The prodomain of the Bordetella two-partner secretion pathway protein FhaB remains intracellular yet affects the conformation of the mature C-terminal domain

Molecular Microbiology

Volumn 86, Issue 4, 2012, Pages 988-1006

  Noël, Christopher R ^a,b   Mazar, Joseph ^b,c   Melvin, Jeffrey A ^a   Sexton, Jessica A ^b,d   Cotter, Peggy A ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BURNHAM INSTITUTE   (United States)

^d NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BORDETELLA VIRULENCE FACTOR; ISOPROTEIN; PROTEIN FHA; PROTEIN FHAB; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL SECRETION SYSTEM; BORDETELLA BRONCHISEPTICA; CARBOXY TERMINAL SEQUENCE; CELL COMPARTMENTALIZATION; CELL SURFACE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PRODOMAIN; PROTEIN SECRETION; SEQUENCE ANALYSIS; STRUCTURAL BIOINFORMATICS; TWO PARTNER SECRETION SYSTEM;

ADHESINS, BACTERIAL; ANIMALS; BACTERIAL ADHESION; EPITHELIAL CELLS; MODELS, BIOLOGICAL; PROTEIN CONFORMATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; RATS; VIRULENCE FACTORS, BORDETELLA;

BORDETELLA; NEGIBACTERIA;

EID: 84871769344     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12036     Document Type: Article

References (51)

