Interaction of the bacterial terminal oxidase cytochrome <i>bd</i> with nitric oxide

Borisov, Vitaliy B.; Forte, Elena; Konstantinov, Alexander A.; Poole, Robert K.; Sarti, Paolo; Giuffrè, Alessandro

doi:10.1016/j.febslet.2004.09.013

Cited by 80 publications

(73 citation statements)

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“…5A). Cytochrome bd has no reported NO 2 Ϫ -reducing activity to our knowledge, nor does it reduce NO (54). Cytochrome boЈ is a member of the heme-copper superfamily of terminal oxidases and thus shares mechanistic properties with mitochondrial cytochrome c oxidase (cytochrome aa 3 ).…”

Section: Discussionmentioning

confidence: 99%

Nitric Oxide Homeostasis in Salmonella typhimurium

Gilberthorpe

Poole

2008

Journal of Biological Chemistry

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113

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Nitric oxide (NO) is generated in biological systems primarily via the activity of NO synthases and nitrate and nitrite reductases. Here we show that Salmonella enterica serovar Typhimurium (S. typhimurium) grown anaerobically with nitrate is capable of generating polarographically detectable NO after nitrite (NO 2 ؊ ) addition. NO accumulation is sensitive to the NO scavenger 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide. Neither an fnr mutant nor an fnr hmp double mutant produces NO, indicating the involvement in NO evolution from NO 2 ؊ of protein(s) positively regulated by FNR. Contrary to previous findings in Escherichia coli, we demonstrate that neither the periplasmic nitrite reductase (NrfA) nor the cytoplasmic nitrite reductase (NirB) is involved in NO production in S. typhimurium. However, mutant cells lacking the membrane-bound nitrate reductase, NarGHI, and membranes derived from these cells are unable to produce NO, demonstrating that, in wild-type S. typhimurium, this enzyme is responsible for NO production. Membrane terminal oxidases cannot account for the NO levels measured. The nitrate reductase inhibitor, azide, abrogates NO evolution by Salmonella, and production of NO occurs only in the absence from the assays of nitrate; both features reveal a marked similarity between the NO-generating activities of this bacterium and plants. Unlike the situation in E. coli, an S. typhimurium hmp mutant produces NO both aerobically and anaerobically. Under aerobic conditions, when a functional flavohemoglobin is present, no NO is detectable. We propose a homeostatic mechanism in S. typhimurium, in which NO produced from NO 2 ؊ by nitrate reductase derepresses Hmp expression (via FNR and NsrR) and NorV expression (via NorR) and thus limits NO toxicity.

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Section: Discussionmentioning

confidence: 99%

Nitric Oxide Homeostasis in Salmonella typhimurium

Gilberthorpe

Poole

2008

Journal of Biological Chemistry

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113

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“…The protein synthesis signature observed for S. aureus obviously showed strong similarities to that found under anaerobic conditions. NO disrupts the respiratory chain by binding to cytochromes (5,8,10,13,71,88,100). Unlike B. subtilis, the extensive switch to the anaerobic metabolism even under high oxygen tension might therefore be a beneficial consequence of NO stress in the more tolerant S. aureus.…”

Section: Vol 190 2008 Nitric Oxide Stress In B Subtilis and S Aurmentioning

confidence: 99%

“…NO directly affects the activity of enzymes by the reaction with bound free radicals or with metal centers (51, 72, 100). For example, the formation of metal-nitrosyl complexes in respiratory enzymes was shown to inhibit bacterial respiration (8,13,71,88) and the formation of a dinitrosyl-iron complex of a protein essential for branched-chain amino acid biosynthesis was recently shown to be the main cause of NO-induced growth arrest in Escherichia coli (44). Moreover, reaction of NO with the tyrosyl radical formed in the catalytic turnover of ribonucleotide reductase is considered to be responsible for the suppression of DNA synthesis (53,54).…”

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confidence: 99%

Nitric Oxide Stress Induces Different Responses but Mediates Comparable Protein Thiol Protection inBacillus subtilisandStaphylococcus aureus

