Artículo

Este artículo es de Acceso Abierto y puede ser descargado en su versión final desde nuestro repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

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.

Registro:

Documento: Artículo
Título:Extracellular DNA: A major proinflammatory component of Pseudomonas aeruginosa biofilms
Autor:Fuxman Bass, J.I.; Russo, D.M.; Gabelloni, M.L.; Geffner, J.R.; Giordano, M.; Catalano, M.; Zorreguieta, Á.; Trevani, A.S.
Filiación:Departamento de Inmunología, Instituto de Investigaciones Hematológicas, Academia Nacional de Medicina, Buenos Aires, Argentina
Departamento de Fisiología y Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Departamento de Microbiología, Facultad de Medicina, Universidad de Buenos Aires, Buenos Aires, Argentina
Fundación Instituto Leloir, Instituto de Investigaciones Bioquímicas, Buenos Aires CONICET, Buenos Aires, Argentina
Palabras clave: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
Año:2010
Volumen:184
Número:11
Página de inicio:6386
Página de fin:6395
DOI: http://dx.doi.org/10.4049/jimmunol.0901640
Título revista:Journal of Immunology
Título revista abreviado:J. Immunol.
ISSN:00221767
CODEN:JOIMA
CAS:DNA, 9007-49-2; deoxyribonuclease I, 9003-98-9; interleukin 8, 114308-91-7; Cytokines; DNA, Bacterial
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_00221767_v184_n11_p6386_FuxmanBass.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00221767_v184_n11_p6386_FuxmanBass

Referencias:

