Amino-terminal maturation of the Bordetella pertussis filamentous haemagglutinin

Molecular Microbiology

Volumn 19, Issue 1, 1996, Pages 65-78

  Jacob Dubuisson, Françoise ^a   Buisine, Corinne ^a   Mielcarek, Nathalie ^a   Clément, Eve ^a   Menozzi, Franco D ^a   Locht, Camille ^a  

^a INSTITUT PASTEUR DE LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; HEMAGGLUTININ; OUTER MEMBRANE PROTEIN;

ARTICLE; BORDETELLA PERTUSSIS; GENE EXPRESSION REGULATION; IMMUNOBLOTTING; PRIORITY JOURNAL; PROTEIN ANALYSIS;

BORDETELLA PERTUSSIS; ESCHERICHIA COLI;

EID: 0030029213     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1996.349883.x     Document Type: Article

References (47)

1. Balloul, J.M., Sondermeyer, P., Dreyer, D., Capron, M., Grzych, J.M., Pierce, R.J., Carvallo, D., Lecocq, J.P., and Capron, A. (1987) Molecular cloning of a protective antigen of Schistosomes. Nature 326: 149-153.
2. Barenkamp, S, and Leininger, E. (1992) Cloning, expression and DNA sequence analysis of genes encoding nontypeable Haemophilus influenzae high-molecular-weight surface-exposed proteins related to filamentous hemagglutinin of Bordetella pertussis. Infect Immun 60: 1302-1313.
3. Barenkamp, S.J., and St Geme, III, J.W. (1994) Genes encoding high-molecular-weight adhesion proteins of nontypeable Haemophilus influenzae are part of gene clusters. Infect Immun 62: 3320-3328.
4. Bieker, K.L., and Silhavy, T.J. (1989) PrlA is important for the translocation of exported proteins across the cytoplasmic membrane of Escherichia coli. Proc Natl Acad Sci USA 86: 968-972.
5. Boucher, P.E., Menozzi, F.D., and Locht, C. (1994) The modular architecture of bacterial response regulator. Insight into the activation mechanism of the BvgA transactivator of Bordetella pertussis. J Mol Biol 241: 363-367.
6. Brown, D.R., and Parker, C.D. (1987) Cloning of the filamentous hemagglutinin of Bordetella pertussis and its expression in Escherichia coli. Infect Immun 55: 154-161.
7. Burnette, W.N., Mar, V.L., Cieplak, W., Morris, C.F., Kaljot, K.T., Marchitto, K.S., Sachdev, R.K., Locht, C., and Keith, J.M. (1988) Direct expression of Bordetella pertussis toxin subunits to high levels in Escherichia coli. Biotechnology 6: 699-706.
8. Delisse-Gathoye, A.-M., Locht, C., Jacob, F., Raaschou-Nielsen, M., Heron, I., Ruelle, J.-L., De Wilde, M., and Cabezon, T. (1990) Cloning, partial sequence, expression and antigenic analysis of the filamentous hemagglutinin gene of Bordetella pertussis. Infect Immun 58: 2895-2905.
9. Domenighini, M., Relman, D., Capiau, C., Falkow, S., Prugnola, A., Scarlato, V., and Rappuoli, R. (1990) Genetic characterization of Bordetella pertussis filamentous haemagglutinin: a protein processed from an unusually large precursor. Mol Microbiol 4: 787-800.
10. Forsberg, A., Rosqvist, R., and Wolf-Watz, H. (1994) Regulation and polarized transfer of the Yersinia outer proteins (Yops) involved in antiphagocytosis. Trends Microbiol 2: 14-19.
11. Fürste, J.P., Pansegrau, W., Frank, R., Blöcker, H., Scholz, P., Bagdasarian, M., and Lanka, E. (1986) Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector. Gene 48: 119-131.
12. Guzman, C.A., Brownlie, R.M., Kadurugamuwa, J., Walker, M.J., and Timmis, K.N. (1991) Antibody responses in the lungs of mice following oral immunization with Salmonella typhimurium aroA and invasive Escherichia coli strains expressing the filamentous hemagglutinin of Bordetella pertussis. Infect Immun 59: 4391-4397.
13. Hannah, J.H., Menozzi, F.D., Renauld, G., Locht, C., and Brennan, M.J. (1994) Sulfated glycoconjugate receptors for the Bordetella pertussis adhesin filamentous hemagglutinin (FHA) and mapping of the heparin-binding domain on FHA. Infect Immun 62: 5010-5019.
14. Harlow, E., and Lane, D. (1988) Antibodies. A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
15. Jacob F., Capiau, C., Gathoye, A.-M., Locht, C., and Cabezon, T. (1988) Molecular cloning of the filamentous hemagglutinin structural gene from Bordetella pertussis in Escherichia coli. In FEMS Symposium on pertussis. Mebel, S., Stompe, H., Drescher, M., and Rustenbach, S. (eds). Berlin: Society of Microbiology and Epidemiology of the GDR, pp. 62-68.
16. Knapp, S., and Mekalanos, J.J. (1988) Two trans-acting regulatory genes (vir and mod) control antigenic modulation in Bordetella pertussis. J Bacteriol 170: 5059-5066.
17. Koronakis, V., and Hughes, C. (1993) Bacterial signal-peptide independent protein export: HlyB-directed secretion of hemolysin. Seminars Cell Biol 4: 7-15.
18. Kovach, M.E., Phillips, R.W., Elzer, P.H., Roop, R.M.I., and Peterson, K.M. (1994) pBBR1MCS: a broad-host-range cloning vector. Bio/Techniques 16: 800-802.
