Chemotactic motility is required for invasion of the host by the fish pathogen Vibrio anguillarum

Molecular Microbiology

Volumn 19, Issue 3, 1996, Pages 625-637

  O'Toole, Ronan ^a   Milton, Debra L ^a   Wolf Watz, Hans ^a  

^a UMEÅ UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL VIRULENCE; CELL MOTILITY; CHEMOTAXIS; FISH; FLAGELLUM; GENE INSERTION; INFECTION; MUTANT; PRIORITY JOURNAL; VIBRIO;

EID: 0030033211     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1996.412927.x     Document Type: Article

References (56)

1. Aguero-Rosenfeld, M.E., Yang, X.-H., and Nachamkin, I. (1990) Infection of adult Syrian hamsters with flagellar variants of Campylobacter jejuni. Infect Immun 58: 2214-2219.
2. Akerley, B.J., and Miller, J.F. (1993) Flagellin gene transcription in Bordetella bronchiseptica is regulated by the BvgAS virulence control system. J Bacteriol 175: 3468-3479.
3. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. (eds) (1987) Current Protocols in Molecular Biology. New York: Wiley.
4. Boyle-Vavra, S., So, M., and Seifert, H.S. (1993) Transcriptional control of gonococcal pilE expression: involvement of an alternative sigma factor. Gene 137: 233-236.
5. Brun, Y.V., and Shapiro, L. (1992) A temporally controlled sigma-factor is required for polar morphogenesis and normal cell division in Caulobacter. Genes Devel 6: 2395-2408.
6. Crosa, J.H. (1980) A plasmid associated with virulence in marine fish pathogen Vibrio anguillarum specifies an iron-sequestering system. Nature 284: 566-567.
7. Crosa, J.H., Hodges, L.L., and Schiewe, M.H. (1980) Curing of a plasmid is correlated with an attenuation of virulence in the marine fish pathogen Vibrio anguillarum. Infect Immun 27: 897-902.
8. Cullen, P.J., Foster-Hartnett, D., Gabbert, K.K., and Krantz, R.G. (1994) Structure and expression of the alternative sigma factor, RpoN, in Rhodobacter capsulatus; physiological relevance of an autoactivated nifU2-rpoN superoperon. Mol Microbiol 11: 51-65.
9. Drake, D., and Montie, T.C. (1988) Flagella, motility and invasive virulence of Pseudomonas aeruginosa. J Gen Microbiol 134: 43-52.
10. Eaton, K.A., Morgan, D.R., and Krakowka, S. (1989) Campylobacter pylori virulence factors in gnotobiotic piglets. Infect Immun 57: 1119-1125.
11. Fellay, R., Rahme, L.G., Mindrinos, M.N., Frederick, R.D., Pisi, A., and Panopoulos, N.J. (1991) Genes and signals controlling the Pseudomonas syringae pv. phaseolicola-plant interaction. In Advances in Molecular Genetics of Plant-Microbe Interactions, vol. 1. Hennecke, H., and Verma, D.P.S. (eds). Dordrecht: Kluwer Academic, pp. 45-52.
12. Frederick, R.D., Majerczak, D.R., and Coplin, D.L. (1993) Erwinia stewartii WstA, a positive regulator of pathogenicity gene expression, is similar to Pseudomonas syringae pv. phaseolicola HrpS. Mol Microbiol 9: 477-485.
13. Freter, R., and O'Brien, P.C.M. (1981) Role of chemotaxis in the association of motile bacteria with intestinal mucosa: fitness and virulence of nonchemotactic Vibrio cholera mutants in infant mice. Infect Immun 34: 222-233.
14. Freter, R., Allweiss, B., O'Brien, P.C.M., Halstead, S.A., and Macsai, M.S. (1981a) Role of chemotaxis in the association of motile bacteria with intestinal mucosa: in vitro studies. Infect Immun 34: 241-249.
15. Freter, R., O'Brien, P.C.M., and Macsai, M.S. (1981b) Role of chemotaxis in the association of motile bacteria with intestinal mucosa: in vivo studies. Infect Immun 34: 234-240.
16. Gay, P., Le Coq, D., Steinmetz, M., Berkelman, T., and Kado, C.I. (1985) Positive selection procedure for entrapment of insertion sequence elements in Gram-negative bacteria. J Bacteriol 164: 918-921.
17. Geis, G., Suerbaum, S., Forsthoff, B., Leying, H., and Opferkuch, W. (1993) Ultrastructure and biochemical studies of the flagellar sheath of Helicobacter pylori. J Med Microbiol 38: 371-377.
18. Guentzel, M.N., and Berry, L.J. (1975) Motility as a virulence factor for Vibrio cholera. Infect Immun 11: 890-897.
19. Herrero, M., de Lorenzo, V., and Timmis, K.N. (1990) Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in Gram-negative bacteria. J Bacteriol 172: 6557-6567.
20. Ho, S.N., Hunt, H.D., Norton, R.M., Pullen, J.K., and Pease, L.R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51-59.
21. Inamura, H., Nakai, T., and Muroga, K. (1985) An extracellular protease produced by Vibrio anguillarum. Bull Jap Soc Scientific Fishers 51: 1915-1920.
