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Abstract:

Brucella spp., like other pathogens, must cope with the environment of diverse host niches during the infection process. In doing this, pathogens evolved different type of transport systems to help them survive and disseminate within the host. Members of the TolC family have been shown to be involved in the export of chemically diverse molecules ranging from large protein toxins to small toxic compounds. The role of proteins from the TolC family in Brucella and other α-2-proteobacteria has been explored little. The gene encoding the unique member of the TolC family from Brucella suis (BepC) was cloned and expressed in an Escherichia coli mutant disrupted in the gene encoding TolC, which has the peculiarity of being involved in diverse transport functions. BepC fully complemented the resistance to drugs such as chloramphenicol and acriflavine but was incapable of restoring hemolysin secretion in the tolC mutant of & coli. An insertional mutation in the bepC gene strongly affected the resistance phenotype of B. suis to bile salts and toxic chemicals such as ethidium bromide and rhodamine and significantly decreased the resistance to antibiotics such as erythromycin, ampicillin, tetracycline, and norfloxacin. Moreover, the B. suis bepC mutant was attenuated in the mouse model of infection. Taken together, these results suggest that BepC-dependent efflux processes of toxic compounds contribute to B. suis survival inside the host. Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Registro:

Documento: Artículo
Título:The TolC homologue of Brucella suis is involved in resistance to antimicrobial compounds and virulence
Autor:Posadas, D.M.; Martín, F.A.; Sabio Y Garcïa, J.V.; Spera, J.M.; Delpino, M.V.; Baldi, P.; Campos, E.; Cravero, S.L.; Zorreguieta, A.
Filiación:Fundación Instituto Leloir, CONICET and FCEyN, University of Buenos Aires, Patricias Argentinas 435, C1405BWE Buenos Aires, Argentina
Instituto de Biotecnología, Centro de Investigaciones en Ciencias Veterinarias y Agronómicas, P.O. Box 77, 1708 Morón, Buenos Aires, Argentina
Instituto de Estudios de la Inmunidad Humoral, Facultad de Farmacia y Bioquímica, Universidad de Buenos Aires, Junín 956, 1113 Buenos Aires, Argentina
Instituto de Investigaciones Biotecnológicas, Universidad de Gral. San Martin, INTI, Av. Gral. Paz 5445, 1650 San Martín, Buenos Aires, Argentina
Fundación Instituto Leloir, Patricias Argentinas 435, C1405BWE Buenos Aires, Argentina
Instituto de Biologia Molecular do Paraná (IBMP), Rua prof. Algacy Munhoz Mader 3775, Curitiba-PR, Brazil
Palabras clave:acriflavine; amikacin; ampicillin; antiinfective agent; berberine; bile salt; carbenicillin; cetrimide; chloramphenicol; deoxycholate sodium; erythromycin; ethidium bromide; hemolysin; nalidixic acid; norfloxacin; rhodamine; rifampicin; spectinomycin; tetracycline; TolC protein; animal cell; antibiotic resistance; article; bacterial gene; bacterial mutation; bacterial survival; bacterial virulence; BepC gene; Brucella suis; controlled study; environmental factor; Escherichia coli; female; gene disruption; gene expression regulation; gene insertion; molecular cloning; mouse; nonhuman; phenotype; phylogeny; priority journal; protein analysis; protein family; Animals; Anti-Infective Agents; Bacterial Outer Membrane Proteins; Brucella suis; Cloning, Molecular; Drug Resistance; Female; Membrane Transport Proteins; Mice; Mice, Inbred BALB C; Phylogeny; Polymerase Chain Reaction; Virulence
Año:2007
Volumen:75
Número:1
Página de inicio:379
Página de fin:389
DOI: http://dx.doi.org/10.1128/IAI.01349-06
Título revista:Infection and Immunity
Título revista abreviado:Infect. Immun.
