Navegar

Colección

Datos Estadísticas

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:

Bacterial DNA activates neutrophils through a CpG- and TLR9-independent mechanism. Neutrophil activation does not require DNA internalization, suggesting that it results from the interaction of bacterial DNA with a neutrophil surface receptor. The aim of this study was to characterize the interaction of bacterial DNA with the neutrophil surface. Bacterial DNA binding showed saturation and was inhibited by unlabeled DNA but not by other polyanions like yeast tRNA and poly-A. Resembling the conditions under which bacterial DNA triggers neutrophil activation, binding was not modified in the presence or absence of calcium, magnesium or serum. Treatment of neutrophils with proteases not only dramatically reduced bacterial DNA binding but also inhibited neutrophil activation induced by bacterial DNA. Experiments performed with DNA samples of different lengths obtained after digestion of bacterial DNA with DNase showed that only DNA fragments greater than ≈170-180 nucleotides competed bacterial DNA binding and retained the ability to trigger cell activation. Treatment of neutrophils with chemoattractants or conventional agonists significantly increased bacterial DNA binding. Moreover, neutrophils that underwent transmigration through human endothelial cell monolayers even in the absence of chemoattractants, exhibited higher binding levels of bacterial DNA. Together, our findings provide evidence that binding of bacterial DNA to neutrophils is a receptor-mediated process that conditions the ability of DNA to trigger cell activation. We speculate that neutrophil recognition of bacterial DNA might be modulated by the balance of agonists present at inflammatory foci. This effect might be relevant in bacterial infections with a biofilm etiology, in which extracellular DNA could function as a potent neutrophil agonist. © 2008 USCAP, Inc All rights reserved.

Registro:

