Nitric Oxide: A Key Mediator of Biofilm Dispersal with Applications in Infectious Diseases

Barraud, Nicolas; Kelso, Michael J.; Rice, Scott A.; Kjelleberg, Staffan

doi:10.2174/1381612820666140905112822

Cited by 206 publications

(205 citation statements)

References 159 publications

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“…Several classes of NO-releasing compounds active in biofilm modulation have been found, whose properties were very recently reviewed by Barraud et al (39).…”

Section: Role Of C-di-gmp In Biofilm Formation and Dispersalmentioning

confidence: 99%

“…In P. aeruginosa, biofilm dispersal has been shown to occur in the presence of exogenous compounds spontaneously releasing NO, such as sodium nitroprusside (SNP), 6-(2-hydroxy-1-methyl-2-nitrosohydrazino)-N-methyl-1-hexanamine (MAHMA NONOate) or aminoxyl free radicals (nitroxides) (reference 39 and references therein). SNP as an NO donor has been shown to deliver an effective NO concentration about 1,000-fold lower than the concentration of the donor over several minutes (up to 30 min) (22), whereas the half-life of MAHMA NONOate is much shorter (1 to 2 min) (39). More recently, prodrugs releasing NO after an activation step in the bacterium, such as diethylamine (DEA) NONOate-cephalosporin prodrug (DEACP), were also shown to promote dispersal (46,47).…”

Section: Properties and Sources Of Nomentioning

confidence: 99%

“…In addition to the c-di-GMP-modulating enzymes, a preliminary report suggests that the periplasmic protease LapG may be involved in the dispersal response to NO, as P. aeruginosa biofilms devoid of LapG did not show a dispersal response upon NO addition (39). LapG is a membrane-bound protease that, in a c-di-GMP-dependent fashion via an inside-out signaling mechanism through the membrane receptor LapD, cleaves the surface adhesion LapA in Pseudomonas putida to mediate dispersal (95,96).…”

Section: No Sensor Proteinsmentioning

confidence: 99%

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Origin and Impact of Nitric Oxide in Pseudomonas aeruginosa Biofilms

Cutruzzolà

Frankenberg‐Dinkel

2016

J Bacteriol

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bThe formation of the organized bacterial community called biofilm is a crucial event in bacterial physiology. Given that biofilms are often refractory to antibiotics and disinfectants to which planktonic bacteria are susceptible, their formation is also an industrially and medically relevant issue. Pseudomonas aeruginosa, a well-known human pathogen causing acute and chronic infections, is considered a model organism to study biofilms. A large number of environmental cues control biofilm dynamics in bacterial cells. In particular, the dispersal of individual cells from the biofilm requires metabolic and morphological reprogramming in which the second messenger bis-(3=-5=)-cyclic dimeric GMP (c-di-GMP) plays a central role. The diatomic gas nitric oxide (NO), a well-known signaling molecule in both prokaryotes and eukaryotes, is able to induce the dispersal of P. aeruginosa and other bacterial biofilms by lowering c-di-GMP levels. In this review, we summarize the current knowledge on the molecular mechanisms connecting NO sensing to the activation of c-di-GMP-specific phosphodiesterases in P. aeruginosa, ultimately leading to c-di-GMP decrease and biofilm dispersal. PSEUDOMONAS AERUGINOSA: A MODEL SYSTEM FOR BIOFILM RESEARCH

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“…Several classes of NO-releasing compounds active in biofilm modulation have been found, whose properties were very recently reviewed by Barraud et al (39).…”

Section: Role Of C-di-gmp In Biofilm Formation and Dispersalmentioning

confidence: 99%

Section: Properties and Sources Of Nomentioning

confidence: 99%

Section: No Sensor Proteinsmentioning

confidence: 99%

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Origin and Impact of Nitric Oxide in Pseudomonas aeruginosa Biofilms

Cutruzzolà

Frankenberg‐Dinkel

2016

J Bacteriol

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“…Others have shown that NO combined with antibiotic treatment resulted in additional reduction in the viability of biofilms in several types of bacteria (28). We therefore tested whether NO treatment of pneumococcal biofilms could further reduce bacterial viability when used as an adjunctive treatment in conjunction with a conventional antibiotic used to treat otitis media.…”

Section: Treatment With the No Donor Snp Decreased The Viability Of Pmentioning

confidence: 99%

“…Multiple regulatory systems have been identified that mediate the diverse responses of bacteria to NO, including conferring protection from oxidative stress and playing a role in toxin biosynthesis (23,25). In biofilms, however, low concentrations of exogenous NO have been shown to trigger a dispersal response in several bacterial species, including Pseudomonas aeruginosa, Escherichia coli, and Staphylococcus epidermidis, a response associated with increased antibacterial efficacy when NO is used as an adjuvant in conjunction with antibiotics (26)(27)(28). Furthermore, NO-releasing nanoparticles and gaseous NO have been shown to exert potent antimicrobial effects against P. aeruginosa, Streptococcus pyogenes, and Enterococcus faecalis (29)(30)(31).…”

mentioning

confidence: 99%

Low Concentrations of Nitric Oxide Modulate Streptococcus pneumoniae Biofilm Metabolism and Antibiotic Tolerance

Allan

Morgan

Brito-Mutunayagam

et al. 2016

Antimicrob Agents Chemother

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g Streptococcus pneumoniae is one of the key pathogens responsible for otitis media (OM), the most common infection in children and the largest cause of childhood antibiotic prescription. Novel therapeutic strategies that reduce the overall antibiotic consumption due to OM are required because, although widespread pneumococcal conjugate immunization has controlled invasive pneumococcal disease, overall OM incidence has not decreased. Biofilm formation represents an important phenotype contributing to the antibiotic tolerance and persistence of S. pneumoniae in chronic or recurrent OM. We investigated the treatment of pneumococcal biofilms with nitric oxide (NO), an endogenous signaling molecule and therapeutic agent that has been demonstrated to trigger biofilm dispersal in other bacterial species. We hypothesized that addition of low concentrations of NO to pneumococcal biofilms would improve antibiotic efficacy and that higher concentrations exert direct antibacterial effects. Unlike in many other bacterial species, low concentrations of NO did not result in S. pneumoniae biofilm dispersal. Instead, treatment of both in vitro biofilms and ex vivo adenoid tissue samples (a reservoir for S. pneumoniae biofilms) with low concentrations of NO enhanced pneumococcal killing when combined with amoxicillin-clavulanic acid, an antibiotic commonly used to treat chronic OM. Quantitative proteomic analysis using iTRAQ (isobaric tag for relative and absolute quantitation) identified 13 proteins that were differentially expressed following low-concentration NO treatment, 85% of which function in metabolism or translation. Treatment with low-concentration NO, therefore, appears to modulate pneumococcal metabolism and may represent a novel therapeutic approach to reduce antibiotic tolerance in pneumococcal biofilms.

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