Extracellular DNA: A major proinflammatory component of Pseudomonas aeruginosa biofilms

Autores
Fuxman Bass, J.I.; Russo, D.M.; Gabelloni, M.L.; Geffner, J.R.; Giordano, M.; Catalano, M.; Zorreguieta, Á.; Trevani, A.S.
Año de publicación
2010
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
We previously demonstrated that extracellular bacterial DNA activates neutrophils through a CpG- and TLR9-independent mechanism. Biofilms are microbial communities enclosed in a polymeric matrix that play a critical role in the pathogenesis of many infectious diseases. Because extracellular DNA is a key component of biofilms of different bacterial species, the aim of this study was to determine whether it plays a role in the ability of biofilms to induce human neutrophil activation. We found that degradation of matrix extracellular DNA with DNase I markedly reduced the capacity of Pseudomonas aeruginosa biofilms to induce the release of the neutrophil proinflammatory cytokines IL-8 and IL-1β (>75%); reduced the upregulation of neutrophil activation markers CD18, CD11b, and CD66b (p < 0.001); reduced the number of bacteria phagocytosed per neutrophil contacting the biofilm; and reduced the production of neutrophil extracellular traps. Consistent with these findings, we found that biofilms formed by the lasI rhlI P. aeruginosa mutant strain, exhibiting a very low content of matrix extracellular DNA, displayed a lower capacity to stimulate the release of proinflammatory cytokines by neutrophils, which was not decreased further by DNase I treatment. Together, our findings support that matrix extracellular DNA is a major proinflammatory component of P. aeruginosa biofilms. Copyright © 2010 by The American Association of Immunologists, Inc.
Fil:Fuxman Bass, J.I. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.
Fil:Russo, D.M. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.
Fil:Gabelloni, M.L. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.
Fil:Giordano, M. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.
Fil:Zorreguieta, Á. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.
Fil:Trevani, A.S. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.
Fuente
J. Immunol. 2010;184(11):6386-6395
Materia
CD11b antigen
CD18 antigen
CD66b antigen
deoxyribonuclease I
DNA
interleukin 1beta
interleukin 8
lymphocyte antigen
unclassified drug
bacterial DNA
cytokine
article
bacterial strain
biofilm
controlled study
cytokine release
degradation
extracellular matrix
human
leukocyte activation
nonhuman
phagocytosis
priority journal
Pseudomonas aeruginosa
upregulation
biosynthesis
chemistry
confocal microscopy
extracellular fluid
growth, development and aging
immunology
leukocyte activation
metabolism
microbiology
neutrophil
physiology
Biofilms
Cytokines
DNA, Bacterial
Extracellular Fluid
Humans
Microscopy, Confocal
Neutrophil Activation
Neutrophils
Pseudomonas aeruginosa
Nivel de accesibilidad
acceso abierto
Condiciones de uso
http://creativecommons.org/licenses/by/2.5/ar
Repositorio
Biblioteca Digital (UBA-FCEN)
Institución
Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturales
OAI Identificador
paperaa:paper_00221767_v184_n11_p6386_FuxmanBass

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oai_identifier_str paperaa:paper_00221767_v184_n11_p6386_FuxmanBass
network_acronym_str BDUBAFCEN
repository_id_str 1896
network_name_str Biblioteca Digital (UBA-FCEN)
spelling Extracellular DNA: A major proinflammatory component of Pseudomonas aeruginosa biofilmsFuxman Bass, J.I.Russo, D.M.Gabelloni, M.L.Geffner, J.R.Giordano, M.Catalano, M.Zorreguieta, Á.Trevani, A.S.CD11b antigenCD18 antigenCD66b antigendeoxyribonuclease IDNAinterleukin 1betainterleukin 8lymphocyte antigenunclassified drugbacterial DNAcytokinearticlebacterial strainbiofilmcontrolled studycytokine releasedegradationextracellular matrixhumanleukocyte activationnonhumanphagocytosispriority journalPseudomonas aeruginosaupregulationbiosynthesischemistryconfocal microscopyextracellular fluidgrowth, development and agingimmunologyleukocyte activationmetabolismmicrobiologyneutrophilphysiologyBiofilmsCytokinesDNA, BacterialExtracellular FluidHumansMicroscopy, ConfocalNeutrophil ActivationNeutrophilsPseudomonas aeruginosaWe previously demonstrated that extracellular bacterial DNA activates neutrophils through a CpG- and TLR9-independent mechanism. Biofilms are microbial communities