Artículo

Bialer, M.G.; Ruiz-Ranwez, V.; Sycz, G.; Estein, S.M.; Russo, D.M.; Altabe, S.; Sieira, R.; Zorreguieta, A. "MapB, the Brucella suis TamB homologue, is involved in cell envelope biogenesis, cell division and virulence" (2019) Scientific Reports. 9(1)
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Brucella species are Gram-negative, facultative intracellular pathogens responsible for a worldwide zoonosis. The envelope of Brucella exhibits unique characteristics that make these bacteria furtive pathogens and resistant to several host defence compounds. We have identified a Brucella suis gene (mapB) that appeared to be crucial for cell envelope integrity. Indeed, the typical resistance of Brucella to both lysozyme and the cationic lipopeptide polymyxin B was markedly reduced in a ∆mapB mutant. MapB turned out to represent a TamB orthologue. This last protein, together with TamA, a protein belonging to the Omp85 family, form a complex that has been proposed to participate in the translocation of autotransporter proteins across the outer membrane (OM). Accordingly, we observed that MapB is required for proper assembly of an autotransporter adhesin in the OM, as most of the autotransporter accumulated in the mutant cell periplasm. Both assessment of the relative amounts of other specific outer membrane proteins (OMPs) and a proteome approach indicated that the absence of MapB did not lead to an extensive alteration in OMP abundance, but to a reduction in the relative amounts of a protein subset, including proteins from the Omp25/31 family. Electron microscopy revealed that ∆mapB cells exhibit multiple anomalies in cell morphology, indicating that the absence of the TamB homologue in B. suis severely affects cell division. Finally, ∆mapB cells were impaired in macrophage infection and showed an attenuated virulence phenotype in the mouse model. Collectively, our results indicate that the role of B. suis TamB homologue is not restricted to participating in the translocation of autotransporters across the OM but that it is essential for OM stability and protein composition and that it is involved in cell envelope biogenesis, a process that is inherently coordinated with cell division. © 2019, The Author(s).

Registro:

Documento: Artículo
Título:MapB, the Brucella suis TamB homologue, is involved in cell envelope biogenesis, cell division and virulence
Autor:Bialer, M.G.; Ruiz-Ranwez, V.; Sycz, G.; Estein, S.M.; Russo, D.M.; Altabe, S.; Sieira, R.; Zorreguieta, A.
Filiación:Fundación Instituto Leloir, IIBBA-CONICET. Patricias Argentinas 435, (C1405BWE), Buenos Aires, Argentina
Laboratorio de Inmunología, Facultad de Ciencias Veterinarias, Centro de Investigación Veterinaria de Tandil (CIVETAN), CONICET-Facultad de Ciencias Veterinarias, Universidad Nacional del Centro de la Provincia de Buenos Aires (U.N.C.P.B.A), Tandil, Argentina
Instituto de Biología Molecular y Celular de Rosario (IBR) and Departamento de Microbiología, Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Esmeralda y Ocampo, Rosario, Argentina
Departamento de Química Biológica, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Año:2019
Volumen:9
Número:1
DOI: http://dx.doi.org/10.1038/s41598-018-37668-3
Título revista:Scientific Reports
Título revista abreviado:Sci. Rep.