19. Kremer, L., Baulard, A., Estaquier, J., Content, J., Capron, A., and Locht, C. (1995) Analysis of the Mycobacterium tuberculosis 85A antigen promoter region. J Bacteriol 177: 642-653.
20. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
21. Locht, C., Geoffroy, M.C., and Renauld, G. (1992) Common accessory genes for the Bordetella pertussis filamentous haemagglutinin and fimbriae share sequence similarities with the papC and papD gene families. EMBO J 11: 3175-3183.
22. Locht, C., Bertin, P., Menozzi, F.D., and Renauld, G. (1993) The filamentous haemagglutinin, a multifaceted adhesin produced by virulent Bordetella spp. Mol Microbiol 9: 653-660.
23. Lory, S. (1992) Determinants of extracellular protein secretion in Gram-negative bacteria. J Bacteriol 174: 3423-3428.
24. Makhov, A.M., Hannah, J.H., Brennan, M.J., Trus, B.L., Kocsis, E., Conway, J.F., Wingfield, P.T., Simon, M.N., and Steven, A.C. (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 β-strands and turns. J Mol Biol 241: 110-124.
25. Manoil, C. (1991) Analysis of membrane protein topology using alkaline phosphatase and β-galactosidase gene fusions. Meth Cell Biol 34: 61-75.
26. Manoil, C., and Beckwith, J. (1985) TnphoA: a transposon probe for protein export signals. Proc Natl Acad Sci USA 82: 8129-8133.
27. Menozzi, F.D., Gantiez, C., and Locht, C. (1991) Interaction of the Bordetella pertussis filamentous hemagglutinin with heparin. FEMS Microbiol Lett 78: 59-64.
28. Menozzi, F.D., Mutombo, R., Renauld, G., Gantiez, C., Hannah, J., Leininger, E., Brennan, M., and Locht, C. (1994) Heparin-inhibitable lectin activity of the filamentous hemagglutinin of Bordetella pertussis. Infect Immun 62: 769-778.
29. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
30. Minton, N.P. (1984) Improved plasmid vectors for the isolation of translational lac gene fusions. Gene 31: 269-273.
31. Molina, C., and Parker, C.D. (1990) Murine antibody response to oral infection with live aroA recombinant Salmonella dublin vaccine strains expressing filamentous hemagglutinin antigen form Bordetella pertussis. Infect Immun 58: 2523-2528.
32. Poole, K., Schiebel, E., and Braun, V. (1988) Molecular characterization of the hemolysin determinant of Serratia marcescens. J Bacteriol 170: 3177-3188.
33. Pugsley, A.P. (1993) The complete general secretory pathway in Gram-negative bacteria. Microbiol Rev 57: 50-108.
34. Renauld-Mongénie, 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 haemagglutinin. J Bacteriol, in press.
35. Rentier-Delrue, F., Swennen, D., and Martial, J. (1988) pIN-III-ompA secretion vectors: modification of the ompA signal peptide sequence for easier insert cloning. Nucl Acids Res 16: 8726.
36. Salmond, G.P.C., and Reeves, P.J. (1993) Membrane traffic wardens and protein secretion in Gram-negative bacteria. Trends Biochem Sci 18: 7-12.
37. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning. A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
38. Sato, Y., Kimura, M., and Fukumi, H. (1984) Development of a pertussis component vaccine in Japan. Lancet i: 124-126.
39. Schönherr, R., Tsolis, R., Focareta, T., and Braun, V. (1993) Amino acid replacements in the Serratia marcescens haemolysin ShIA define sites involved in activation and secretion. Mol Microbiol 9: 1229-1237.
40. Shaw, W.V. (1975) Chloramphenicol acetyl transferase from chloramphenicol-resistant bacteria. Meth Enzymol 43: 737-755.
41. Uphoff, T.S., and Welch, R.A. (1990) Nucleotide sequencing of the Proteus mirabilis calcium-independent hemolysin genes (hpmA and hpmB) reveals sequence similarity with the Serratia marcescens hemolysin genes (shlA and shlB). J Bacteriol 172: 1206-1216.
42. Van Gijsegem, F., Genin, S., and Boucher, C. (1993) Conservation of secretion pathways for pathogenicity determinants of plant and animal bacteria. Trends Microbiol 1: 175-180.
43. Wandersman, C. (1992) Secretion across the bacterial outer membrane. Trends Genet 8: 317-322.
44. Wattiau, P., Bernier, P., Deslée, P., Michiels, T., and Cornelis, G.R. (1994) Individual chaperones required for Yop secretion by Yersinia. Proc Natl Acad Sci USA 91: 10493-10497.
45. Weiss, A.A., and Hewlett, E.L. (1986) Virulence factors of Bordetella pertussis. Annu Rev Microbiol 40: 661-686.
46. Weiss, A.A., Hewlett, E.L., Myers, G.A., and Falkow, S. (1983) Tn5-induced mutations affecting virulence factors of Bordetella pertussis. Infect Immun 42: 33-41.
47. Willems, R.J.L., Geuijen, C., van der Heide, H.G.J., Renauld, G., Bertin, P., van der Akker, W.M.R., Locht, C., and Mooi, F.R. (1994) Mutational analysis of the Bordetella pertussis fim/fha gene cluster: identification of a gene with sequence similarities to haemolysin accessory genes involved in export of FHA. Mol Microbiol 11: 337-347.