PilP, a pilus biogenesis lipoprotein in Neisseria gonorrhoeae, affects expression of PilQ as a high-molecular-mass multimer

Molecular Microbiology

Volumn 23, Issue 4, 1997, Pages 657-668

  Drake, Sandra L ^a,b   Sandstedt, Sara A ^a,c   Koomey, Michael ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b EASTERN MICHIGAN UNIVERSITY   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN;

ARTICLE; CELL MEMBRANE; CELL ORGANELLE; GENETIC ANALYSIS; MEMBRANE TRANSPORT; MUTANT; NEISSERIA GONORRHOEAE; PHENOTYPE; PRIORITY JOURNAL; PSEUDOMONAS; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY;

ESCHERICHIA COLI; HEDYOTIS MANNII; NEISSERIA; NEISSERIA GONORRHOEAE; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS SYRINGAE;

EID: 0031025472     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1997.2511618.x     Document Type: Article

References (66)

1. Albano, M., Breitling, R., and Dubnau, D.A. (1989) Nucleotide sequence and genetic organization of the Bacillus subtilis comG operon. J Bacteriol 171: 5386-5404.
2. Allaoui, A., Sansonetti, P.J., and Parsot, C. (1992) MxiJ, a lipoprotein involved in secretion of Shigella Ipa invasins, is homologous to YscJ, a secretion factor of the Yersinia Yop proteins. J Bacteriol 174: 7661-7669.
3. Allaoui, A., Sansonetti, P.J., and Parsot, C. (1993) MxiD, an outer membrane protein necessary for the secretion of the Shigella flexneri Ipa invasins. Mol Micriobiol 7: 59-68.
4. Blake, M.S., Johnston, K.H., Russell, J.G., and Gotschlich, E.C. (1984) A rapid, sensitive method for detection of alkaline phosphatase-conjugated anti-antibody on Western blots. Anal Biochem 136: 175-179.
5. Brissette, J.L, and Russel, M. (1990) Secretion and membrane integration of a filamentous phage-encoded morphogenetic protein. J Mol Biol 211: 565-580.
6. Catlin, B.W. (1973) Nutritional profiles of Neisseria gonorrhoeae, Neisseria meningitidis, and Neisseria lactamica in chemically defined media and the use of growth requirements for gonococcal typing. J Infect Dis 128: 178-194.
7. Chen, L., Chen, D., Miaw, J., and Hu, N. (1996) XpsD, an outer membrane protein required for protein secretion by Xanthomonas campestris pv. campestris, forms a multimer. J Biol Chem 271: 2703-2708.
8. Condemine, G., Dorel, C., Hugouvieux-Cotte-Pattat, N., and Robert-Baudouy, J. (1992) Some of the out genes involved in the secretion of pectate lyases in Erwinia chrysanthemi are regulated by kdgR. Mol Microbiol 6: 3199-3211.
9. Devereux, J., Haeberli, P., and Smithies, O. (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12: 387-395.
10. Doran, T.J., Loh, S.M., Firth, N., and Skurray, R.A. (1994) Molecular analysis of the F plasmid traVR region: traV encodes a lipoprotein. J Bacteriol 176: 4182-4186.
11. Drake, S.L., and Koomey, M. (1995) The product of the pilQ gene is essential for the biogenesis of type IV pili in Neisseria gonorrhoeae. Mol Microbiol 18: 975-986.
12. d'Enfert, C., and Pugsley, A.P. (1989) Klebsiella pneumoniae pulS gene encodes an outer membrane lipoprotein required for pullulanase secretion. J Bacteriol 171: 3673-3679.
13. d'Enfert, C., Reyss, I., Wandersman, C., and Pugsley, A.P. (1989) Protein secretion by Gram-negative bacteria. Characterization of two membrane proteins required for pullulanase secretion by Escherichia coli K-12. J Biol Chem 264: 17462-17468.
14. Fernandez, D., Spudich, G.M., Zhou, X.-R., and Christie, P.J. (1996) The Agrobacterium tumefaciens VirB7 lipoprotein is required for stabilization of VirB proteins during assembly of the T-DNA complex transport apparatus. J Bacteriol 178: 3168-3176.
15. Freitag, N., Seifert, H.S., and Koomey, M. (1995) Characterization of the pilF-pilD pilus assembly locus of Neisseria gonorrhoeae. Mol Microbiol 16: 575-586.
16. Genin, S., and Boucher, C.A. (1994) A superfamily of proteins involved in different secretion pathways in Gramnegative bacteria: modular structure and specificity of the N-terminal domain. Mol Gen Genet 243: 112-118.
17. Giron, J.A., Ho, A.S.Y., and Schoolnik, G.K. (1991) An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science 254: 710-713.
18. Gish, W., and States, D.J. (1993) Identification of protein coding regions by database similarity search. Nat Genet 3: 266-272.
