The vibrio cholerae trh gene is coordinately regulated in vitro with type iii secretion system genes by VttrA/VttrB but does not contribute to caco2-bbe cell cytotoxicity

Infection and Immunity

Volumn 80, Issue 12, 2012, Pages 4444-4455

  Miller, Kelly A ^a   Hamilton, Elaine ^a   Dziejman, Michelle ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR VTTRA; TRANSCRIPTION FACTOR VTTRB; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; CONTROLLED STUDY; CYTOTOXICITY; GENE EXPRESSION REGULATION; GENE FUSION; GENE OVEREXPRESSION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; TYPE III SECRETION SYSTEM; VIBRIO CHOLERAE;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, NEWBORN; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CACO-2 CELLS; CHOLERA; GENE EXPRESSION REGULATION, BACTERIAL; HEMOLYSIN PROTEINS; HUMANS; MICE; MOLECULAR SEQUENCE DATA; VIBRIO CHOLERAE; VIRULENCE FACTORS;

EID: 84870789928     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00832-12     Document Type: Article

References (72)

1. Alam A, Miller KA, Chaand M, Butler JS, Dziejman M. 2011. Identification of Vibrio cholerae type III secretion system effector proteins. Infect. Immun. 79:1728-1740.
2. B encode ToxR family proteins that mediate bile-induced expression of type three secretion system genes in a non-O1/non-O139 Vibrio cholerae strain. Infect. Immun. 78:2554-2570.
3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
4. Baba K, Yamasaki S, Nishibuchi M, Takeda Y. 1992. Examination by site-directed mutagenesis of the amino acid residues of the thermostable direct hemolysin of Vibrio parahaemolyticus required for its hemolytic activity. Microb. Pathog. 12:279-287.
5. Bagchi K, et al. 1993. Epidemic of diarrhea caused by Vibrio cholerae non-O1 that produced heat-stable toxin among Khmers in a camp in Thailand. J. Clin. Microbiol. 31:1315-1317.
6. Broberg CA, Calder TJ, Orth K. 2011. Vibrio parahaemolyticus cell biology and pathogenicity determinants. Microbes Infect. 13:992-1001.
7. Brutinel ED, Yahr TL. 2008. Control of gene expression by type III secretory activity. Curr. Opin. Microbiol. 11:128-133.
8. Butler SM, Camilli A. 2005. Going against the grain: chemotaxis and infection in Vibrio cholerae. Nat. Rev. Microbiol. 3:611-620.
9. Charles RC, Ryan ET. 2011. Cholera in the 21st century. Curr. Opin. Infect. Dis. 24:472-477.
10. Chatterjee SN, Chaudhuri K. 2003. Lipopolysaccharides of Vibrio cholerae. I. Physical and chemical characterization. Biochim. Biophys. Acta 1639:65-79.
11. Chen Y, et al. 2011. Comparative genomic analysis of Vibrio parahaemolyticus:serotype conversion and virulence. BMC Genomics 12:294. doi:10.1186/1471-2164-12-994.
12. Chowdhury F, et al. 2011. Impact of rapid urbanization on the rates of infection by Vibrio cholerae O1 and enterotoxigenic Escherichia coli in Dhaka, Bangladesh. PLoS Negl. Trop. Dis. 5:e999. doi:10.1371/journal.pone.
13. Chun J, et al. 2009. Comparative genomics reveals mechanism for shortterm and long-term clonal transitions in pandemic Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A. 106:15442-15447.
14. Colwell RR. 2004. Infectious disease and environment: cholera as a paradigm for waterborne disease. Int. Microbiol. 7:285-289.
15. Dalsgaard A, et al. 1995. Characterization of Vibrio cholerae non-O1 serogroups obtained from an outbreak of diarrhea in Lima, Peru. J. Clin. Microbiol. 33:2715-2722.
16. Dalsgaard A, et al. 1999. A high proportion of Vibrio cholerae strains isolated from children with diarrhoea in Bangkok, Thailand are multiple antibiotic resistant and belong to heterogenous non-O1, non-O139 Oserotypes. Epidemiol. Infect. 122:217-226.
17. Dalsgaard A, Forslund A, Mortensen HF, Shimada T. 1998. Ribotypes of clinical Vibrio cholerae non-O1 non-O139 strains in relation to Oserotypes. Epidemiol. Infect. 121:535-545.
18. Dalsgaard A, et al. 1997. Molecular evolution of Vibrio cholerae O1 strains isolated in Lima, Peru, from 1991 to 1995. J. Clin. Microbiol. 35:1151-1156.
19. 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.
20. Dziejman M, et al. 2005. Genomic characterization of non-O1, non-O139 Vibrio cholerae reveals genes for a type III secretion system. Proc. Natl. Acad. Sci. U. S. A. 102:3465-3470.
21. Fabbri A, et al. 1999. Vibrio parahaemolyticus thermostable direct hemolysin modulates cytoskeletal organization and calcium homeostasis in intestinal cultured cells. Infect. Immun. 67:1139-1148.
