Am J Physiol Cell Physiol AJP: Regulatory, Integrative and Comparative Physiology
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Am J Physiol Cell Physiol 271: C1424-C1437, 1996;
0363-6143/96 $5.00
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AJP - Cell Physiology, Vol 271, Issue 5 C1424-C1437, Copyright © 1996 by American Physiological Society

ARTICLES

Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly

J. S. Beckman and W. H. Koppenol
Department of Anesthesiology, University of Alabama at Birmingham 35233, USA.

Nitric oxide contrasts with most intercellular messengers because it diffuses rapidly and isotropically through most tissues with little reaction but cannot be transported through the vasculature due to rapid destruction by oxyhemoglobin. The rapid diffusion of nitric oxide between cells allows it to locally integrate the responses of blood vessels to turbulence, modulate synaptic plasticity in neurons, and control the oscillatory behavior of neuronal networks. Nitric oxide is not necessarily short lived and is intrinsically no more reactive than oxygen. The reactivity of nitric oxide per se has been greatly overestimated in vitro because no drain is provided to remove nitric oxide. Nitric oxide persists in solution for several minutes in micromolar concentrations before it reacts with oxygen to form much stronger oxidants like nitrogen dioxide. Nitric oxide is removed within seconds in vivo by diffusion over 100 microns through tissues to enter red blood cells and react with oxyhemoglobin. The direct toxicity of nitric oxide is modest but is greatly enhanced by reacting with superoxide to form peroxynitrite (ONOO-). Nitric oxide is the only biological molecule produced in high enough concentrations to out-compete superoxide dismutase for superoxide. Peroxynitrite reacts relatively slowly with most biological molecules, making peroxynitrite a selective oxidant. Peroxynitrite modifies tyrosine in proteins to create nitrotyrosines, leaving a footprint detectable in vivo. Nitration of structural proteins, including neurofilaments and actin, can disrupt filament assembly with major pathological consequences. Antibodies to nitrotyrosine have revealed nitration in human atherosclerosis, myocardial ischemia, septic and distressed lung, inflammatory bowel disease, and amyotrophic lateral sclerosis.


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S. Lancel, S. Tissier, S. Mordon, X. Marechal, F. Depontieu, A. Scherpereel, C. Chopin, and R. Neviere
Peroxynitrite decomposition catalysts prevent myocardial dysfunction and inflammation in endotoxemic rats
J. Am. Coll. Cardiol., June 16, 2004; 43(12): 2348 - 2358.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
R. Johansson and K. Persson
Phenotypic modulation of cultured bladder smooth muscle cells and the expression of inducible nitric oxide synthase
Am J Physiol Regulatory Integrative Comp Physiol, April 1, 2004; 286(4): R642 - R648.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
M. M. Tarpey, D. A. Wink, and M. B. Grisham
Methods for detection of reactive metabolites of oxygen and nitrogen: in vitro and in vivo considerations
Am J Physiol Regulatory Integrative Comp Physiol, March 1, 2004; 286(3): R431 - R444.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
D. H. Evans, R. E. Rose, J. M. Roeser, and J. D. Stidham
NaCl transport across the opercular epithelium of Fundulus heteroclitus is inhibited by an endothelin to NO, superoxide, and prostanoid signaling axis
Am J Physiol Regulatory Integrative Comp Physiol, March 1, 2004; 286(3): R560 - R568.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
N. M. Tsoukias, M. Kavdia, and A. S. Popel
A theoretical model of nitric oxide transport in arterioles: frequency- vs. amplitude-dependent control of cGMP formation
Am J Physiol Heart Circ Physiol, March 1, 2004; 286(3): H1043 - H1056.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
K. S. Aulak, T. Koeck, J. W. Crabb, and D. J. Stuehr
Dynamics of protein nitration in cells and mitochondria
Am J Physiol Heart Circ Physiol, January 1, 2004; 286(1): H30 - H38.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
S. L. Elfering, V. L. Haynes, N. J. Traaseth, A. Ettl, and C. Giulivi
Aspects, mechanism, and biological relevance of mitochondrial protein nitration sustained by mitochondrial nitric oxide synthase
Am J Physiol Heart Circ Physiol, January 1, 2004; 286(1): H22 - H29.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
P. S. Brookes and V. M. Darley-Usmar
Role of calcium and superoxide dismutase in sensitizing mitochondria to peroxynitrite-induced permeability transition
Am J Physiol Heart Circ Physiol, January 1, 2004; 286(1): H39 - H46.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
J. Belik, R. P. Jankov, J. Pan, M. Yi, C. R. Pace-Asciak, and A. K. Tanswell
Effect of 8-isoprostaglandin F2{alpha} on the newborn rat pulmonary arterial muscle and endothelium
J Appl Physiol, November 1, 2003; 95(5): 1979 - 1985.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Renal Physiol.Home page
S. Muto, Y. Asano, W. Wang, D. Seldin, and G. Giebisch
Activity of the basolateral K+ channels is coupled to the Na+-K+-ATPase in the cortical collecting duct
Am J Physiol Renal Physiol, November 1, 2003; 285(5): F945 - F954.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Gastrointest. Liver Physiol.Home page
D. A. Potoka, J. S. Upperman, X.-R. Zhang, J. R. Kaplan, S. J. Corey, A. Grishin, R. Zamora, and H. R. Ford
Peroxynitrite inhibits enterocyte proliferation and modulates Src kinase activity in vitro
Am J Physiol Gastrointest Liver Physiol, November 1, 2003; 285(5): G861 - G869.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
R. C. Venema, V. J. Venema, H. Ju, M. B. Harris, C. Snead, T. Jilling, C. Dimitropoulou, M. E. Maragoudakis, and J. D. Catravas
Novel complexes of guanylate cyclase with heat shock protein 90 and nitric oxide synthase
Am J Physiol Heart Circ Physiol, July 11, 2003; 285(2): H669 - H678.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
J. Herget, J. Novotna, J. Bibova, V. Povysilova, M. Vankova, and V. Hampl
Metalloproteinase inhibition by Batimastat attenuates pulmonary hypertension in chronically hypoxic rats
Am J Physiol Lung Cell Mol Physiol, July 1, 2003; 285(1): L199 - L208.
[Abstract] [Full Text] [PDF]