ISSN:20452322
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_20452322_v9_n1_p_Bialer

Referencias:

  • Seleem, M.N., Boyle, S.M., Sriranganathan, N., Brucellosis: A re-emerging zoonosis (2010) Vet Microbiol, 140, pp. 392-398
  • von Bargen, K., Gorvel, J.P., Salcedo, S.P., Internal affairs: investigating the Brucella intracellular lifestyle (2012) FEMS Microbiol Rev, 36, pp. 533-562
  • Martirosyan, A., Moreno, E., Gorvel, J.P., An evolutionary strategy for a stealthy intracellular Brucella pathogen (2011) Immunol Rev, 240, pp. 211-234
  • Vizcaino, N., Cloeckaert, A., Zygmunt, M.S., Dubray, G., Cloning, nucleotide sequence, and expression of the Brucella melitensis omp31 gene coding for an immunogenic major outer membrane protein (1996) Infect Immun, 64, pp. 3744-3751. , COI: 1:CAS:528:DyaK28XltlKhtrY%3D, PID: 8751924
  • Moriyon, I., Lopez-Goni, I., Structure and properties of the outer membranes of Brucella abortus and Brucella melitensis (1998) International microbiology: the official journal of the Spanish Society for Microbiology, 1, pp. 19-26. , COI: 1:CAS:528:DyaK1MXmtV2gsrg%3D
  • Cloeckaert, A., Vizcaíno, N., Paquet, J.-Y., Bowden, R.A., Elzer, P.H., Major outer membrane proteins of Brucella spp.: past, present and future (2002) Vet Microbiol, 90, pp. 229-247. , COI: 1:CAS:528:DC%2BD38XotF2jt7g%3D, PID: 12414146
  • Cloeckaert, A., Zygmunt, M.S., de Wergifosse, P., Dubray, G., Limet, J.N., Demonstration of peptidoglycan-associated Brucella outer-membrane proteins by use of monoclonal antibodies (1992) J Gen Microbiol, 138, pp. 1543-1550
  • Cardoso, P.G., Macedo, G.C., Azevedo, V., Oliveira, S.C., Brucella spp noncanonical LPS: structure, biosynthesis, and interaction with host immune system (2006) Microb Cell Fact, 5, p. 13. , PID: 16556309
  • Martínez de Tejada, G., Pizarro-Cerdá, J., Moreno, E., Moriyón, I., The outer membranes of Brucella spp. are resistant to bactericidal cationic peptides (1995) Infect Immun, 63, pp. 3054-3061. , PID: 7622230
  • Freer, E., Brucella-Salmonella lipopolysaccharide chimeras are less permeable to hydrophobic probes and more sensitive to cationic peptides and EDTA than are their native Brucella sp. counterparts (1996) J Bacteriol, 178, pp. 5867-5876. , COI: 1:CAS:528:DyaK28XmtFOksrk%3D, PID: 8830680
  • Barquero-Calvo, E., Brucella abortus uses a stealthy strategy to avoid activation of the innate immune system during the onset of infection (2007) PLoS ONE, 2. , PID: 17637846
  • Posadas, D.M., Ruiz-Ranwez, V., Bonomi, H.R., Martin, F.A., Zorreguieta, A., BmaC, a novel autotransporter of Brucella suis, is involved in bacterial adhesion to host cells (2012) Cell Microbiol, 14, pp. 965-982
  • Ruiz-Ranwez, V., BtaE, an adhesin that belongs to the trimeric autotransporter family, is required for full virulence and defines a specific adhesive pole of Brucella suis (2013) Infect Immun, 81, pp. 996-1007
  • Ruiz-Ranwez, V., The BtaF trimeric autotransporter of Brucella suis is involved in attachment to various surfaces, resistance to serum and virulence (2013) PLoS ONE, 8
  • Benz, I., Schmidt, M.A., Structures and functions of autotransporter proteins in microbial pathogens (2011) Int J Med Microbiol, 301, pp. 461-468
  • Lyskowski, A., Leo, J.C., Goldman, A., Structure and biology of trimeric autotransporter adhesins (2011) Adv Exp Med Biol, 715, pp. 143-158
  • Leyton, D.L., Rossiter, A.E., Henderson, I.R., From self sufficiency to dependence: mechanisms and factors important for autotransporter biogenesis (2012) Nat Rev Microbiol, 10, pp. 213-225
  • Heinz, E., Lithgow, T., A comprehensive analysis of the Omp85/TpsB protein superfamily structural diversity, taxonomic occurrence, and evolution (2014) Frontiers in microbiology, 5, p. 370