  • Nathan, C., Neutrophils and immunity: Challenges and opportunities (2006) Nat. Rev. Immunol., 6, pp. 173-182
  • Witko-Sarsat, V., Rieu, P., Descamps-Latscha, B., Lesavre, P., Halbwachs-Mecarelli, L., Neutrophils: Molecules, functions and pathophysiological aspects (2000) Lab. Invest., 80, pp. 617-653
  • Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., Matsumoto, M., Akira, S., A Toll-like receptor recognizes bacterial DNA (2000) Nature, 408 (6813), pp. 740-745. , DOI 10.1038/35047123
  • Ishii, K.J., Akira, S., Innate immune recognition of, and regulation by, DNA (2006) Trends in Immunology, 27 (11), pp. 525-532. , DOI 10.1016/j.it.2006.09.002, PII S1471490606002602
  • Kawai, T., Akira, S., TLR signaling (2006) Cell Death Differ., 13, pp. 816-825
  • Ishii, K.J., Coban, C., Kato, H., Takahashi, K., Torii, Y., Takeshita, F., Ludwig, H., Hemmi, H., A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA (2006) Nat. Immunol., 7, pp. 40-48
  • Hornung, V., Ablasser, A., Charrel-Dennis, M., Bauernfeind, F., Horvath, G., Caffrey, D.R., Latz, E., Fitzgerald, K.A., AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC (2009) Nature, 458, pp. 514-518
  • Ablasser, A., Bauernfeind, F., Hartmann, G., Latz, E., Fitzgerald, K.A., Hornung, V., RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate (2009) Nat. Immunol., 10, pp. 1065-1072
  • Chiu, Y.H., Macmillan, J.B., Chen, Z.J., RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway (2009) Cell, 138, pp. 576-591
  • Trevani, A.S., Chorny, A., Salamone, G., Vermeulen, M., Gamberale, R., Schettini, J., Raiden, S., Geffner, J., Bacterial DNA activates human neutrophils by a CpG-independent pathway (2003) Eur. J. Immunol., 33, pp. 3164-3174
  • Alvarez, M.E., Fuxman Bass, J.I., Geffner, J.R., Calotti, P.X., Costas, M., Coso, O.A., Gamberale, R., Martinez, D., Neutrophil signaling pathways activated by bacterial DNA stimulation (2006) J. Immunol., 177, pp. 4037-4046
  • Fuxman Bass, J.I., Gabelloni, M.L., Alvarez, M.E., Vermeulen, M.E., Russo, D.M., Zorreguieta, A., Geffner, J.R., Trevani, A.S., Characterization of bacterial DNA binding to human neutrophil surface (2008) Lab. Invest., 88, pp. 926-937
  • Whitchurch, C.B., Tolker-Nielsen, T., Ragas, P.C., Mattick, J.S., Extracellular DNA required for bacterial biofilm formation (2002) Science, 295, p. 1487
  • Costerton, J.W., Stewart, P.S., Greenberg, E.P., Bacterial biofilms: A common cause of persistent infections (1999) Science, 284, pp. 1318-1322
  • Hall-Stoodley, L., Costerton, J.W., Stoodley, P., Bacterial biofilms: From the natural environment to infectious diseases (2004) Nat. Rev. Microbiol., 2, pp. 95-108
  • Donlan, R.M., Costerton, J.W., Biofilms: Survival mechanisms of clinically relevant microorganisms (2002) Clin. Microbiol. Rev., 15, pp. 167-193
  • Parsek, M.R., Singh, P.K., Bacterial biofilms: An emerging link to disease pathogenesis (2003) Annu. Rev. Microbiol., 57, pp. 677-701
  • Hall-Stoodley, L., Stoodley, P., Evolving concepts in biofilm infections (2009) Cell. Microbiol., 11, pp. 1034-1043
  • James, G.A., Swogger, E., Wolcott, R., Pulcini, E., Secor, P., Sestrich, J., Costerton, J.W., Stewart, P.S., Biofilms in chronic wounds (2008) Wound Repair Regen., 16, pp. 37-44
  • Fux, C.A., Costerton, J.W., Stewart, P.S., Stoodley, P., Survival strategies of infectious biofilms (2005) Trends Microbiol., 13, pp. 34-40
  • Gilbert, P., Das, J., Foley, I., Biofilm susceptibility to antimicrobials (1997) Adv. Dent. Res., 11, pp. 160-167
  • Del Pozo, J.L., Patel, R., The challenge of treating biofilm-associated bacterial infections (2007) Clin. Pharmacol. Ther., 82, pp. 204-209
  • Mah, T.F., O'Toole, G.A., Mechanisms of biofilm resistance to antimicrobial agents (2001) Trends Microbiol., 9, pp. 34-39
  • Mah, T.F., Pitts, B., Pellock, B., Walker, G.C., Stewart, P.S., O'Toole, G.A., A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance (2003) Nature, 426, pp. 306-310
  • Lewis, K., Multidrug tolerance of biofilms and persister cells (2008) Curr. Top. Microbiol. Immunol., 322, pp. 107-131
  • Anderson, G.G., O'Toole, G.A., Innate and induced resistance mechanisms of bacterial biofilms (2008) Curr. Top. Microbiol. Immunol., 322, pp. 85-105
  • Nemoto, K., Hirota, K., Murakami, K., Taniguti, K., Murata, H., Viducic, D., Miyake, Y., Effect of Varidase (streptodornase) on biofilm formed by Pseudomonas aeruginosa (2003) Chemotherapy, 49 (3), pp. 121-125. , DOI 10.1159/000070617
  • Murakawa, T., Slime production by Pseudomonas aeruginosa. IV. Chemical analysis of two varieties of slime produced by Pseudomonas aeruginosa (1973) Jpn. J. Microbiol., 17, pp. 513-520
  • Murakawa, T., Slime production by Pseudomonas aeruginosa. 3. Purification of slime and its physicochemical properties (1973) Jpn. J. Microbiol., 17, pp. 273-281
  • Petersen, F.C., Tao, L., Scheie, A.A., DNA binding-uptake system: A link between cell-to-cell communication and biofilm formation (2005) J. Bacteriol., 187, pp. 4392-4400
  • Thomas, V.C., Thurlow, L.R., Boyle, D., Hancock, L.E., Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development (2008) J. Bacteriol., 190, pp. 5690-5698
  • Qin, Z., Ou, Y., Yang, L., Zhu, Y., Tolker-Nielsen, T., Molin, S., Qu, D., Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis (2007) Microbiology, 153 (7), pp. 2083-2092. , DOI 10.1099/mic.0.2007/006031-0
  • Izano, E.A., Amarante, M.A., Kher, W.B., Kaplan, J.B., Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms (2008) Appl. Environ. Microbiol., 74, pp. 470-476
  • Moscoso, M., Garcia, E., Lopez, R., Biofilm formation by Streptococcus pneumoniae: Role of choline, extracellular DNA, and capsular polysaccharide in microbial accretion (2006) Journal of Bacteriology, 188 (22), pp. 7785-7795. , DOI 10.1128/JB.00673-06
  • Jurcisek, J.A., Bakaletz, L.O., Biofilms formed by nontypeable Haemophilus influenzae in vivo contain both double-stranded DNA and type IV pilin protein (2007) J. Bacteriol., 189, pp. 3868-3875
  • Jesaitis, A.J., Franklin, M.J., Berglund, D., Sasaki, M., Lord, C.I., Bleazard, J.B., Duffy, J.E., Lewandowski, Z., Compromised host defense on Pseudomonas aeruginosa biofilms: Characterization of neutrophil and biofilm interactions (2003) J. Immunol., 171, pp. 4329-4339
  • Jensen, E.T., Kharazmi, A., Lam, K., Costerton, J.W., Høiby, N., Human polymorphonuclear leukocyte response to Pseudomonas aeruginosa grown in biofilms (1990) Infect. Immun., 58, pp. 2383-2385
