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:

Brucella is an intracellular pathogen responsible of a zoonotic disease called brucellosis. Brucella survives and proliferates within several types of phagocytic and non-phagocytic cells. Like in other pathogens, adhesion of brucellae to host surfaces was proposed to be an important step in the infection process. Indeed, Brucella has the capacity to bind to culture human cells and key components of the extracellular matrix, such as fibronectin. However, little is known about the molecular bases of Brucella adherence. In an attempt to identify bacterial genes encoding adhesins, a phage display library of Brucella suis was panned against fibronectin. Three fibronectin-binding proteins of B. suis were identified using this approach. One of the candidates, designated BmaC was a very large protein of 340kDa that is predicted to belong to the type I (monomeric) autotransporter family. Microscopy studies showed that BmaC is located at one pole on the bacterial surface. The phage displaying the fibronectin-binding peptide of BmaC inhibited the attachment of brucellae to both, HeLa cells and immobilized fibronectin in vitro. In addition, a bmaC deletion mutant was impaired in the ability of B. suis to attach to immobilized fibronectin and to the surface of HeLa and A549 cells and was out-competed by the wild-type strain in co-infection experiments. Finally, anti-fibronectin or anti-BmaC antibodies significantly inhibited the binding of wild-type bacteria to HeLa cells. Our results highlight the role of a novel monomeric autotransporter protein in the adhesion of B. suis to the extracellular matrix and non-phagocytic cells via fibronectin binding. © 2012 Blackwell Publishing Ltd.

Registro:

Documento: Artículo
Título:BmaC, a novel autotransporter of Brucella suis, is involved in bacterial adhesion to host cells
Autor:Posadas, D.M.; Ruiz-Ranwez, V.; Bonomi, H.R.; Martín, F.A.; Zorreguieta, A.
Filiación:Fundación Instituto Leloir, IIBBA CONICET and FCEyN, Universidad de Buenos Aires, Patricias Argentinas 435, (C1405BWE) Buenos Aires, Argentina
Institut Pasteur, Unité de Génétique des Biofilms, Paris, France
Palabras clave:bacterial protein; binding protein; bmac protein; fibronectin; unclassified drug; article; bacterial survival; bacterium adherence; Brucella suis; cell culture; controlled study; HeLa cell; host cell; human; human cell; in vitro study; nonhuman; priority journal; protein immobilization; Adhesins, Bacterial; Animals; Bacterial Adhesion; Brucella suis; Fibronectins; Gene Knockout Techniques; HeLa Cells; Host-Pathogen Interactions; Humans; Immobilized Proteins; Macrophages; Membrane Transport Proteins; Mice; Microbial Viability; Peptide Library; Protein Structure, Tertiary; Sequence Analysis, DNA; Bacteria (microorganisms); Brucella; Brucella melitensis biovar Suis
Año:2012
Volumen:14
Número:6
Página de inicio:965
Página de fin:982
DOI: http://dx.doi.org/10.1111/j.1462-5822.2012.01771.x
Título revista:Cellular Microbiology
Título revista abreviado:Cell. Microbiol.
