Pathoadaptive conditional regulation of the type VI secretion system in vibrio cholerae O1 strains

Infection and Immunity

Volumn 80, Issue 2, 2012, Pages 575-584

  Ishikawa, Takahiko ^a   Sabharwal, Dharmesh ^a   Bröms, Jeanette ^a   Milton, Debra L ^a   Sjöstedt, Anders ^a   Uhlin, Bernt Eric ^a   Wai, Sun Nyunt ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; ESCHERICHIA COLI; GENE EXPRESSION; LOW TEMPERATURE; NONHUMAN; OSMOLARITY; OSMOREGULATION; PHOTOACCLIMATIZATION; PRIORITY JOURNAL; SURVIVAL; TYPE VI SECRETION SYSTEM; VIBRIO CHOLERAE; WILD TYPE;

BACTERIAL PROTEINS; BACTERIOLOGICAL TECHNIQUES; ENVIRONMENT; ESCHERICHIA COLI K12; GENE EXPRESSION REGULATION, BACTERIAL; OSMOLAR CONCENTRATION; PLASMIDS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SECRETORY PATHWAY; TEMPERATURE; VIBRIO CHOLERAE; VIRULENCE;

EID: 84857163366     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05510-11     Document Type: Article

References (57)

1. Aspedon A, Palmer K, Whiteley M. 2006. Microarray analysis of the osmotic stress response in Pseudomonas aeruginosa. J. Bacteriol. 188: 2721-2725.
2. Balsalobre C, et al. 2006. Release of the type I secreted alpha-haemolysin via outer membrane vesicles from Escherichia coli. Mol. Microbiol. 59:99-112.
3. Bernard CS, Brunet YR, Gueguen E, Cascales E. 2010. Nooks and crannies in type VI secretion regulation. J. Bacteriol. 192:3850-3860.
4. Bingle LE, Bailey CM, Pallen MJ. 2008. Type VI secretion: a beginner's guide. Curr. Opin. Microbiol. 11:3-8.
5. Bleves S, et al. 2010. Protein secretion systems in Pseudomonas aeruginosa: a wealth of pathogenic weapons. Int. J. Med. Microbiol. 300:534-543.
6. Bolivar F, et al. 1977. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene 2:95-113.
7. Casadaban MJ. 1976. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J. Mol. Biol. 104:541-555.
8. Colwell RR, Kaper J, Joseph SW. 1977. Vibrio cholerae, Vibrio parahaemolyticus, and other vibrios: occurrence and distribution in Chesapeake Bay. Science 198:394-396.
9. Constantin de Magny G, et al. 2009. Predicting the distribution of Vibrio spp. in the Chesapeake Bay: a Vibrio cholerae case study. EcoHealth 6:378-389.
10. Das S, Chaudhuri K. 2003. Identification of a unique IAHP (IcmF associated homologous proteins) cluster in Vibrio cholerae and other proteobacteria through in silico analysis. In Silico Biol. 3:287-300.
11. Donnenberg MS, Kaper JB. 1991. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect. Immun. 59:4310-4317.
12. Faruque SM, Nair GB. 2002. Molecular ecology of toxigenic Vibrio cholerae. Microbiol. Immunol. 46:59-66.
13. Filloux A, Hachani A, Bleves S. 2008. The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology 154:1570-1583.
14. Furste JP, et al. 1986. Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector. Gene 48:119-131.
15. Guzman LM, Belin D, Carson MJ, Beckwith J. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177:4121-4130.
16. Hachani A, et al. 2011. Type VI secretion system in Pseudomonas aeruginosa: secretion and multimerization of VgrG proteins. J. Biol. Chem. 286: 12317-12327.
17. Han Y, et al. 2004. Microarray analysis of temperature-induced transcriptome of Yersinia pestis. Microbiol. Immunol. 48:791-805.
18. Hanahan D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
19. Hood RD, et al. 2010. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7:25-37.
20. Ishikawa T, Rompikuntal PK, Lindmark B, Milton DL, Wai SN. 2009. Quorum sensing regulation of the two hcp alleles in Vibrio cholerae O1 strains. PLoS One 4:e6734.
21. Jubelin G, et al. 2005. CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J. Bacteriol. 187:2038-2049.
22. Kaper JB, Morris JG Jr, Levine MM. 1995. Cholera. Clin. Microbiol. Rev. 8:48-86.
23. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
24. MacIntyre DL, Miyata ST, Kitaoka M, Pukatzki S. 2010. The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proc. Natl. Acad. Sci. U. S. A. 107:19520-19524.
25. Mildiner-Earley S, Walker KA, Miller VL. 2007. Environmental stimuli affecting expression of the Ysa type three secretion locus. Adv. Exp. Med. Biol. 603:211-216.
26. Miller VL, DiRita VJ, Mekalanos JJ. 1989. Identification of toxS, a regulatory gene whose product enhances toxR-mediated activation of the cholera toxin promoter. J. Bacteriol. 171:1288-1293.
27. Miller VL, Mekalanos JJ. 1988. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170:2575-2583.
28. Miller VL, Taylor RK, Mekalanos JJ. 1987. Cholera toxin transcriptional activator toxR is a transmembraneDNAbinding protein. Cell 48:271-279.
