Identification of the Vibrio cholerae type 4 prepilin peptidase required for cholera toxin secretion and pilus formation

Molecular Microbiology

Volumn 29, Issue 6, 1998, Pages 1481-1492

  Marsh, Jane W ^a   Taylor, Ronald K ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; CHOLERA TOXIN; PREPILIN PEPTIDASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; BACTERIUM PILUS; GENE DELETION; GENE DISRUPTION; GENE LOCUS; HEMAGGLUTINATION INHIBITION; LD 50; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; PSEUDOMONAS AERUGINOSA; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STRUCTURE ACTIVITY RELATION; TOXIN SYNTHESIS; VIBRIO CHOLERAE;

ADHESINS, BACTERIAL; AMINO ACID SEQUENCE; ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BASE SEQUENCE; CHOLERA TOXIN; DATABASES, FACTUAL; DNA, BACTERIAL; ENDOPEPTIDASES; ESCHERICHIA COLI; FIMBRIAE, BACTERIAL; GENE DELETION; GENES, BACTERIAL; GENOME, BACTERIAL; HEMAGGLUTINATION; MICE; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE HOMOLOGY, AMINO ACID; VIBRIO CHOLERAE; VIRULENCE;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; VIBRIO CHOLERAE; VIBRIO CHOLERAE O1 BIOVAR ELTOR; VIBRIO VULNIFICUS;

EID: 0031687564     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1998.01031.x     Document Type: Article