ISSN:14625814
CODEN:CEMIF
CAS:fibronectin, 86088-83-7; Adhesins, Bacterial; Fibronectins; Immobilized Proteins; Membrane Transport Proteins; Peptide Library
PDF:https://bibliotecadigital.exactas.uba.ar/download/paper/paper_14625814_v14_n6_p965_Posadas.pdf
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_14625814_v14_n6_p965_Posadas

Referencias:

  • Arico, B., Nuti, S., Scarlato, V., Rappuoli, R., Adhesion of Bordetella pertussis to eukaryotic cells requires a time-dependent export and maturation of filamentous hemagglutinin (1993) Proc Natl Acad Sci USA, 90, pp. 9204-9208
  • Bandara, A.B., Sriranganathan, N., Schurig, G.G., Boyle, S.M., Putative outer membrane autotransporter protein influences survival of Brucella suis in BALB/c mice (2005) Vet Microbiol, 109, pp. 95-104
  • Benz, I., Schmidt, M.A., AIDA-I, the adhesin involved in diffuse adherence of the diarrhoeagenic Escherichia coli strain 2787 (O126:H27), is synthesized via a precursor molecule (1992) Mol Microbiol, 6, pp. 1539-1546
  • Bjerketorp, J., Rosander, A., Nilsson, M., Jacobsson, K., Frykberg, L., Sorting a Staphylococcus aureus phage display library against ex vivo biomaterial (2004) J Med Microbiol, 53, pp. 945-951
  • Boschiroli, M.L., Foulongne, V., O'Callaghan, D., Brucellosis: a worldwide zoonosis (2001) Curr Opin Microbiol, 4, pp. 58-64
  • Campbell, G.A., Adams, L.G., Sowa, B.A., Mechanisms of binding of Brucella abortus to mononuclear phagocytes from cows naturally resistant or susceptible to brucellosis (1994) Vet Immunol Immunopathol, 41, pp. 295-306
  • Castañeda-Roldán, E.I., Avelino-Flores, F., Dall'Agnol, M., Freer, E., Cedillo, L., Dornand, J., Giron, J.A., Adherence of Brucella to human epithelial cells and macrophages is mediated by sialic acid residues (2004) Cell Microbiol, 6, pp. 435-445
  • Castañeda-Roldán, E.I., Ouahrani-Bettache, S., Saldana, Z., Avelino, F., Rendon, M.A., Dornand, J., Giron, J.A., Characterization of SP41, a surface protein of Brucella associated with adherence and invasion of host epithelial cells (2006) Cell Microbiol, 8, pp. 1877-1887
  • Celli, J., Gorvel, J.P., Organelle robbery: Brucella interactions with the endoplasmic reticulum (2004) Curr Opin Microbiol, 7, pp. 93-97
  • Chain, P.S., Comerci, D.J., Tolmasky, M.E., Larimer, F.W., Malfatti, S.A., Vergez, L.M., Whole-genome analyses of speciation events in pathogenic Brucellae (2005) Infect Immun, 73, pp. 8353-8361
  • Chain, P.S.G., Comerci, D.J., Tolmasky, M.E., Larimer, F.W., Malfatti, S.A., Vergez, L.M., Whole-genome analyses of speciation events in pathogenic Brucellae (2005) Infect Immun, 73, pp. 8353-8361
  • Charles, M., Perez, M., Kobil, J.H., Goldberg, M.B., Polar targeting of Shigella virulence factor IcsA in Enterobacteriacae and Vibrio (2001) Proc Natl Acad Sci USA, 98, pp. 9871-9876
  • Clarke, S.R., Foster, S.J., Surface adhesins of Staphylococcus aureus (2006) Adv Microb Physiol, 51, pp. 187-224
  • Dautin, N., Bernstein, H.D., Protein secretion in gram-negative bacteria via the autotransporter pathway (2007) Annu Rev Microbiol, 61, pp. 89-112
  • Dautin, N., Barnard, T.J., Anderson, D.E., Bernstein, H.D., Cleavage of a bacterial autotransporter by an evolutionarily convergent autocatalytic mechanism (2007) EMBO J, 26, pp. 1942-1952