  • Selkrig, J., Discovery of an archetypal protein transport system in bacterial outer membranes (2012) Nature structural & molecular biology, 19 (506-510), p. S501
  • Josts, I., The Structure of a Conserved Domain of TamB Reveals a Hydrophobic beta Taco Fold (2017) Structure, 25, pp. 1898-1906. , e1895
  • Heinz, E., Selkrig, J., Belousoff, M.J., Lithgow, T., Evolution of the Translocation and Assembly Module (TAM) (2015) Genome biology and evolution, 7, pp. 1628-1643
  • Azari, F., Ultrastructural analysis of the rugose cell envelope of a member of the Pasteurellaceae family (2013) J Bacteriol, 195, pp. 1680-1688
  • Smith, K.P., Alteration in abundance of specific membrane proteins of Aggregatibacter actinomycetemcomitans is attributed to deletion of the inner membrane protein MorC (2015) Proteomics, 15, pp. 1859-1867
  • Iqbal, H., Kenedy, M.R., Lybecker, M., Akins, D.R., The TamB ortholog of Borrelia burgdorferi interacts with the beta-barrel assembly machine (BAM) complex protein BamA (2016) Mol Microbiol, 102, pp. 757-774
  • Yu, J., A tamB homolog is involved in maintenance of cell envelope integrity and stress resistance of Deinococcus radiodurans (2017) Scientific reports, 7
  • Selkrig, J., Conserved features in TamA enable interaction with TamB to drive the activity of the translocation and assembly module (2015) Scientific reports, 5
  • Dohmer, P.H., Valguarnera, E., Czibener, C., Ugalde, J.E., Identification of a type IV secretion substrate of Brucella abortus that participates in the early stages of intracellular survival (2014) Cell Microbiol, 16, pp. 396-410
  • Freer, E., The outer membrane of Brucella ovis shows increased permeability to hydrophobic probes and is more susceptible to cationic peptides than are the outer membranes of mutant rough Brucella abortus strains (1999) Infect Immun, 67, pp. 6181-6186. , COI: 1:CAS:528:DyaK1MXntV2qs70%3D, PID: 10531286
  • White, P.G., Wilson, J.B., Differentiation of smooth and nonsmooth colonies of Brucellae (1951) J Bacteriol, 61, pp. 239-240. , COI: 1:STN:280:DyaG3M%2FltlKmsA%3D%3D, PID: 14824102
  • Gamazo, C., Vitas, A.I., Moriyón, I., López-Goñi, I., Díaz, R., Brucella group 3 outer membrane proteins contain a heat-modifiable protein (1993) FEMS Microbiol Lett, 112, pp. 141-146. , COI: 1:CAS:528:DyaK3sXmsVGisLY%3D, PID: 8405955
  • Chang, Y.Y., Cronan, J.E., Jr., Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli (1999) Mol Microbiol, 33, pp. 249-259. , COI: 1:CAS:528:DyaK1MXkvVGmsLk%3D, PID: 10411742
  • Gatsos, X., Protein secretion and outer membrane assembly in Alphaproteobacteria (2008) FEMS Microbiol Rev, 32, pp. 995-1009
  • Mobasheri, H., Ficht, T.A., Marquis, H., Lea, E.J., Lakey, J.H., Brucella Omp2a and Omp2b porins: single channel measurements and topology prediction (1997) FEMS Microbiol Lett, 155, pp. 23-30. , COI: 1:CAS:528:DyaK2sXmtFKntb0%3D, PID: 9345760
  • Salhi, I., Characterization of new members of the group 3 outer membrane protein family of Brucella spp (2003) Infect Immun, 71, pp. 4326-4332. , COI: 1:CAS:528:DC%2BD3sXlvFykt7w%3D, PID: 12874309
  • Tibor, A., Decelle, B., Letesson, J.J., Outer membrane proteins Omp10, Omp16, and Omp19 of Brucella spp. are lipoproteins (1999) Infect Immun, 67, pp. 4960-4962. , COI: 1:CAS:528:DyaK1MXlsFClsLg%3D, PID: 10456959
  • Cloeckaert, A., de Wergifosse, P., Dubray, G., Limet, J.N., Identification of seven surface-exposed Brucella outer membrane proteins by use of monoclonal antibodies: immunogold labeling for electron microscopy and enzyme-linked immunosorbent assay (1990) Infect Immun, 58, pp. 3980-3987. , COI: 1:CAS:528:DyaK3MXit1Smug%3D%3D, PID: 1701417
  • Martin-Martin, A.I., 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