29. Molina-Henares AJ, Krell T, Eugenia Guazzaroni M, Segura A, Ramos JL. 2006. Members of the IclR family of bacterial transcriptional regulators function as activators and/or repressors. FEMS Microbiol. Rev. 30:157-186.
30. Motin VL, et al. 2004. Temporal global changes in gene expression during temperature transition in Yersinia pestis. J. Bacteriol. 186:6298-6305.
31. Mougous JD, et al. 2006. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312:1526-1530.
32. Mougous JD, Gifford CA, Ramsdell TL, Mekalanos JJ. 2007. Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa. Nat. Cell Biol. 9:797-803.
33. Oscarsson J, et al. 2002. Characterization of a pore-forming cytotoxin expressed by Salmonella enterica serovars Typhi and Paratyphi A. Infect. Immun. 70:5759-5769.
34. Pieper R, et al. 2009. Temperature and growth phase influence the outermembrane proteome and the expression of a type VI secretion system in Yersinia pestis. Microbiology 155:498-512.
35. Pratt LA, Hsing W, Gibson KE, Silhavy TJ. 1996. From acids to osmZ: multiple factors influence synthesis of the OmpF and OmpC porins in Escherichia coli. Mol. Microbiol. 20:911-917.
36. Pukatzki S, Ma AT, Revel AT, Sturtevant D, Mekalanos JJ. 2007. Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc. Natl. Acad. Sci. U. S. A. 104:15508-15513.
37. Pukatzki S, et al. 2006. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc. Natl. Acad. Sci. U. S. A. 103:1528-1533.
38. Ramamurthy T, Yamasaki S, Takeda Y, Nair GB. 2003. Vibrio cholerae O139 Bengal: odyssey of a fortuitous variant. Microbes Infect. 5:329-344.
39. Rawlings TK, Ruiz GM, Colwell RR. 2007. Association of Vibrio cholera O1 El Tor and O139 Bengal with the Copepods Acartia tonsa and Eurytemora affinis. Appl. Environ. Microbiol. 73:7926-7933.
40. Reidl J, Klose KE. 2002. Vibrio cholerae and cholera: out of the water and into the host. FEMS Microbiol. Rev. 26:125-139.
41. Robinson JB, et al. 2009. Evaluation of a Yersinia pestis mutant impaired in a thermoregulated type VI-like secretion system in flea, macrophage and murine models. Microb. Pathog. 47:243-251.
42. Sack DA, Sack RB, Nair GB, Siddique AK. 2004. Cholera. Lancet 363: 223-233.
43. Schwarz S, Hood RD, Mougous JD. 2010. What is type VI secretion doing in all those bugs? Trends Microbiol. 18:531-537.
44. Schwarz S, et al. 2010. Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog. 6:e1001068.
45. Shikuma NJ, Yildiz FH. 2009. Identification and characterization of OscR, a transcriptional regulator involved in osmolarity adaptation in Vibrio cholerae. J. Bacteriol. 191:4082-4096.
46. Shimada T, Sakazaki R. 1988. A serogroup of non-O1 Vibrio cholerae possessing the Inaba antigen of Vibrio cholerae O1. J. Appl. Bacteriol. 64:141-144.
47. Shrivastava S, Mande SS. 2008. Identification and functional characterization of gene components of type VI secretion system in bacterial genomes. PLoS One 3:e2955.
48. Singleton FL, Attwell R, Jangi S, Colwell RR. 1982. Effects of temperature and salinity on Vibrio cholerae growth. Appl. Environ. Microbiol. 44:1047-1058.
49. Song T, et al. 2008. A new Vibrio cholerae sRNA modulates colonization and affects release of outer membrane vesicles. Mol. Microbiol. 70:100-111.
50. Tow LA, Coyne VE. 1999. Cloning and characterisation of a novel ompB operon from Vibrio cholerae 569B. Biochim. Biophys. Acta 1444: 269-275.
51. Towbin H, Staehelin T, Gordon J. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U. S. A. 76:4350-4354.
52. Vaitkevicius K, et al. 2006. A Vibrio cholerae protease needed for killing of Caenorhabditis elegans has a role in protection from natural predator grazing. Proc. Natl. Acad. Sci. U. S. A. 103:9280-9285.
53. Valeru SP, et al. 2009. Role of melanin pigment in expression of Vibrio cholerae virulence factors. Infect. Immun. 77:935-942.
54. Walker KA, Miller VL. 2004. Regulation of the Ysa type III secretion system of Yersinia enterocolitica by YsaE/SycB and YsrS/YsrR. J. Bacteriol. 186:4056-4066.
55. Yildiz FH, Schoolnik GK. 1998. Role of rpoS in stress survival and virulence of Vibrio cholerae. J. Bacteriol. 180:773-784.
56. Zheng J, Shin OS, Cameron DE, Mekalanos JJ. 2010. Quorum sensing and a global regulator TsrA control expression of type VI secretion and virulence in Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A. 107:21128-21133.
57. Zinnaka Y, Carpenter CC Jr. 1972. An enterotoxin produced by noncholera vibrios. Johns Hopkins Med. J. 131:403-411.