Documento: Artículo
Título:Characterization of bacterial DNA binding to human neutrophil surface
Autor:Fuxman Bass, J.I.; Gabelloni, M.L.; Alvarez, M.E.; Vermeulen, M.E.; Russo, D.M.; Zorreguieta, Á.; Geffner, J.R.; 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, IIB-BA CONICET, Buenos Aires, Argentina
Department of Immunology, IIHEMA-Academia Nacional de Medicina, Pacheco de Melo 3081, 1425 Buenos Aires, Argentina
Palabras clave:Bacterial DNA binding; Biofilm; CpG; Inflammation; Neutrophils; TLR9; bacterial DNA; chemoattractant; deoxyribonuclease; article; biotinylation; cell culture; cell isolation; cell migration; cell surface; controlled study; DNA binding; human; human cell; neutrophil; priority journal; Base Sequence; Biofilms; Cells, Cultured; DNA Primers; DNA, Bacterial; Escherichia coli; Humans; Neutrophils
Año:2008
Volumen:88
Número:9
Página de inicio:926
Página de fin:937
DOI: http://dx.doi.org/10.1038/labinvest.2008.59
Título revista:Laboratory Investigation
Título revista abreviado:Lab. Invest.
ISSN:00236837
CODEN:LAINA
CAS:deoxyribonuclease, 37211-67-9; DNA Primers; DNA, Bacterial
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_00236837_v88_n9_p926_FuxmanBass.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00236837_v88_n9_p926_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., Neutrophils: Molecules, functions and pathophysiological aspects (2000) Lab Invest, 80, pp. 617-653
  • Hemmi, H., Takeuchi, O., Kawai, T., A Toll-like receptor recognizes bacterial DNA (2000) Nature, 408, pp. 740-745
  • Ishii, K.J., Akira, S., Innate immune recognition of, and regulation by, DNA (2006) Trends Immunol, 27, pp. 525-532
  • Kawai, T., Akira, S., TLR signaling (2006) Cell Death Differ, 13, pp. 816-825
  • Trevani, A.S., Chorny, A., Salamone, G., 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., Neutrophil signaling pathways activated by bacterial DNA stimulation (2006) J Immunol, 177, pp. 4037-4046
  • Yoshinaga, T., Yasuda, K., Ogawa, Y., Efficient uptake and rapid degradation of plasmid DNA by murine dendritic cells via a specific mechanism (2002) Biochem Biophys Res Commun, 299, pp. 389-394
  • Wang, Y., Krieg, A.M., Synergy between CpG- or non-CpG DNA and specific antigen for B cell activation (2003) Int Immunol, 15, pp. 223-231
  • Elias, F., Flo, J., Lopez, R.A., Strong cytosine-guanosine- independent immunostimulation in humans and other primates by synthetic oligodeoxynucleotides with PyNTTTTGT motifs (2003) J Immunol, 171, pp. 3697-3704
  • Yasuda, K., Yu, P., Kirschning, C.J., Endosomal translocation of vertebrate DNA activates dendritic cells via TLR9-dependent and -independent pathways (2005) J Immunol, 174, pp. 6129-6136
  • Yasuda, K., Rutz, M., Schlatter, B., CpG motif-independent activation of TLR9 upon endosomal translocation of 'natural' phosphodiester DNA (2006) Eur J Immunol, 36, pp. 431-436
  • Zhao, H., Hemmi, H., Akira, S., Contribution of Toll-like receptor 9 signaling to the acute inflammatory response to nonviral vectors (2004) Mol Ther, 9, pp. 241-248
  • Stetson, D.B., Medzhitov, R., Recognition of cytosolic DNA activates an IRF3-dependent innate immune response (2006) Immunity, 24, pp. 93-103
  • Krieg, A.M., CpG motifs in bacterial DNA and their immune effects (2002) Annu Rev Immunol, 20, pp. 709-760
  • Lorenz, M.G., Gerjets, D., Wackernagel, W., Release of transforming plasmid and chromosomal DNA from two cultured soil bacteria (1991) Arch Microbiol, 156, pp. 319-326
  • Lorenz, M.G., Wackernagel, W., Bacterial gene transfer by natural genetic transformation in the environment (1994) Microbiol Rev, 58, pp. 563-602
  • Allesen-Holm, M., Barken, K.B., Yang, L., A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms (2006) Mol Microbiol, 59, pp. 1114-1128
  • Palchevskiy, V., Finkel, S.E., Escherichia coli competence gene homologs are essential for competitive fitness and the use of DNA as a nutrient (2006) J Bacteriol, 188, pp. 3902-3910
  • Moscoso, M., Claverys, J.P., Release of DNA into the medium by competent Streptococcus pneumoniae: Kinetics, mechanism and stability of the liberated DNA (2004) Mol Microbiol, 54, pp. 783-794
  • Ottolenghi, E., Hotchkiss, R.D., Appearance of genetic transforming activity in pneumococcal cultures (1960) Science, 132, pp. 1257-1258
  • Steinberger, R.E., Holden, P.A., Extracellular DNA in single- and multiple-species unsaturated biofilms (2005) Appl Environ Microbiol, 71, pp. 5404-5410
  • Steinmoen, H., Knutsen, E., Havarstein, 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
  • Whitchurch, C.B., Tolker-Nielsen, T., Ragas, P.C., Extracellular DNA required for bacterial biofilm formation (2002) Science, 295, p. 1487
  • 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
  • Soler-Rodriguez, A.M., Zhang, H., Lichenstein, H.S., Neutrophil activation by bacterial lipoprotein versus lipopolysaccharide: Differential requirements for serum and CD14 (2000) J Immunol, 164, pp. 2674-2683
  • Hailman, E., Lichenstein, H.S., Wurfel, M.M., Lipopolysaccharide (LPS)-binding protein accelerates the binding of LPS to CD14 (1994) J Exp Med, 179, pp. 269-277
  • Jaffe, E.A., Nachman, R.L., Becker, C.G., Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria (1973) J Clin Invest, 52, pp. 2745-2756
  • Issekutz, A.C., Chuluyan, H.E., Lopes, N., CD11/CD18-independent transendothelial migration of human polymorphonuclear leukocytes and monocytes: Involvement of distinct and unique mechanisms (1995) J Leukoc Biol, 57, pp. 553-561
  • Krieg, A.M., Yi, A.K., Matson, S., CpG motifs in bacterial DNA trigger direct B-cell activation (1995) Nature, 374, pp. 546-549
  • Sun, S., Beard, C., Jaenisch, R., Mitogenicity of DNA from different organisms for murine B cells (1997) J Immunol, 159, pp. 3119-3125
  • Middelhoven, P.J., Van Buul, J.D., Hordijk, P.L., Different proteolytic mechanisms involved in Fc gamma RIIIb shedding from human neutrophils (2001) Clin Exp Immunol, 125, pp. 169-175
  • Gaudry, M., Bregerie, O., Andrieu, V., Intracellular pool of vascular endothelial growth factor in human neutrophils (1997) Blood, 90, pp. 4153-4161
  • Borregaard, N., Sorensen, O.E., Theilgaard-Monch, K., Neutrophil granules: A library of innate immunity proteins (2007) Trends Immunol, 28, pp. 340-345
  • Bennett, R.M., Gabor, G.T., Merritt, M.M., DNA binding to human leukocytes. Evidence for a receptor-mediated association, internalization, and degradation of DNA (1985) J Clin Invest, 76, pp. 2182-2190
  • Loke, S.L., Stein, C.A., Zhang, X.H., Characterization of oligonucleotide transport into living cells (1989) Proc Natl Acad Sci USA, 86, pp. 3474-3478
  • Yakubov, L.A., Deeva, E.A., Zarytova, V.F., Mechanism of oligonucleotide uptake by cells: Involvement of specific receptors? (1989) Proc Natl Acad Sci USA, 86, pp. 6454-6458
  • Basner-Tschakarjan, E., Mirmohammadsadegh, A., Baer, A., Uptake and trafficking of DNA in keratinocytes: Evidence for DNA-binding proteins (2004) Gene Therapy, 11, pp. 765-774
  • Benimetskaya, L., Loike, J.D., Khaled, Z., Mac-1 (CD11b/CD18) is an oligodeoxynucleotide-binding protein (1997) Nat Med, 3, pp. 414-420
  • Emlen, W., Rifai, A., Magilavy, D., Hepatic binding of DNA is mediated by a receptor on nonparenchymal cells (1988) Am J Pathol, 133, pp. 54-60
  • Zhu, F.G., Reich, C.F., Pisetsky, D.S., The role of the macrophage scavenger receptor in immune stimulation by bacterial DNA and synthetic oligonucleotides (2001) Immunology, 103, pp. 226-234
  • McCoy, S.L., Kurtz, S.E., Hausman, F.A., Activation of RAW264.7 macrophages by bacterial DNA and lipopolysaccharide increases cell surface DNA binding and internalization (2004) J Biol Chem, 279, pp. 17217-17223
  • Kindrachuk, J., Potter, J.E., Brownlie, R., Nucleic acids exert a sequence-independent cooperative effect on sequence-dependent activation of Toll-like receptor 9 (2007) J Biol Chem, 282, pp. 13944-13953
  • Rutz, M., Metzger, J., Gellert, T., Toll-like receptor 9 binds single-stranded CpG-DNA in a sequence- and pH-dependent manner (2004) Eur J Immunol, 34, pp. 2541-2550
  • Latz, E., Verma, A., Visintin, A., Ligand-induced conformational changes allosterically activate Toll-like receptor 9 (2007) Nat Immunol, 8, pp. 772-779
  • Brinkmann, V., Zychlinsky, A., Beneficial suicide: Why neutrophils die to make NETs (2007) Nat Rev Microbiol, 5, pp. 577-582
  • Brinkmann, V., Reichard, U., Goosmann, C., Neutrophil extracellular traps kill bacteria (2004) Science, 303, pp. 1532-1535
  • Boxer, L.A., Haak, R.A., Yang, H.H., Membrane-bound lactoferrin alters the surface properties of polymorphonuclear leukocytes (1982) J Clin Invest, 70, pp. 1049-1057
  • Bennett, R.M., Davis, J., Lactoferrin interacts with deoxyribonucleic acid: A preferential reactivity with double-stranded DNA and dissociation of DNA-anti-DNA complexes (1982) J Lab Clin Med, 99, pp. 127-138
  • Romanowski, G., Lorenz, M.G., Wackernagel, W., Adsorption of plasmid DNA to mineral surfaces and protection against DNase I (1991) Appl Environ Microbiol, 57, pp. 1057-1061
  • Romanowski, G., Lorenz, M.G., Sayler, G., Persistence of free plasmid DNA in soil monitored by various methods, including a transformation assay (1992) Appl Environ Microbiol, 58, pp. 3012-3019
  • Romanowski, G., Lorenz, M.G., Wackernagel, W., Plasmid DNA in a groundwater aquifer microcosm - adsorption, DNAase resistance and natural genetic transformation of Bacillus subtilis (1993) Mol Ecol, 2, pp. 171-181
  • Matsukawa, M., Greenberg, E.P., Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development (2004) J Bacteriol, 186, pp. 4449-4456

