Vibrio parahaemolyticus cell biology and pathogenicity determinants

Microbes and Infection

Volumn 13, Issue 12-13, 2011, Pages 992-1001

  Broberg, Christopher A ^a   Calder, Thomas J ^a   Orth, Kim ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Gastroenteritis; Hemolysin; Pathogenesis; Type III secretion system; Vibrio parahaemolyticus

Indexed keywords

CHOLERA TOXIN; IRON;

ACUTE GASTROENTERITIS; BACTERIAL FLAGELLUM; BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BIOFILM; CYTOLOGY; CYTOTOXICITY; HEMOLYSIS; HOST CELL; HUMAN; NONHUMAN; PRIORITY JOURNAL; SEPTICEMIA; SHORT SURVEY; TYPE III SECRETION SYSTEM; VIBRIO PARAHAEMOLYTICUS; VIBRIO PARAHAEMOLYTICUS INFECTION; WOUND INFECTION;

ANIMALS; BACTERIAL PROTEINS; DISEASE MODELS, ANIMAL; GASTROENTERITIS; HUMANS; SEAFOOD; SEPSIS; VIBRIO INFECTIONS; VIBRIO PARAHAEMOLYTICUS; VIRULENCE; VIRULENCE FACTORS; WOUND INFECTION;

VIBRIO PARAHAEMOLYTICUS;

EID: 80053385574     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2011.06.013     Document Type: Short Survey

References (79)