ISSN:00199567
CODEN:INFIB
CAS:acriflavine, 65431-33-6, 65589-70-0, 68518-47-8, 69235-50-3, 8018-07-3, 86-40-8; amikacin, 37517-28-5, 39831-55-5; ampicillin, 69-52-3, 69-53-4, 7177-48-2, 74083-13-9, 94586-58-0; berberine, 2086-83-1, 633-65-8; carbenicillin, 17230-86-3, 4697-36-3, 4800-94-6; cetrimide, 57-09-0, 6899-10-1, 8044-71-1; chloramphenicol, 134-90-7, 2787-09-9, 56-75-7; deoxycholate sodium, 302-95-4; erythromycin, 114-07-8, 70536-18-4; ethidium bromide, 1239-45-8; nalidixic acid, 389-08-2; norfloxacin, 70458-96-7; rifampicin, 13292-46-1; spectinomycin, 1695-77-8, 21736-83-4, 23312-56-3; tetracycline, 23843-90-5, 60-54-8, 64-75-5; Anti-Infective Agents; Bacterial Outer Membrane Proteins; Membrane Transport Proteins
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Referencias:

  • Ahn, J.H., Pan, J.G., Rhee, J.S., Identification of the tliDEF ABC transporter specific for lipase in Pseudomonas fluorescens SIK W1 (1999) J. Bacteriol, 181, pp. 1847-1852
  • Akatsuka, H., Binet, R., Kawai, E., Wandersman, C., Omori, K., Lipase secretion by bacterial hybrid ATP-binding cassette exporters: Molecular recognition of the LipBCD, PrtDEF, and HasDEF exporters (1997) J. Bacteriol, 179, pp. 4754-4760
  • Akatsuka, H., Kawai, E., Omori, K., Shibatani, T., The three genes lipB, lipC, and lipD involved in the extracellular secretion of the Serratia marcescens lipase which lacks an N-terminal signal peptide (1995) J. Bacteriol, 177, pp. 6381-6389
  • Allen, C.A., Adams, L.G., Ficht, T.A., Transposon-derived Brucella abortus rough mutants are attenuated and exhibit reduced intracellular survival (1998) Infect. Immun, 66, pp. 1008-1016
  • al-Sibai, M.B., Halim, M.A., el-Shaker, M.M., Khan, B.A., Qadri, S.M., Efficacy of ciprofloxacin for treatment of Brucella melitensis infections (1992) Antimicrob. Agents Chemother, 36, pp. 150-152
  • al-Sibai, M.B., Qadri, S.M., Development of ciprofloxacin resistance in Brucella melitensis (1990) J. Antimicrob. Chemother, 25, pp. 302-303
  • Andersen, C., Hughes, C., Koronakis, V., Chunnel vision. Export and efflux through bacterial channel-tunnels (2000) EMBO Rep, 1, pp. 313-318
  • Baldi, P.C., Giambartolomei, G.H., Wallach, J.C., Velikovsky, C.A., Fossati, C.A., Limited diagnostic usefulness of antibodies to cytoplasmic proteins of Brucella in early-treated human brucellosis (2001) Scand. J. Infect. Dis, 33, pp. 200-205
  • Barabote, R.D., Johnson, O.L., Zetina, E., San Francisco, S.K., Fralick, J.A., San Francisco, M.J., Erwinia chrysantherni tolC is involved in resistance to antimicrobial plant chemicals and is essential for phytopathogenesis (2003) J. Bacteriol, 185, pp. 5772-5778
  • Batut, J., Andersson, S.G., O'Callaghan, D., The evolution of chronic infection strategies in the alpha-proteobacteria (2004) Nat. Rev. Microbiol, 2, pp. 933-945
  • Baucheron, S., Imberechts, H., Chaslus-Dancla, E., Cloeckaert, A., The AcrB multidrug transporter plays a major role in high-level fluoroquinolone resistance in Salmonella enterica serovar Typhimurium phage type DT204 (2002) Microb. Drug Resist, 8, pp. 281-289
