The identification of exported proteins with gene fusions to invasin

Molecular Microbiology

Volumn 29, Issue 6, 1998, Pages 1471-1480

  Worley, Micah J ^a   Stojiljkovic, Igor ^b   Heffron, Fred ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; BACTERIAL PROTEIN; BETA LACTAMASE; CELL SURFACE MARKER; GENTAMICIN; HEMOLYSIN; INTEGRIN; INVASIN; PROTEINASE; SIGNAL PEPTIDE;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIAL OUTER MEMBRANE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; DNA CLEAVAGE; EXOCYTOSIS; EXTRACELLULAR MATRIX; FIMBRIA; GENE FUSION; GENE INSERTION; MEMBRANE BINDING; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; SALMONELLA TYPHIMURIUM; SEQUENCE HOMOLOGY; YERSINIA PSEUDOTUBERCULOSIS;

ADHESINS, BACTERIAL; AMINO ACID SEQUENCE; ARTIFICIAL GENE FUSION; BACTERIAL PROTEINS; BASE SEQUENCE; CELL MEMBRANE; CLONING, MOLECULAR; DNA, BACTERIAL; ESCHERICHIA COLI; GENES, BACTERIAL; GENETIC COMPLEMENTATION TEST; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; PHENOTYPE; SALMONELLA TYPHIMURIUM; SEQUENCE DELETION; VIRULENCE; YERSINIA PSEUDOTUBERCULOSIS;

BACTERIA (MICROORGANISMS); EUKARYOTA; NEGIBACTERIA; SALMONELLA TYPHIMURIUM; TYPHIMURIUM; YERSINIA PSEUDOTUBERCULOSIS;

EID: 0031718287     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1998.01030.x     Document Type: Article

References (79)