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 J. Appl. Physiol.Home page
C. Coirault, B. Pignol, R. N. Cooper, G. Butler-Browne, P.-E. Chabrier, and Y. Lecarpentier
Severe muscle dysfunction precedes collagen tissue proliferation in mdx mouse diaphragm
J Appl Physiol, May 1, 2003; 94(5): 1744 - 1750.
[Abstract] [Full Text] [PDF]

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 JAMAHome page
M. H. Shishehbor, R. J. Aviles, M.-L. Brennan, X. Fu, M. Goormastic, G. L. Pearce, N. Gokce, J. F. Keaney Jr, M. S. Penn, D. L. Sprecher, et al.
Association of Nitrotyrosine Levels With Cardiovascular Disease and Modulation by Statin Therapy
JAMA, April 2, 2003; 289(13): 1675 - 1680.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
D. M. Lenda, E. Kikawada, E. R. Stanley, and V. R. Kelley
Reduced Macrophage Recruitment, Proliferation, and Activation in Colony-Stimulating Factor-1-Deficient Mice Results in Decreased Tubular Apoptosis During Renal Inflammation
J. Immunol., March 15, 2003; 170(6): 3254 - 3262.
[Abstract] [Full Text] [PDF]

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 J. Leukoc. Biol.Home page
M. K. Clements, D. W. Siemsen, S. D. Swain, A. J. Hanson, L. K. Nelson-Overton, T. T. Rohn, and M. T. Quinn
Inhibition of actin polymerization by peroxynitrite modulates neutrophil functional responses
J. Leukoc. Biol., March 1, 2003; 73(3): 344 - 355.
[Abstract] [Full Text] [PDF]

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 Vet PatholHome page
M. Maeda, A. Yabuki, S. Suzuki, M. Matsumoto, K. Taniguchi, and H. Nishinakagawa
Renal Lesions in Spontaneous Insulin-dependent Diabetes Mellitus in the Nonobese Diabetic Mouse: Acute Phase of Diabetes
Vet. Pathol., March 1, 2003; 40(2): 187 - 195.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
R. A. Kowluru
Effect of Reinstitution of Good Glycemic Control on Retinal Oxidative Stress and Nitrative Stress in Diabetic Rats
Diabetes, March 1, 2003; 52(3): 818 - 823.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
M. Walia, S. E. Samson, T. Schmidt, K. Best, M. Whittington, C. Y. Kwan, and A. K. Grover
Peroxynitrite and nitric oxide differ in their effects on pig coronary artery smooth muscle
Am J Physiol Cell Physiol, March 1, 2003; 284(3): C649 - C657.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
T. Vassilakopoulos, G. Deckman, M. Kebbewar, G. Rallis, R. Harfouche, and S. N. A. Hussain
Regulation of nitric oxide production in limb and ventilatory muscles during chronic exercise training
Am J Physiol Lung Cell Mol Physiol, March 1, 2003; 284(3): L452 - L457.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
H. Qiu, F.W. Orr, D. Jensen, H. H. Wang, A. R. McIntosh, B. B. Hasinoff, D. M. Nance, S. Pylypas, K. Qi, C. Song, et al.
Arrest of B16 Melanoma Cells in the Mouse Pulmonary Microcirculation Induces Endothelial Nitric Oxide Synthase-Dependent Nitric Oxide Release that Is Cytotoxic to the Tumor Cells
Am. J. Pathol., February 1, 2003; 162(2): 403 - 412.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
W. H. Cerwinka, D. Cooper, C. F. Krieglstein, C. R. Ross, J. M. McCord, and D. N. Granger
Superoxide mediates endotoxin-induced platelet-endothelial cell adhesion in intestinal venules
Am J Physiol Heart Circ Physiol, February 1, 2003; 284(2): H535 - H541.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
D. Z. Ellis, J. Rabe, and K. J. Sweadner
Global Loss of Na,K-ATPase and Its Nitric Oxide-Mediated Regulation in a Transgenic Mouse Model of Amyotrophic Lateral Sclerosis
J. Neurosci., January 1, 2003; 23(1): 43 - 51.
[Abstract] [Full Text] [PDF]