22. Faruque SM, Albert MJ, Mekalanos JJ. 1998. Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae. Microbiol. Mol. Biol. Rev. 62:1301-1314.
23. Faruque SM, et al. 2004. Genetic diversity and virulence potential of environmental Vibrio cholerae population in a cholera-endemic area. Proc. Natl. Acad. Sci. U. S. A. 101:2123-2128.
24. Faruque SM, Mekalanos JJ. 2003. Pathogenicity islands and phages in Vibrio cholerae evolution. Trends Microbiol. 11:505-510.
25. Feng L, et al. 2008. A recalibrated molecular clock and independent origins for the cholera pandemic clones. PLoS One 3:e4053. doi:10.1371/journal.pone.0004053.
26. Fullner KJ, Mekalanos JJ. 2000. In vivo covalent cross-linking of cellular actin by the Vibrio cholerae RTX toxin. EMBO J. 19:5315-5323.
27. Galan JE, Wolf-Watz H. 2006. Protein delivery into eukaryotic cells by type III secretion machines. Nature 444:567-573.
28. Gardel C, Mekalanos JJ. 1996. Alterations in Vibrio cholerae motility phenotypes correlate with changes in virulence factor expression. J. Bacteriol.64:2246-2255.
29. Gotoh K, et al. 2010. Bile acid-induced virulence gene expression of Vibrio parahaemolyticus reveals a novel therapeutic potential for bile acid sequestrants. PLoS One 5:e13365. doi:10.1371/journal.pone.0013365.
30. 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.
31. 31. Hiyoshi H, Kodama T, Iida T, Honda T. 2010. Contribution of Vibrio parahaemolyticus virulence factors to cytotoxicity, enterotoxicity, and lethality in mice. Infect. Immun. 78:1772-1780.
32. Honda T, et al. 1989. A mutant hemolysin with lower biological activity produced by a mutant Vibrio parahaemolyticus. FEMS Microbiol. Lett.52:95-100.
33. Honda T, Ni YX, Miwatani T. 1988. Purification and characterization of a hemolysin produced by a clinical isolate of Kanagawa phenomenonnegative Vibrio parahaemolyticus and related to the thermostable direct hemolysin. Infect. Immun. 56:961-965.
34. Honda T, Nishibuchi M, Miwatani T, Kaper JB. 1986. Demonstration of a plasmid-borne gene encoding a thermostable direct hemolysin in Vibrio cholerae non-O1 strains. Appl. Environ. Microbiol. 52:1218-1220.
35. Horton RM, Hunt HD, Ho SN, Pullen JK, Pease LR. 1989. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77:61-68.
36. Iida T, et al. 1995. Isolation of mutant toxins of Vibrio parahaemolyticus hemolysin by in vitro mutagenesis. Toxicon 33:209-216.
37. Kishishita M, et al. 1992. Sequence variation in the thermostable direct hemolysin-related hemolysin (trh) gene of Vibrio parahaemolyticus. Appl. Environ. Microbiol. 58:2449-2457.
38. Kodama T, et al. 2010. Two regulators of Vibrio parahaemolyticus play important roles in enterotoxicity by controlling the expression of genes in the Vp-PAI region. PLoS One 5:e8678. doi:10.1371/journal.pone.008678.
39. Kodama T, et al. 2007. Identification and characterization of VopT, a novel ADP-ribosyltransferase effector protein secreted via the Vibrio parahaemolyticus type III secretion system 2. Cell. Microbiol. 9:2598-2609.
40. Larkin MA, et al. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
41. Lin Z, Kumagai K, Baba K, Mekalanos JJ, Nishibuchi M. 1993. Vibrio parahaemolyticus has a homolog of the Vibrio cholerae toxRS operon that mediates environmentally induced regulation of the thermostable direct hemolysin gene. J. Bacteriol. 175:3844-3855.
42. Makino K, et al. 2003. Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V. cholerae. Lancet 361:743-749.
43. Matson JS, Withey JH, DiRita VJ. 2007. Regulatory networks controlling Vibrio cholerae virulence gene expression. Infect. Immun. 75:5542-5549.
44. Matsumoto C, et al. 2000. Pandemic spread of an O3:K6 clone of Vibrio parahaemolyticus and emergence of related strains evidenced by arbitrarily primed PCR and toxRS sequence analyses. J. Clin. Microbiol. 38:578-585.
45. Miller VL, Mekalanos JJ. 1984. Synthesis of cholera toxin is positively regulated at the transcriptional level by toxR. Proc. Natl. Acad. Sci. U. S. A.81:3471-3475.
46. Miyamoto Y, et al. 1969. In vitro hemolytic characteristic of Vibrio parahaemolyticus:its close correlation with human pathogenicity. J. Bacteriol.100:1147-1149.
47. Nair GB, et al. 2007. Global dissemination of Vibrio parahaemolyticus serotype O3:K6 and its serovariants. Clin. Microbiol. Rev. 20:39-48.