1. McCarter L. The multiple identities of Vibrio parahaemolyticus. J. Mol. Microbiol. Biotechnol. 1999, 1:51-57.
2. Yeung P.S., Boor K.J. Epidemiology, pathogenesis, and prevention of foodborne Vibrio parahaemolyticus infections. Foodborne Pathog. Dis. 2004, 1:74-88.
3. Su Y.C., Liu C. Vibrio parahaemolyticus: a concern of seafood safety. Food Microbiol. 2007, 24:549-558.
4. Joseph S.W., Colwell R.R., Kaper J.B. Vibrio parahaemolyticus and related halophilic Vibrios. Crit. Rev. Microbiol. 1982, 10:77-124.
5. Honda T., Iida T., Akeda Y., Kodama T. Sixty years of Vibrio parahaemolyticus. Microbe 2008, 3:462-466.
6. Morris J.G. Cholera and other types of vibriosis: a story of human pandemics and oysters on the half shell. Clin. Infect. Dis. 2003, 37:272-280.
7. Nair G.B., Ramamurthy T., Bhattacharya S.K., Dutta B., Takeda Y., Sack D.A. Global dissemination of Vibrio parahaemolyticus serotype O3:K6 and its serovariants. Clin. Microbiol. Rev. 2007, 20:39-48.
8. Daniels N.A., MacKinnon L., Bishop R., Altekruse S., Ray B., Hammond R.M., Thompson S., Wilson S., Bean N.H., Griffin P.M., Slutsker L. Vibrio parahaemolyticus infections in the United States, 1973-1998. J. Infect. Dis. 2000, 181:1661-1666.
9. Baffone W., Tarsi R., Pane L., Campana R., Repetto B., Mariottini G.L., Pruzzo C. Detection of free-living and plankton-bound vibrios in coastal waters of the Adriatic Sea (Italy) and study of their pathogenicity-associated properties. Environ. Microbiol. 2006, 8:1299-1305.
10. Gamble M.D., Lovell C.R. Infaunal burrows are enrichment zones for Vibrio parahaemolyticus. Appl. Environ. Microbiol. 2011.
11. Johnson C.N., Flowers A.R., Noriea N.F., Zimmerman A.M., Bowers J.C., DePaola A., Grimes D.J. Relationships between environmental factors and pathogenic vibrios in the Northern Gulf of Mexico. Appl. Environ. Microbiol. 2010, 76:7076-7084.
12. Vasconcelos G.J., Stang W.J., Laidlaw R.H. Isolation of Vibrio parahaemolyticus and Vibrio alginolyticus from estuarine areas of Southeastern Alaska. Appl. Microbiol. 1975, 29:557-559.
13. McLaughlin J.B., DePaola A., Bopp C.A., Martinek K.A., Napolilli N.P., Allison C.G., Murray S.L., Thompson E.C., Bird M.M., Middaugh J.P. Outbreak of Vibrio parahaemolyticus gastroenteritis associated with Alaskan oysters. N. Engl. J. Med. 2005, 353:1463-1470.
14. Gonzalez-Escalona N., Strain E.A., De Jesus A.J., Jones J.L., Depaola A. Genome sequence of a clinical O4:K12 serotype Vibrio parahaemolyticus strain 10329. J. Bacteriol. 2011, 10.1128/JB.05044-05011.
15. Makino K., Oshima K., Kurokawa K., Yokoyama K., Uda T., Tagomori K., Iijima Y., Najima M., Nakano M., Yamashita A., Kubota Y., Kimura S., Yasunaga T., Honda T., Shinagawa H., Hattori M., Iida T. Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V cholerae. Lancet 2003, 361:743-749.
16. Boyd E.F., Cohen A.L., Naughton L.M., Ussery D.W., Binnewies T.T., Stine O.C., Parent M.A. Molecular analysis of the emergence of pandemic Vibrio parahaemolyticus. BMC Microbiol. 2008, 8:110.
17. Bej A.K., Patterson D.P., Brasher C.W., Vickery M.C., Jones D.D., Kaysner C.A. Detection of total and hemolysin-producing Vibrio parahaemolyticus in shellfish using multiplex PCR amplification of tlh, tdh and trh. J. Microbiol. Methods 1999, 36:215-225.
18. Zhou X., Konkel M.E., Call D.R. Type III secretion system 1 of Vibrio parahaemolyticus induces oncosis in both epithelial and monocytic cell lines. Microbiology 2009, 155:837-851.
19. Hlady W.G., Klontz K.C. The epidemiology of Vibrio infections in Florida, 1981-1993. J. Infect. Dis. 1996, 173:1176-1183.
20. Blake P.A., Merson M.H., Weaver R.E., Hollis D.G., Heublein P.C. Disease caused by a marine Vibrio. Clinical characteristics and epidemiology. N. Engl. J. Med. 1979, 300:1-5.
21. Okada N., Matsuda S., Matsuyama J., Park K.S., de los Reyes C., Kogure K., Honda T., Iida T. Presence of genes for type III secretion system 2 in Vibrio mimicus strains. BMC Microbiol. 2010, 10:302.