1. Abramson, T., Kedem, H., and Relman, D.A. (2008) Modulation of the NF-kappaB pathway by Bordetella pertussis filamentous hemagglutinin. PLoS ONE 3: e3825.
2. Aoki, S.K., Pamma, R., Hernday, A.D., Bickham, J.E., Braaten, B.A., and Low, D.A. (2005) Contact-dependent inhibition of growth in Escherichia coli. Science 309: 1245- 1248.
3. Aoki, S.K., Diner, E.J., de Roodenbeke, C.T., Burgess, B.R., Poole, S.J., Braaten, B.A., et al. (2010) A widespread family of polymorphic contact-dependent toxin delivery systems in bacteria. Nature 468: 439-442.
4. Buscher, A.Z., Grass, S., Heuser, J., Roth, R., and St Geme, J.W. (2006) Surface anchoring of a bacterial adhesin secreted by the two-partner secretion pathway. Mol Microbiol 61: 470-483.
5. Chevalier, N., Moser, M., Koch, H.G., Schimz, K.L., Willery, E., Locht, C., et al. (2004) Membrane targeting of a bacterial virulence factor harbouring an extended signal peptide. J Mol Microbiol Biotechnol 8: 7-18.
6. Clantin, B., Hodak, H., Willery, E., Locht, C., Jacob- Dubuisson, F., and Villeret, V. (2004) The crystal structure of filamentous hemagglutinin secretion domain and its implications for the two-partner secretion pathway. Proc Natl Acad Sci USA 101: 6194-6199.
7. Clantin, B., Delattre, A.S., Rucktooa, P., Saint, N., Meli, A.C., Locht, C., et al. (2007) Structure of the membrane protein FhaC: a member of the Omp85-TpsB transporter superfamily. Science 317: 957-961.
8. Cotter, P.A., Yuk, M.H., Mattoo, S., Akerley, B.J., Boschwitz, J., Relman, D.A., and Miller, J.F. (1998) Filamentous hemagglutinin of Bordetella bronchiseptica is required for efficient establishment of tracheal colonization. Infect Immun 66: 5921-5929.
9. Coutte, L., Antoine, R., Drobecq, H., Locht, C., and Jacob-Dubuisson, F. (2001) Subtilisin-like autotransporter serves as maturation protease in a bacterial secretion pathway. EMBO J 20: 5040-5048.
10. Coutte, L., Alonso, S., Reveneau, N., Willery, E., Quatannens, B., Locht, C., and Jacob-Dubuisson, F. (2003) Role of adhesin release for mucosal colonization by a bacterial pathogen. J Exp Med 197: 735-742.
11. Crooks, G.E., Hon, G., Chandonia, J.-M., and Brenner, S.E. (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190.
12. Delisse-Gathoye, A.M., Locht, C., Jacob, F., Raaschou-Nielsen, M., Heron, I., Ruelle, J.L., et al. (1990) Cloning, partial sequence, expression, and antigenic analysis of the filamentous hemagglutinin gene of Bordetella pertussis. Infect Immun 58: 2895-2905.
13. Desvaux, M., Scott-Tucker, A., Turner, S.M., Cooper, L.M., Huber, D., Nataro, J.P., and Henderson, I.R. (2007) A conserved extended signal peptide region directs posttranslational protein translocation via a novel mechanism. Microbiology 153: 59-70.
14. Dieterich, C., and Relman, D.A. (2011) Modulation of the host interferon response and ISGylation pathway by B. pertussis filamentous hemagglutinin. PLoS ONE 6: e27535.
15. Genevrois, S., Steeghs, L., Roholl, P., Letesson, J.-J., and van der Ley, P. (2003) The Omp85 protein of Neisseriameningitidis is required for lipid export to the outer membrane. EMBO J 22: 1780-1789.
16. Grass, S., and St Geme, J.W. (2000) Maturation and secretion of the non-typable Haemophilus influenzae HMW1 adhesin: roles of the N-terminal and C-terminal domains. Mol Microbiol 36: 55-67.
17. Hagan, C.L., Silhavy, T.J., and Kahne, D. (2011) b-Barrel membrane protein assembly by the Bam complex. Annu Rev Biochem 80: 189-210.
18. Hayes, C.S., Aoki, S.K., and Low, D.A. (2010) Bacterial contact-dependent delivery systems. Annu Rev Genet 44: 71-90.
19. Henderson, M.W., Inatsuka, C.S., Sheets, A.J., Williams, C.L., Benaron, D.J., Donato, G.M., et al. (2012) Contribution of Bordetella filamentous hemagglutinin and adenylate cyclase toxin to suppression and evasion of interleukin-17-mediated inflammation. Infect Immun 80: 2061-2075.
20. Hertle, R. (2005) The family of Serratia type pore forming toxins. Curr Protein Pept Sci 6: 313-325.
21. Hodak, H., Clantin, B., Willery, E., Villeret, V., Locht, C., and Jacob-Dubuisson, F. (2006) Secretion signal of the filamentous haemagglutinin, a model two-partner secretion substrate. Mol Microbiol 61: 368-382.
22. 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 USA 106: 19120-19125.
23. Inatsuka, C.S., Julio, S.M., and Cotter, P.A. (2005) Bordetella filamentous hemagglutinin plays a critical role in immunomodulation, suggesting a mechanism for host specificity. Proc Natl Acad Sci USA 102: 18578-18583.
24. Jacob-Dubuisson, F., Kehoe, B., Willery, E., Reveneau, N., Locht, C., and Relman, D.A. (2000) Molecular characterization of Bordetella bronchiseptica filamentous haemagglutinin and its secretion machinery. Microbiology 146: 1211-1221.
25. Jacob-Dubuisson, F., Fernandez, R., and Coutte, L. (2004) Protein secretion through autotransporter and two-partner pathways. Biochim Biophys Acta 1694: 235-257.
26. Jacob-Dubuisson, F., Villeret, V., Clantin, B., Delattre, A.S., and Saint, N. (2009) First structural insights into the TpsB/ Omp85 superfamily. Biol Chem 390: 675-684.