  • Caro-Hernandez, P., Role of the Omp25/Omp31 family in outer membrane properties and virulence of Brucella ovis (2007) Infect Immun, 75, pp. 4050-4061
  • Posadas, D.M., The TolC homologue of Brucella suis is involved in resistance to antimicrobial compounds and virulence (2007) Infect Immun, 75, pp. 379-389. , COI: 1:CAS:528:DC%2BD2sXjsV2jtw%3D%3D, PID: 17088356
  • Magnet, S., Dubost, L., Marie, A., Arthur, M., Gutmann, L., Identification of the L,D-transpeptidases for peptidoglycan cross-linking in Escherichia coli (2008) J Bacteriol, 190, pp. 4782-4785
  • Grangeon, R., Zupan, J.R., Anderson-Furgeson, J., Zambryski, P.C., PopZ identifies the new pole, and PodJ identifies the old pole during polar growth in Agrobacterium tumefaciens (2015) Proc Natl Acad Sci USA, 112, pp. 11666-11671
  • Cook, P.D., Holden, H.M., GDP-perosamine synthase: structural analysis and production of a novel trideoxysugar (2008) Biochemistry, 47, pp. 2833-2840
  • Gamazo, C., Moriyón, I., Release of outer membrane fragments by exponentially growing Brucella melitensis cells (1987) Infect Immun, 55, pp. 609-615. , COI: 1:CAS:528:DyaL2sXhtlCqu7o%3D, PID: 3818086
  • Lamontagne, J., Extensive cell envelope modulation is associated with virulence in Brucella abortus (2007) Journal of proteome research, 6, pp. 1519-1529. , COI: 1:CAS:528:DC%2BD2sXisFSjtbs%3D, PID: 17343405
  • Delpino, M.V., A bile salt hydrolase of Brucella abortus contributes to the establishment of a successful infection through the oral route in mice (2007) Infect Immun, 75, pp. 299-305
  • Manterola, L., The lipopolysaccharide of Brucella abortus BvrS/BvrR mutants contains lipid A modifications and has higher affinity for bactericidal cationic peptides (2005) J Bacteriol, 187, pp. 5631-5639. , COI: 1:CAS:528:DC%2BD2MXosVartLg%3D, PID: 16077108
  • Sieira, R., Combinatorial control of adhesion of Brucella abortus 2308 to host cells by transcriptional rewiring of the trimeric autotransporter btaE gene (2017) Mol Microbiol, 103, pp. 553-565
  • Francis, N., CtrA controls cell division and outer membrane composition of the pathogen Brucella abortus (2017) Mol Microbiol, 103, pp. 780-797
  • Kulp, A., Kuehn, M.J., Biological functions and biogenesis of secreted bacterial outer membrane vesicles (2010) Annu Rev Microbiol, 64, pp. 163-184
  • Deatherage, B.L., Biogenesis of bacterial membrane vesicles (2009) Mol Microbiol, 72, pp. 1395-1407
  • Katsui, N., Heat-induced blebbing and vesiculation of the outer membrane of Escherichia coli (1982) J Bacteriol, 151, pp. 1523-1531. , COI: 1:CAS:528:DyaL38XlsF2nsr0%3D, PID: 7050091
  • Mug-Opstelten, D., Witholt, B., Preferential release of new outer membrane fragments by exponentially growing Escherichia coli (1978) Biochim Biophys Acta, 508, pp. 287-295. , COI: 1:CAS:528:DyaE1cXhs1Kmtrs%3D, PID: 346062
  • Haurat, M.F., Elhenawy, W., Feldman, M.F., Prokaryotic membrane vesicles: new insights on biogenesis and biological roles (2015) Biological chemistry, 396, pp. 95-109
  • Gallant, C.V., Sedic, M., Chicoine, E.A., Ruiz, T., Mintz, K.P., Membrane morphology and leukotoxin secretion are associated with a novel membrane protein of Aggregatibacter actinomycetemcomitans (2008) J Bacteriol, 190, pp. 5972-5980
  • Moriyon, I., Berman, D.T., Effects of nonionic, ionic, and dipolar ionic detergents and EDTA on the Brucella cell envelope (1982) J Bacteriol, 152, pp. 822-828. , COI: 1:CAS:528:DyaL38XmtFahsbc%3D, PID: 6813315
  • Conde-Alvarez, R., The lipopolysaccharide core of Brucella abortus acts as a shield against innate immunity recognition (2012) PLoS Pathog, 8
  • Kerrinnes, T., Phospholipase A1 modulates the cell envelope phospholipid content of Brucella melitensis, contributing to polymyxin resistance and pathogenicity (2015) Antimicrob Agents Chemother, 59, pp. 6717-6724