22. Chao G., Jiao X., Zhou X., Wang F., Yang Z., Huang J., Pan Z., Zhou L., Qian X. Distribution of genes encoding four pathogenicity islands (VPaIs), T6SS, biofilm, and type I pilus in food and clinical strains of Vibrio parahaemolyticus in China. Foodborne Pathog. Dis. 2010, 7:649-658.
23. Gotoh K., Kodama T., Hiyoshi H., Izutsu K., Park K.S., Dryselius R., Akeda Y., Honda T., Iida T. Bile acid-induced virulence gene expression of Vibrio parahaemolyticus reveals a novel therapeutic potential for bile acid sequestrants. PLoS One 2010, 5:e13365.
24. Jaques S., McCarter L.L. Three new regulators of swarming in Vibrio parahaemolyticus. J. Bacteriol. 2006, 188:2625-2635.
25. Ferreira R.B., Antunes L.C., Greenberg E.P., McCarter L.L. Vibrio parahaemolyticus ScrC modulates cyclic dimeric GMP regulation of gene expression relevant to growth on surfaces. J. Bacteriol. 2008, 190:851-860.
26. Kim Y.K., McCarter L.L. ScrG, a GGDEF-EAL protein, participates in regulating swarming and sticking in Vibrio parahaemolyticus. J. Bacteriol. 2007, 189:4094-4107.
27. Gode-Potratz C.J., Kustusch R.J., Breheny P.J., Weiss D.S., McCarter L.L. Surface sensing in Vibrio parahaemolyticus triggers a programme of gene expression that promotes colonization and virulence. Mol. Microbiol. 2011, 79:240-263.
28. Krachler A.M., Ham H., Orth K. The outer membrane adhesion factor MAM7 initiates host cell binding during infection by Gram-negative pathogens. Proc. Natl. Acad. Sci. U S A 2011.
29. Kustusch R.J., Kuehl C.J., Crosa J.H. Power plays: iron transport and energy transduction in pathogenic vibrios. Biometals 2011, 24:559-566.
30. Tanabe T., Funahashi T., Nakao H., Miyoshi S., Shinoda S., Yamamoto S. Identification and characterization of genes required for biosynthesis and transport of the siderophore vibrioferrin in Vibrio parahaemolyticus. J. Bacteriol. 2003, 185:6938-6949.
31. Funahashi T., Tanabe T., Shiuchi K., Nakao H., Yamamoto S. Identification and characterization of genes required for utilization of desferri-ferrichrome and aerobactin in Vibrio parahaemolyticus. Biol. Pharm. Bull. 2009, 32:359-365.
32. O'Malley S.M., Mouton S.L., Occhino D.A., Deanda M.T., Rashidi J.R., Fuson K.L., Rashidi C.E., Mora M.Y., Payne S.M., Henderson D.P. Comparison of the heme iron utilization systems of pathogenic Vibrios. J. Bacteriol. 1999, 181:3594-3598.
33. Nishibuchi M., Kaper J.B. Thermostable direct hemolysin gene of Vibrio parahaemolyticus: a virulence gene acquired by a marine bacterium. Infect. Immun. 1995, 63:2093-2099.
34. Hongping W., Jilun Z., Ting J., Yixi B., Xiaoming Z. Insufficiency of the Kanagawa hemolytic test for detecting pathogenic Vibrio parahaemolyticus in Shanghai, China. Diagn. Microbiol. Infect. Dis. 2011, 69:7-11.
35. Fukui T., Shiraki K., Hamada D., Hara K., Miyata T., Fujiwara S., Mayanagi K., Yanagihara K., Iida T., Fukusaki E., Imanaka T., Honda T., Yanagihara I. Thermostable direct hemolysin of Vibrio parahaemolyticus is a bacterial reversible amyloid toxin. Biochemistry 2005, 44:9825-9832.
36. Matsuda S., Kodama T., Okada N., Okayama K., Honda T., Iida T. Association of Vibrio parahaemolyticus thermostable direct hemolysin with lipid rafts is essential for cytotoxicity but not hemolytic activity. Infect. Immun. 2010, 78:603-610.
37. Yanagihara I., Nakahira K., Yamane T., Kaieda S., Mayanagi K., Hamada D., Fukui T., Ohnishi K., Kajiyama S., Shimizu T., Sato M., Ikegami T., Ikeguchi M., Honda T., Hashimoto H. Structure and functional characterization of Vibrio parahaemolyticus thermostable direct hemolysin. J. Biol. Chem. 2010, 285:16267-16274.
38. Honda T., Ni Y., Miwatani T., Adachi T., Kim J. The thermostable direct hemolysin of Vibrio parahaemolyticus is a pore-forming toxin. Can. J. Microbiol. 1992, 38:1175-1180.
39. Park K.S., Ono T., Rokuda M., Jang M.H., Iida T., Honda T. Cytotoxicity and enterotoxicity of the thermostable direct hemolysin-deletion mutants of Vibrio parahaemolyticus. Microbiol. Immunol. 2004, 48:313-318.