1. Ahmer, B.M., van Reeuwijk, J., Timmers, C.D., Valentine, P.J., and Heffron, F. (1998) Salmonella typhimurium encodes an SdiA homolog, a putative quorum sensor of the LuxR family, that regulates genes on the virulence plasmid. J Bacteriol 180: 1118-1193.
2. Alexander, D.M., and St John, A.C. (1994) Characterization of the carbon starvation-inducible and stationary phase-inducible gene slp encoding an outer membrane lipoprotein in Escherichia coli. Mol Microbiol 11: 1059-1071.
3. 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.
4. Anraku, Y. (1966) Cyclic phosphodiesterase of Escherichia coli. New York: Harper and Row.
5. Bardwell, J.C., McGovern, K., and Beckwith, J. (1991) Identification of a protein required for disulfide bond formation in vivo. Cell 67: 581-589.
6. Baumler, A.J., Tsolis, R.M., Bowe, F.A., Kusters, J.G., Hoffmann, S., and Heffron, F. (1996) The pef fimbrial operon of Salmonella typhimurium mediates adhesion to murine small intestine and is necessary for fluid accumulation in the infant mouse. Infect Immun 64: 61-68.
7. Berks, B.C. (1996) A common export pathway for proteins binding complex redox cofactors? Mol Microbiol 22: 393-404.
8. Binet, R., Letoffe, S., Ghigo, J.M., Delepelaire, P., and Wandersman, C. (1997) Protein Secretion by Gram-negative Bacterial ABC Exporters. Gene 192: 7-11.
9. Blanco, D.R., Giladi, M., Champion, C.I., Haake, D.A., Chikami, G.K., Miller, J.N., and Lovett, M.A. (1991) Identification of Treponema pallidum subspecies pallidum genes encoding signal peptides and membrane-spanning sequences using a novel alkaline phosphatase expression vector. Mol Microbiol 5: 2405-2415.
10. Blattner, F.R., Plunkett, G.R., Bloch, C.A., Perna, N.T., Burland, V., Riley, M., et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1474.
11. Broome-Smith, J.K., and Spratt, B.G. (1986) A vector for the construction of translational fusions to TEM beta-lactamase and the analysis of protein export signals and membrane protein topology. Gene 49: 341-349.
12. Broome-Smith, J.K., Tadayyon, M., and Zhang, Y. (1990) Beta-lactamase as a probe of membrane protein assembly and protein export. Mol Microbiol 4: 1637-1644.
13. Calamia, J., and Manoil, C. (1992) Membrane protein spanning segments as export signals. J Mol Biol 224: 539-543.
14. Cleavinger, C.M., Kim, M.F., Im, J.H., and Wise, K.S. (1995) Identification of mycoplasma membrane proteins by systematic TnphoA mutagenesis of a recombinant library. Mol Microbiol 18: 283-293.
15. Cornells, G.R., and Wolf-Watz, H. (1997) The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol Microbiol 23: 861-867.
16. Delahay, R.M., Robertson, B.D., Balthazar, J.T., Shafer, W.M., and Ison, C.A. (1997) Involvement of the gonococcal MtrE protein in the resistance of Neisseria gonorrhoeae to toxic hydrophobic agents. Microbiology 143: 2127-2133.
17. Dijkstra, B.W., and Thunnissen, A.M. (1994) 'Holy' proteins. II: The soluble lytic transglycosylase. Curr Opin Struct Biol 4: 810-813.
18. Dillard, J.P., and Seifert, H.S. (1997) A peptidoglycan hydrolase similar to bacteriophage endolysins acts as an autolysin in Neissena gonorrhoeae. Mol Microbiol 25: 893-901.
19. Ehlert, K., Holtje, J.V., and Templin, M.F. (1995) Cloning and expression of a murein hydrolase lipoprotein from Escherichia coli. Mol Microbiol 16: 761-768.
20. Eichler, K., Bourgis, F., Buchet, A., Kleber, H.P., and Mandrand-Berthelot, M.A. (1994) Molecular characterization of the cai operon necessary for carnitine metabolism in Escherichia coli. Mol Microbiol 13: 775-786.
21. Fath, M.J., and Kolter, R. (1993) ABC transporters: bacterial exporters. Microbiol Rev 57: 995-1017.
22. Finlay, B.B., and Falkow, S. (1997) Common themes in microbial pathogenicity revisited. Microbiol Mol Biol Rev 61: 136-169.
23. Fleischmann, R.D., Adams, M.D., White, O., Clayton, R.A., Kirkness, E.F., Kerlavage, A.R., et al. (1995) Wholegenome random sequencing and assembly of Haemophilus influenzae Rd. Science 269: 496-512.
24. Foreman, D.T., Martinez, Y., Coombs, G., Torres, A., and Kupersztoch, Y.M. (1995) TolC and DsbA are needed for the secretion of STB, a heat-stable enterotoxin of Escherichia coli. Mol Microbiol 18: 237-245.
25. Friedlander, M., and Blobel, G. (1985) Bovine opsin has more than one signal sequence. Nature 318: 338-343.
26. Friedrich, M.J., Kinsey, N.E., Vila, J., and Kadner, R.J. (1993) Nucleotide sequence of a 13.9 kb segment of the 90 kb virulence plasmid of Salmonella typhimurium: the presence of fimbrial biosynthetic genes. Mol Microbiol 8: 543-558.
27. Gennity, J.M., and Inouye, M. (1991) The protein sequence responsible for lipoprotein membrane localization in Escherichia coli exhibits remarkable specificity. J Biol Chem 266: 16458-16464.