  • Gerding, M.A., Ogata, Y., Pecora, N.D., Niki, H., de Boer, P.A., The trans-envelope Tol-Pal complex is part of the cell division machinery and required for proper outer-membrane invagination during cell constriction in E. coli (2007) Mol Microbiol, 63, pp. 1008-1025
  • Bernadac, A., Gavioli, M., Lazzaroni, J.C., Raina, S., Lloubes, R., Escherichia coli tol-pal mutants form outer membrane vesicles (1998) J Bacteriol, 180, pp. 4872-4878. , COI: 1:CAS:528:DyaK1cXmt1Sns78%3D, PID: 9733690
  • Webster, R.E., The tol gene products and the import of macromolecules into Escherichia coli (1991) Mol Microbiol, 5, pp. 1005-1011. , COI: 1:CAS:528:DyaK3MXks1yiu70%3D, PID: 1683466
  • De Bolle, X., Crosson, S., Matroule, J.Y., Letesson, J.J., Brucella abortus Cell Cycle and Infection Are Coordinated (2015) Trends Microbiol, 23, pp. 812-821
  • Deghelt, M., G1-arrested newborn cells are the predominant infectious form of the pathogen Brucella abortus (2014) Nature communications, 5
  • Schafer, 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. , COI: 1:STN:280:DyaK2czitVOruw%3D%3D, PID: 8045426
  • Kovach, M.E., Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes (1995) Gene, 166, pp. 175-176. , COI: 1:CAS:528:DyaK2MXps1WqtLw%3D, PID: 8529885
  • Sycz, G., LOV Histidine Kinase Modulates the General Stress Response System and Affects the virB Operon Expression in Brucella abortus (2015) PLoS One, 10
  • Rouot, B., Production of the type IV secretion system differs among Brucella species as revealed with VirB5- and VirB8-specific antisera (2003) Infect Immun, 71, pp. 1075-1082. , COI: 1:CAS:528:DC%2BD3sXhvFWhu7Y%3D, PID: 12595417
  • Zhang, X., Ren, J., Li, N., Liu, W., Wu, Q., Disruption of the BMEI0066 gene attenuates the virulence of Brucella melitensis and decreases its stress tolerance (2009) International journal of biological sciences, 5, pp. 570-577. , COI: 1:CAS:528:DC%2BD1MXhtlegur7N, PID: 19742243
  • Sekiguchi, M., Iida, S., Mutants of Escherichia coli permeable to actinomycin (1967) Proc Natl Acad Sci USA, 58, pp. 2315-2320. , COI: 1:CAS:528:DyaF1cXkslaltA%3D%3D, PID: 4173585
  • Heesemann, J., Plasmids of human strains of Yersinia enterocolitica: molecular relatedness and possible importance for pathogenesis (1983) J Infect Dis, 147, pp. 107-115. , COI: 1:CAS:528:DyaL3sXhtVWqtr8%3D, PID: 6822745
  • Garin-Bastuji, B., Bowden, R.A., Dubray, G., Limet, J.N., Sodium dodecyl sulfate-polyacrylamide gel electrophoresis and immunoblotting analysis of smooth-lipopolysaccharide heterogeneity among Brucella biovars related to A and M specificities (1990) J Clin Microbiol, 28, pp. 2169-2174. , COI: 1:CAS:528:DyaK3MXjtV2q, PID: 2229339
  • Moreno, E., Pitt, M.W., Jones, L.M., Schurig, G.G., Berman, D.T., Purification and characterization of smooth and rough lipopolysaccharides from Brucella abortus (1979) J Bacteriol, 138, pp. 361-369. , COI: 1:CAS:528:DyaE1MXktlGnsrs%3D, PID: 108257
  • Tsai, C.M., Frasch, C.E., A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels (1982) Anal Biochem, 119, pp. 115-119. , COI: 1:CAS:528:DyaL38Xot1agsg%3D%3D, PID: 6176137
  • Nielsen, K.H., Kelly, L., Gall, D., Nicoletti, P., Kelly, W., Improved competitive enzyme immunoassay for the diagnosis of bovine brucellosis (1995) Vet Immunol Immunopathol, 46, pp. 285-291. , COI: 1:STN:280:DyaK287itFyguw%3D%3D, PID: 7502488
  • Cloeckaert, A., Zygmunt, M.S., Dubray, G., Limet, J.N., Characterization of O-polysaccharide specific monoclonal antibodies derived from mice infected with the rough Brucella melitensis strain B115 (1993) J Gen Microbiol, 139, pp. 1551-1556
