Regulation of Vibrio anguillarum empA metalloprotease expression and its role in virulence

Applied and Environmental Microbiology

Volumn 70, Issue 7, 2004, Pages 4193-4204

  Denkin, Steven M ^a,b   Nelson, David R ^a  

^a UNIVERSITY OF RHODE ISLAND   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPLIFICATION; ATTENUATION; DATA ACQUISITION; GASTROENTEROLOGY; MUTAGENESIS; STRAIN;

ANAL INTUBATION; SUPERNATANTS;

MICROBIOLOGY;

ACYL HOMOSERINE LACTONE DERIVATIVE; LACTONE DERIVATIVE; METALLOPROTEINASE; PROTEINASE; UNCLASSIFIED DRUG;

MICROBIOLOGY;

ARTICLE; ATLANTIC SALMON; ATTENUATION; BACTERIAL GENE; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; EMPA GENE; GASTROINTESTINAL SECRETION; GENE EXPRESSION REGULATION; GENE LOCATION; INTUBATION; LISTONELLA ANGUILLARUM; MOLECULAR BIOLOGY; MUCUS; MUTATOR GENE; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE DIFFERENCE; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; RANDOM AMPLIFIED POLYMORPHIC DNA; RAPID AMPLIFICATION OF COMPLEMENTARY DNA ENDS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RPOS GENE; SITE DIRECTED MUTAGENESIS; SPECIES COMPARISON; TRANSLATION INITIATION; VIBRIO ANGUILLARUM M93SM; VIBRIO ANGUILLARUM NB10; WILD TYPE;

BACTERIAL PROTEINS; BASE SEQUENCE; BLOTTING, NORTHERN; CARBON-SULFUR LYASES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; METALLOENDOPEPTIDASES; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA; SIGMA FACTOR; TRANSCRIPTION, GENETIC; VIBRIO; VIRULENCE;

BACTERIA (MICROORGANISMS); LISTONELLA ANGUILLARUM; LURIA; NEGIBACTERIA; SALMO; SALMO SALAR; VIBRIO;

EID: 3242790338     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.70.7.4193-4204.2004     Document Type: Article

References (50)

1. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Andersen, J. B., A. Heydorn, M. Hentzer, L. Eberl, O. Geisenberger, B. B. Christensen, S. Molin, and M. Givskov. 2001. gfp-based N-acyl homoserinelactone sensor systems for detection of bacterial communication. Appl. Environ. Microbiol. 67:575-585.
3. Austin, B., and D. A. Austin. 1993. Bacterial fish pathogens: diseases in farmed and wild fish, 2nd ed. Ellis Horwood, Ltd., Chichester, United Kingdom.
4. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1987. Current protocols in molecular biology. Wiley, New York, N.Y.
5. Bassler, B. L., M. Wright, and M. R. Silverman. 1994. Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol. Microbiol. 13:273-286.
6. Benitez, J. A., A. J. Silva, and R. A. Finkelstein. 2001. Environmental signals controlling production of hemagglutinin/protease in Vibrio cholerae. Infect. Immun. 69:6549-6553.
7. Bever, R. A., and B. H. Iglewski. 1988. Molecular characterization and nucleotide sequence of the Pseudomonas aeruginosa elastase structural gene. J. Bacteriol. 170:4309-4314.
8. Bolinches, J., A. E. Toranzo, A. Silva, and J. L. Barja. 1986. Vibriosis as the main causative factor of heavy mortalities in the oyster culture industry in northwestern Spain. Bull. Eur. Assoc. Fish Pathol. 6:1-4.
9. Bordas, M. A., M. C. Balebona, J. M. Rodriguez-Maroto, J. J. Borrego, and M. A. Moriñigo. 1998. Chemotaxis of pathogenic Vibrio strains towards mucus surfaces of gilt-head sea bream (Sparus aurata L.). Appl. Environ. Microbiol. 64:1573-1575.
10. Bowser, P. R., R. Rosemark, and C. R. Reiner. 1981. A preliminary report of vibriosis in cultured American lobsters, Homarus americanus. J. Invertebr. Pathol. 37:80-85.
11. Chen, X., S. Schauder, N. Potier, A. Van Dorsselaer, I. Pelezer, B. L. Bassler, and F. M. Hughson. 2002. Structural identification of a bacterial quorumsensing signal containing boron. Nature 415:545-549.
12. Croxatto, A., V. J. Chalker, J. Lauritz, J. Jass, A. Hardman, P. Williams, M. Cámara, and D. L. Milton. 2002. VanT, a homologue of Vibrio harveyi LuxR, regulates serine, metalloprotease, pigment, and biofilm production in Vibrio anguillarum. J. Bacteriol. 184:1617-1629.
13. Denkin, S. M., and D. R. Nelson. 1999. Induction of protease activity in Vibrio anguillarum by gastrointestinal mucus. Appl. Environ. Microbiol. 65: 3555-3560.
14. Eberhard, A., A. L. Burlingame, C. Eberhard, G. L. Kenyon, K. H. Nealson, and N. J. Oppenheimer. 1981. Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20:2444-2449.
15. Garcia, T., K. Otto, S. Kjelleberg, and D. R. Nelson. 1997. Growth of Vibrio anguillarum in salmon intestinal mucus. Appl. Environ. Microbiol. 63:1034-1039.
16. Greenberg, E. P., J. W. Hastings, and S. Ulitzur. 1979. Induction of luciferase synthesis in Beneckea harveyi by other marine bacteria. Arch. Microbiol. 120:87-91.
17. Hengge-Aronis, R. 1993. The role of rpoS in early stationary-phase gene regulation in Escherichia coli K12, p. 171-200. In S. Kjelleberg (ed.), Starvation in bacteria, Plenum Press, New York, N.Y.
18. Holden, M. T., S. Ram Chhabra, R. de Nys, P. Stead, N. J. Bainton, P. J. Hill, M. Manefield, N. Kumar, M. Labatte, D. England, S. Rice, M. Givskov, G. P. Salmond, G. S. Stewart, B. W. Bycroft, S. Kjelleberg, and P. Williams. 1999. Quorum-sensing cross talk: isolation and chemical characterization of cyclic dipeptides from Pseudomonas aeruginosa and other gram-negative bacteria. Mol. Microbiol. 33:1254-1266.
19. Horne, M. T., R. H. Richards, R. J. Roberts, and P. C. Smith. 1977. Peracute vibriosis in juvenile turbot Scophthalmus maximus. J. Fish Pathol. 11:355-361.
20. Hülsmann, A., T. M. Rosche, I.-S. Kong, H. M. Hassan, D. M. Beam, and J. D. Oliver. 2003. RpoS-dependent stress response and exoenzyme production in Vibrio vulnificus. Appl. Environ. Microbiol. 69:6114-6120.
21. Jeong, H. S., M. H. Lee, K. H. Lee, S. J. Park, and S. H. Choi. 2003. SmcR and CRP coactivate Vibrio vulnificus vvpE encoding elastase through RpoS-dependent promoter in synergistic manner. J. Biol. Chem. 278:45072-45081.
22. Kovacikova, G., and K. Skorupski. 2000. Differential activation of the tcpPH promoter by AphB determines biotype specificity of virulence gene expression in Vibrio cholerae. J. Bacteriol. 182:3228-3238.
23. McFall-Ngai, M. J., and E. G. Ruby. 2000. Developmental biology in marine invertebrate symbioses. Curr, Opin. Microbiol. 3:603-607.
24. Milton, D. L., V. J. Chalker, D. Kirke, A. Hardman, M. Camara, and P. Williams. 2001, The LuxM homologue VanM from Vibrio anguillarum directs the synthesis of N-(3-hydroxyhexanoyl)homoserine lactone and N-hexanoylhomoserine lactone, J. Bacteriol. 183:3537-3547.
25. Milton, D. L., A. Hardman, M. Camara, S. R. Chhabra, B. W. Bycroft, G. S. A. B. Stewart, and P. Williams. 1997, Quorum sensing in Vibrio anguillarum: characterization of the vanI/vanR locus and identification of the autoinducer N-(3-oxodecanoyl)-L-homoserine lactone. J. Bacteriol. 179: 3004-3012.