  • Baucheron, S., Tyler, S., Boyd, D., Mulvey, M.R., Chaslus-Dancla, E., Cloeckaert, A., AcrAB-TolC directs efflux-mediated multidrug resistance in Salmonella enterica serovar Typhimurium DT104 (2004) Antimicrob. Agents Chemother, 48, pp. 3729-3735
  • Baykam, N., Esener, H., Ergonul, O., Eren, S., Celikbas, A.K., Dokuzoguz, B., In vitro antimicrobial susceptibility of Brucella species (2004) Int. J. Antimicrob. Agents, 23, pp. 405-407
  • Bina, J.E., Mekalanos, J.J., Vibrio cholerae tolC is required for bile resistance and colonization (2001) Infect. Immun, 69, pp. 4681-4685
  • Binet, R., Wandersman, C., Cloning of the Serratia marcescens hasF gene encoding the Has ABC exporter outer membrane component: A TolC analogue (1996) Mol. Microbiol, 22, pp. 265-273
  • Boschiroli, M.L., Foulongne, V., O'Callaghan, D., Brucellosis: A worldwide zoonosis (2001) Curr. Opin. Microbiol, 4, pp. 58-64
  • Bouveret, E., Rigal, A., Lazdunski, C., Benedetti, H., Distinct regions of the colicin A translocation domain are involved in the interaction with TolA and TolB proteins upon import into Escherichia coli (1998) Mol. Microbiol, 27, pp. 143-157
  • Braibant, M., Guilloteau, L., Zygmunt, M.S., Functional characterization of Brucella melitensis NorMI, an efflux pump belonging to the multidrug and toxic compound extrusion family (2002) Antimicrob. Agents Chemother, 46, pp. 3050-3053
  • Cazalet, C., Rusniok, C., Bruggemann, H., Zidane, N., Magnier, A., Ma, L., Tichit, M., Buchrieser, C., Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity (2004) Nat. Genet, 36, pp. 1165-1173
  • Chain, P.S., Comerci, D.J., Tolmasky, M.E., Larimer, F.W., Malfatti, S.A., Vergez, L.M., Aguero, F., Garcia, E., Whole-genome analyses of speciation events in pathogenic brucellae (2005) Infect. Immun, 73, pp. 8353-8361
  • Chatterjee, A., Chaudhuri, S., Saha, G., Gupta, S., Chowdhury, R., Effect of bile on the cell surface permeability barrier and efflux system of Vibrio cholerae (2004) J. Bacteriol, 186, pp. 6809-6814
  • Corbel, M.J., Brucellosis: An overview (1997) Emerg. Infect. Dis, 3, pp. 213-221
  • DelVecchio, V.G., Kapatral, V., Elzer, P., Patra, G., Mujer, C.V., The genome of Brucella melitensis (2002) Vet. Microbiol, 90, pp. 587-592
  • DelVecchio, V.G., Kapatral, V., Redkar, R.J., Patra, G., Mujer, C., Los, T., Ivanova, N., Overbeek, R., The genome sequence of the facultative intracellular pathogen Brucella melitensis (2002) Proc. Natl. Acad. Sci. USA, 99, pp. 443-448
  • Duong, F., Lazdunski, A., Cami, B., Murgier, M., Sequence of a cluster of genes controlling synthesis and secretion of alkaline protease in Pseudomonas aeruginosa: Relationships to other secretory pathways (1992) Gene, 121, pp. 47-54
  • Elkins, C.A., Mullis, L.B., Mammalian steroid hormones are substrates for the major RND- and MFS-type tripartite multidrug efflux pumps of Escherichia coli (2006) J. Bacteriol, 188, pp. 1191-1195
  • Eswaran, J., Koronakis, E., Higgins, M.K., Hughes, C., Koronakis, V., Three's company: Component structures bring a closer view of tripartite drug efflux pumps (2004) Curr. Opin. Struct. Biol, 14, pp. 741-747
  • Finnie, C., Hartley, N.M., Findlay, K.C., Downie, J.A., The Rhizobium leguminosarum prsDE genes are required for secretion of several proteins, some of which influence nodulation, symbiotic nitrogen fixation and exopolysaccharide modification (1997) Mol. Microbiol, 25, pp. 135-146
