Trimeric autotransporter adhesins in members of the Burkholderia cepacia complex: A multifunctional family of proteins implicated in virulence

Frontiers in Cellular and Infection Microbiology

Volumn 1, Issue , 2011, Pages

  Mil Homens, Dalila ^a   Fialho, Arsénio M ^a  

^a INSTITUTO SUPERIOR TÉCNICO   (Portugal)

Author keywords

Burkholderia cepacia complex; Trimeric autotransporter adhesins; Virulence factors

Indexed keywords

ADHESIN; DNA FRAGMENT; OUTER MEMBRANE PROTEIN; TRIMERIC AUTOTRANSPORTER ADHESIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL INFECTION; BACTERIAL VIRULENCE; BIOINFORMATICS; BURKHOLDERIA CENOCEPACIA; CELL ADHESION; EXTRACELLULAR MATRIX; GENE; GENE EXPRESSION; GENE MAPPING; GENE TRANSLOCATION; GENOME SIZE; IMMUNE RESPONSE; NONHUMAN; PHYLOGENY; REAL TIME POLYMERASE CHAIN REACTION; TAA GENE; BACTERIAL GENOME; BURKHOLDERIA CEPACIA COMPLEX; BURKHOLDERIA INFECTIONS; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN; MICROBIOLOGY; MOLECULAR EVOLUTION; MULTIGENE FAMILY; PATHOGENICITY; PHYSIOLOGY; PROTEIN QUATERNARY STRUCTURE; VIRULENCE;

ADHESINS, BACTERIAL; BURKHOLDERIA CEPACIA COMPLEX; BURKHOLDERIA INFECTIONS; EVOLUTION, MOLECULAR; GENOME, BACTERIAL; HUMANS; MODELS, MOLECULAR; MULTIGENE FAMILY; PHYLOGENY; PROTEIN STRUCTURE, QUATERNARY; VIRULENCE; VIRULENCE FACTORS;

EID: 84864365299     PISSN: None     EISSN: 22352988     Source Type: Journal    
DOI: 10.3389/fcimb.2011.00013     Document Type: Article

References (44)