26. Milton, D. L., A. Norqvist, and H. Wolf-Watz. 1992. Cloning of a metalloprotease gene involved in the virulence mechanism of Vibrio anguillarum. J. Bacteriol. 174:7235-7244.
27. Milton, D. L., A. Norqvist, and H. Wolf-Watz. 1995. Sequence of a novel virulence-mediating gene, virC, from Vibrio anguillarum. Gene 164:95-100.
28. Milton, D. L., R. O'Toole, P. Hörstedt, and H. Wolf-Watz. 1996. Flagellin A is essential for the virulence of Vibrio anguillarum. J. Bacteriol. 178:1310-1319.
29. Miyoshi, S.-I., H. Nakazawa, K. Kawata, K.-I. Tomochika, K. Tobe, and S. Shinoda. 1998. Characterization of the hemorrhagic reaction caused by Vibrio vulnificus metalloprotease, a member of the thermolysin family. Infect. Immun. 66:4851-4855.
30. Munn, C. B. 1977. Vibriosis in fish and its control. Fish Manag. 8:11-15.
31. Murley, Y. M., P. A. Carroll, K. Skorupski, R. K. Taylor, and S. B. Calderwood. 1999. Differential transcription of the tcpPH operon confers biotype-specific control of the Vibrio cholerae ToxR virulence regulon. Infect. Immun. 67:5117-5123.
32. Nealson, K. H., T. Platt, and J. W. Hastings. 1970. Cellular control of the synthesis and activity of the bacterial luminescent system. J. Bacteriol. 104: 313-322.
33. Nicas, T. I., and B. H. Iglewski. 1985. The contribution of exoproducts to virulence of Pseudomonas aeruginosa. Can. J. Microbiol. 31:387-392.
34. Olsson, J. C., A. Jobörn, A. Westerdahl, L. Blomberg, S. Kjelleberg, and P. L. Conway. 1996. Is the turbot, Sophthalmus maximus (L.), intestine a portal of entry for the fish pathogen Vibrio anguillarum? J. Fish Dis. 19:225-234.
35. Passador, L., J. M. Cook, M. J. Gambello, L. Rust, and B. H. Iglewski. 1993. Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science 260:1127-1130.
36. Ransom, D. P. 1978. Bacteriologic, immunologic and pathologic studies of Vibrio sp. pathogenic to salmonids. Ph.D. thesis. Oregon State University, Corvallis,
37. Ransom, D. P., C. N. Lannan, J. S. Rohovecm, and J. L. Fryer. 1984, Comparison of histopathology caused by Vibrio anguillarum and Vibrio ordalii in three species of Pacific salmon. J. Fish Dis. 7:107-115.
38. Ruby, E. G., and K. H. Nealson. 1976. Symbiotic association of Photobacterium fischeri with the marine luminous fish Monocentris japonica: a model of symbiosis based on bacterial studies. Biol. Bull. 151:574-586,
39. Schaefer, A. L., D. L. Val, B. L. Hanzelka, J. E. Cronan, Jr., and E. P. Greenberg. 1996. Generation of cell-to-cell signals in quorum sensing: acyl homoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein. Proc. Natl. Acad. Sci. USA 93:9505-9509.
40. Schauder, S., K. Shokat, M. G. Surette, and B. L. Bassler. 2001. The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol, Microbiol. 41:463-476.
41. Sperandio, V., A. G. Torres, J. A. Girón, and J. B. Kaper. 2001. Quorum sensing is a global regulatory mechanism in enterohemorrhagic Escherichia coli O157:H7. J. Bacteriol. 183:5187-5197.
42. Sperandio, V., A. G. Torres, B. Jarvis, J. P. Nataro, and J. B. Kaper. 2003, Bacteria-host communication: the language of hormones. Proc, Natl, Acad. Sci. USA 100:8951-8956.
43. Surette, M. G., and B. L. Bassler. 1998. Quorum sensing in Escherichia coli and Salmonella typhimurium. Proc. Natl, Acad. Sci. USA 95:7046-7050.
44. Vaantanen, P. 1976, Microbiological studies in coastal waters of the northern Baltic Sea. I. Distribution and abundance of bacteria and yeasts in the Tvarminne area. Walter Ander Nottbeck Found. Sci. Rep. 1:1-58.
45. Windle, H. J. P., and D. Kelleher. 1997. Identification and characterization of a metalloprotease activity from Helicobacter pylori. Infect. Immun. 65: 3132-3137.
46. Winson, M. K., M. Camara, A. Latifi, M. Foglino, S. R. Chhabra, M. Daykin, M. Bally, V. Chapon, G. P. Salmond, B. W. Bycroft et al. 1995. Multiple N-acyl-L-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 92:9427-9431.
47. Winson, M. K., S. Swift, L. Fish, J. P. Throup, F. Jorgensen, S. R. Chhabra, B. W. Bycroft, P. Williams, and G. S. Stewart. 1998. Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol. Lett. 163:185-192.
48. Winzer, K., K. R. Hardie, N. Burgess, N. Doherty, D. Kirke, M. T. Holden, R. Linforth, K. A. Cornell, A. J. Taylor, P. J. Hill, and P. Williams. 2002. LuxS: its role in central metabolism and the in vitro synthesis of 4-hydroxy-5-methyl-3(2H)-furanone. Microbiology 148:909-922.
49. Woods, D. E., S. J. Cryz, R. L. Friedman, and B. H. Iglewski. 1982. Contribution of toxin A and elastase to virulence of Pseudomonas aeruginosa in chronic lung infections of rats. Infect. Immun. 36:1223-1228.
50. 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. (First published 19 February 2002; 10.1073/pnas.052694299.)