  • Finnie, C., Zorreguieta, A., Hartley, N.M., Downie, J.A., Characterization of Rhizobium leguminosarum exopolysaccharide glycanases that are secreted via a type I exporter and have a novel heptapeptide repeat motif (1998) J. Bacteriol, 180, pp. 1691-1699
  • Garcia-Rodriguez, J.A., Garcia Sanchez, J.E., Trujillano, I., Lack of effective bactericidal activity of new quinolones against Brucella spp (1991) Antimicrob. Agents Chemother, 35, pp. 756-759
  • Gillor, O., Kirkup, B.C., Riley, M.A., Colicins and microcins: The next generation antimicrobials (2004) Adv. Appl. Microbiol, 54, pp. 129-146
  • Godfroid, F., Taminiau, B., Danese, I., Denoel, P., Tiber, A., Weynants, V., Cloeckaert, A., Letesson, J.J., Identification of the perosamine synthetase gene of Brucella melitensis 16M and involvement of lipopolysaccharide O side chain in Brucella survival in mice and in macrophages (1998) Infect. Immun, 66, pp. 5485-5493
  • Gorvel, J.P., Moreno, E., Brucella intracellular life: From invasion to intracellular replication (2002) Vet. Microbiol, 90, pp. 281-297
  • Grass, G., Grosse, C., Nies, D.H., Regulation of the cnr cobalt and nickel resistance determinant from Ralstonia sp. strain CH34 (2000) J. Bacteriol, 182, pp. 1390-1398
  • Halling, S.M., Peterson-Burch, B.D., Bricker, B.J., Zuerner, R.L., Qing, Z., Li, L.L., Kapur, V., Olsen, S.C., 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
  • Hassan, M.T., van der Lelie, D., Springael, D., Romling, U., Ahmed, N., Mergeay, M., Identification of a gene cluster, czr, involved in cadmium and zinc resistance in Pseudomonas aeruginosa (1999) Gene, 238, pp. 417-425
  • Kaneko, T., Nakamura, Y., Sato, S., Minamisawa, K., Uchiumi, T., Sasamoto, S., Watanabe, A., Tabata, S., Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110 supplement) (2002) DNA Res, 9, pp. 225-256
  • 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
  • Köhler, T., van Delden, C., Curty, L.K., Hamzehpour, M.M., Pechere, J.-C., Overexpression of the MexEF-OprN multidrug efflux system affects cell-to-cell signaling in Pseudomonas aeruginosa (2001) J. Bacteriol, 183, pp. 5213-5222
  • Koronakis, V., TolC-the bacterial exit duct for proteins and drugs (2003) FEBS Lett, 555, pp. 66-71
  • Koronakis, V., Sharff, A., Koronakis, E., Luisi, B., Hughes, C., Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export (2000) Nature, 405, pp. 914-919
  • Kovach, M.E., Phillips, R.W., Elzer, P.H., Roop II, R.M., Peterson, K.M., pBBR1MCS: A broad-host-range cloning vector (1994) BioTechniques, 16, pp. 800-802
  • Kumar, A., Worobec, E.A., HasF, a TolC-homolog of Serratia marcescens, is involved in energy-dependent efflux (2005) Can. J. Microbiol, 51, pp. 497-500
  • Lazdunski, C.J., Bouveret, E., Rigal, A., Journet, L., Lloubes, R., Benedetti, H., Colicin import into Escherichia coli cells (1998) J. Bacteriol, 180, pp. 4993-5002
  • Letoffe, S., Delepelaire, P., Wandersman, C., Protease secretion by Erwinia chrysanthemi: The specific secretion functions are analogous to those of Escherichia coli alpha-haemolysin (1990) EMBO J, 9, pp. 1375-1382