28. Gennity, J.M., Kim, H., and Inouye, M. (1992) Structural determinants in addition to the amino-terminal sorting sequence influence membrane localization of Escherichia coli lipoproteins. J Bacteriol 174: 2095-2101.
29. Giladi, M., Champion, C.I., Haake, D.A., Blanco, D.R., Miller, J.F., Miller, J.N., and Lovett, M.A. (1993) Use of the 'blue halo' assay in the identification of genes encoding exported proteins with cleavable signal peptides: cloning of a Borrelia burgdorferi plasmid gene with a signal peptide. J Bacteriol 175: 4129-4136.
30. Hagman, K.E., Pan, W., Spratt, B.G., Balthazar, J.T., Judd, R.C., and Shafer, W.M. (1995) Resistance of Neisseria gonorrhoeae to antimicrobial hydrophobic agents is modulated by the mtrRCDE efflux system. Microbiology 141: 611-622.
31. Hagman, K.E., Lucas, C.E., Balthazar, JT., Snyder, L., Milles, M., Judd, R.C., and Shafer, W.M. (1997) The MtrD protein of Neisseria gonorrhoeae is a member of the resistance/nodulation/division protein family constituting part of an efflux system. Microbiology 143: 2117-2125.
32. Higgins, C.F., and Ames, G.F. (1981) Two periplasmic transport proteins which interact with a common membrane receptor show extensive homology: complete nucleotide sequences. Proc Natl Acad Sci USA 78: 6038-6042.
33. Hoffman, C.S., and Wright, A. (1985) Fusions of secreted proteins to alkaline phosphatase: an approach for studying protein secretion. Proc Natl Acad Sci USA 82: 5107-5111.
34. Holtje, J.V., and Tuomanen, E.I. (1991) The murein hydrolases of Escherichia coli: properties, functions and impact on the course of infections in vivo. J Gen Microbiol 137: 441-454.
35. Isberg, R.R., and Falkow, S. (1985) A single genetic locus encoded by Yersinia pseudotuberculosis permits invasion of cultured animal cells by Escherichia coli K-12. Nature 317: 262-264.
36. Isberg, R.R., and Leong, J.M. (1990) Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell 60: 861-871.
37. Isberg, R.R., Voorhis, D.L., and Falkow, S. (1987) Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell 50: 769-778.
38. Ito, H., Uchida, I., Sekizaki, T., and Terakado, N. (1993) A cryptic DNA sequence, isolated from Actinobacillus pleuropneumoniae, confers a hemolytic activity upon Escherichia coli K12 strains. J Vet Med Sci 55: 173-175.
39. Kier, L.D., Weppelman, R., and Ames, B.N. (1977) Regulation of two phosphatases and a cyclic phosphodiesterase of Salmonella typhimurium. J Bacteriol 130: 420-428.
40. Lee, E., and Manoil, C. (1994) Mutations eliminating the protein export function of a membrane-spanning sequence. J Biol Chem 269: 28822-28828.
41. Leong, J.M., Fournier, R.S., and Isberg, R.R. (1990) Identification of the integrin binding domain of the Yersinia pseudotuberculosis invasin protein. EMBO J 9: 1979-89.
42. Li, X.Z., Nikaido, H., and Poole, K. (1995) Role of mexA-mexB-oprM in antibiotic efflux in Pseudomonas aeruginosa. Antimicrob Agents Chemother 39: 1948-53.
43. Liu, J., and Beacham, I.R. (1990) Transcription and regulation of the cpdB gene in Escherichia coli K12 and Salmonella typhimurium LT2: evidence for modulation of constitutive promoters by cyclic AMP-CRP complex. Mol Gen Genet 222: 161-165.
44. Liu, J., Burns, D.M., and Beacham, I.R. (1986) Isolation and sequence analysis of the gene (cpdB) encoding periplasmic 2′, 3′-cyclic phosphodiesterase. J Bacteriol 165: 1002-1010.
45. Ma, D., Cook, D.N., Hearst, J.E., and Nikaido, H. (1994) Efflux pumps and drug resistance in gram-negative bacteria. Trends Microbiol 2: 489-493.
46. Maier, T.W., Zubrzycki, L., Coyle, M.B., Chila, M., and Warner, P. (1975) Genetic analysis of drug resistance in Neisseria gonorrhoeae: production of increased resistance by the combination of two antibiotic resistance loci. J Bacteriol 124: 834-842.
47. Maneewannakul, S., Maneewannakul, K., and Ippen-Ihler, K. (1991) Characterization of trbC, a new F plasmid tra operon gene that is essential to conjugative transfer. J Bacteriol 173: 3872-3878.
48. Maneewannakul, S., Maneewannakul, K., and Ippen-Ihler, K. (1992) Characterization, localization, and sequence of F transfer region products: the pilus assembly gene product TraW and a new product, Trbl. J Bacteriol 174: 5567-5574.
49. Manoil, C., and Beckwith, J. (1985) TnphoA: a transposon probe for protein export signals. Proc Natl Acad Sci USA 82: 8129-8133.
50. Manoil, C., and Beckwith, J. (1986) A genetic approach to analyzing membrane protein topology. Science 233: 1403-1408.
51. Melly, M.A., McGee, Z.A., and Rosenthal, R.S. (1984) Ability of monomeric peptidoglycan fragments from Neisseria gonorrhoeae to damage human fallopian-tube mucosa. J Infect Dis 149: 378-386.
52. Neidhardt, F.C. (1996) Esherichia coli and Salmonella: Cellular and Molecular Biology. Washington, DC: ASM.
