Levels of the secreted Vibrio cholerae attachment factor GbpA are modulated by quorum-sensing-induced proteolysis

Journal of Bacteriology

Volumn 191, Issue 22, 2009, Pages 6911-6917

  Jude, Brooke A ^a,b   Martinez, Raquel M ^a   Skorupski, Karen ^a   Taylor, Ronald K ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b BARD COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; BACTERIAL PROTEIN; GLCNAC BINDING PROTEIN A; HAPA ENZYME; PROTEIN HAPR; PRTV ENZYME; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; CELL DENSITY; CONTROLLED STUDY; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; QUORUM SENSING; VIBRIO CHOLERAE; VIRULENCE;

BACTERIAL PROTEINS; BLOTTING, WESTERN; GENE EXPRESSION REGULATION, BACTERIAL; METALLOENDOPEPTIDASES; MUTATION; PEPTIDE HYDROLASES; QUORUM SENSING; VIBRIO CHOLERAE;

BACTERIA (MICROORGANISMS); VIBRIO CHOLERAE;

EID: 70350468864     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00747-09     Document Type: Article

References (48)

1. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1987. Current protocols in molecular biology. Greene Publishing Associates and J. Wiley, New York, NY.
2. Benitez, J. A., R. G. Spelbrink, A. Silva, T. E. Phillips, C. M. Stanley, M. Boesman-Finkelstein, and R. A. Finkelstein. 1997. Adherence of Vibrio cholerae to cultured differentiated human intestinal cells: an in vitro colonization model. Infect. Immun. 65:3474-3477.
3. Bjork, S., M. E. Breimer, G. C. Hansson, K. A. Karlsson, and H. Leffler. 1987. Structures of blood group glycosphingolipids of human small intestine. A relation between the expression of fucolipids of epithelial cells and the ABO, Le and Se phenotype of the donor. J. Biol. Chem. 262:6758-6765.
4. Booth, B. A., M. Boesman-Finkelstein, and R. A. Finkelstein. 1983. Vibrio cholerae soluble hemagglutinin/protease is a metalloenzyme. Infect. Immun. 42:639-644.
5. Booth, B. A., M. Boesman-Finkelstein, and R. A. Finkelstein. 1984. Vibrio cholerae hemagglutinin/protease nicks cholera enterotoxin. Infect. Immun. 45:558-560.
6. Burnet, F. M. 1948. The mucinase of V. cholerae. Aust. J. Exp. Biol. Med. Sci. 26:71-80.
7. Castro-Rosas, J., and E. F. Escartin. 2002. Adhesion and colonization of Vibrio cholerae O1 on shrimp and crab carapaces. J. Food Prot. 65:492-498.
8. Chowdhury, M. A., A. Huq, B. Xu, F. J. Madeira, and R. R. Colwell. 1997. Effect of alum on free-living and copepod-associated Vibrio cholerae O1 and O139. Appl. Environ. Microbiol. 63:3323-3326.
9. Colwell, R. R., A. Huq, M. S. Islam, K. M. Aziz, M. Yunus, N. H. Khan, A. Mahmud, R. B. Sack, G. B. Nair, J. Chakraborty, D. A. Sack, and E. Russek-Cohen. 2003. Reduction of cholera in Bangladeshi villages by simple filtration. Proc. Natl. Acad. Sci. USA 100:1051-1055.
10. Colwell, R. R., J. Kaper, and S. W. Joseph. 1977. Vibrio cholerae, Vibrio parahaemolyticus, and other vibrios: occurrence and distribution in Chesapeake Bay. Science 198:394-396.
11. Colwell, R. R., and W. M. Spira. 1992. The ecology of Vibrio cholerae, p. 107-127. In Barua, D., and I. I. I. W. B. Greenough (ed.), Cholera. Plenum Medical Book Co, New York, NY.
12. Connell, T. D., D. J. Metzger, J. Lynch, and J. P. Folster. 1998. Endochitinase is transported to the extracellular milieu by the eps-encoded general secretory pathway of Vibrio cholerae. J. Bacteriol. 180:5591-5600.
13. de Lorenzo, V., and K. N. Timmis. 1994. Analysis and construction of stable phenotypes in gram-negative bacteria with Tn5- and Tn10-derived minitransposons. Methods Enzymol. 235:386-405.