40. Liverman A.D., Cheng H.C., Trosky J.E., Leung D.W., Yarbrough M.L., Burdette D.L., Rosen M.K., Orth K. Arp2/3-independent assembly of actin by Vibrio type III effector VopL. Proc. Natl. Acad. Sci. U S A 2007, 104:17117-17122.
41. Lynch T., Livingstone S., Buenaventura E., Lutter E., Fedwick J., Buret A.G., Graham D., DeVinney R. Vibrio parahaemolyticus disruption of epithelial cell tight junctions occurs independently of toxin production. Infect. Immun. 2005, 73:1275-1283.
42. Park K.S., Ono T., Rokuda M., Jang M.H., Okada K., Iida T., Honda T. Functional characterization of two type III secretion systems of Vibrio parahaemolyticus. Infect. Immun. 2004, 72:6659-6665.
43. Ohnishi K., Nakahira K., Unzai S., Mayanagi K., Hashimoto H., Shiraki K., Honda T., Yanagihara I. Relationship between heat-induced fibrillogenicity and hemolytic activity of thermostable direct hemolysin and a related hemolysin of Vibrio parahaemolyticus. FEMS Microbiol. Lett. 2011, 318:10-17.
44. Galan J.E., Wolf-Watz H. Protein delivery into eukaryotic cells by type III secretion machines. Nature 2006, 444:567-573.
45. Izore T., Job V., Dessen A. Biogenesis, regulation, and targeting of the type III secretion system. Structure 2011, 19:603-612.
46. Marlovits T.C., Stebbins C.E. Type III secretion systems shape up as they ship out. Curr. Opin. Microbiol. 2010, 13:47-52.
47. Cornelis G.R. The type III secretion injectisome. Nat. Rev. Microbiol. 2006, 4:811-825.
48. Burdette D.L., Seemann J., Orth K. Vibrio VopQ induces PI3-kinase-independent autophagy and antagonizes phagocytosis. Mol. Microbiol. 2009, 73:639-649.
49. Mukherjee S., Keitany G., Li Y., Wang Y., Ball H.L., Goldsmith E.J., Orth K. Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 2006, 312:1211-1214.
50. Ogawa M., Yoshimori T., Suzuki T., Sagara H., Mizushima N., Sasakawa C. Escape of intracellular Shigella from autophagy. Science 2005, 307:727-731.
51. Von Pawel-Rammingen U., Telepnev M.V., Schmidt G., Aktories K., Wolf-Watz H., Rosqvist R. GAP activity of the Yersinia YopE cytotoxin specifically targets the Rho pathway: a mechanism for disruption of actin microfilament structure. Mol. Microbiol. 2000, 36:737-748.
52. Yarbrough M.L., Li Y., Kinch L.N., Grishin N.V., Ball H.L., Orth K. AMPylation of Rho GTPases by Vibrio VopS disrupts effector binding and downstream signaling. Science 2009, 323:269-272.
53. Akeda Y., Galan J.E. Chaperone release and unfolding of substrates in type III secretion. Nature 2005, 437:911-915.
54. Arnold R., Jehl A., Rattei T. Targeting effectors: the molecular recognition of Type III secreted proteins. Microbes Infect. 2010, 12:346-358.
55. Galan J.E. Common themes in the design and function of bacterial effectors. Cell Host Microbe 2009, 5:571-579.
56. Ono T., Park K.S., Ueta M., Iida T., Honda T. Identification of proteins secreted via Vibrio parahaemolyticus type III secretion system 1. Infect. Immun. 2006, 74:1032-1042.
57. Panina E.M., Mattoo S., Griffith N., Kozak N.A., Yuk M.H., Miller J.F. A genome-wide screen identifies a Bordetella type III secretion effector and candidate effectors in other species. Mol. Microbiol. 2005, 58:267-279.
58. Kodama T., Gotoh K., Hiyoshi H., Morita M., Izutsu K., Akeda Y., Park K.S., Cantarelli V.V., Dryselius R., Iida T., Honda T. Two regulators of Vibrio parahaemolyticus play important roles in enterotoxicity by controlling the expression of genes in the Vp-PAI region. PLoS One 2010, 5:e8678.
59. Monack D.M., Mecsas J., Ghori N., Falkow S. Yersinia signals macrophages to undergo apoptosis and YopJ is necessary for this cell death. Proc. Natl. Acad. Sci. U S A 1997, 94:10385-10390.
60. Kodama T., Yamazaki C., Park K.S., Akeda Y., Iida T., Honda T. Transcription of Vibrio parahaemolyticus T3SS1 genes is regulated by a dual regulation system consisting of the ExsACDE regulatory cascade and H-NS. FEMS Microbiol. Lett. 2010.
61. Dorman C.J. H-NS: a universal regulator for a dynamic genome. Nat. Rev. Microbiol. 2004, 2:391-400.