Citas:

---------- APA ----------
Fuxman Bass, J.I., Gabelloni, M.L., Alvarez, M.E., Vermeulen, M.E., Russo, D.M., Zorreguieta, Á., Geffner, J.R.,..., Trevani, A.S. (2008) . Characterization of bacterial DNA binding to human neutrophil surface. Laboratory Investigation, 88(9), 926-937.
http://dx.doi.org/10.1038/labinvest.2008.59
---------- CHICAGO ----------
Fuxman Bass, J.I., Gabelloni, M.L., Alvarez, M.E., Vermeulen, M.E., Russo, D.M., Zorreguieta, Á., et al. "Characterization of bacterial DNA binding to human neutrophil surface" . Laboratory Investigation 88, no. 9 (2008) : 926-937.
http://dx.doi.org/10.1038/labinvest.2008.59
---------- MLA ----------
Fuxman Bass, J.I., Gabelloni, M.L., Alvarez, M.E., Vermeulen, M.E., Russo, D.M., Zorreguieta, Á., et al. "Characterization of bacterial DNA binding to human neutrophil surface" . Laboratory Investigation, vol. 88, no. 9, 2008, pp. 926-937.
http://dx.doi.org/10.1038/labinvest.2008.59
---------- VANCOUVER ----------
Fuxman Bass, J.I., Gabelloni, M.L., Alvarez, M.E., Vermeulen, M.E., Russo, D.M., Zorreguieta, Á., et al. Characterization of bacterial DNA binding to human neutrophil surface. Lab. Invest. 2008;88(9):926-937.
http://dx.doi.org/10.1038/labinvest.2008.59