14. Finkelstein, R. A., M. Boesman-Finkelstein, Y. Chang, and C. C. Hase. 1992. Vibrio cholerae hemagglutinin/protease, colonial variation, virulence, and detachment. Infect. Immun. 60:472-478.
15. Finkelstein, R. A., M. Boesman-Finkelstein, and P. Holt. 1983. Vibrio cholerae hemagglutinin/lectin/protease hydrolyzes fibronectin and ovomucin: F.M. Burnet revisited. Proc. Natl. Acad. Sci. USA 80:1092-1095.
16. Finne, J., M. E. Breimer, G. C. Hansson, K. A. Karlsson, H. Leffler, J. F. Vliegenthart, and H. van Halbeek. 1989. Novel polyfucosylated N-linked glycopeptides with blood group A, H, X, and Y determinants from human small intestinal epithelial cells. J. Biol. Chem. 264:5720-5735.
17. Hammer, B. K., and B. L. Bassler. 2003. Quorum sensing controls biofilm formation in Vibrio cholerae. Mol. Microbiol. 50:101-104.
18. Heidelberg, J. F., J. A. Eisen, W. C. Nelson, R. A. Clayton, M. L. Gwinn, R. J. Dodson, D. H. Haft, E. K. Hickey, J. D. Peterson, L. Umayam, S. R. Gill, K. E. Nelson, T. D. Read, H. Tettelin, D. Richardson, M. D. Ermolaeva, J. Vamathevan, S. Bass, H. Qin, I. Dragoi, P. Sellers, L. McDonald, T. Utterback, R. D. Fleishmann, W. C. Nierman, O. White, S. L. Salzberg, H. O. Smith, R. R. Colwell, J. J. Mekalanos, J. C. Venter, and C. M. Fraser. 2000. DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406:477-483.
19. Huq, A., E. B. Small, P. A. West, M. I. Huq, R. Rahman, and R. R. Colwell. 1983. Ecological relationships between Vibrio cholerae and planktonic crustacean copepods. Appl. Environ. Microbiol. 45:275-283.
20. Huq, A., P. A. West, E. B. Small, M. I. Huq, and R. R. Colwell. 1984. Influence of water temperature, salinity, and pH on survival and growth of toxigenic Vibrio cholerae serovar O1 associated with live copepods in laboratory microcosms. Appl. Environ. Microbiol. 48:420-424.
21. Islam, M. S., B. S. Drasar, and D. J. Bradley. 1989. Attachment of toxigenic Vibrio cholerae 01 to various freshwater plants and survival with a filamentous green alga, Rhizoclonium fontanum. J. Trop. Med. Hyg. 92:396-401.
22. Islam, M. S., B. S. Drasar, and D. J. Bradley. 1990. Long-term persistence of toxigenic Vibrio cholerae 01 in the mucilaginous sheath of a blue-green alga, Anabaena variabilis. J. Trop. Med. Hyg. 93:133-139.
23. Jobling, M. G., and R. K. Holmes. 1997. Characterization of hapR, a positive regulator of the Vibrio cholerae HA/protease gene hap, and its identification as a functional homologue of the Vibrio harveyi luxR gene. Mol. Microbiol. 26:1023-1034.
24. Joelsson, A., Z. Liu, and J. Zhu. 2006. Genetic and phenotypic diversity of quorum-sensing systems in clinical and environmental isolates of Vibrio cholerae. Infect. Immun. 74:1141-1147. (Pubitemid 43185552)
25. Kierek, K., and P. I. Watnick. 2003. Environmental determinants of Vibrio cholerae biofilm development. Appl. Environ. Microbiol. 69:5079-5088.
26. Kirn, T. J., B. A. Jude, and R. K. Taylor. 2005. A colonization factor links Vibrio cholerae environmental survival and human infection. Nature 438:863-866.
27. Kirn, T. J., M. J. Lafferty, C. M. Sandoe, and R. K. Taylor. 2000. Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae. Mol. Microbiol. 35:896-910.
28. Kovacikova, G., W. Lin, and K. Skorupski. 2003. The virulence activator AphA links quorum sensing to pathogenesis and physiology in Vibrio cholerae by repressing the expression of a penicillin amidase gene on the small chromosome. J. Bacteriol. 185:4825-4836.
29. Kovacikova, G., and K. Skorupski. 2002. Regulation of virulence gene expression in Vibrio cholerae by quorum sensing: HapR functions at the aphA promoter. Mol. Microbiol. 46:1135-1147. (Pubitemid 35370599)