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 Mol. Pharmacol.Home page
Y. Ji and B. M. Bennett
Activation of Microsomal Glutathione S-Transferase by Peroxynitrite
Mol. Pharmacol., January 1, 2003; 63(1): 136 - 146.
[Abstract] [Full Text] [PDF]

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 Arterioscler. Thromb. Vasc. Bio.Home page
F. S. Gragasin, Y. Xu, I. A. Arenas, N. Kainth, and S. T. Davidge
Estrogen Reduces Angiotensin II-Induced Nitric Oxide Synthase and NAD(P)H Oxidase Expression in Endothelial Cells
Arterioscler Thromb Vasc Biol, January 1, 2003; 23(1): 38 - 44.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Renal Physiol.Home page
M. Poljakovic and K. Persson
Urinary tract infection in iNOS-deficient mice with focus on bacterial sensitivity to nitric oxide
Am J Physiol Renal Physiol, January 1, 2003; 284(1): F22 - F31.
[Abstract] [Full Text] [PDF]

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 Pharmacol. Rev.Home page
I. V. Turko and F. Murad
Protein Nitration in Cardiovascular Diseases
Pharmacol. Rev., December 1, 2002; 54(4): 619 - 634.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
D. Eguchi, L. V. d'Uscio, C. Wambi, D. Weiler, I. Kovesdi, T. O'Brien, and Z. S. Katusic
Inhibitory effect of recombinant iNOS gene expression on vasomotor function of canine basilar artery
Am J Physiol Heart Circ Physiol, December 1, 2002; 283(6): H2560 - H2566.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
P. Condorelli and S. C. George
Free nitric oxide diffusion in the bronchial microcirculation
Am J Physiol Heart Circ Physiol, December 1, 2002; 283(6): H2660 - H2670.
[Abstract] [Full Text] [PDF]

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 DiabetesHome page
J. M. Forbes, M. E. Cooper, V. Thallas, W. C. Burns, M. C. Thomas, G. C. Brammar, F. Lee, S. L. Grant, L. A. Burrell, G. Jerums, et al.
Reduction of the Accumulation of Advanced Glycation End Products by ACE Inhibition in Experimental Diabetic Nephropathy
Diabetes, November 1, 2002; 51(11): 3274 - 3282.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
Y. Sun, J. Zhang, L. Lu, S. S. Chen, M. T. Quinn, and K. T. Weber
Aldosterone-Induced Inflammation in the Rat Heart : Role of Oxidative Stress
Am. J. Pathol., November 1, 2002; 161(5): 1773 - 1781.
[Abstract] [Full Text] [PDF]

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 J. Pharmacol. Exp. Ther.Home page
C. Vergely, C. Perrin-Sarrado, G. Clermont, and L. Rochette
Postischemic Recovery and Oxidative Stress Are Independent of Nitric-Oxide Synthases Modulation in Isolated Rat Heart
J. Pharmacol. Exp. Ther., October 1, 2002; 303(1): 149 - 157.
[Abstract] [Full Text] [PDF]

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 J. Leukoc. Biol.Home page
S. Heigold and G. Bauer
RAW 264.7 macrophages induce apoptosis selectively in transformed fibroblasts: intercellular signaling based on reactive oxygen and nitrogen species
J. Leukoc. Biol., September 1, 2002; 72(3): 554 - 563.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
S. J. Armstrong, Y. Zhang, K. G. Stewart, and S. T. Davidge
Estrogen replacement reduces PGHS-2-dependent vasoconstriction in the aged rat
Am J Physiol Heart Circ Physiol, September 1, 2002; 283(3): H893 - H898.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
F. H. Khadour, D. Panas, P. Ferdinandy, C. Schulze, T. Csont, M. M. Lalu, S. M. Wildhirt, and R. Schulz
Enhanced NO and superoxide generation in dysfunctional hearts from endotoxemic rats
Am J Physiol Heart Circ Physiol, September 1, 2002; 283(3): H1108 - H1115.
[Abstract] [Full Text] [PDF]


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