  • Li, X.Z., Zhang, L., Poole, K., SmeC, an outer membrane multidrug efflux protein of Stenotrophomonas maltophilia (2002) Antimicrob. Agents Chemother, 46, pp. 333-343
  • Ma, D., Cook, D.N., Hearst, J.E., Nikaido, H., Efflux pumps and drug resistance in gram-negative bacteria (1994) Trends Microbiol, 2, pp. 489-493
  • Mackman, N., Nicaud, J.M., Gray, L., Holland, I.B., Genetical and functional organisation of the Escherichia coli haemolysin determinant 2001 (1985) Mol. Gen. Genet, 201, pp. 282-288
  • Mackman, N., Nicaud, J.M., Gray, L., Holland, I.B., Secretion of haemolysin by Escherichia coli (1986) Curr. Top. Microbiol. Immunol, 125, pp. 159-181
  • Maneewannakul, K., Levy, S.B., Identification for mar mutants among quinolone-resistant clinical isolates of Escherichia coli (1996) Antimicrob. Agents Chemother, 40, pp. 1695-1698
  • Masuda, N., Sakagawa, E., Ohya, S., Outer membrane proteins responsible for multiple drug resistance in Pseudomonas aeruginosa (1995) Antimicrob. Agents Chemother, 39, pp. 645-649
  • McQuiston, J.R., Vemulapalli, R., Inzana, T.J., Schurig, G.G., Sriranganathan, N., Fritzinger, D., Hadfield, T.L., Boyle, S.M., Genetic characterization of a Tn5-disrupted glycosyltransferase gene homolog in Brucella abortus and its effect on lipopolysaccharide composition and virulence (1999) Infect. Immun, 67, pp. 3830-3835
  • Memish, Z., Mah, M.W., Al Mahmoud, S., Al Shaalan, M., Khan, M.Y., Brucella bacteraemia: Clinical and laboratory observations in 160 patients (2000) J. Infect, 40, pp. 59-63
  • Moreno, E., Moriyon, I., Brucella melitensis: A nasty bug with hidden credentials for virulence (2002) Proc. Natl. Acad. Sci. USA, 99, pp. 1-3
  • Nies, D.H., Nies, A., Chu, L., Silver, S., Expression and nucleotide sequence of a plasmid-determined divalent cation efflux system from Alcaligenes eutrophus (1989) Proc. Natl. Acad. Sci. USA, 86, pp. 7351-7355
  • Otsuji, N., Soejima, T., Maki, S., Shinagawa, H., Cloning of colicin E1 tolerant tolC (mtcB) gene of Escherichia coli K12 and identification of its gene product (1982) Mol. Gen. Genet, 187, pp. 30-36
  • Paulsen, I.T., Multidrug efflux pumps and resistance: Regulation and evolution (2003) Curr. Opin. Microbiol, 6, pp. 446-451
  • Paulsen, I. T., R. Seshadri, K. E. Nelson, J. A. Eisen, J. F. Heidelberg, T. D. Read, R. J. Dodson, L. Umayam, L. M. Brinkac, M. J. Beanan, S. C. Daugherty, R. T. Deboy, A. S. Durkin, J. F. Kolonay, R. Madupu, W. C. Nelson, B. Ayodeji, M. Kraul, J. Shetty, J. Malek, S. E. Van Aken, S. Riedmuller, H. Tettelin, S. R. Gill, O. White, S. L. Salzberg, D. L. Hoover, L. E. Lindler, S. M. Halling, S. M. Boyle, and C. M. Fraser. 2002. The Brucella suis genome reveals fundamental similarities between animal and plant pathogens and symbionts. Proc. Natl. Acad. Sci. USA 99:13148-13153; Pearson, J.P., Van Delden, C., Iglewski, B.H., Active efflux and diffusion are involved in transport of Pseudomonas aeruginosa cell-to-cell signals (1999) J. Bacteriol, 181, pp. 1203-1210
  • Poole, K., Mechanisms of bacterial biocide and antibiotic resistance (2002) J. Appl. Microbiol, 92 (SUPPL.), pp. 55S-64S