  • DelVecchio, V.G., Kapatral, V., Redkar, R.J., Patra, G., Mujer, C., Los, T., The genome sequence of the facultative intracellular pathogen Brucella melitensis (2002) Proc Natl Acad Sci USA, 99, pp. 443-448
  • Ding, J., Pan, Y., Jiang, H., Cheng, J., Liu, T., Qin, N., The whole genome sequences of four Brucella strains (2011) J Bacteriol, 193, pp. 3674-3675
  • Dozot, M., Boigegrain, R.A., Delrue, R.M., Hallez, R., Ouahrani-Bettache, S., Danese, I., The stringent response mediator Rsh is required for Brucella melitensis and Brucella suis virulence, and for expression of the type IV secretion system virB (2006) Cell Microbiol, 8, pp. 1791-1802
  • Ferrero, M.C., Fossati, C.A., Baldi, P.C., Smooth Brucella strains invade and replicate in human lung epithelial cells without inducing cell death (2009) Microbes Infect, 11, pp. 476-483
  • Ferrero, M.C., Bregante, J., Delpino, M.V., Barrionuevo, P., Fossati, C.A., Giambartolomei, G.H., Baldi, P.C., Proinflammatory response of human endothelial cells to Brucella infection (2011) Microbes Infect, 13, pp. 852-861
  • Ficht, T., Brucella taxonomy and evolution (2010) Future Microbiol, 5, pp. 859-866
  • Ficht, T.A., Kahl-McDonagh, M.M., Arenas-Gamboa, A.M., Rice-Ficht, A.C., Brucellosis: the case for live, attenuated vaccines (2009) Vaccine, 27 (4 SUPPL.), pp. D40-D43
  • Foster, T.J., Hook, M., Surface protein adhesins of Staphylococcus aureus (1998) Trends Microbiol, 6, pp. 484-488
  • Gay, B., Mauss, H., Sanchez-Teff, S., Identification of fibronectins in peritoneal macrophages during the phagocytosis of Brucella. An immunocytochemical study by electron microscopy (1986) Virchows Arch B Cell Pathol Incl Mol Pathol, 52, pp. 169-176
  • Giomarelli, B., Visai, L., Hijazi, K., Rindi, S., Ponzio, M., Iannelli, F., Binding of Streptococcus gordonii to extracellular matrix proteins (2006) FEMS Microbiol Lett, 265, pp. 172-177
  • Godefroid, M., Svensson, M.V., Cambier, P., Uzureau, S., Mirabella, A., De Bolle, X., Brucella melitensis 16M produces a mannan and other extracellular matrix components typical of a biofilm (2010) FEMS Immunol Med Microbiol, 59, pp. 364-377
  • Halling, S.M., Peterson-Burch, B.D., Bricker, B.J., Zuerner, R.L., Qing, Z., Li, L.L., Completion of the genome sequence of Brucella abortus and comparison to the highly similar genomes of Brucella melitensis and Brucella suis (2005) J Bacteriol, 187, pp. 2715-2726
  • Hannah, J.H., Menozzi, F.D., Renauld, G., Locht, C., Brennan, M.J., Sulfated glycoconjugate receptors for the Bordetella pertussis adhesin filamentous hemagglutinin (FHA) and mapping of the heparin-binding domain on FHA (1994) Infect Immun, 62, pp. 5010-5019
  • Heilmann, C., Herrmann, M., Kehrel, B.E., Peters, G., Platelet-binding domains in 2 fibrinogen-binding proteins of Staphylococcus aureus identified by phage display (2002) J Infect Dis, 186, pp. 32-39
  • Henderson, B., Nair, S., Pallas, J., Williams, M.A., Fibronectin: a multidomain host adhesin targeted by bacterial fibronectin-binding proteins (2011) FEMS Microbiol Rev, 35, pp. 147-200
  • Henderson, I.R., Nataro, J.P., Virulence functions of autotransporter proteins (2001) Infect Immun, 69, pp. 1231-1243
  • Henderson, I.R., Meehan, M., Owen, P., Antigen 43, a phase-variable bipartite outer membrane protein, determines colony morphology and autoaggregation in Escherichia coli K-12 (1997) FEMS Microbiol Lett, 149, pp. 115-120
