1887

Abstract

is a Gram-negative, naturally occurring marine bacterium. Subpopulations of strains belonging to this species cause an acute self-limiting gastroenteritis in humans and, less commonly, wound infections. models to differentiate avirulent and virulent strains and evaluate the pathogenic potential of strains of this species have been largely focused on the presence of known virulence factors such as the thermostable direct haemolysin (TDH), the TDH-related haemolysin (TRH) or the contributions of the type 3 secretion systems. However, virulence is likely to be multifactorial, and additional, yet to be identified factors probably contribute to virulence in this bacterium. In this study, we investigated an adult zebrafish model to assess the overall virulence of strains. The model could detect differences in the virulence potential of strains when animals were challenged intraperitoneally, based on survival time. Differences in survival were noted irrespective of the source of isolation of the strain (environmental or clinical) and regardless of the presence or absence of the known virulence factors TDH and TRH, suggesting the influence of additional virulence factors. The model was also effective in comparing differences in virulence between the wild-type strain RIMD2210633 and isogenic pilin mutants Δ and Δ, a double mutant Δ : Δ, as well as a putative chitin-binding protein mutant, Δ.

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2013-12-01
2021-10-22
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References

  1. Brenot A., King K. Y., Janowiak B., Griffith O., Caparon M. G. ( 2004). Contribution of glutathione peroxidase to the virulence of Streptococcus pyogenes . Infect Immun 72:408–413 [View Article][PubMed]
    [Google Scholar]
  2. Centers for Disease Control and Prevention (CDC) ( 2005). Vibrio illnesses after Hurricane Katrina – multiple states, August-September 2005. MMWR Morb Mortal Wkly Rep 54:928–931[PubMed]
    [Google Scholar]
  3. Chiavelli D. A., Marsh J. W., Taylor R. K. ( 2001). The mannose-sensitive hemagglutinin of Vibrio cholerae promotes adherence to zooplankton. Appl Environ Microbiol 67:3220–3225 [View Article][PubMed]
    [Google Scholar]
  4. Davis J. M., Clay H., Lewis J. L., Ghori N., Herbomel P., Ramakrishnan L. ( 2002). Real-time visualization of mycobacterium-macrophage interactions leading to initiation of granuloma formation in zebrafish embryos. Immunity 17:693–702 [View Article][PubMed]
    [Google Scholar]
  5. Fournie J., Krol R., Hawkins W. ( 2000). Fixation of fish tissues. The Laboratory Fish, The Handbook of Experimental Animals569–578 Ostrander G. New York: Academic Press; [View Article]
    [Google Scholar]
  6. Frischkorn K. R., Stojanovski A., Paranjpye R. ( 2013). Vibrio parahaemolyticus type IV pili mediate interactions with diatom-derived chitin and point to an unexplored mechanism of environmental persistence. Environ Microbiol 15:1416–1427 [View Article][PubMed]
    [Google Scholar]
  7. Fullner K. J., Mekalanos J. J. ( 1999). Genetic characterization of a new type IV-A pilus gene cluster found in both classical and El Tor biotypes of Vibrio cholerae . Infect Immun 67:1393–1404[PubMed]
    [Google Scholar]
  8. Goldberg J. B., Hancock R. E., Parales R. E., Loper J., Cornelis P. ( 2008). Pseudomonas 2007. J Bacteriol 190:2649–2662 [View Article][PubMed]
    [Google Scholar]
  9. 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 [View Article][PubMed]
    [Google Scholar]
  10. Honda T., Iida T. ( 1993). The pathogenicity of Vibrio parahaemolyticus and the role of the thermostable direct haemolysin and related haemolysins. Rev Med Microbiol 4:106–113 [View Article]
    [Google Scholar]
  11. Hurley C. C., Quirke A., Reen F. J., Boyd E. F. ( 2006). Four genomic islands that mark post-1995 pandemic Vibrio parahaemolyticus isolates. BMC Genomics 7:104–123 [View Article][PubMed]
    [Google Scholar]
  12. Izutsu K., Kurokawa K., Tashiro K., Kuhara S., Hayashi T., Honda T., Iida T. ( 2008). Comparative genomic analysis using microarray demonstrates a strong correlation between the presence of the 80-kilobase pathogenicity island and pathogenicity in Kanagawa phenomenon-positive Vibrio parahaemolyticus strains. Infect Immun 76:1016–1023 [View Article][PubMed]