  • Poole, K., Multidrug efflux pumps and antimicrobial resistance in Pseudomonas aeruginosa and related organisms (2001) J. Mol. Microbiol. Biotechnol, 3, pp. 255-264
  • Poole, K., Gotoh, N., Tsujimoto, H., Zhao, Q., Wada, A., Yamasaki, T., Neshat, S., Nishino, T., Overexpression of the mexC-mexD-oprJ efflux operon in nfxB-type multidrug-resistant strains of Pseudomonas aeruginosa (1996) Mol. Microbiol, 21, pp. 713-724
  • Prentki, P., Krisch, H.M., In vitro insertional mutagenesis with a selectable DNA fragment (1984) Gene, 29, pp. 303-313
  • Qadri, S.M., Akhtar, M., Ueno, Y., al-Sibai, M.B., Susceptibility of Brucella melitensis to fluoroquinolones (1989) Drugs Exp. Clin. Res, 15, pp. 483-485
  • Rajashekara, G., Glover, D.A., Krepps, M., Splitter, G.A., Temporal analysis of pathogenic events in virulent and avirulent Brucella melitensis infections (2005) Cell. Microbiol, 7, pp. 1459-1473
  • Ricci, V., Tzakas, P., Buckley, A., Piddock, L.J., Ciprofloxacin-resistant Salmonella enterica serovar Typhimurium strains are difficult to select in the absence of AcrB and TolC (2006) Antimicrob. Agents Chemother, 50, pp. 38-42
  • Rivilla, R., Sutton, J.M., Downie, J.A., Rhizobium leguminosarum NodT is related to a family of outer-membrane transport proteins that includes TolC, PrtF, CyaE and AprF (1995) Gene, 161, pp. 27-31
  • Rolain, J.M., Maurin, M., Raoult, D., Bactericidal effect of antibiotics on Bartonella and Brucella spp.: Clinical implications (2000) J. Antimicrob. Chemother, 46, pp. 811-814
  • Roop II, R.M., Bellaire, B.H., Valderas, M.W., Cardelli, J.A., Adaptation of the brucellae to their intracellular niche (2004) Mol. Microbiol, 52, pp. 621-630
  • Russo, D.M., Williams, A., Edwards, A., Posadas, D.M., Finnie, C., Dankert, M., Downie, J.A., Zorreguieta, A., Proteins exported via the PrsD-PrsE type I secretion system and the acidic exopolysaccharide are involved in biofilm formation by Rhizobium leguminosarum (2006) J. Bacteriol, 188, pp. 4474-4486
  • Santiviago, C.A., Fuentes, J.A., Bueno, S.M., Trombert, A.N., Hildago, A.A., Socias, L.T., Youderian, P., Mora, G.C., The Salmonella enterica sv. Typhimurium smvA, yddG and ompD (porin) genes are required for the efficient efflux of methyl viologen (2002) Mol. Microbiol, 46, pp. 687-698
  • Sukchawalit, R., P. Vattanaviboon, R. Sallabhan, and S. Mongkolsuk. 1999. Construction and characterization of regulated L-arabinose-inducible broad host range expression vectors in Xanthomonas. FEMS Miciobiol. Lett. 181: 217-223; Surin, B.P., Watson, J.M., Hamilton, W.D., Economou, A., Downie, J.A., Molecular characterization of the nodulation gene, nodT, from two biovars of Rhizobium leguminosarum (1990) Mol. Microbiol, 4, pp. 245-252
  • Taminiau, B., Daykin, M., Swift, S., Boschiroli, M.L., Tibor, A., Lestrate, P., De Bolle, X., Letesson, J.J., Identification of a quorum-sensing signal molecule in the facultative intracellular pathogen Brucella melitensis (2002) Infect. Immun, 70, pp. 3004-3011
  • Thanabalu, T., Koronakis, E., Hughes, C., Koronakis, V., Substrate-induced assembly of a contiguous channel for protein export from E.coli: Reversible bridging of an inner-membrane translocase to an outer membrane exit pore (1998) EMBO J, 17, pp. 6487-6496