  • Henderson, I.R., Navarro-Garcia, F., Nataro, J.P., The great escape: structure and function of the autotransporter proteins (1998) Trends Microbiol, 6, pp. 370-378
  • Henderson, I.R., Navarro-Garcia, F., Desvaux, M., Fernandez, R.C., Ala'Aldeen, D., Type V protein secretion pathway: the autotransporter story (2004) Microbiol Mol Biol Rev, 68, pp. 692-744
  • Inan, M.B., Eyileten, Z.B., Ozcinar, E., Yazicioglu, L., Sirlak, M., Eryilmaz, S., Native valve Brucella endocarditis (2010) Clin Cardiol, 33, pp. E20-E26
  • Jacobsson, K., A novel family of fibrinogen-binding proteins in Streptococcus agalactiae (2003) Vet Microbiol, 96, pp. 103-113
  • Jacobsson, K., Frykberg, L., Cloning of ligand-binding domains of bacterial receptors by phage display (1995) Biotechniques, 18, pp. 878-885
  • Jacobsson, K., Rosander, A., Bjerketorp, J., Frykberg, L., Shotgun phage display - selection for bacterial receptins or other exported proteins (2003) Biol Proced Online, 5, pp. 123-135
  • Jain, S., van Ulsen, P., Benz, I., Schmidt, M.A., Fernandez, R., Tommassen, J., Goldberg, M.B., Polar localization of the autotransporter family of large bacterial virulence proteins (2006) J Bacteriol, 188, pp. 4841-4850
  • Jeroudi, M.O., Halim, M.A., Harder, E.J., Al-Siba'i, M.B., Ziady, G., Mercer, E., Brucella endocarditis (1987) Br Heart J, 58, pp. 279-283
  • Kingsley, R.A., Santos, R.L., Keestra, A.M., Adams, L.G., Baumler, A.J., Salmonella enterica serotype Typhimurium ShdA is an outer membrane fibronectin-binding protein that is expressed in the intestine (2002) Mol Microbiol, 43, pp. 895-905
  • Kingsley, R.A., Abi Ghanem, D., Puebla-Osorio, N., Keestra, A.M., Berghman, L., Baumler, A.J., Fibronectin binding to the Salmonella enterica serotype Typhimurium ShdA autotransporter protein is inhibited by a monoclonal antibody recognizing the A3 repeat (2004) J Bacteriol, 186, pp. 4931-4939
  • Kingsley, R.A., Keestra, A.M., de Zoete, M.R., Baumler, A.J., The ShdA adhesin binds to the cationic cradle of the fibronectin 13FnIII repeat module: evidence for molecular mimicry of heparin binding (2004) Mol Microbiol, 52, pp. 345-355
  • Kline, K.A., Falker, S., Dahlberg, S., Normark, S., Henriques-Normark, B., Bacterial adhesins in host-microbe interactions (2009) Cell Host Microbe, 5, pp. 580-592
  • Ko, J., Splitter, G.A., Molecular host-pathogen interaction in brucellosis: current understanding and future approaches to vaccine development for mice and humans (2003) Clin Microbiol Rev, 16, pp. 65-78
  • Kovach, M.E., Elzer, P.H., Hill, D.S., Robertson, G.T., Farris, M.A., Roop 2nd, R.M., Peterson, K.M., Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes (1995) Gene, 166, pp. 175-176
  • Leininger, E., Roberts, M., Kenimer, J.G., Charles, I.G., Fairweather, N., Novotny, P., Brennan, M.J., Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells (1991) Proc Natl Acad Sci USA, 88, pp. 345-349
  • Loveless, B.J., Saier Jr., M.H., A novel family of channel-forming, autotransporting, bacterial virulence factors (1997) Mol Membr Biol, 14, pp. 113-123
  • McKeown-Longo, P.J., Fibronectin-cell surface interactions (1987) Rev Infect Dis, 9 (4 SUPPL.), pp. S322-S334
  • Marchesini, M.I., Connolly, J., Delpino, M.V., Baldi, P.C., Mujer, C.V., Delvecchio, V.G., Comerci, D.J., Brucella abortus choloylglycine hydrolase affects cell envelope composition and host cell internalization (2011) PLoS ONE, 6, pp. e28480