53. Neu, H.C. (1968) The cyclic phosphodiesterases (3′-nucleotidases) of the enterobacteriaceae. Biochemistry 7: 3774-3780.
54. Nikaido, H. (1996) Multidrug efflux pumps of gram-negative bacteria. J Bacteriol 178: 5853-5859.
55. Okamoto, K., Baba, T., Yamanaka, H., Akashi, N., and Fujii, Y. (1995) Disulfide bond formation and secretion of Escherichia coli heat-stable enterotoxin II. J Bacteriol 177: 4579-4586.
56. Pan, W., and Spratt, B.G. (1994) Regulation of the permeability of the gonococcal cell envelope by the mtr system. Mol Microbiol 11: 769-775.
57. Paulsen, I.T., Brown, M.H., and Skurray, R.A. (1996) Proton-dependent multidrug efflux systems. Microbiol Rev 60: 575-608.
58. Pohlschroder, M., Prinz, W.A., Hartmann, E., and Beckwith, J. (1997) Protein translocation in the three domains of life: variations on a theme. Cell 91: 563-566.
59. Poole, K., Heinrichs, D.E., and Neshat, S. (1993a) Cloning and sequence analysis of an EnvCD homologue in Pseudomonas aeruginosa: regulation by iron and possible involvement in the secretion of the siderophore pyoverdine. Mol Microbiol 10: 529-544.
60. Poole, K., Krebes, K., McNally, C., and Neshat, S. (1993b) Multiple antibiotic resistance in Pseudomonas aeruginosa: evidence for involvement of an efflux operon. J Bacteriol 175: 7363-7372.
61. Pugsley, A.P. (1993) The complete general secretory pathway in gram-negative bacteria. Microbiol Rev 57: 50-108.
62. Rankin, S., Isberg, R.R., and Leong, J.M. (1992) The integrin-binding domain of invasin is sufficient to allow bacterial entry into mammalian cells. Infect Immun 60: 3909-3912.
63. Rodriguez-Pena, J.M., Alvarez, I., Ibanez, M., and Rotger, R. (1997) Homologous regions of the Salmonella enteritidis virulence plasmid and the chromosome of Salmonella typhi encode thiol: disulphide oxidoreductases belonging to the DsbA thioredoxin family. Microbiology 143: 1405-1413.
64. Santini, C.L., Ize, B., Chanal, A., Muller, M., Giordano, G., and Wu, L.F. (1998) A novel Sec-independent periplasmic protein translocation pathway in Escherichia coli. EMBO J 17: 101-112.
65. Shafer, W.M., Qu, X.-D., Waring, A.J., and Lehrer, R.I. (1998) Modulation of Neisseria gonorrhoeae susceptibility to vertebrate antibacterial peptides due to a member of the resistance/nodulation/division efflux pump family. Proc Natl Acad Sci USA 95: 1829-1833.
66. Smith, H., Bron, S., Van Ee, J., and Venema, G. (1987) Construction and use of signal sequence selection vectors in Escherichia coli and Bacillus subtilis. J Bacteriol 169: 3321-3328.
67. Stephens, C., and Shapiro, L. (1996) Delivering the payload. Bacterial pathogenesis. Curr Biol 6: 927-930.
68. Taddei, F., Matic, I., and Radman, M. (1995) cAMP-dependent SOS induction and mutagenesis in resting bacterial populations. Proc Natl Acad Sci USA 92: 11736-11740.
69. Takada, H., Tsujimoto, M., Kato, K., Kotani, S., Kusumoto, S., Inage, M., et al. (1979) Macrophage activation by bacterial cell walls and related synthetic compounds. Infect Immun 25: 48-53.
70. Taylor, R.K., Manoil, C., and Mekalanos, J.J. (1989) Broad-host-range vectors for delivery of TnphoA: use in genetic analysis of secreted virulence determinants of Vibrio cholerae. J Bacteriol 171: 1870-1878.
71. Thanassi, D.G., Cheng, L.W., and Nikaido, H. (1997) Active efflux of bile salts by Escherichia coli. J Bacteriol 179: 2512-2518.
72. Tomb, J.F., White, O., Kerlavage, A.R., Clayton, R.A., Sutton, G.G., Fleischmann, R.D., Ketchum, K.A. et al. (1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388: 539-547.
73. van der Velden, A.W., Baumler, A.J., Tsolis, R.M., and Heffron, F. (1998) Multiple fimbrial adhesins are required for full virulence of Salmonella typhimurium in mice. Infect Immun 66: 2803-2808.
74. Wang, R.F., and Kushner, S.R. (1991) Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100: 195-199.
75. Watarai, M., Tobe, T., Yoshikawa, M., and Sasakawa, C. (1995) Disulfide oxidoreductase activity of Shigella flexneri is required for release of Ipa proteins and invasion of epithelial cells. Proc Natl Acad Sci USA 92: 4927-4931.
76. Weiner, J.H., Bilous, P.T., Shaw, G.M., Lubitz, S.P., Frost, L., Thomas, G.H., et al. (1998) A Novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins. Cell 93: 93-101.
77. Yamaguchi, K., Yu, F., and Inouye, M. (1988) A single amino acid determinant of the membrane localization of lipoproteins in E. coli. Cell 53: 423-432.
78. Yamanaka, H., Kameyama, M., Baba, T., Fujii, Y., and Okamoto, K. (1994) Maturation pathway of Escherichia coli heat-stable enterotoxin I: requirement of DsbA for disulfide bond formation. J Bacteriol 176: 2906-2913.
79. Zhang, H.Z., and Donnenberg, M.S. (1996) DsbA is required for stability of the type IV pilin of enteropathogenic Escherichia coli. Mol Microbiol 21: 787-797.