    [Google Scholar]
  13. Johnson D. E., Weinberg L., Ciarkowski J., West P., Colwell R. R. ( 1984). Wound infection caused by Kanagawa-negative Vibrio parahaemolyticus . J Clin Microbiol 20:811–812[PubMed]
    [Google Scholar]
  14. Kirn T. J., Jude B. A., Taylor R. K. ( 2005). A colonization factor links Vibrio cholerae environmental survival and human infection. Nature 438:863–866 [View Article][PubMed]
    [Google Scholar]
  15. Kodama T., Hiyoshi H., Gotoh K., Akeda Y., Matsuda S., Park K. S., Cantarelli V. V., Iida T., Honda T. ( 2008). Identification of two translocon proteins of Vibrio parahaemolyticus type III secretion system 2. Infect Immun 76:4282–4289 [View Article][PubMed]
    [Google Scholar]
  16. Lefebvre K. A., Tilton S. C., Bammler T. K., Beyer R. P., Srinouanprachan S., Stapleton P. L., Farin F. M., Gallagher E. P. ( 2009). Gene expression profiles in zebrafish brain after acute exposure to domoic acid at symptomatic and asymptomatic doses. Toxicol Sci 107:65–77 [View Article][PubMed]
    [Google Scholar]
  17. Link A. J., Phillips D., Church G. M. ( 1997). Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: application to open reading frame characterization. J Bacteriol 179:6228–6237[PubMed]
    [Google Scholar]
  18. Ljungh A., Wadstrom T. ( 1982). Toxins of Vibrio parahaemolyticus and Aeromonas hydrophila . Toxin Reviews 1:257–307 [View Article]
    [Google Scholar]
  19. Makino K., Oshima K., Kurokawa K., Yokoyama K., Uda T., Tagomori K., Iijima Y., Najima M., Nakano M. & other authors ( 2003). Genome sequence of Vibrio parahaemolyticus: a pathogenic mechanism distinct from that of V cholerae . Lancet 361:743–749 [View Article][PubMed]
    [Google Scholar]
  20. Mead P. S., Slutsker L., Dietz V., McCaig L. F., Bresee J. S., Shapiro C., Griffin P. M., Tauxe R. V. ( 1999). Food-related illness and death in the United States. Emerg Infect Dis 5:607–625 [View Article][PubMed]
    [Google Scholar]
  21. Menudier A., Rougier F. P., Bosgiraud C. ( 1996). Comparative virulence between different strains of Listeria in zebrafish (Brachydanio rerio) and mice. Pathol Biol (Paris) 44:783–789[PubMed]
    [Google Scholar]
  22. Miyamoto Y., Obara Y., Nikkawa T., Yamai S., Kato T., Yamada Y., Ohashi M. ( 1980). Simplified purification and biophysicochemical characteristics of Kanagawa phenomenon-associated hemolysin of Vibrio parahaemolyticus . Infect Immun 28:567–576[PubMed]
    [Google Scholar]
  23. Moyer T. R., Hunnicutt D. W. ( 2007). Susceptibility of zebra fish Danio rerio to infection by Flavobacterium columnare and F. johnsoniae . Dis Aquat Organ 76:39–44 [View Article][PubMed]
    [Google Scholar]
  24. Neely M. N., Pfeifer J. D., Caparon M. ( 2002). Streptococcus-zebrafish model of bacterial pathogenesis. Infect Immun 70:3904–3914 [View Article][PubMed]
    [Google Scholar]
  25. Newton A., Kendall M., Vugia D. J., Henao O. L., Mahon B. E. ( 2012). Increasing rates of vibriosis in the United States, 1996-2010: review of surveillance data from 2 systems. Clin Infect Dis 54:Suppl. 5S391–S395 [View Article][PubMed]
    [Google Scholar]
  26. Nishibuchi M., Fasano A., Russell R. G., Kaper J. B. ( 1992). Enterotoxigenicity of Vibrio parahaemolyticus with and without genes encoding thermostable direct hemolysin. Infect Immun 60:3539–3545[PubMed]
    [Google Scholar]
  27. O’Toole G. A., Pratt L. A., Watnick P. I., Newman D. K., Weaver V. B., Kolter R. ( 1999). Genetic approaches to study of biofilms. Methods Enzymol 310:91–109 [View Article][PubMed]
    [Google Scholar]
  28. O’Toole R., Von Hofsten J., Rosqvist R., Olsson P. E., Wolf-Watz H. ( 2004). Visualisation of zebrafish infection by GFP-labelled Vibrio anguillarum . Microb Pathog 37:41–46 [View Article][PubMed]
    [Google Scholar]
  29. Okada N., Iida T., Park K.-S., Goto N., Yasunaga T., Hiyoshi H., Matsuda S., Kodama T., Honda T. ( 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 [View Article][PubMed]
    [Google Scholar]
  30. Paranjpye R. N., Strom M. S. ( 2005). A Vibrio vulnificus type IV pilin contributes to biofilm formation, adherence to epithelial cells, and virulence. Infect Immun 73:1411–1422 [View Article][PubMed]
    [Google Scholar]