enclosed in a polymeric matrix that play a critical role in the pathogenesis of many infectious diseases. Because extracellular DNA is a key component of biofilms of different bacterial species, the aim of this study was to determine whether it plays a role in the ability of biofilms to induce human neutrophil activation. We found that degradation of matrix extracellular DNA with DNase I markedly reduced the capacity of Pseudomonas aeruginosa biofilms to induce the release of the neutrophil proinflammatory cytokines IL-8 and IL-1β (>75%); reduced the upregulation of neutrophil activation markers CD18, CD11b, and CD66b (p < 0.001); reduced the number of bacteria phagocytosed per neutrophil contacting the biofilm; and reduced the production of neutrophil extracellular traps. Consistent with these findings, we found that biofilms formed by the lasI rhlI P. aeruginosa mutant strain, exhibiting a very low content of matrix extracellular DNA, displayed a lower capacity to stimulate the release of proinflammatory cytokines by neutrophils, which was not decreased further by DNase I treatment. Together, our findings support that matrix extracellular DNA is a major proinflammatory component of P. aeruginosa biofilms. Copyright © 2010 by The American Association of Immunologists, Inc.Fil:Fuxman Bass, J.I. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.Fil:Russo, D.M. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.Fil:Gabelloni, M.L. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.Fil:Giordano, M. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.Fil:Zorreguieta, Á. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.Fil:Trevani, A.S. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.2010info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfhttp://hdl.handle.net/20.500.12110/paper_00221767_v184_n11_p6386_FuxmanBassJ. Immunol. 2010;184(11):6386-6395reponame:Biblioteca Digital (UBA-FCEN)instname:Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturalesinstacron:UBA-FCENenginfo:eu-repo/semantics/openAccesshttp://creativecommons.org/licenses/by/2.5/ar2025-12-18T09:00:14Zpaperaa:paper_00221767_v184_n11_p6386_FuxmanBassInstitucionalhttps://digital.bl.fcen.uba.ar/Universidad públicaNo correspondehttps://digital.bl.fcen.uba.ar/cgi-bin/oaiserver.cgiana@bl.fcen.uba.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:18962025-12-18 09:00:15.651Biblioteca Digital (UBA-FCEN) - Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturalesfalse
dc.title.none.fl_str_mv Extracellular DNA: A major proinflammatory component of Pseudomonas aeruginosa biofilms
title Extracellular DNA: A major proinflammatory component of Pseudomonas aeruginosa biofilms
spellingShingle Extracellular DNA: A major proinflammatory component of Pseudomonas aeruginosa biofilms
Fuxman Bass, J.I.
CD11b antigen
CD18 antigen
CD66b antigen
deoxyribonuclease I
DNA
interleukin 1beta
interleukin 8
lymphocyte antigen
unclassified drug
bacterial DNA
cytokine
article
bacterial strain
biofilm
controlled study
cytokine release
degradation
extracellular matrix
human
leukocyte activation
nonhuman
phagocytosis
priority journal
Pseudomonas aeruginosa
upregulation
biosynthesis
chemistry
confocal microscopy
extracellular fluid
growth, development and aging
immunology
leukocyte activation
metabolism
microbiology
neutrophil
physiology
Biofilms
Cytokines
DNA, Bacterial
Extracellular Fluid
Humans
Microscopy, Confocal
Neutrophil Activation
Neutrophils
Pseudomonas aeruginosa
title_short Extracellular DNA: A major proinflammatory component of Pseudomonas aeruginosa biofilms
title_full Extracellular DNA: A major proinflammatory component of Pseudomonas aeruginosa biofilms
title_fullStr Extracellular DNA: A major proinflammatory component of Pseudomonas aeruginosa biofilms
title_full_unstemmed Extracellular DNA: A major proinflammatory component of Pseudomonas aeruginosa biofilms
title_sort Extracellular DNA: A major proinflammatory component of Pseudomonas aeruginosa biofilms
dc.creator.none.fl_str_mv Fuxman Bass, J.I.
Russo, D.M.
Gabelloni, M.L.
Geffner, J.R.
Giordano, M.
Catalano, M.
Zorreguieta, Á.
Trevani, A.S.
author Fuxman Bass, J.I.
author_facet Fuxman Bass, J.I.
Russo, D.M.
Gabelloni, M.L.
Geffner, J.R.
Giordano, M.
Catalano, M.
Zorreguieta, Á.
Trevani, A.S.
author_role author
author2 Russo, D.M.
Gabelloni, M.L.
Geffner, J.R.
Giordano, M.
Catalano, M.
Zorreguieta, Á.
Trevani, A.S.