27. Julio, S.M., Inatsuka, C.S., Mazar, J., Dieterich, C., Relman, D.A., and Cotter, P.A. (2009) Natural-host animal models indicate functional interchangeability between the filamentous haemagglutinins of Bordetella pertussis and Bordetella bronchiseptica and reveal a role for the mature C-terminal domain, but not the RGD motif, during infection. Mol Microbiol 71: 1574-1590.
28. Junker, M., Besingi, R.N., and Clark, P.L. (2009) Vectorial transport and folding of an autotransporter virulence protein during outer membrane secretion. Mol Microbiol 71: 1323-1332.
29. Kajava, A.V., Cheng, N., Cleaver, R., Kessel, M., Simon, M.N., Willery, E., et al. (2001) Beta-helix model for the filamentous haemagglutinin adhesin of Bordetella pertussis and related bacterial secretory proteins. Mol Microbiol 42: 279-292.
30. Kozjak, V., Wiedemann, N., Milenkovic, D., Lohaus, C., Meyer, H.E., Guiard, B., et al. (2003) An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane. J Biol Chem 278: 48520-48523.
31. Lambert-Buisine, C., Willery, E., Locht, C., and Jacob-Dubuisson, F. (1998) N-terminal characterization of the Bordetella pertussis filamentous haemagglutinin. Mol Microbiol 28: 1283-1293.
32. Locht, C., Geoffroy, M.C., and Renauld, G. (1992) Common accessory genes for the Bordetella pertussis filamentous hemagglutinin and fimbriae share sequence similarities with the papC and papD gene families. EMBO J 11: 3175-3183.
33. Locht, C., Bertin, P., Menozzi, F.D., and Renauld, G. (1993) The filamentous haemagglutinin, a multifaceted adhesion produced by virulent Bordetella spp. Mol Microbiol 9: 653-660.
34. McGuirk, P., and Mills, K.H. (2000) Direct anti-inflammatory effect of a bacterial virulence factor: IL-10-dependent suppression of IL-12 production by filamentous hemagglutinin from Bordetella pertussis. Eur J Immunol 30: 415-422.
35. Makhov, A.M., Hannah, J.H., Brennan, M.J., Trus, B.L., Kocsis, E., Conway, J.F., et al. (1994) Filamentous hemagglutinin of Bordetella pertussis. A bacterial adhesin formed as a 50-nm monomeric rigid rod based on a 19-residue repeat motif rich in beta strands and turns. J Mol Biol 241: 110-124.
36. Mattoo, S., Miller, J.F., and Cotter, P.A. (2000) Role of Bordetella bronchiseptica fimbriae in tracheal colonization and development of a humoral immune response. Infect Immun 68: 2024-2033.
37. Mazar, J., and Cotter, P.A. (2006) Topology and maturation of filamentous haemagglutinin suggest a new model for twopartner secretion. Mol Microbiol 62: 641-654.
38. Mazar, J., and Cotter, P.A. (2007) New insight into the molecular mechanisms of two-partner secretion. Trends Microbiol 15: 508-515.
39. Relman, D., Tuomanen, E., Falkow, S., Golenbock, D.T., Saukkonen, K., and Wright, S.D. (1990) Recognition of a bacterial adhesion by an integrin: macrophage CR3 (alpha M beta 2, CD11b/CD18) binds filamentous hemagglutinin of Bordetella pertussis. Cell 61: 1375-1382.
40. Renauld-Mongenie, G., Cornette, J., Mielcarek, N., Menozzi, F.D., and Locht, C. (1996) Distinct roles of the N-terminal and C-terminal precursor domains in the biogenesis of the Bordetella pertussis filamentous hemagglutinin. J Bacteriol 178: 1053-1060.
41. Reumann, S., and Keegstra, K. (1999) The endosymbiotic origin of the protein import machinery of chloroplastic envelope membranes. Trends Plant Sci 4: 302-307.
42. Sanchez-Pulido, L., Devos, D., Genevrois, S., Vicente, M., and Valencia, A. (2003) POTRA: a conserved domain in the FtsQ family and a class of beta-barrel outer membrane proteins. Trends Biochem Sci 28: 523-526.
43. Sato, Y., and Sato, H. (1999) Development of acellular pertussis vaccines. Biologicals 27: 61-69.
44. Schneider, C.A., Rasband, W.S., and Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671-675.
45. Shinde, U., and Thomas, G. (2011) Insights from bacterial subtilases into the mechanisms of intramolecular chaperone-mediated activation of furin. Methods Mol Biol 768: 59-106.
46. Szabady, R.L., Peterson, J.H., Skillman, K.M., and Bernstein, H.D. (2005) An unusual signal peptide facilitates late steps in the biogenesis of a bacterial autotransporter. Proc Natl Acad Sci USA 102: 221-226.
47. Thanassi, D.G., Stathopoulos, C., Karkal, A., and Li, H. (2005) Protein secretion in the absence of ATP: the autotransporter, two-partner secretion and chaperone/ usher pathways of gram-negative bacteria. Mol Membr Biol 22: 63-72.
48. Urisu, A., Cowell, J.L., and Manclark, C.R. (1986) Filamentous hemagglutinin has a major role in mediating adherence of Bordetella pertussis to human WiDr cells. Infect Immun 52: 695-701.
49. Voulhoux, R., Bos, M.P., Geurtsen, J., Mols, M., and Tommassen, J. (2003) Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299: 262-265.
50. Wu, T., Malinverni, J., Ruiz, N., Kim, S., Silhavy, T.J., and Kahne, D. (2005) Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121: 235-245.
51. Yen, M.R., Peabody, C.R., Partovi, S.M., Zhai, Y., Tseng, Y.H., and Saier, M.H. (2002) Protein-translocating outer membrane porins of Gram-negative bacteria. Biochim Biophys Acta 1562: 6-31