  • Martin-Martin, A.I., Caro-Hernandez, P., Sancho, P., Tejedor, C., Cloeckaert, A., Fernandez-Lago, L., Vizcaino, N., Analysis of the occurrence and distribution of the Omp25/Omp31 family of surface proteins in the six classical Brucella species (2009) Vet Microbiol, 137, pp. 74-82
  • Martirosyan, A., Moreno, E., Gorvel, J.P., An evolutionary strategy for a stealthy intracellular Brucella pathogen (2011) Immunol Rev, 240, pp. 211-234
  • Mullen, L.M., Nair, S.P., Ward, J.M., Rycroft, A.N., Williams, R.J., Henderson, B., Comparative functional genomic analysis of Pasteurellaceae adhesins using phage display (2007) Vet Microbiol, 122, pp. 123-134
  • Nguyen, V.Q., Caprioli, R.M., Cover, T.L., Carboxy-terminal proteolytic processing of Helicobacter pylori vacuolating toxin (2001) Infect Immun, 69, pp. 543-546
  • Pappas, G., Papadimitriou, P., Christou, L., Akritidis, N., Future trends in human brucellosis treatment (2006) Expert Opin Investig Drugs, 15, pp. 1141-1149
  • Parkhill, J., Wren, B.W., Thomson, N.R., Titball, R.W., Holden, M.T., Prentice, M.B., Genome sequence of Yersinia pestis, the causative agent of plague (2001) Nature, 413, pp. 523-527
  • Parkhill, J., Sebaihia, M., Preston, A., Murphy, L.D., Thomson, N., Harris, D.E., Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica (2003) Nat Genet, 35, pp. 32-40
  • Paulsen, I.T., Seshadri, R., Nelson, K.E., Eisen, J.A., Heidelberg, J.F., Read, T.D., The Brucella suis genome reveals fundamental similarities between animal and plant pathogens and symbionts (2002) Proc Natl Acad Sci USA, 99, pp. 13148-13153
  • Perkins, S.D., Smither, S.J., Atkins, H.S., Towards a Brucella vaccine for humans (2011) FEMS Microbiol Rev, , in press
  • Pizarro-Cerda, J., Cossart, P., Bacterial adhesion and entry into host cells (2006) Cell, 124, pp. 715-727
  • Pizarro-Cerda, J., Moreno, E., Sanguedolce, V., Mege, J.L., Gorvel, J.P., Virulent Brucella abortus prevents lysosome fusion and is distributed within autophagosome-like compartments (1998) Infect Immun, 66, pp. 2387-2392
  • Pizarro-Cerdá, J., Méresse, S., Parton, R.G., van der Goot, G., Sola-Landa, A., Lopez-Goñi, I., Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes (1998) Infect Immun, 66, pp. 5711-5724
  • Pizarro-Cerdá, J., Moreno, E., Gorvel, J.P., Brucella abortus: invasion and survival within professional and non-professional phagocytes (1999) Advances in Cell and Molecular Biology of Membranes and Organelles, Vol. 6: Phagocytosis and Pathogens, pp. 201-232. , Tartakoff, A., and Gordon, S. (eds). Greenwich, CT: JAI Press
  • Pohlner, J., Halter, R., Beyreuther, K., Meyer, T.F., Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease (1987) Nature, 325, pp. 458-462
  • Rajashekara, G., Glasner, J.D., Glover, D.A., Splitter, G.A., Comparative whole-genome hybridization reveals genomic islands in Brucella species (2004) J Bacteriol, 186, pp. 5040-5051
  • Reguera, J.M., Alarcon, A., Miralles, F., Pachon, J., Juarez, C., Colmenero, J.D., Brucella endocarditis: clinical, diagnostic, and therapeutic approach (2003) Eur J Clin Microbiol Infect Dis, 22, pp. 647-650
  • Rocha Gracia, R.C., Castaneda-Roldan, E.I., Giono-Cerezo, S., Giron, J.A., Brucella sp. bind to sialic acid residues on human and animal red blood cells (2002) FEMS Microbiol Lett, 213, pp. 219-224