author2_role author
author
author
author
author
author
author
dc.subject.none.fl_str_mv CD11b antigen
CD18 antigen
CD66b antigen
deoxyribonuclease I
DNA
interleukin 1beta
interleukin 8
lymphocyte antigen
unclassified drug
bacterial DNA
cytokine
article
bacterial strain
biofilm
controlled study
cytokine release
degradation
extracellular matrix
human
leukocyte activation
nonhuman
phagocytosis
priority journal
Pseudomonas aeruginosa
upregulation
biosynthesis
chemistry
confocal microscopy
extracellular fluid
growth, development and aging
immunology
leukocyte activation
metabolism
microbiology
neutrophil
physiology
Biofilms
Cytokines
DNA, Bacterial
Extracellular Fluid
Humans
Microscopy, Confocal
Neutrophil Activation
Neutrophils
Pseudomonas aeruginosa
topic CD11b antigen
CD18 antigen
CD66b antigen
deoxyribonuclease I
DNA
interleukin 1beta
interleukin 8
lymphocyte antigen
unclassified drug
bacterial DNA
cytokine
article
bacterial strain
biofilm
controlled study
cytokine release
degradation
extracellular matrix
human
leukocyte activation
nonhuman
phagocytosis
priority journal
Pseudomonas aeruginosa
upregulation
biosynthesis
chemistry
confocal microscopy
extracellular fluid
growth, development and aging
immunology
leukocyte activation
metabolism
microbiology
neutrophil
physiology
Biofilms
Cytokines
DNA, Bacterial
Extracellular Fluid
Humans
Microscopy, Confocal
Neutrophil Activation
Neutrophils
Pseudomonas aeruginosa
dc.description.none.fl_txt_mv We previously demonstrated that extracellular bacterial DNA activates neutrophils through a CpG- and TLR9-independent mechanism. Biofilms are microbial communities enclosed in a polymeric matrix that play a critical role in the pathogenesis of many infectious diseases. Because extracellular DNA is a key component of biofilms of different bacterial species, the aim of this study was to determine whether it plays a role in the ability of biofilms to induce human neutrophil activation. We found that degradation of matrix extracellular DNA with DNase I markedly reduced the capacity of Pseudomonas aeruginosa biofilms to induce the release of the neutrophil proinflammatory cytokines IL-8 and IL-1β (>75%); reduced the upregulation of neutrophil activation markers CD18, CD11b, and CD66b (p < 0.001); reduced the number of bacteria phagocytosed per neutrophil contacting the biofilm; and reduced the production of neutrophil extracellular traps. Consistent with these findings, we found that biofilms formed by the lasI rhlI P. aeruginosa mutant strain, exhibiting a very low content of matrix extracellular DNA, displayed a lower capacity to stimulate the release of proinflammatory cytokines by neutrophils, which was not decreased further by DNase I treatment. Together, our findings support that matrix extracellular DNA is a major proinflammatory component of P. aeruginosa biofilms. Copyright © 2010 by The American Association of Immunologists, Inc.
Fil:Fuxman Bass, J.I. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.
Fil:Russo, D.M. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.
Fil:Gabelloni, M.L. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.
Fil:Giordano, M. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.
Fil:Zorreguieta, Á. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.
Fil:Trevani, A.S. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales; Argentina.
description We previously demonstrated that extracellular bacterial DNA activates neutrophils through a CpG- and TLR9-independent mechanism. Biofilms are microbial communities enclosed in a polymeric matrix that play a critical role in the pathogenesis of many infectious diseases. Because extracellular DNA is a key component of biofilms of different bacterial species, the aim of this study was to determine whether it plays a role in the ability of biofilms to induce human neutrophil activation. We found that degradation of matrix extracellular DNA with DNase I markedly reduced the capacity of Pseudomonas aeruginosa biofilms to induce the release of the neutrophil proinflammatory cytokines IL-8 and IL-1β (>75%); reduced the upregulation of neutrophil activation markers CD18, CD11b, and CD66b (p < 0.001); reduced the number of bacteria phagocytosed per neutrophil contacting the biofilm; and reduced the production of neutrophil extracellular traps. Consistent with these findings, we found that biofilms formed by the lasI rhlI P. aeruginosa mutant strain, exhibiting a very low content of matrix extracellular DNA, displayed a lower capacity to stimulate the release of proinflammatory cytokines by neutrophils, which was not decreased further by DNase I treatment. Together, our findings support that matrix extracellular DNA is a major proinflammatory component of P. aeruginosa biofilms. Copyright © 2010 by The American Association of Immunologists, Inc.
publishDate 2010
dc.date.none.fl_str_mv 2010
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/20.500.12110/paper_00221767_v184_n11_p6386_FuxmanBass
url http://hdl.handle.net/20.500.12110/paper_00221767_v184_n11_p6386_FuxmanBass
dc.language.none.fl_str_mv eng
language eng
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
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eu_rights_str_mv openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/2.5/ar
dc.format.none.fl_str_mv application/pdf
dc.source.none.fl_str_mv J. Immunol. 2010;184(11):6386-6395
reponame:Biblioteca Digital (UBA-FCEN)
instname:Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturales
instacron:UBA-FCEN
reponame_str Biblioteca Digital (UBA-FCEN)
collection Biblioteca Digital (UBA-FCEN)
instname_str Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturales
instacron_str UBA-FCEN
institution UBA-FCEN
repository.name.fl_str_mv Biblioteca Digital (UBA-FCEN) - Universidad Nacional de Buenos Aires. Facultad de Ciencias Exactas y Naturales
repository.mail.fl_str_mv ana@bl.fcen.uba.ar
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