Cargando…

DNA Is an Antimicrobial Component of Neutrophil Extracellular Traps

Neutrophil extracellular traps (NETs) comprise an ejected lattice of chromatin enmeshed with granular and nuclear proteins that are capable of capturing and killing microbial invaders. Although widely employed to combat infection, the antimicrobial mechanism of NETs remains enigmatic. Efforts to elu...

Descripción completa

Detalles Bibliográficos
Autores principales: Halverson, Tyler W.R., Wilton, Mike, Poon, Karen K. H., Petri, Björn, Lewenza, Shawn
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4295883/
https://www.ncbi.nlm.nih.gov/pubmed/25590621
http://dx.doi.org/10.1371/journal.ppat.1004593
_version_ 1782352894728601600
author Halverson, Tyler W.R.
Wilton, Mike
Poon, Karen K. H.
Petri, Björn
Lewenza, Shawn
author_facet Halverson, Tyler W.R.
Wilton, Mike
Poon, Karen K. H.
Petri, Björn
Lewenza, Shawn
author_sort Halverson, Tyler W.R.
collection PubMed
description Neutrophil extracellular traps (NETs) comprise an ejected lattice of chromatin enmeshed with granular and nuclear proteins that are capable of capturing and killing microbial invaders. Although widely employed to combat infection, the antimicrobial mechanism of NETs remains enigmatic. Efforts to elucidate the bactericidal component of NETs have focused on the role of NET-bound proteins including histones, calprotectin and cathepsin G protease; however, exogenous and microbial derived deoxyribonuclease (DNase) remains the most potent inhibitor of NET function. DNA possesses a rapid bactericidal activity due to its ability to sequester surface bound cations, disrupt membrane integrity and lyse bacterial cells. Here we demonstrate that direct contact and the phosphodiester backbone are required for the cation chelating, antimicrobial property of DNA. By treating NETs with excess cations or phosphatase enzyme, the antimicrobial activity of NETs is neutralized, but NET structure, including the localization and function of NET-bound proteins, is maintained. Using intravital microscopy, we visualized NET-like structures in the skin of a mouse during infection with Pseudomonas aeruginosa. Relative to other bacteria, P. aeruginosa is a weak inducer of NETosis and is more resistant to NETs. During NET exposure, we demonstrate that P. aeruginosa responds by inducing the expression of surface modifications to defend against DNA-induced membrane destabilization and NET-mediated killing. Further, we show induction of this bacterial response to NETs is largely due to the bacterial detection of DNA. Therefore, we conclude that the DNA backbone contributes both to the antibacterial nature of NETs and as a signal perceived by microbes to elicit host-resistance strategies.
format Online
Article
Text
id pubmed-4295883
institution National Center for Biotechnology Information
language English
publishDate 2015
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-42958832015-01-22 DNA Is an Antimicrobial Component of Neutrophil Extracellular Traps Halverson, Tyler W.R. Wilton, Mike Poon, Karen K. H. Petri, Björn Lewenza, Shawn PLoS Pathog Research Article Neutrophil extracellular traps (NETs) comprise an ejected lattice of chromatin enmeshed with granular and nuclear proteins that are capable of capturing and killing microbial invaders. Although widely employed to combat infection, the antimicrobial mechanism of NETs remains enigmatic. Efforts to elucidate the bactericidal component of NETs have focused on the role of NET-bound proteins including histones, calprotectin and cathepsin G protease; however, exogenous and microbial derived deoxyribonuclease (DNase) remains the most potent inhibitor of NET function. DNA possesses a rapid bactericidal activity due to its ability to sequester surface bound cations, disrupt membrane integrity and lyse bacterial cells. Here we demonstrate that direct contact and the phosphodiester backbone are required for the cation chelating, antimicrobial property of DNA. By treating NETs with excess cations or phosphatase enzyme, the antimicrobial activity of NETs is neutralized, but NET structure, including the localization and function of NET-bound proteins, is maintained. Using intravital microscopy, we visualized NET-like structures in the skin of a mouse during infection with Pseudomonas aeruginosa. Relative to other bacteria, P. aeruginosa is a weak inducer of NETosis and is more resistant to NETs. During NET exposure, we demonstrate that P. aeruginosa responds by inducing the expression of surface modifications to defend against DNA-induced membrane destabilization and NET-mediated killing. Further, we show induction of this bacterial response to NETs is largely due to the bacterial detection of DNA. Therefore, we conclude that the DNA backbone contributes both to the antibacterial nature of NETs and as a signal perceived by microbes to elicit host-resistance strategies. Public Library of Science 2015-01-15 /pmc/articles/PMC4295883/ /pubmed/25590621 http://dx.doi.org/10.1371/journal.ppat.1004593 Text en © 2015 Halverson et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Halverson, Tyler W.R.
Wilton, Mike
Poon, Karen K. H.
Petri, Björn
Lewenza, Shawn
DNA Is an Antimicrobial Component of Neutrophil Extracellular Traps
title DNA Is an Antimicrobial Component of Neutrophil Extracellular Traps
title_full DNA Is an Antimicrobial Component of Neutrophil Extracellular Traps
title_fullStr DNA Is an Antimicrobial Component of Neutrophil Extracellular Traps
title_full_unstemmed DNA Is an Antimicrobial Component of Neutrophil Extracellular Traps
title_short DNA Is an Antimicrobial Component of Neutrophil Extracellular Traps
title_sort dna is an antimicrobial component of neutrophil extracellular traps
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4295883/
https://www.ncbi.nlm.nih.gov/pubmed/25590621
http://dx.doi.org/10.1371/journal.ppat.1004593
work_keys_str_mv AT halversontylerwr dnaisanantimicrobialcomponentofneutrophilextracellulartraps
AT wiltonmike dnaisanantimicrobialcomponentofneutrophilextracellulartraps
AT poonkarenkh dnaisanantimicrobialcomponentofneutrophilextracellulartraps
AT petribjorn dnaisanantimicrobialcomponentofneutrophilextracellulartraps
AT lewenzashawn dnaisanantimicrobialcomponentofneutrophilextracellulartraps