19. Hardie, K.R., Lory, S., and Pugsley, A.P. (1996) Insertion of an outer membrane protein in Escherichia coli requires a chaperone-like protein. EMBO J 15: 978-988.
20. Heckels, J.E. (1989) Structure and function of pili of pathogenic Neisseria species. Clin Microbiol Rev 2: S66-S73.
21. Hermodson, M.A., Chen, K.C., and Buchanan, T.M. (1978) Neisseria pili proteins: amino-terminal amino acid sequences and identification of an unusual amino acid. Biochemistry 17: 442-445.
22. Hoyne, P.A., Hass, R., Meyer, T.F., Davies, J.K., and Elleman, T.C. (1993) Production of Neisseria gonorrhoeae pili (fimbriae) in Pseudomonas aeruginosa. J Bacteriol 174: 7321-7327.
23. Hu, N., Hung, M., Liao, C., and Lin, M. (1995) Subcellular location of XpsD, a protein required for extracellular protein secretion by Xanthomonas campestris pv. campestris. Microbiology 141: 1395-1406.
24. Jonsson, A.-B., Nyberg, G., and Normark, S. (1991) Phase variation of gonococcal pili by frameshift mutation in pilC, a novel gene for pilus assembly. EMBO J 10: 477-488.
25. Kaniga, K., Bossio, J.C., and Galan, J.E. (1994) Salmonella typhimurium invasion genes invF and invG encode homologues to the PuID and AraC family of proteins. Mol Microbiol 13: 555-568.
26. Kazmierczak, B.I., Mielke, D.L., and Russel, M. (1994) pIV, a filamentous phage protein that mediates phage export across the bacterial cell envelope, forms a multimer. J Mol Biol 238: 187-198.
27. Koomey, M., Gotschlich, E.C., Robbins, K., Bergstrom, S., and Swanson, J. (1987) Effects of recA mutations on pilus antigenic variation and phase transitions in Neisseria gonorrhoeae. Genetics 117: 391-398.
28. van der Ley, P., van der Biezen, J., and Poolman, J.T. (1995) Construction of Neisseria meningitidis strains carrying multiple chromosomal copies of the porA gene for use in the production of a multivalent outer membrane vesicle vaccine. Vaccine 13: 401-407.
29. Linderoth, N.A., Model, P., and Russel, M. (1996) Essential role of a sodium dodecyl sulfate-resistant protein IV multimer in assembly export of filamentous phage. J Bacteriol 178: 1962-1970.
30. Lory, S. (1992) Determinants of extracellular protein secretion in Gram-negative bacteria. J Bacteriol 174: 3423-3428.
31. Martin, P.R., Hobbs, M., Free, P.D., Jeske, Y., and Mattick, J.S. (1993) Characterization of pilQ, a new gene required for the biogenesis of type 4 fimbriae in Pseudomonas aeruginosa. Mol Microbiol 9: 857-868.
32. Martin, P.R., Watson, A.A., McCaul, T.F., and Mattick, J.S. (1995) Characterization of a five-gene cluster required for the biogenesis of type 4 fimbriae in Pseudomonas aeruginosa. Mol Microbiol 16: 497-508.
33. Michiels, T., Vanooteghem, J.C., Lambert de Rouvrait, C., China, B., Gustin, A., Boudry, P., and Cornelis, G.R. (1991) Analysis of virC, an operon involved in the secretion of Yops proteins by Yersinia enterocolitica. J Bacteriol 173: 4994-5009.
34. Newhall, W.J., Wilde, C.E., Sawyer, W.D., and Haak, R.A. (1980) High-molecular-weight antigenic protein complex in the outer membrane of Neisseria gonorrhoeae. Infect Immun 27: 475-482.
35. Ottow, J.C.G. (1975) Ecology, physiology, and genetics of fimbriae and pili. Annu Rev Microbiol 29: 79-108.
36. Parsot, C., Taxman, E., and Mekalanos, J.J. (1991) ToxR regulates the production of lipoproteins and the expression of serum resistance in Vibrio cholerae. Proc Natl Acad Sci USA 88: 1641-1645.
37. Patel, P., Marrs, C.F., Mattick, J.S., Ruehl, W.W., Taylor, R.K., and Koomey, M. (1991) Shared antigenicity and immunogenicity of type IV pilins expressed by Pseudomonas aeruginosa, Moraxella bovis, Neisseria gonorrhoeae, Dichelobacter nodosus and Vibrio cholerae. Infect Immun 59: 4674-4676.
38. Perumal, N.B., and Minckley, E.G.J. (1984) The product of the F sex factor traT surface exclusion gene is a lipoprotein. J Biol Chem 259: 5357-5360.
39. Plano, G.V., and Straley, S.C. (1995) Mutations in yscC, yscD, and yscG prevent high-level expression and secretion of V antigen and Yops in Yersinia pestis. J Bacteriol 177: 3843-3854.
40. Pohlman, R.F., Genetti, H.D., and Winans, S.C. (1994) Common ancestry between IncN conjugal transfer genes and macromolecular export systems of plant and animal pathogens. Mol Microbiol 14: 655-668.
