Nitric oxide evokes an adaptive response to oxidative stress by arresting respiration

Maroof Husain, Travis J. Bourret, Bruce D. McCollister, Jessica Jones-Carson, James Laughlin, Andrés Vázquez-Torres

Research output: Contribution to journalArticle

56 Citations (Scopus)

Abstract

Aerobic metabolism generates biologically challenging reactive oxygen species (ROS) by the endogenous autooxidation of components of the electron transport chain (ETC). Basal levels of oxidative stress can dramatically rise upon activation of the NADPH oxidase-dependent respiratory burst. To minimize ROS toxicity, prokaryotic and eukaryotic organisms express a battery of low-molecular-weight thiol scavengers, a legion of detoxifying catalases, peroxidases, and superoxide dismutases, as well as a variety of repair systems.Wepresent herein blockage of bacterial respiration as a novel strategy that helps the intracellular pathogen Salmonella survive extreme oxidative stress conditions. A Salmonella strain bearing mutations in complex I NADH dehydrogenases is refractory to the early NADPHoxidasedependent antimicrobial activity of IFNγ-activated macrophages. The ability of NADH-rich, complex I-deficient Salmonella to survive oxidative stress is associated with resistance to peroxynitrite (ONOO-) and hydrogen peroxide (H2O 2). Inhibition of respiration with nitric oxide (NO) also triggered a protective adaptive response against oxidative stress. Expression of the NDH-II dehydrogenase decreases NADH levels, thereby abrogating resistance of NO-adapted Salmonella to H2O2. NADH antagonizes the hydroxyl radical (OH.) generated in classical Fenton chemistry or spontaneous decomposition of peroxynitrous acid (ONOOH), while fueling AhpCF alkylhydroperoxidase. Together, these findings identify the accumulation of NADH following the NO-mediated inhibition of Salmonella's ETC as a novel antioxidant strategy. NO-dependent respiratory arrest may help mitochondria and a plethora of organisms cope with oxidative stress engendered in situations as diverse as aerobic respiration, ischemia reperfusion, and inflammation.

Original languageEnglish
Pages (from-to)7682-7689
Number of pages8
JournalJournal of Biological Chemistry
Volume283
Issue number12
DOIs
StatePublished - Mar 21 2008
Externally publishedYes

Fingerprint

Salmonella
Oxidative stress
Nitric Oxide
Respiration
Oxidative Stress
NAD
Peroxynitrous Acid
Electron Transport
Reactive Oxygen Species
Bearings (structural)
Electron Transport Complex I
Peroxidases
Mitochondria
Fueling
Respiratory Burst
Macrophages
NADPH Oxidase
Pathogens
Sulfhydryl Compounds
Metabolism

All Science Journal Classification (ASJC) codes

  • Biochemistry
  • Cell Biology
  • Molecular Biology

Cite this

Husain, M., Bourret, T. J., McCollister, B. D., Jones-Carson, J., Laughlin, J., & Vázquez-Torres, A. (2008). Nitric oxide evokes an adaptive response to oxidative stress by arresting respiration. Journal of Biological Chemistry, 283(12), 7682-7689. https://doi.org/10.1074/jbc.M708845200

Nitric oxide evokes an adaptive response to oxidative stress by arresting respiration. / Husain, Maroof; Bourret, Travis J.; McCollister, Bruce D.; Jones-Carson, Jessica; Laughlin, James; Vázquez-Torres, Andrés.

In: Journal of Biological Chemistry, Vol. 283, No. 12, 21.03.2008, p. 7682-7689.

Research output: Contribution to journalArticle

Husain, M, Bourret, TJ, McCollister, BD, Jones-Carson, J, Laughlin, J & Vázquez-Torres, A 2008, 'Nitric oxide evokes an adaptive response to oxidative stress by arresting respiration', Journal of Biological Chemistry, vol. 283, no. 12, pp. 7682-7689. https://doi.org/10.1074/jbc.M708845200
Husain, Maroof ; Bourret, Travis J. ; McCollister, Bruce D. ; Jones-Carson, Jessica ; Laughlin, James ; Vázquez-Torres, Andrés. / Nitric oxide evokes an adaptive response to oxidative stress by arresting respiration. In: Journal of Biological Chemistry. 2008 ; Vol. 283, No. 12. pp. 7682-7689.
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