30. Lenz, D. H., K. C. Mok, B. N. Lilley, R. V. Kulkarni, N. S. Wingreen, and B. L. Bassler. 2004. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118:69-82.
31. Lin, W., G. Kovacikova, and K. Skorupski. 2005. Requirements for Vibrio cholerae HapR binding and transcriptional repression at the hapR promoter are distinct from those at the aphA promoter. J. Bacteriol. 187:3013-3019. (Pubitemid 40571593)
32. Matz, C., D. McDougald, A. M. Moreno, P. Y. Yung, F. H. Yildiz, and S. Kjelleberg. 2005. Biofilm formation and phenotypic variation enhance predation-driven persistence of Vibrio cholerae. Proc. Natl. Acad. Sci. USA 102:16819-16824. (Pubitemid 41688860)
33. Meibom, K. L., X. B. Li, A. T. Nielsen, C. Y. Wu, S. Roseman, and G. K. Schoolnik. 2004. The Vibrio cholerae chitin utilization program. Proc. Natl. Acad. Sci. USA 101:2524-2529.
34. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, NY.
35. Miller, M. B., K. Skorupski, D. H. Lenz, R. K. Taylor, and B. L. Bassler. 2002. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110:303-314.
36. Moorthy, S., and P. I. Watnick. 2005. Identification of novel stage-specific genetic requirements through whole genome transcription profiling of Vibrio cholerae biofilm development. Mol. Microbiol. 57:1623-1635.
37. Richardson, K., and C. D. Parker. 1985. Identification and occurrence of Vibrio cholerae flagellar core proteins in isolated outer membrane. Infect. Immun. 47:674-679.
38. Robert, A., A. Silva, J. A. Benitez, B. L. Rodriguez, R. Fando, J. Campos, D. K. Sengupta, M. Boesman-Finkelstein, and R. A. Finkelstein. 1996. Tagging a Vibrio cholerae El Tor candidate vaccine strain by disruption of its hemagglutinin/protease gene using a novel reporter enzyme: Clostridium thermocellum endoglucanase A. Vaccine 14:1517-1522.
39. Sack, D. A., R. B. Sack, G. B. Nair, and A. K. Siddique. 2004. Cholera. Lancet. 363:223-233.
40. Scott, M. E., Z. Y. Dossani, and M. Sandkvist. 2001. Directed polar secretion of protease from single cells of Vibrio cholerae via the type II secretion pathway. Proc. Natl. Acad. Sci. USA 98:13978-13983.
41. Skorupski, K., and R. K. Taylor. 1996. Positive selection vectors for allelic exchange. Gene 169:47-52. (Pubitemid 26075696)
42. Tamplin, M. L., A. L. Gauzens, A. Huq, D. A. Sack, and R. R. Colwell. 1990. Attachment of Vibrio cholerae serogroup O1 to zooplankton and phytoplankton of Bangladesh waters. Appl. Environ. Microbiol. 56:1977-1980.
43. Taylor, R. K., V. L. Miller, D. B. Furlong, and J. J. Mekalanos. 1987. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. Proc. Natl. Acad. Sci. USA 84:2833-2837.
44. Thelin, K. H., and R. K. Taylor. 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.
45. Vaitkevicius, K., B. Lindmark, G. Ou, T. Song, C. Toma, M. Iwanaga, J. Zhu, A. Andersson, M. L. Hammarstrom, S. Tuck, and S. N. Wai. 2006. A Vibrio cholerae protease needed for killing of Caenorhabditis elegans has a role in protection from natural predator grazing. Proc. Natl. Acad. Sci. USA 103:9280-9285.
46. Yildiz, F. H., X. S. Liu, A. Heydorn, and G. K. Schoolnik. 2004. Molecular analysis of rugosity in a Vibrio cholerae O1 El Tor phase variant. Mol. Microbiol. 53:497-515.
47. Zhu, J., and J. J. Mekalanos. 2003. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev. Cell 5:647-656. (Pubitemid 37243052)
48. Zhu, J., M. B. Miller, R. E. Vance, M. Dziejman, B. L. Bassler, and J. J. Mekalanos. 2002. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 99:3129-3134.