62. Burdette D.L., Yarbrough M.L., Orvedahl A., Gilpin C.J., Orth K. Vibrio parahaemolyticus orchestrates a multifaceted host cell infection by induction of autophagy, cell rounding, and then cell lysis. Proc. Natl. Acad. Sci. U S A 2008, 105:12497-12502.
63. Broberg C.A., Zhang L., Gonzalez H., Laskowski-Arce M.A., Orth K. A Vibrio effector protein is an inositol phosphatase and disrupts host cell membrane integrity. Science 2010, 329:1660-1662.
64. Matlawska-Wasowska K., Finn R., Mustel A., O'Byrne C.P., Baird A.W., Coffey E.T., Boyd A. The Vibrio parahaemolyticus Type III Secretion Systems manipulate host cell MAPK for critical steps in pathogenesis. BMC Microbiol. 2010, 10:329.
65. Shimohata T., Nakano M., Lian X., Shigeyama T., Iba H., Hamamoto A., Yoshida M., Harada N., Yamamoto H., Yamato M., Mawatari K., Tamaki T., Nakaya Y., Takahashi A. Vibrio parahaemolyticus infection induces modulation of IL-8 secretion through dual pathway via VP1680 in Caco-2 cells. J. Infect. Dis. 2011, 203:537-544.
66. Luong P., Kinch L.N., Brautigam C.A., Grishin N.V., Tomchick D.R., Orth K. Kinetic and structural insights into the mechanism of AMPylation by VopS Fic domain. J. Biol. Chem. 2010, 285:20155-20163.
67. Woolery A.R., Luong P., Broberg C.A., Orth K. AMPylation: something old is new again. Front. Microbiol. 2010, 1:1-6.
68. Zhao Z., Chen C., Hu C.Q., Ren C.H., Zhao J.J., Zhang L.P., Jiang X., Luo P., Wang Q.B. The type III secretion system of Vibrio alginolyticus induces rapid apoptosis, cell rounding and osmotic lysis of fish cells. Microbiol. 2010, 156:2864-2872.
69. Caburlotto G., Lleo M.M., Hilton T., Huq A., Colwell R.R., Kaper J.B. Effect on human cells of environmental Vibrio parahaemolyticus strains carrying type III secretion system 2. Infect. Immun. 2010, 78:3280-3287.
70. Miraglia A.G., Travaglione S., Meschini S., Falzano L., Matarrese P., Quaranta M.G., Viora M., Fiorentini C., Fabbri A. Cytotoxic necrotizing factor 1 prevents apoptosis via the Akt/IkappaB kinase pathway: role of nuclear factor-kappaB and Bcl-2. Mol. Biol. Cell 2007, 18:2735-2744.
71. Kodama T., Rokuda M., Park K.S., Cantarelli V.V., Matsuda S., Iida T., Honda T. Identification and characterization of VopT, a novel ADP-ribosyltransferase effector protein secreted via the Vibrio parahaemolyticus type III secretion system 2. Cell Microbiol. 2007, 9:2598-2609.
72. M.C. Lawrence, A. Jivan, C. Shao, L. Duan, D. Goad, E. Zaganjor, J. Osborne, K. McGlynn, S. Stippec, S. Earnest, W. Chen, M. Cobb, The roles of MAPKs in disease, Cell Res. 18 (2008) 436-442.
73. Trosky J.E., Li Y., Mukherjee S., Keitany G., Ball H., Orth K. VopA inhibits ATP binding by acetylating the catalytic loop of MAPK kinases. J. Biol. Chem. 2007, 282:34299-34305.
74. Trosky J.E., Mukherjee S., Burdette D.L., Roberts M., McCarter L., Siegel R.M., Orth K. Inhibition of MAPK signaling pathways by VopA from Vibrio parahaemolyticus. J. Biol. Chem. 2004, 279:51953-51957.
75. Tam V.C., Suzuki M., Coughlin M., Saslowsky D., Biswas K., Lencer W.I., Faruque S.M., Mekalanos J.J. Functional analysis of VopF activity required for colonization in Vibrio cholerae. MBio 2010, 1. 10.1128/mBio.00289-00210.
76. Laskowski-Arce M.A., Orth K. Acanthamoeba castellanii promotes the survival of Vibrio parahaemolyticus. Appl. Environ. Microbiol. 2008, 74:7183-7188.
77. Matz C., Nouri B., McCarter L., Martinez-Urtaza J. Acquired type III secretion system determines environmental fitness of Epidemic Vibrio parahaemolyticus in the interaction with Bacterivorous protists. PLoS One 2011, 6:e20275.
78. Hiyoshi H., Kodama T., Iida T., Honda T. Contribution of Vibrio parahaemolyticus virulence factors to cytotoxicity, enterotoxicity, and lethality in mice. Infect. Immun. 2010, 78:1772-1780.
79. Pineyro P., Zhou X., Orfe L.H., Friel P.J., Lahmers K., Call D.R. Development of two animal models to study the function of Vibrio parahaemolyticus type III secretion systems. Infect. Immun. 2010, 78:4551-4559.