48. National Research Council. 1996. Guide for the care and use of laboratory animals. National Academies Press, Washington, DC.
49. Nelson EJ, Harris JB, Morris JG, Jr, Calderwood SB, Camilli A. 2009.Cholera transmission: the host, pathogen and bacteriophage dynamic. Nat. Rev. Microbiol. 7:693-702.
50. Nishibuchi M, Fasano A, Russell RG, Kaper JB. 1992. Enterotoxigenicity of Vibrio parahaemolyticus with and without genes encoding thermostable direct hemolysin. Infect. Immun. 60:3539-3545.
51. Nishibuchi M, Kaper JB. 1995. Thermostable direct hemolysin gene of Vibrio parahaemolyticus: a virulence gene acquired by a marine bacterium. Infect. Immun. 63:2093-2099.
52. Okada N, et al. 2009. Identification and characterization of a novel type III secretion system in trh-positive Vibrio parahaemolyticus strain TH3996 reveal genetic lineage and diversity of pathogenic machinery beyond the species level. Infect. Immun. 77:904-913.
53. Park KS, et al. 2004. Cytotoxicity and enterotoxicity of the thermostable direct hemolysin-deletion mutants of Vibrio parahaemolyticus. Microbiol. Immunol. 48:313-318.
54. Peterson MD, Mooseker MS. 1992. Characterization of the enterocyte-like brush border cytoskeleton of the C2BBe clones of the human intestinal cell line, Caco-2. J. Cell Sci. 102:581-600.
55. Raimondi F, et al. 2000. Enterotoxicity and cytotoxicity of Vibrio parahaemolyticus thermostable direct hemolysin in in vitro systems. Infect. Immun. 68:3180-3185.
56. Ritchie JM, Rui H, Bronson RT, Waldor MK. 2010. Back to the future:studying cholera pathogenesis using infant rabbits. mBio 1:e00047-10.
57. Ritchie JM, et al. 2012. Inflammation and disintegration of intestinal villi in an experimental model for Vibrio parahaemolyticus-induced diarrhea. PLoS Pathog. 8:e1002593. doi:10.1371/journal.ppat.1002593.
58. Sack DA, Sack RB, Nair GB, Siddique AK. 2004. Cholera. Lancet 363:223-233.
59. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
60. Sharma C, et al. 1998. Molecular analysis of non-O1, non-O139 Vibrio cholerae associated with an unusual upsurge in the incidence of choleralike disease in Calcutta, India. J. Clin. Microbiol. 36:756-763.
61. Shin OS, et al. 2011. Type III secretion is essential for the rapidly fatal diarrheal disease caused by non-O1, non-O139 Vibrio cholerae. mBio 2:e00106-11.
62. Shirai H, et al. 1990. Molecular epidemiologic evidence for association of thermostable direct hemolysin (TDH) and TDH-related hemolysin of Vibrio parahaemolyticus with gastroenteritis. Infect. Immun. 58:3568-3573.
63. Singh DV, et al. 2001. Molecular analysis of Vibrio cholerae O1, O139,non-O1, and non-O139 strains: clonal relationships between clinical and environmental isolates. Appl. Environ. Microbiol. 67:910-921.
64. Su YC, Liu C. 2007. Vibrio parahaemolyticus: a concern of seafood safety. Food Microbiol. 24:549-558.
65. Tam VC, Serruto D, Dziejman M, Brieher W, Mekalanos JJ. 2007. A type III secretion system in Vibrio cholerae translocates a formin/spire hybrid-like actin nucleator to promote intestinal colonization. Cell Host Microbe 1:95-107.
66. Tang GQ, Iida T, Yamamoto K, Honda T. 1994. A mutant toxin of Vibrio parahaemolyticus thermostable direct hemolysin which has lost hemolytic activity but retains ability to bind to erythrocytes. Infect. Immun. 62:3299-3304.
67. Thompson FL, Iida T, Swings J. 2004. Biodiversity of vibrios. Microbiol. Mol. Biol. Rev. 68:403-431.
68. Toda H, Sakiyama F, Yoh M, Honda T, Miwatani T. 1991. Tryptophan 65 is essential for hemolytic activity of the thermostable direct hemolysin from Vibrio parahaemolyticus. Toxicon 29:837-844.
69. Urbanowski ML, Brutinel ED, Yahr TL. 2007. Translocation of ExsE into Chinese hamster ovary cells is required for transcriptional induction of the Pseudomonas aeruginosa type III secretion system. Infect. Immun. 75:4432-4439.
70. Xu M, Yamamoto K, Honda T, Ming X. 1994. Construction and characterization of an isogenic mutant of Vibrio parahaemolyticus having a deletion in the thermostable direct hemolysin-related hemolysin gene (trh). J. Bacteriol. 176:4757-4760
71. Yahr TL, Wolfgang MC. 2006. Transcriptional regulation of the Pseudomonas aeruginosa type III secretion system. Mol. Microbiol. 62:631-640.
72. Zuckerman JN, Rombo L, Fisch A. 2007. The true burden and risk of cholera: implications for prevention and control. Lancet Infect. Dis.7:521-530.