41. Pugsley, A.P. (1993) The complete general secretory pathway in Gram-negative bacteria. Microbiol Rev 57: 50-108.
42. Roine, E., Nunn, D.N., Paulin, L., and Romantschuk, M. (1996) Characterization of genes required for pilus expression in Pseudomonas syringae pathovar phaseolicola. J Bacteriol 178: 410-417.
43. Rudel, T., van Putten, J.P.M., Gibbs, C.P., Hass, R., and Meyer, T.F. (1992) Interaction of two variable proteins (PilE and PilC) required for pilus-mediated adherence of Neisseria gonorrhoeae to human epithelial cells. Mol Microbiol 6: 3439-3450.
44. Rudel, T., Boxberger, H.-J., and Meyer, T.F. (1995a) Pilus biogenesis and epithelial cell adherence of Neisseria gonorrhoeae pilC double knock-out mutants. Mol Microbiol 1057-1071.
45. Rudel, T., Scheuerpflug, I., and Meyer, T.F. (1995b) Neisseria PilC protein identified as type-4 pilus tip-located adhesin. Nature 373: 357-359.
46. Russel, M. (1991) Filamentous phage assembly. Mol Microbiol 5: 1607-1613.
47. Russel, M. (1994a) Mutants at conserved positions in gene IV, a gene required for assembly and secretion of filamentous phages. Mol Microbiol 14: 357-369.
48. Russel, M. (1994b) Phage assembly: a paradigm for bacterial virulence factor export. Science 265: 612-614.
49. Russel, M. (1995) Moving through the membrane with filamentous phages. Trends Microbiol 3: 223-228.
50. Russel, M., and Kazmierczak, B. (1993) Analysis of the structure and subcellular location of filamentous phage pIV. J Bacteriol 175: 3998-4007.
51. Sanger, F., Nicklen, S., and Coulson, A.R. (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463-5467.
52. Seifert, H.S., Chen, E.Y., So, M., and Heffron, F. (1986) Shuttle mutagenesis: a method of transposon mutagenesis for Saccharomyces cerevisiae. Proc Natl Acad Sci USA 83: 735-739.
53. Seifert, H.S., Ajioka, R.S., Paruchuri, D., Heffron, F., and So, M. (1990) Shuttle mutagenesis of Neisseria gonorrhoeae: pilin null mutations lower DNA transformation competence. J Bacteriol 172: 40-46.
54. Shaw, C.E., and Taylor, R.K. (1990) Vibrio cholerae 0395 tcpA pilin gene sequence and comparison of the predicted protein structural features to those of type IV pilins. Infect Immun 58: 3042-3049.
55. Stone, K.D., Zhange, H., Carlson, L.K., and Donnenberg, M.S. (1996) A cluster of fourteen genes from enteropathogenic Escherichia coli is sufficient for the biogenesis of a type IV pilus. Mol Microbiol 20: 325-337.
56. Strom, M.S., and Lory, S. (1986) Cloning and expression of the pilin gene of Pseudomonas aeruginosa PAK in Escherichia coli. J Bacteriol 165: 367-372.
57. Studier, F.W., and Moffatt, B.A. (1986) Use of bacteriophages T7 RNA polymerase to direct selective high-level expression of cloned genes. J Mol Biol 189: 113-130.
58. Swanson, J. (1973) Studies on gonococcus infection. IV. Pili: their role in attachment of gonococci to tissue culture cells. J Exp Med 137: 571-589.
59. Swanson, J. (1978) Studies on gonococcus infection XII. Colony color and opacity variants of gonococci. Infect Immun 19: 320-331.
60. Swanson, J., Kraus, S.J., and Gotschlich, E.C. (1971) Studies on gonococcus infection. I. Pili and zones of adhesion: their relation to gonococcal growth patterns. J Exp Med 134: 886-906.
61. Tabor, S., and Richardson, C.C. (1985) A bacteriophage T7 RNA polymerase/promoter specific system for controlled exclusive expression of specific genes. Proc Natl Acad Sci USA 82: 1074-1078.
62. Thomas, S.R., and Trust, R.J. (1995) A specific PuID homolog is required for the secretion of paracrystalline surface array subunits in Aeromonas hydrophilia. J Bacteriol 177: 3932-3939.
63. Tomb, J., El-Hajj, H., and Smith, H.O. (1991) Nucleotide sequence of a cluster of genes involved in the transformation of Haemophilus influenzae Rd. Gene 104: 1-10.
64. Tonjum, T., Freitag, N.E., Normark, E., and Koomey, M. (1995) Identification and characterization of pilG, a highly conserved pilus assembly gene in pathogenic Neisseria. Mol Microbiol 16: 451-464.
65. Yamaguchi, K., Yu, F., and Inouye, M. (1988) A single amino acid determinant of membrane localization of lipoproteins in E. coli. Cell 53: 423-432.
66. Zhang, Q.Y., DeRyckere, D., Lauer, P., and Koomey, M. (1992) Gene conversion in Neisseria gonorrhoeae: evidence for its role in pilus antigenic variation. Proc Natl Acad Sci USA 89: 5366-5370.