References (43)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Cassel, D., and Pfeuffer, T. (1978) Mechanism of cholera toxin action: covalent modification of the guanyl nucleotide-binding protein of the adenylate cyclase system. Proc Natl Acad Sci USA 75: 2669-2673.
3. Chang, A.C., and Cohen, S.N. (1978) Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 134: 1141-1156.
4. de Lorenzo, V., and Timmis, K.N. (1994) Analysis and construction of stable phenotypes in gram-negative bacteria with Tn5- and Tn10-derived minitransposons. Methods Enzymol 235: 386-405.
5. Finkelstein, R.A., and Mukerjee, S. (1963) Haemagglutination. A rapid method for the differentiating Vibrio cholerae from El Tor vibrios. Proc Soc Exp Biol Med 112: 355-359.
6. Francetic, O., and Pugsley, A.P. (1996) The cryptic general secretory pathway (gsp) operon of Escherichia coli K-12 encodes functional proteins. J Bacteriol 178: 3544-3549.
7. Francetic, O., Lory, S., and Pugsley, A.P. (1998) A second prepilin peptidase gene in Escherichia coli K-12. Mol Microbiol 27: 763-775.
8. Freter, R., and Jones, G.W. (1976) Adhesive properties of Vibrio cholerae: nature of the interaction with intact mucosal surfaces. Infect Immun 14: 2246-2256.
9. Friedman, A.M., Long, S., Brown, S., Buikema, W., and Ausubel, F. (1982) Construction of a broad host range cosmid cloning vector and its use in the genetic analysis of Rhizobium mutants. Gene 18: 289-296.
10. Gardel, C.L., and Mekalanos, J.J. (1996) Alterations in Vibrio cholerae motility phenotypes correlate with changes in virulence factor expression. Infect Immun 64: 2246-2255.
11. Gill, D.M. (1976) The arrangement of subunits in cholera toxin. Biochemistry 15: 1242-1248.
12. Gill, D.M., and Meren, R. (1978) ADP-ribosylation of membrane proteins catalyzed by cholera toxin: basis of the activation of adenylate cyclase. Proc Natl Acad Sci USA 75: 3050-3054.
13. Hirst, T.R., and Holmgren, J. (1987) Transient entry of enterotoxin subunits into the periplasm occurs during their secretion from Vibrio cholerae. J Bacteriol 169: 1037-1045.
14. Hobbs, M., and Mattick, J.S. (1993) Common components in the assembly of type 4 fimbriae, DNA transfer systems, filamentous phage and protein-secretion apparatus: a general system for the formation of surface-associated protein complexes. Mol Microbiol 10: 233-243.
15. Jahagirdar, R., and Howard, S.P. (1994) Isolation and characterization of a second exe operon required for extracellular protein secretion in Aeromonas hydrophila. J Bacteriol 176: 6819-6826.
16. Jonson, G., Lebens, M., and Holmgren, J. (1994) Cloning and sequencing of Vibrio cholerae mannose-sensitive haemagglutinin pilin gene: localization of mshA within a cluster of type 4 pilin genes. Mol Microbiol 13: 109-118.
17. Kaufman, M.R., Seyer, J.M., and Taylor, R.K. (1991) Processing of TCP pilin by TcpJ typifies a common step intrinsic to a newly recognized pathway of extracellular protein secretion by gram-negative bacteria. Genes Dev 5: 1834-1846.
18. King, C.A., and Van Heyningen, W.E. (1973) Deactivation of cholera toxin by a sialidase-resistant monosialosylganglioside. J Infect Dis 127: 639-647.
19. Lory, S., and Strom, M.S. (1997) Structure-function relationship of type-IV prepilin peptidase of Pseudomonas aeruginosa - a review. Gene 192: 117-121.
20. Lospalluto, J.J., and Finkelstein, R.A. (1972) Chemical and physical properties of cholera exo-enterotoxin (choleragen) and its spontaneously formed toxoid (choleragenoid). Biochim Biophys Acta 257: 158-166.
21. Mekalanos, J.J., Swartz, D.J., Pearson, G.D., Harford, N., Groyne, F., and de Wilde, M. (1983) Cholera toxin genes: nucleotide sequence, deletion analysis and vaccine development. Nature 306: 551-557.
22. Nakai, K., and Kanehisa, M. (1991) Expert system for predicting protein localization sites in gram-negative bacteria. Proteins 11: 95-110.
23. Nunn, D.N., and Lory, S. (1992) Components of the protein-excretion apparatus of Pseudomonas aeruginosa are processed by the type IV prepilin peptidase. Proc Natl Acad Sci USA 89: 47-51.
24. Nunn, D.N., and Lory, S. (1993) Cleavage, methylation, and localization of the Pseudomonas aeruginosa export proteins XcpT, -U, -V, and -W. J Bacteriol 175: 4375-4382.
25. Nunn, D., Bergman, S., and Lory, S. (1990) Products of three accessory genes, pilB, pilC, and pilD, are required for biogenesis of Pseudomonas aeruginosa pili. J Bacteriol 172: 2911-2919.
26. Overbye, L.J., Sandkvist, M., and Bagdasarian, M. (1993) Genes required for extracellular secretion of enterotoxin are clustered in Vibrio cholerae. Gene 132: 101-106.
27. Pugsley, A.P. (1993) The complete general secretory pathway in gram-negative bacteria. Microbiol Rev 57: 50-108.
28. Pugsley, A.P., and Dupuy, B. (1992) An enzyme with type IV prepilin peptidase activity is required to process components of the general extracellular protein secretion pathway of Klebsiella oxytoca. Mol Microbiol 6: 751-760.
29. Reeves, P.J., Whitcombe, D., Wharam, S., Gibson, M., Allison, G., Bunce, N., et al. (1993) Molecular cloning and characterization of 13 out genes from Erwinia carotovora subspecies carotovora: genes encoding members of a general secretion pathway (GSP) widespread in Gram-negative bacteria. Mol Microbiol 8: 443-456.
30. Sandkvist, M., Morales, V., and Bagdasanan, M. (1993) A protein required for secretion of cholera toxin through the outer membrane of Vibrio cholerae. Gene 123: 81-86.
31. Sandkvist, M., Overbye, Michel L., Hough, L.P., Morales, V.M., Bagdasarian, M.M.K., DiRita, V.J., and Bagdasarian, M. (1997) General secretion pathway (eps) genes required for toxin secretion and outer membrane biogenesis in Vibrio cholerae. J Bacteriol 179: 6994-7003.
32. Silhavy, T.J., Berman, M.L., and Enquist, L.W. (1984) Experiments with Gene Fusions. Cold Spring Harbor, NY. Cold Spring Harbor Laboratory Press.
33. Skorupski, K., and Taylor, R.K. (1996) Positive selection vectors for allelic exchange. Gene 169: 47-52.
34. Stoker, N.G., Fairweather, N.F., and Spratt, B.G. (1982) Versatile low-copy-number plasmid vectors for cloning in Escherichia coli. Gene 18: 335-341.
35. Strom, M.S., and Lory, S. (1993) Structure-function and biogenesis of the type IV pili. Annu Rev Microbiol 47: 565-596.
36. Strom, M.S., Nunn, D.N., and Lory, S. (1993) A single bifunctional enzyme, PilD, catalyzes cleavage and N-methylation of proteins belonging to the type IV pilin family. Proc Natl Acad Sci USA 90: 2404-2408.
37. Strom, M., Pepe, C., Paranjpye, R., Pepe, J., and Bell, J. (1997) Characterization of type IV peptidase mutants of Aeromonas hydrophila and Vibrio vulnificus may lead to the identification of novel virulence determinants. Abstracts of papers presented at the 1997 meeting on Microbial Pathogenesis and Host Response, Cold Spring Harbor Laboratory, NY, pp. 102.
38. Svennerholm, A.M., and Holmgren, J. (1978) Identification of Escherichia coli heat-labile enterotoxin by means of a ganglioside immunosorbant assay (GM1-ELISA) procedure. Curr Microbiol 1: 19-23.
39. Tacket, C.O., Taylor, R.K., Losonsky, G., Lim, Y., Nataro, J.P., Kaper, J.B., and Levine, M.M. (1998) Investigation of the roles of toxin-coregulated pili and mannose-sensitive hemagglutinin pili in the pathogenesis of Vibrio cholerae O139 infection. Infect Immun 66: 692-695.
40. Taylor, R.K., Miller, V.L., Furlong, D.B., and Mekalanos, J.J. (1987) Use of phoA gene fusions to identify a pilus colonization factor regulated with cholera toxin. Proc Natl Acad Sci USA 84: 2833-2837.
41. Thelin, K.H., and Taylor, R.K. (1996) Toxin-coregulated pilus. but not mannose-sensitive hemagglutinin, is required for colonization by Vibrio cholerae O1 El Tor biotype and O139 strains. Infect Immun 64: 2853-2856.
42. Yanisch-Perron, C., Vieira, J., and Messing, J. (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33: 103-119.
43. Zhang, H.Z., Lory, S., and Donnenberg, M.S. (1994) A plasmid-encoded prepilin peptidase gene from enteropathogenic Escherichia coli. J Bacteriol 176: 6885-6891.