1. Alamuri, P., Lower, M., Hiss, J. A., Himpsl, S. D., Schneider, G., and Mobley, H. L. T. (2010). Adhesion, invasion, and agglutination mediated by two trimeric autotransporters in the human uropathogen Proteus mirabilis. Infect. Immun. 78, 4882-4894.
2. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006). The SWISSMODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201.
3. Baldwin, A., Sokol, P. A., Parkhill, J., and Mahenthiralingam, E. (2004). The Burkholderia cepacia epidemic strain marker is part of a novel genomic island encoding both virulence and metabolism-associated genes in Burkholderia cenocepacia. Infect. Immun. 72, 1537-1547.
4. Bensing, B. A., Gibson, B. W., and Sullam, P. M. (2004). The Streptococcus gordonii platelet binding protein GspB undergoes glycosylation independently of export. J. Bacteriol. 186, 638-645.
5. Capecchi, B., Adu-Bobie, J., Di Marcello, F., Ciucchi, L., Masignani, V., Taddei, A., Rappuoli, R., Pizza, M., and Aricò, B. (2005). Neisseria meningitidis NadA is a new invasin which promotes bacterial adhesion to and penetration into human epithelial cells. Mol. Microbiol. 55, 687-698.
6. Comeau, S. R., Gatchell, D. W., Vajda, S., and Camacho, C. J. (2004). ClusPro: an automated docking and discrimination method for the prediction of protein complexes. Bioinformatics 20, 45-50.
7. Cotter, S. E., Surana, N. K., and St Geme, J. W. III. (2005). Trimeric autotransporters: a distinct subfamily of autotransporter proteins. Trends Microbiol. 13, 199-205.
8. Drevinek, P., and Mahenthiralingam, E. (2010). Burkholderia cenocepacia in cystic fibrosis: epidemiology and molecular mechanisms of virulence. Clin. Microbiol. Infect. 16, 821-830.
9. Edwards, T. E., Phan, I., Abendroth, J., Dieterich, S. H., Masoudi, A., Guo, W., Hewitt, S. N., Kelley, A., Leibly, D., Brittnacher, M. J., Staker, B. L., Miller, S. I., Van Voorhis, W. C., Myler, P. J., and Stewart, L. J. (2010). Structure of a Burkholderia pseudomallei trimeric autotransporter adhesin head. PLoS ONE 5, e12803. doi:10.1371/journal. pone.0012803
10. Finn, R. D., Mistry, J., Tate, J., Coggill, P., Heger, A., Pollington, J. E., Gavin, O. L., Gunasekaran, P., Ceric, G., Forslund, K., Holm, L., Sonnhammer, E. L. L., Eddy, S. R., and Bateman, A. (2010). The Pfam protein families database. Nucleic Acids Res. 38, 211-222.
11. Handley, P. S., Correia, F. F., Russell, K., Rosan, B., and DiRienzo, J. M. (2005). Association of a novel high molecular weight, serine-rich protein (SrpA) with fibril-mediated adhesion of the oral biofilm bacterium Streptococcus cristatus. Oral Microbiol. Immunol. 20, 131-140.
12. Heise, T., and Dersch, P. (2006). Identification of a domain in Yersinia virulence factor YadA that is crucial for extracellular matrix-specific cell adhesion and uptake. Proc. Natl. Acad. Sci. U.S.A. 103, 3375-3380.
13. Holden, M. T. G., Seth-Smith, H. M. B., Crossman, L. C., Sebaihia, M., Bentley, S. D., Cerdeño-Tárraga, A. M., Thomson, N. R., Bason, N., Quail, M. A., Sharp, S., Cherevach, I., Churcher, C., Goodhead, I., Hauser, H., Holroyd, N., Mungall, K., Scott, P., Walker, D., White, B., Rose, H., Iversen, P., Mil-Homens, D., Rocha, E. P. C., Fialho, A. M., Baldwin, A., Dowson, C., Barrell, B. G., Govan, J. R., Vandamme, P., Hart, C. A., Mahenthiralingam, E., and Parkhill, J. (2009). The genome of Burkholderia cenocepacia J2315, an epidemic pathogen of cystic fibrosis patients. J. Bacteriol. 191, 261-277.
14. Ieva, R., and Bernstein, H. D. (2009). Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane. Proc. Natl. Acad. Sci. U.S.A. 106, 19120-19125.
15. Jones, A. M., Boucher, P. E., Williams, C. L., Stibitz, S., and Cotter, P. A. (2005). Role of BvgA phosphorylation and DNA binding affinity in control of Bvg-mediated phenotypic phase transition in Bordetella pertussis. Mol. Microbiol. 58, 700-713.
16. Kline,K. A.,Fälker, S., Dahlberg, S., Normark, S., and Henriques-Normark, B. (2009). Bacterial adhesins in host-microbe interactions. Cell Host Microbe 5, 580-592.
17. Koretke, K. K., Szczesny, P., Gruber, M., and Lupas, A. N. (2006). Model structure of the prototypical nonfimbrial adhesin YadA of Yersinia enterocolitica. J. Struct. Biol. 155, 154-161.
18. Lehr, U., Schütz, M., Oberhettinger, P., Ruiz-Perez, F., Donald, J. W., Palmer, T., Linke, D., Henderson, I. R., and Autenrieth, I. B. (2010). C-terminal amino acid residues of the trimeric autotransporter adhesin YadA of Yersinia enterocolitica are decisive for its recognition and assembly by BamA. Mol. Microbiol. 78, 932-946.
19. Linke, D., Riess, T., Autenrieth, I. B., Lupas, A., and Kempf, V. A. J. (2006). Trimeric autotransporter adhesins: variable structure, common function. Trends Microbiol. 14, 264-270.
20. Mahenthiralingam, E., Simpson, D. A., and Speert, D. P. (1997). Identification and characterization of a novel DNA marker associated with epidemic Burkholderia cepacia strains recovered from patients with cystic fibrosis. J. Clin. Microbiol. 35, 808-816.
21. McCarthy, Y., Yang, L., Twomey, K. B., Sass, A., Tolker-Nielsen, T., Mahenthiralingam, E., Dow, J. M., and Ryan, R. P. (2010). A sensor kinase recognizing the cell-cell signal BDSF (cis-2-dodecenoic acid) regulates virulence in Burkholderia cenocepacia. Mol. Microbiol. 77, 1220-1236.