  • Corbel, M.G., Thomas, E.L., Hendrylfd, D.M., (1983), KPW, ed. Alnwick MAFFPublications, UK; Plommet, M., Minimal requirements for growth of Brucella suis and other Brucella species (1991) Zentralblatt fur Bakteriologie: international journal of medical microbiology, 275, pp. 436-450. , COI: 1:CAS:528:DyaK2cXhsFygu7c%3D, PID: 1755918
  • Bligh, E.G., Dyer, W.J., A rapid method of total lipid extraction and purification (1959) Canadian journal of biochemistry and physiology, 37, pp. 911-917
  • Klingman, K.L., Murphy, T.F., Purification and characterization of a high-molecular-weight outer membrane protein of Moraxella (Branhamella) catarrhalis (1994) Infect Immun, 62, pp. 1150-1155. , COI: 1:CAS:528:DyaK2cXitFahs7w%3D, PID: 8132320
  • Cloeckaert, A., Protection conferred on mice by monoclonal antibodies directed against outer-membrane-protein antigens of Brucella (1991) J Med Microbiol, 34, pp. 175-180
  • Fischer, E.R., Hansen, B.T., Nair, V., Hoyt, F.H., Dorward, D.W., Scanning electron microscopy (2012) Curr Protoc Microbiol, , https://doi.org/10.1002/9780471729259.mc02b02s25, Chapter 2, Unit2B 2
  • Finn, R.D., Pfam: the protein families database (2014) Nucleic Acids Res, 42, pp. D222-D230
  • Altschul, S.F., Gapped BLAST and PSI-BLAST: A new generation of protein database search programs (1997) Nucleic Acids Res, 25, pp. 3389-3402. , gka562 [pii]
  • Bendtsen, J.D., Nielsen, H., von Heijne, G., Brunak, S., Improved prediction of signal peptides: SignalP 3.0 (2004) J Mol Biol, 340, pp. 783-795
  • Shen, H.B., Chou, K.C., Gneg-mPLoc: a top-down strategy to enhance the quality of predicting subcellular localization of Gram-negative bacterial proteins (2010) Journal of theoretical biology, 264, pp. 326-333
  • Edgar, R.C., MUSCLE: multiple sequence alignment with high accuracy and high throughput (2004) Nucleic Acids Res, 32, pp. 1792-1797
  • Hofmann, K., Stoffel, W., (1993) Biol. Chem. Hoppe-Seyler, 374
  • Wilkins, M.R., Protein identification and analysis tools in the ExPASy server (1999) Methods in molecular biology, 112, pp. 531-552. , COI: 1:CAS:528:DyaK1cXotVGrtrg%3D, PID: 10027275
  • Price, M.N., Huang, K.H., Alm, E.J., Arkin, A.P., A novel method for accurate operon predictions in all sequenced prokaryotes (2005) Nucleic Acids Res, 33, pp. 880-892
  • Kelley, L.A., Mezulis, S., Yates, C.M., Wass, M.N., Sternberg, M.J., The Phyre2 web portal for protein modeling, prediction and analysis (2015) Nature protocols, 10, pp. 845-858
  • Drozdetskiy, A., Cole, C., Procter, J., Barton, G.J., JPred4: a protein secondary structure prediction server (2015) Nucleic Acids Res, 43, pp. W389-W394

Citas:

---------- APA ----------
Bialer, M.G., Ruiz-Ranwez, V., Sycz, G., Estein, S.M., Russo, D.M., Altabe, S., Sieira, R.,..., Zorreguieta, A. (2019) . MapB, the Brucella suis TamB homologue, is involved in cell envelope biogenesis, cell division and virulence. Scientific Reports, 9(1).
http://dx.doi.org/10.1038/s41598-018-37668-3
---------- CHICAGO ----------
Bialer, M.G., Ruiz-Ranwez, V., Sycz, G., Estein, S.M., Russo, D.M., Altabe, S., et al. "MapB, the Brucella suis TamB homologue, is involved in cell envelope biogenesis, cell division and virulence" . Scientific Reports 9, no. 1 (2019).
http://dx.doi.org/10.1038/s41598-018-37668-3
---------- MLA ----------
Bialer, M.G., Ruiz-Ranwez, V., Sycz, G., Estein, S.M., Russo, D.M., Altabe, S., et al. "MapB, the Brucella suis TamB homologue, is involved in cell envelope biogenesis, cell division and virulence" . Scientific Reports, vol. 9, no. 1, 2019.
http://dx.doi.org/10.1038/s41598-018-37668-3
---------- VANCOUVER ----------
Bialer, M.G., Ruiz-Ranwez, V., Sycz, G., Estein, S.M., Russo, D.M., Altabe, S., et al. MapB, the Brucella suis TamB homologue, is involved in cell envelope biogenesis, cell division and virulence. Sci. Rep. 2019;9(1).
http://dx.doi.org/10.1038/s41598-018-37668-3