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Volume 271, Number 1, Issue of January 5, 1996 pp. 40-47
©1996 by The American Society for Biochemistry and Molecular Biology, Inc.
Modulation of Superoxide-dependent Oxidation and Hydroxylation Reactions by Nitric Oxide

(Received for publication, July 12, 1995; and in revised form, October 23, 1995)

Allen M. Miles,  D. Scott Bohle ,  Peter A. Glassbrenner ,  Bernhard Hansert ,  David A. Wink ,  Matthew B. Grisham

The rapid and spontaneous interaction between superoxide (O(2)) and nitric oxide (NO) to yield the potent oxidants peroxynitrite (ONOO) and peroxynitrous acid (ONOOH), has been suggested to represent an important pathway by which tissue may be injured during inflammation. Although several groups of investigators have demonstrated substantial oxidizing and cytotoxic activities of chemically synthesized ONOO, there has been little information available quantifying the interaction between O(2) and NO in the absence or the presence of redox-active iron. Using the hypoxanthine (HX)/xanthine oxidase system to generate various fluxes of O(2) and H(2)O(2) and the spontaneous decomposition of the spermine/NO adduct to produce various fluxes of NO, we found that in the absence of redox-active iron, the simultaneous production of equimolar fluxes of O(2) and NO increased the oxidation of dihydrorhodamine (DHR) from normally undetectable levels to approximately 15 µM, suggesting the formation of a potent oxidant. Superoxide dismutase, but not catalase, inhibited this oxidative reaction, suggesting that O(2) and not hydrogen peroxide (H(2)O(2)) interacts with NO to generate a potent oxidizing agent. Excess production of either radical virtually eliminated the oxidation of DHR. In the presence of 5 µM Fe-EDTA to insure optimum O(2)-driven Fenton chemistry, NO enhanced modestly HX/xanthine oxidase-induced oxidation of DHR. As expected, both superoxide dismutase and catalase inhibited this Fe-catalyzed oxidation reaction. Excess NO production with respect to O(2) flux produced only modest inhibition (33%) of DHR oxidation. In a separate series of studies, we found that equimolar fluxes of O(2) and NO in the absence of iron only modestly enhanced hydroxylation of benzoic acid from undetectable levels to 0.6 µM 2-hydroxybenzoate. In the presence of 5 µM Fe-EDTA, HX/xanthine oxidase-mediated hydroxylation of benzoic acid increased dramatically from undetectable levels to 4.5 µM of the hydroxylated product. Superoxide dismutase and catalase were both effective at inhibiting this classic O(2)-driven Fenton reaction. Interestingly, NO inhibited this iron-catalyzed hydroxylation reaction in a concentration-dependent manner such that fluxes of NO approximating those of O(2) and H(2)O(2) virtually abolished the hydroxylation of benzoic acid. We conclude that in the absence of iron, equimolar fluxes of NO and O(2) interact to yield potent oxidants such as ONOO/ONOOH, which oxidize organic compounds. Excess production of either radical remarkably inhibits these oxidative reactions. In the presence of low molecular weight redox-active iron complexes, NO may enhance or inhibit O(2)-dependent oxidation and hydroxylation reactions depending upon their relative fluxes.



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