  • Tibor, A., Wansard, V., Bielartz, V., Delrue, R.M., Danese, I., Michel, P., Walravens, K., Letesson, J.J., Effect of omp10 or omp19 deletion on Brucella abortus outer membrane properties and virulence in mice (2002) Infect. Immun, 70, pp. 5540-5546
  • Ugalde, J.E., Czibener, C., Feldman, M.F., Ugalde, R.A., Identification and characterization of the Brucella abortus phosphoglucomutase gene: Role of lipopolysaccharide in virulence and intracellular multiplication (2000) Infect. Immun, 68, pp. 5716-5723
  • Utsumi, R., Yagi, T., Katayama, S., Katsuragi, K., Tachibana, K., Toyoda, H., Ouchi, S., Noda, M., Molecular cloning and characterization of the fusaric acid-resistance gene from Pseudomonas cepacia (1991) Agric. Biol. Chem, 55, pp. 1913-1918
  • Wandersman, C., Delepelaire, P., TolC, an Escherichia coli outer membrane protein required for hemolysin secretion (1990) Proc. Natl. Acad. Sci. USA, 87, pp. 4776-4780
  • Wassif, C., Cheek, D., Belas, R., Molecular analysis of a metalloprotease from Proteus mirabilis (1995) J. Bacteriol, 177, pp. 5790-5798
  • Webber, M.A., Piddock, L.J., Absence of mutations in marRAB or soxRS in acrB-overexpressing fluoroquinolone-resistant clinical and veterinary isolates of Escherichia coli (2001) Antimicrob. Agents Chemother, 45, pp. 1550-1552
  • Zakharov, S.D., Eroukova, V.Y., Rokitskaya, T.I., Zhalnina, M.V., Sharma, O., Loll, P.J., Zgurskaya, H.I., Cramer, W.A., Colicin occlusion of OmpF and TolC channels: Outer membrane translocons for colicin import (2004) Biophys. J, 87, pp. 3901-3911
  • Zgurskaya, H.I., Nikaido, H., Multidrug resistance mechanisms: Drug efflux across two membranes (2000) Mol. Microbiol, 37, pp. 219-225
  • Zhang, Y., Bak, D.D., Heid, H., Gelder, K., Molecular characterization of a protease secreted by Erwinia amylovora (1999) J. Mol. Biol, 289, pp. 1239-1251

Citas:

---------- APA ----------
Posadas, D.M., Martín, F.A., Sabio Y Garcïa, J.V., Spera, J.M., Delpino, M.V., Baldi, P., Campos, E.,..., Zorreguieta, A. (2007) . The TolC homologue of Brucella suis is involved in resistance to antimicrobial compounds and virulence. Infection and Immunity, 75(1), 379-389.
http://dx.doi.org/10.1128/IAI.01349-06
---------- CHICAGO ----------
Posadas, D.M., Martín, F.A., Sabio Y Garcïa, J.V., Spera, J.M., Delpino, M.V., Baldi, P., et al. "The TolC homologue of Brucella suis is involved in resistance to antimicrobial compounds and virulence" . Infection and Immunity 75, no. 1 (2007) : 379-389.
http://dx.doi.org/10.1128/IAI.01349-06
---------- MLA ----------
Posadas, D.M., Martín, F.A., Sabio Y Garcïa, J.V., Spera, J.M., Delpino, M.V., Baldi, P., et al. "The TolC homologue of Brucella suis is involved in resistance to antimicrobial compounds and virulence" . Infection and Immunity, vol. 75, no. 1, 2007, pp. 379-389.
http://dx.doi.org/10.1128/IAI.01349-06
---------- VANCOUVER ----------
Posadas, D.M., Martín, F.A., Sabio Y Garcïa, J.V., Spera, J.M., Delpino, M.V., Baldi, P., et al. The TolC homologue of Brucella suis is involved in resistance to antimicrobial compounds and virulence. Infect. Immun. 2007;75(1):379-389.
http://dx.doi.org/10.1128/IAI.01349-06