  • Steinberg, D., Poran, S., Shapira, L., The effect of extracellular polysaccharides from Streptococcus mutans on the bactericidal activity of human neutrophils (1999) Arch. Oral Biol., 44, pp. 437-444
  • Bjarnsholt, T., Jensen, P.O., Burmolle, M., Hentzer, M., Haagensen, J.A.J., Hougen, H.P., Calum, H., Givskov, M., Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent (2005) Microbiology, 151 (2), pp. 373-383. , DOI 10.1099/mic.0.27463-0
  • Jensen, P.O., Bjarnsholt, T., Phipps, R., Rasmussen, T.B., Calum, H., Christoffersen, L., Moser, C., Høiby, N., Rapid necrotic killing of polymorphonuclear leukocytes is caused by quorum-sensing-controlled production of rhamnolipid by Pseudomonas aeruginosa (2007) Microbiology, 153, pp. 1329-1338
  • Walker, T.S., Tomlin, K.L., Worthen, G.S., Poch, K.R., Lieber, J.G., Saavedra, M.T., Fessler, M.B., Nick, J.A., Enhanced Pseudomonas aeruginosa biofilm development mediated by human neutrophils (2005) Infect. Immun., 73, pp. 3693-3701
  • Allesen-Holm, M., Barken, K.B., Yang, L., Klausen, M., Webb, J.S., Kjelleberg, S., Molin, S., Tolker-Nielsen, T., A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms (2006) Mol. Microbiol., 59, pp. 1114-1128
  • O'Toole, G.A., Pratt, L.A., Watnick, P.I., Newman, D.K., Weaver, V.B., Kolter, R., Genetic approaches to study of biofilms (1999) Methods Enzymol., 310, pp. 91-109
  • Steinberger, R.E., Holden, P.A., Extracellular DNA in single- and multiple-species unsaturated biofilms (2005) Appl. Environ. Microbiol., 71, pp. 5404-5410
  • Zouali, M., Stollar, B.D., A rapid ELISA for measurement of antibodies to nucleic acid antigens using UV-treated polystyrene microplates (1986) J. Immunol. Methods, 90, pp. 105-110
  • Schwartz, J., Leidal, K.G., Femling, J.K., Weiss, J.P., Nauseef, W.M., Neutrophil bleaching of GFP-expressing staphylococci: Probing the intraphagosomal fate of individual bacteria (2009) J. Immunol., 183, pp. 2632-2641
  • Moulton, P., Martin, H., Ainger, A., Cross, A., Hoare, C., Doel, J., Harrison, R., Hancock, J., The inhibition of flavoproteins by phenoxaiodonium, a new iodonium analogue (2000) Eur. J. Pharmacol., 401, pp. 115-120
  • Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D.S., Weinrauch, Y., Zychlinsky, A., Neutrophil Extracellular Traps Kill Bacteria (2004) Science, 303 (5663), pp. 1532-1535. , DOI 10.1126/science.1092385
  • Smith, E.E., Buckley, D.G., Wu, Z., Saenphimmachak, C., Hoffman, L.R., D'Argenio, D.A., Miller, S.I., Moskowitz, S.M., Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients (2006) Proc. Natl. Acad. Sci. USA, 103, pp. 8487-8492
  • Pedersen, S.S., Høiby, N., Espersen, F., Koch, C., Role of alginate in infection with mucoid Pseudomonas aeruginosa in cystic fibrosis (1992) Thorax, 47, pp. 6-13
  • Govan, J.R., Deretic, V., Microbial pathogenesis in cystic fibrosis: Mucoid Pseudomonas aeruginosa and Burkholderia cepacia (1996) Microbiol. Rev., 60, pp. 539-574
  • Lyczak, J.B., Cannon, C.L., Pier, G.B., Lung infections associated with cystic fibrosis (2002) Clin. Microbiol. Rev., 15, pp. 194-222
  • Smith, R.S., Iglewski, B.H., P. aeruginosa quorum-sensing systems and virulence (2003) Curr. Opin. Microbiol., 6, pp. 56-60
  • Passador, L., Cook, J.M., Gambello, M.J., Rust, L., Iglewski, B.H., Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication (1993) Science, 260, pp. 1127-1130
  • Latifi, A., Winson, M.K., Foglino, M., Bycroft, B.W., Stewart, G.S., Lazdunski, A., Williams, P., Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1 (1995) Mol. Microbiol., 17, pp. 333-343
  • Latifi, A., Foglino, M., Tanaka, K., Williams, P., Lazdunski, A., A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationaryphase sigma factor RpoS (1996) Mol. Microbiol., 21, pp. 1137-1146
  • Lieberman, J., Inhibition of protease activity in purulent sputum by DNA (1967) J. Lab. Clin. Med., 70, pp. 595-605
  • Kim, J.S., Hackley, G.H., Okamoto, K., Rubin, B.K., Sputum processing for evaluation of inflammatory mediators (2001) Pediatr. Pulmonol., 32, pp. 152-158
  • Lau, D., Mollnau, H., Eiserich, J.P., Freeman, B.A., Daiber, A., Gehling, U.M., Brümmer, J., Heitzer, T., Myeloperoxidase mediates neutrophil activation by association with CD11b/CD18 integrins (2005) Proc. Natl. Acad. Sci. USA, 102, pp. 431-436
  • El Kebir, D., József, L., Pan, W., Filep, J.G., Myeloperoxidase delays neutrophil apoptosis through CD11b/CD18 integrins and prolongs inflammation (2008) Circ. Res., 103, pp. 352-359
  • Plotkowski, M.C., Beck, G., Tournier, J.M., Bernardo-Filho, M., Marques, E.A., Puchelle, E., Adherence of Pseudomonas aeruginosa to respiratory epithelium and the effect of leucocyte elastase (1989) J. Med. Microbiol., 30, pp. 285-293
  • McKenzie, S.G., Chowdhury, S., Strandvik, B., Hodson, M.E., Dornase alfa is well tolerated: Data from the epidemiologic registry of cystic fibrosis (2007) Pediatr. Pulmonol., 42, pp. 928-937. , Investigators of the Epidemiologic Registry of Cystic Fibrosis
  • Paul, K., Rietschel, E., Ballmann, M., Griese, M., Worlitzsch, D., Shute, J., Chen, C., Van Koningsbruggen, S., Effect of treatment with dornase alpha on airway inflammation in patients with cystic fibrosis (2004) Am. J. Respir. Crit. Care Med., 169, pp. 719-725. , Bronchoalveolar Lavage for the Evaluation of Antiinflammatory Treatment Study Group
  • Matsukawa, M., Greenberg, E.P., Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development (2004) J. Bacteriol., 186, pp. 4449-4456
  • Webb, J.S., Thompson, L.S., James, S., Charlton, T., Tolker-Nielsen, T., Koch, B., Givskov, M., Kjelleberg, S., Cell death in Pseudomonas aeruginosa biofilm development (2003) Journal of Bacteriology, 185 (15), pp. 4585-4592. , DOI 10.1128/JB.185.15.4585-4592.2003
  • Palmen, R., Hellingwerf, K.J., Acinetobacter calcoaceticus liberates chromosomal DNA during induction of competence by cell lysis (1995) Curr. Microbiol., 30, pp. 7-10
  • Steinmoen, H., Knutsen, E., Håvarstein, L.S., Induction of natural competence in Streptococcus pneumoniae triggers lysis and DNA release from a subfraction of the cell population (2002) Proc. Natl. Acad. Sci. USA, 99, pp. 7681-7686
  • Hendrickx, L., Hausner, M., Wuertz, S., Natural genetic transformation in monoculture Acinetobacter sp. strain BD413 biofilms (2003) Appl. Environ. Microbiol., 69, pp. 1721-1727
  • Wang, B.Y., Chi, B., Kuramitsu, H.K., Genetic exchange between Treponema denticola and Streptococcus gordonii in biofilms (2002) Oral Microbiol. Immunol., 17, pp. 108-112