et al. 2008

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The nonpathogenic Bacillus subtilis and the pathogen Staphylococcus aureus are gram-positive model organisms that have to cope with the radical nitric oxide (NO) generated by nitrite reductases of denitrifying bacteria and by the inducible NO synthases of immune cells of the host, respectively. The response of both microorganisms to NO was analyzed by using a two-dimensional gel approach. Metabolic labeling of the proteins revealed major changes in the synthesis pattern of cytosolic proteins after the addition of the NO donor MAHMA NONOate. Whereas B. subtilis induced several oxidative stress-responsive regulons controlled by Fur, PerR, OhrR, and Spx, as well as the general stress response controlled by the alternative sigma factor SigB, the more resistant S. aureus showed an increased synthesis rate of proteins involved in anaerobic metabolism. These data were confirmed by nuclear magnetic resonance analyses indicating that NO causes a drastically higher increase in the formation of lactate and butanediol in S. aureus than in B. subtilis. Monitoring the intracellular protein thiol state, we observed no increase in reversible or irreversible protein thiol modifications after NO stress in either organism. Obviously, NO itself does not cause general protein thiol oxidations. In contrast, exposure of cells to NO prior to peroxide stress diminished the irreversible thiol oxidation caused by hydrogen peroxide.Bacillus subtilis and Staphylococcus aureus are gram-positive model bacteria. Whereas B. subtilis is considered to be harmless, S. aureus is a facultative pathogen and the leading cause of nosocomial and community-acquired infections. Both microorganisms have to cope with high amounts of nitric oxide (NO) (up to the M range) generated from coexisting denitrifying bacteria or from the innate immune response of the host, respectively (17,31,55,68). Hence, the ability of B. subtilis and S. aureus to protect themselves against NO might be crucial for survival in their respective natural habitats.The cytotoxic properties of the small, lipophilic, and freely diffusible radical NO are attributed to its high reactivity. Indirect effects of NO are caused by the reaction of the radical with oxygen or superoxide, resulting in the formation of a number of additional reactive nitrogen species, including nitrogen dioxide, peroxynitrite, and dinitrogen trioxide. These nitrogen species differ in reactivity, stability, and biological activity but result in a broad spectrum of antimicrobial activity (25). In general, reactive oxygen and nitrogen species can interact with numerous targets, including thiols, metal centers, tyrosine residues in proteins, nucleotide bases, and lipids (20,69). NO directly affects the activity of enzymes by the reaction with bound free radicals or with metal centers (51, 72, 100). For example, the formation of metal-nitrosyl complexes in respiratory enzymes was shown to inhibit bacterial respiration (8,13,71,88) and the formation of a dinitrosyl-iron complex of a protein essential for branched-chain am...

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“…NO is known to inhibit bacterial respiration by direct reaction with these proteins (12,13). Both cytochromes modulate the quinone pool, in turn modulating ArcAB activity (36).…”

Section: Transcriptome Network Component Analysis Identified No-respomentioning

confidence: 99%

“…NO has been reported to react with various protein Fe-S clusters (4)(5)(6)(7), and this reactivity has been implicated in the inhibition of tumor proliferation (8)(9)(10). NO also binds to the metal centers of respiratory enzymes, inhibiting bacterial respiration (11)(12)(13). Because NO is used to combat Escherichia coli in low oxygen environments, it is likely that respiration is not the only system targeted by NO.…”

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confidence: 99%

Integrated network analysis identifies nitric oxide response networks and dihydroxyacid dehydratase as a crucial target in Escherichia coli

Hyduke

Jarboe

Tran

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

137

171

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Nitric oxide (NO) is used by mammalian immune systems to counter microbial invasions and is produced by bacteria during denitrification. As a defense, microorganisms possess a complex network to cope with NO. Here we report a combined transcriptomic, chemical, and phenotypic approach to identify direct NO targets and construct the biochemical response network. In particular, network component analysis was used to identify transcription factors that are perturbed by NO. Such information was screened with potential NO reaction mechanisms and phenotypic data from genetic knockouts to identify active chemistry and direct NO targets in Escherichia coli. This approach identified the comprehensive E. coli NO response network and evinced that NO halts bacterial growth via inhibition of the branched-chain amino acid biosynthesis enzyme dihydroxyacid dehydratase. Because mammals do not synthesize branched-chain amino acids, inhibition of dihydroxyacid dehydratase may have served to foster the role of NO in the immune arsenal.systems biology ͉ chemoinformatics M ammals possess complex immune systems that have evolved to prevent microbial invasion. Nitric oxide (NO) is one of the key chemicals used by mammalian cells to combat infections (1). Although NO is known to act in a bacteriostatic fashion (2), the mechanism underlying this action is not completely understood. NO interferes with biological processes either directly, by reacting with metal centers and free radicals, or indirectly, by promoting the formation of reactive nitrogen oxide species (RNOS), such as peroxynitrite and N 2 O 3 (3). NO has been reported to react with various protein Fe-S clusters (4-7), and this reactivity has been implicated in the inhibition of tumor proliferation (8)(9)(10). NO also binds to the metal centers of respiratory enzymes, inhibiting bacterial respiration (11-13). Because NO is used to combat Escherichia coli in low oxygen environments, it is likely that respiration is not the only system targeted by NO.E. coli contains NO-consuming proteins NO reductase NorV (14), NO oxidase HmpA (15, 16), and cytochrome c nitrite reductase NrfA (17). Expression of norV and hmpA is increased in response to NO by NO-specific transcription factors (TFs) NorR (18) and NsrR, respectively (19,20). Our goal here was to identify the comprehensive NO response network, consisting of the direct NO targets leading to bacteriostasis, the response network resulting from bacteriostasis, bacterial NO sensors for self-defense, and the response network for self-defense.Previous genome-scale studies have used DNA microarrays to identify the global genetic response to [21][22][23][24]. Although transcriptome analysis provides substantial information regarding changes in gene expression, examination of individual genes cannot distinguish primary from secondary effects and does not directly identify the TFs and pathways leading to the transcriptional changes. Because many promoters are controlled by multiple TFs, the identity of the TF responsible for mediating transcr...

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Interaction of the bacterial terminal oxidase cytochrome bd with nitric oxide

Cited by 80 publications

References 50 publications

Nitric Oxide Homeostasis in Salmonella typhimurium

Nitric Oxide Homeostasis in Salmonella typhimurium

Nitric Oxide Stress Induces Different Responses but Mediates Comparable Protein Thiol Protection inBacillus subtilisandStaphylococcus aureus

Integrated network analysis identifies nitric oxide response networks and dihydroxyacid dehydratase as a crucial target in Escherichia coli

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