  • Schafer, A., Tauch, A., Jager, W., Kalinowski, J., Thierbach, G., Puhler, A., Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum (1994) Gene, 145, pp. 69-73
  • Schwarz-Linek, U., Hook, M., Potts, J.R., The molecular basis of fibronectin-mediated bacterial adherence to host cells (2004) Mol Microbiol, 52, pp. 631-641
  • Seleem, M.N., Boyle, S.M., Sriranganathan, N., Brucellosis: a re-emerging zoonosis (2010) Vet Microbiol, 140, pp. 392-398
  • Sherlock, O., Schembri, M.A., Reisner, A., Klemm, P., Novel roles for the AIDA adhesin from diarrheagenic Escherichia coli: cell aggregation and biofilm formation (2004) J Bacteriol, 186, pp. 8058-8065
  • Sillanpaa, J., Nallapareddy, S.R., Singh, K.V., Ferraro, M.J., Murray, B.E., Adherence characteristics of endocarditis-derived Streptococcus gallolyticus ssp. gallolyticus (Streptococcus bovis biotype I) isolates to host extracellular matrix proteins (2008) FEMS Microbiol Lett, 289, pp. 104-109
  • Silva, T.M., Costa, E.A., Paixao, T.A., Tsolis, R.M., Santos, R.L., Laboratory animal models for brucellosis research (2011) J Biomed Biotechnol, 2011, p. 518323
  • Starr, T., Ng, T.W., Wehrly, T.D., Knodler, L.A., Celli, J., Brucella intracellular replication requires trafficking through the late endosomal/lysosomal compartment (2008) Traffic, 9, pp. 678-694
  • Stein, M., Kenny, B., Stein, M.A., Finlay, B.B., Characterization of EspC, a 110-kilodalton protein secreted by enteropathogenic Escherichia coli which is homologous to members of the immunoglobulin A protease-like family of secreted proteins (1996) J Bacteriol, 178, pp. 6546-6554
  • Viadas, C., Rodriguez, M.C., Garcia-Lobo, J.M., Sangari, F.J., Lopez-Goni, I., Construction and evaluation of an ORFeome-based Brucella whole-genome DNA microarray (2009) Microb Pathog, 47, pp. 189-195
  • Viadas, C., Rodriguez, M.C., Sangari, F.J., Gorvel, J.P., Garcia-Lobo, J.M., Lopez-Goni, I., Transcriptome analysis of the Brucella abortus BvrR/BvrS two-component regulatory system (2010) PLoS ONE, 5, pp. e10216
  • Wierzbicka-Patynowski, I., Schwarzbauer, J.E., The ins and outs of fibronectin matrix assembly (2003) J Cell Sci, 116, pp. 3269-3276

Citas:

---------- APA ----------
Posadas, D.M., Ruiz-Ranwez, V., Bonomi, H.R., Martín, F.A. & Zorreguieta, A. (2012) . BmaC, a novel autotransporter of Brucella suis, is involved in bacterial adhesion to host cells. Cellular Microbiology, 14(6), 965-982.
http://dx.doi.org/10.1111/j.1462-5822.2012.01771.x
---------- CHICAGO ----------
Posadas, D.M., Ruiz-Ranwez, V., Bonomi, H.R., Martín, F.A., Zorreguieta, A. "BmaC, a novel autotransporter of Brucella suis, is involved in bacterial adhesion to host cells" . Cellular Microbiology 14, no. 6 (2012) : 965-982.
http://dx.doi.org/10.1111/j.1462-5822.2012.01771.x
---------- MLA ----------
Posadas, D.M., Ruiz-Ranwez, V., Bonomi, H.R., Martín, F.A., Zorreguieta, A. "BmaC, a novel autotransporter of Brucella suis, is involved in bacterial adhesion to host cells" . Cellular Microbiology, vol. 14, no. 6, 2012, pp. 965-982.
http://dx.doi.org/10.1111/j.1462-5822.2012.01771.x
---------- VANCOUVER ----------
Posadas, D.M., Ruiz-Ranwez, V., Bonomi, H.R., Martín, F.A., Zorreguieta, A. BmaC, a novel autotransporter of Brucella suis, is involved in bacterial adhesion to host cells. Cell. Microbiol. 2012;14(6):965-982.
http://dx.doi.org/10.1111/j.1462-5822.2012.01771.x