. Radi R, Cassina A, Hodara R, Quijano C, and Castro L. Peroxynitrite reactions and formation in mitochondria. Free Radic Biol Med 33: 1451-1464, 2002.
41. Ragan CI, Wilson MT, Darley-Usmar VM, and Lowe PN. In: Mitochondria: A Practical Approach, edited by Darley-Usmar VM, Rickwood D, and Wilson MT. Oxford, UK: IRL, p. 79-112, 1997.
42. Rickwood D, Ford T, and Steensgaard S. In: Centrifugation Essential Data: Centrifugation Conditions for Various Samples, edited by Rickwood D, Hames BD. Chichester, UK: Wiley, 1994, p. 24-27.
43. Riobo NA, Clementi E, Melani M, Boveris A, Cadenas E, Moncada S, and Poderoso JJ. Nitric oxide inhibits mitochondrial NADH:ubiquinone reductase activity through peroxynitrite formation. Biochem J 359: 139-145, 2001.
44. Rivers E, Nguyen B, Havstad S, Ressler J, Muzzin A, Knoblich B, Peterson E, and Tomlanovich M. Early Goal-Directed Therapy Collaborative Group. Early goal-directed therapy in the treatment of severe sepsis and septic shock. N Engl J Med 345: 1368-1377, 2001.
45. Schumacker PT. Current paradigms in cellular oxygen sensing. Adv Exp Med Biol 543: 57-71, 2003.
46. Singer M, De Santis V, Vitale D, and Jeffcoate W. Multi-organ failure is an adaptive, endocrine-mediated, metabolic response to overwhelming systemic inflammation. Lancet 364: 545-548, 2004.