22. McClean, S., and Callaghan, M. (2009). Burkholderia cepacia complex: epithelial cell-pathogen confrontations and potential for therapeutic intervention. J. Med. Microbiol. 58, 1-12.
23. Meng, G., Surana, N. K., St Geme, J. W., and Waksman, G. (2006). Structure of the outer membrane translocator domain of the Haemophilus influenzae Hia trimeric autotransporter. EMBO J. 25, 2297-2304.
24. Mil-Homens, D., Rocha, E. P. C., and Fialho, A. M. (2010). Genome-wide analysis of DNA repeats in Burkholderia cenocepacia J2315 identifies a novel adhesin-like gene unique to epidemic-associated strains of the ET-12 lineage. Microbiology 156, 1084-1096.
25. Müller, J. E. N., Papic, D., Ulrich, T., Grin, I., Schã1tz, M., Oberhettinger, P., Tommassen, J., Linke, D., Dimmer, K. S., Autenrieth, I. B., and Rapaport, D. (2011a). Mitochondria can recognize and assemble fragments of a beta-barrel structure. Mol. Biol. Cell 22, 1638-1647.
26. Müller, N. F., Kaiser, P. O., Linke, D., Schwarz, H., Riess, T., Schäfer, A., Eble, J. A., and Kempf, V. A. J. (2011). Trimeric autotransporter adhesin-dependent adherence of Bartonella henselae, Bartonella quintana and Yersinia enterocolitica to matrix components and endothelial cells under static and dynamic flow conditions. Infect. Immun. 79, 2544-2553.
27. Nummelin, H., Merckel, M. C., Leo, J. C., Lankinen, H., Skurnik, M., and Goldman, A. (2004). The Yersinia adhesin YadA collagenbinding domain structure is a novel left-handed parallel beta-roll. EMBO J. 23, 701-711.
28. Perriere, G., and Gouy, M. (1996). WWW-query: an on-line retrieval system for biological sequence banks. Biochimie 78, 364-369.
29. Raghunathan, D., Wells, T. J., Morris, F. C., Shaw, R. K., Bobat, S., Peters, S. E., Paterson, G. K., Jensen, K. T., Leyton, D. L., Blair, J. M. A., Browning, D. F., Pravin, J., Flores-Langarica, A., Hitchcock, J. R., Moraes, C. T. P., Piazza, R. M. F., Maskell, D. J., Webber, M. A., May, R. C., MacLennan, C. A., Piddock, L. J., Cunningham, A. F., and Henderson, I. R. (2011). SadA, a trimeric autotransporter from Salmonella enterica serovar Typhimurium, can promote biofilm formation and provides limited protection against infection. Infect. Immun. 79, 4342-4352.
30. Riesbeck, K., Tan, T., and Forsgren, A. (2006). MID and UspA1/A2 of the human respiratory pathogen Moraxella catarrhalis, and interactions with the human host as basis for vaccine development. Acta Biochim. Pol. 53, 445-456.
31. Riess, T., Andersson, S. G. E., Lupas, A., Schaller, M., Schäfer, A., Kyme, P., Martin, J., Wälzlein, J.-H., Ehehalt, U., Lindroos, H., Schirle, M., Nordheim, A., Autenrieth, I. B., and Kempf, V. A. J. (2004). Bartonella adhesin a mediates a proangiogenic host cell response. J. Exp. Med. 200, 1267-1278.
32. Ruiz-Perez, F., Henderson, I. R., Leyton, D. L., Rossiter, A. E., Zhang, Y., and Nataro, J. P. (2009). Roles of periplasmic chaperone proteins in the biogenesis of serine protease autotransporters of Enterobacteriaceae. J. Bacteriol. 191, 6571-6583.
33. Saitou, N., and Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
34. Sajjan, U., Liu, L., Lu, A., Spilker, T., Forstner, J., and LiPuma, J. J. (2002). Lack of cable pili expression by cblA-containing Burkholderia cepacia complex. Microbiology 148, 3477-3484.
35. Sajjan, U., Wu,Y., Kent, G., and Forstner, J. (2000). Preferential adherence of cable-piliated Burkholderia cepacia to respiratory epithelia of CF knockout mice and human cystic fibrosis lung explants. J. Med. Microbiol. 49, 875-885.
36. Serruto, D., Spadafina, T., Scarselli, M., Bambini, S., Comanducci, M., Höhle, S., Kilian, M., Veiga, E., Cossart, P., Oggioni, M. R., Savino, S., Ferlenghi, I., Taddei, A. R., Rappuoli, R., Pizza, M., Masignani, V., and Aricò, B. (2009). HadA is an atypical new multifunctional trimeric coiled-coil adhesin of Haemophilus influenzae biogroup aegyptius, which promotes entry into host cells. Cell. Microbiol. 11, 1044-1063.
37. Sheets, A. J., and St Geme, J. W. III. (2011). Adhesive activity of the Haemophilus cryptic genospecies cha autotransporter is modulated by variation in tandem peptide repeats. J. Bacteriol. 193, 329-339.
38. Szczesny, P., and Lupas, A. (2008). Domain annotation of trimeric autotransporter adhesins-daTAA. Bioinformatics 24, 1251-1256.
39. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739.
40. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
41. Tiyawisutsri, R., Holden, M., Tumapa, S., Rengpipat, S., Clarke, S., Foster, S., Nierman, W., Day, N., and Peacock, S. (2007). Burkholderia Hep_Hag autotransporter (BuHA) proteins elicit a strong antibody response during experimental glanders but not human melioidosis. BMC Microbiol. 7, 19. doi:10.1186/1471-2180-7-19
42. Wagner, J. K., Heindl, J. E., Gray, A. N., Jain, S., and Goldberg, M. B. (2009). Contribution of the periplasmic chaperone Skp to efficient presentation of the autotransporter IcsA on the surface of Shigella flexneri. J. Bacteriol. 191, 815-821.
43. Wu, H., Zeng, M., and Fives-Taylor, P. (2007). The glycan moieties and the N-terminal polypeptide backbone of a fimbria-associated adhesin, Fap1, play distinct roles in the biofilm development of Streptococcus parasanguinis. Infect. Immun. 75, 2181-2188.
44. Zhou, M., and Wu, H. (2009). Glycosylation and biogenesis of a family of serine-rich bacterial adhesins. Microbiology 155, 317-327.