  31. Paranjpye R., Hamel O. S., Stojanovski A., Liermann M. ( 2012). Genetic diversity of clinical and environmental Vibrio parahaemolyticus strains from the Pacific Northwest. Appl Environ Microbiol 78:8631–8638 [View Article][PubMed]
    [Google Scholar]
  32. Park K.-S., Ono T., Rokuda M., Jang M.-H., Iida T., Honda T. ( 2004). Cytotoxicity and enterotoxicity of the thermostable direct hemolysin-deletion mutants of Vibrio parahaemolyticus . Microbiol Immunol 48:313–318[PubMed] [CrossRef]
    [Google Scholar]
  33. Phelps H. A., Runft D. L., Neely M. N. ( 2009). Adult zebrafish model of streptococcal infection. Curr Protoc Microbiol, Chapter 9Unit 9D.1
    [Google Scholar]
  34. Piñeyro P., Zhou X., Orfe L. H., Friel P. J., Lahmers K., Call D. R. ( 2010). Development of two animal models to study the function of Vibrio parahaemolyticus type III secretion systems. Infect Immun 78:4551–4559 [View Article][PubMed]
    [Google Scholar]
  35. Pressley M. E., Phelan P. E. III, Witten P. E., Mellon M. T., Kim C. H. ( 2005). Pathogenesis and inflammatory response to Edwardsiella tarda infection in the zebrafish. Dev Comp Immunol 29:501–513 [View Article][PubMed]
    [Google Scholar]
  36. Prouty M. G., Correa N. E., Barker L. P., Jagadeeswaran P., Klose K. E. ( 2003). Zebrafish-Mycobacterium marinum model for mycobacterial pathogenesis. FEMS Microbiol Lett 225:177–182 [View Article][PubMed]
    [Google Scholar]
  37. Rawls J. F., Mahowald M. A., Goodman A. L., Trent C. M., Gordon J. I. ( 2007). In vivo imaging and genetic analysis link bacterial motility and symbiosis in the zebrafish gut. Proc Natl Acad Sci U S A 104:7622–7627 [View Article][PubMed]
    [Google Scholar]
  38. Reed L. J., Muench H. ( 1938). A simple method of estimating fifty percent endpoints. Am J Hyg 27:493–497
    [Google Scholar]
  39. Ritchie J. M., Rui H., Zhou X., Iida T., Kodoma T., Ito S., Davis B. M., Bronson R. T., Waldor M. K. ( 2012). Inflammation and disintegration of intestinal villi in an experimental model for Vibrio parahaemolyticus-induced diarrhea. PLoS Pathog 8e1002593 [CrossRef]
    [Google Scholar]
  40. Rojo I., de Ilárduya O. M., Estonba A., Pardo M. A. ( 2007). Innate immune gene expression in individual zebrafish after Listonella anguillarum inoculation. Fish Shellfish Immunol 23:1285–1293 [View Article][PubMed]
    [Google Scholar]
  41. Stemple D. L., Driever W. ( 1996). Zebrafish: tools for investigating cellular differentiation. Curr Opin Cell Biol 8:858–864 [View Article][PubMed]
    [Google Scholar]
  42. Sullivan C., Kim C. H. ( 2008). Zebrafish as a model for infectious disease and immune function. Fish Shellfish Immunol 25:341–350 [View Article][PubMed]
    [Google Scholar]
  43. Tacket C. O., Taylor R. K., Losonsky G., Lim Y., Nataro J. P., Kaper J. B., Levine M. M. ( 1998). Investigation of the roles of toxin-coregulated pili and mannose-sensitive hemagglutinin pili in the pathogenesis of Vibrio cholerae O139 infection. Infect Immun 66:692–695[PubMed]
    [Google Scholar]
  44. Takeda Y. ( 1982). Thermostable direct hemolysin of Vibrio parahaemolyticus . Pharmacol Ther 19:123–146 [View Article][PubMed]
    [Google Scholar]
  45. Thelin K. H., Taylor R. K. ( 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[PubMed]
    [Google Scholar]
  46. Turner J. W., Paranjpye R. N., Landis E. D., Biryukov S. V., González-Escalona N., Nilsson W. B., Strom M. S. ( 2013). Population structure of clinical and environmental Vibrio parahaemolyticus from the Pacific Northwest Coast of the United States. PLoS ONE 8e55726 [CrossRef]
    [Google Scholar]
  47. Venables W. N., Ripley B. D. (editors) ( 2002). Modern Applied Statistics with S. (Statistics and Computing), 4th edn. New York: Springer;
    [Google Scholar]
  48. Watnick P. I., Fullner K. J., Kolter R. ( 1999). A role for the mannose-sensitive hemagglutinin in biofilm formation by Vibrio cholerae El Tor. J Bacteriol 181:3606–3609[PubMed]
    [Google Scholar]
  49. Weis K. E., Hammond R. M., Hutchinson R., Blackmore C. G. M. ( 2011). Vibrio illness in Florida, 1998-2007. Epidemiol Infect 139:591–598 [View Article][PubMed]
    [Google Scholar]
  50. Zon L. I. ( 1999). Zebrafish: a new model for human disease. Genome Res 9:99–100[PubMed]
    [Google Scholar]
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