Citas:

---------- APA ----------
Fuxman Bass, J.I., Russo, D.M., Gabelloni, M.L., Geffner, J.R., Giordano, M., Catalano, M., Zorreguieta, Á.,..., Trevani, A.S. (2010) . Extracellular DNA: A major proinflammatory component of Pseudomonas aeruginosa biofilms. Journal of Immunology, 184(11), 6386-6395.
http://dx.doi.org/10.4049/jimmunol.0901640
---------- CHICAGO ----------
Fuxman Bass, J.I., Russo, D.M., Gabelloni, M.L., Geffner, J.R., Giordano, M., Catalano, M., et al. "Extracellular DNA: A major proinflammatory component of Pseudomonas aeruginosa biofilms" . Journal of Immunology 184, no. 11 (2010) : 6386-6395.
http://dx.doi.org/10.4049/jimmunol.0901640
---------- MLA ----------
Fuxman Bass, J.I., Russo, D.M., Gabelloni, M.L., Geffner, J.R., Giordano, M., Catalano, M., et al. "Extracellular DNA: A major proinflammatory component of Pseudomonas aeruginosa biofilms" . Journal of Immunology, vol. 184, no. 11, 2010, pp. 6386-6395.
http://dx.doi.org/10.4049/jimmunol.0901640
---------- VANCOUVER ----------
Fuxman Bass, J.I., Russo, D.M., Gabelloni, M.L., Geffner, J.R., Giordano, M., Catalano, M., et al. Extracellular DNA: A major proinflammatory component of Pseudomonas aeruginosa biofilms. J. Immunol. 2010;184(11):6386-6395.
http://dx.doi.org/10.4049/jimmunol.0901640