22. Inouye, S., Kimoto, M., Nakazawa, A., and Nakazawa, T. (1990) Presence of flagella in Pseudomonas putida is dependent on the ntrA (rpoN) gene. Mol Gen Genet 221: 295-298.
23. Ishimoto, K.S., and Lory, S. (1989) Formation of pilin in Pseudomonas aeruginosa requires the alternative sigma factor (RpoN) of RNA polyrnerase. Proc Natl Acad Sci USA 86: 1954-1957.
24. Jones, B.D., Lee, C.A., and Falkow, S. (1992) Invasion by Salmonella typhimurium is affected by the direction of flagellar rotation. Infect Immun 60: 2475-2480.
25. Kaniga, K., Delor, I., and Cornelis, G.R. (1991) A wide-host-range suicide vector for improving reverse genetics in Gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica. Gene 109: 137-141.
26. Khoramian-Falsafi, T., Harayama, S., Kutsukake, K., and Pechere, J.C. (1990) Effect of motility and chemotaxis on the invasion of Salmonella typhimurium into HeLa cells. Microb Pathogen 9: 47-53.
27. Komeda, Y. (1982) Fusions of flagellar operons to lactose genes on a Mu lac bacteriophage. J Bacteriol 150: 16-26.
28. Kubori, T., Shimamoto, N., Yamaguchi, S., Namba, K., and Aizawa, S.-I. (1992) Morphological pathway of flagellar assembly in Salmonella typhimurium. J Mol Biol 226: 433-446.
29. Kutsukake, K., Ohya, Y., and Iino, T. (1990) Transcriptional analysis of the flagellar regulon of Salmonella typhimurium. J Bacteriol 172: 741-747.
30. Laemmli, U.K. (1970) Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227: 680-685.
31. Liu, S.-L., Takayuki, E., Miura, H., Matsui, K., and Yabuuchi, E. (1988) Intact motility as a Salmonella typhi invasion-related factor. Infect Immun 56: 1967-1973.
32. Lockmann, H.A., and Curtiss, R. (1990) Salmonella typhimurium mutants lacking flagella or motility remain virulent in Balb/c mice. Infect Immun 58: 137-143.
33. de Lorenzo, V., Herrero, M., Jakubzik, U., and Timmis, K.N. (1990) Mini-Tn5 transposon derivatives for insertional mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in Gram-negative eubacteria. J Bacteriol 172: 6568-6572.
34. McCarter, L. (1995) Genetic and molecular characterization of the polar flagellum of Vibrio parahaemolyticus. J Bacteriol 177: 1595-1609.
35. Macnab, R.M. (1987) Motility and chemotaxis. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, vol. 1. Neidhardt, F.C., Ingraham, J.L., Low, B.L., Magasanik, B., Schaechter, M., and Umbarger, H.E. (eds). Washington DC: American Society for Microbiology, pp. 732-759.
36. Macnab, R.M. (1992) Genetics and biogenesis of bacterial flagella. Annu Rev Genet 26: 131-158.
37. N). Mol Microbiol 10: 903-909.
38. Meyer, T.F., Billyard, E., Haas, R., Storzbach, S., and So, M. (1984) Pilus genes of Neisseria gonorrhoeae: chromosomal organisation and DNA sequence. Proc Natl Acad Sci USA 81: 6110-6114.
39. Miller, V.L., and Mekalanos, J.J. (1988) A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholera requires toxR. J Bacteriol 170: 2575-2583.
40. Munn, C.B. (1980) Production and properties of a haemolytic toxin by Vibrio anguillarum. In Fish Diseases, Third COPRAQ Session. Ahne, W. (ed.). Berlin: Springer Verlag, pp. 69-74.
41. Nachamkin, J., Yang, X.-H., and Stern, N.J. (1993) Role of Campylobacter jejuni flagella as colonisation factors for three-day-old mice chicks: analysis with flagellar variants. Appl Environ Microbiol 59: 1269-1273.
42. Norqvist, A., and Wolf-Watz, H. (1993) Characterisation of a novel chromosomal virulence locus involved in expression of a major surface flagellar sheath antigen of the fish pathogen Vibrio anguillarum. Infect Immun 61: 2434-2444.
43. Norqvist, A., Hagström, Å., and Wolf-Watz, H. (1989) Protection of rainbow trout against vibriosis and furunculosis by the use of attenuated strains of Vibrio anguillarum. Appl Environ Microbiol 55: 1400-1405.
44. Norqvist, A., Norrman, B., and Wolf-Watz, H. (1990) Identification and characterization of a zinc metalloprotease associated with invasion by the fish pathogen Vibrio anguillarum. Infect Immun 58: 3731-3736.
45. O'Toole, P.W., Kostrzynska, M., and Trust, T.J. (1994) Non-motile mutants of Helicobacter pylori and Helicobacter mustelae defective in flagellar hook production. Mol Microbiol 14: 691-703.
46. Reed, L.J., and Muench, H. (1938) A simple method of estimating fifty per cent endpoints. Am J Hyg 27: 493-497.
47. Richardson, K. (1991) Roles of motility and flagellar structure in pathogenicity of Vibrio cholera: analysis of motility mutants in three animal models. Infect Immun 59: 2727-2736.
48. Rucker, R.R., Earp, B., and Ordal, E.J. (1953) Infectious diseases of Pacific Salmon. Trans Am Fisheries Soc 83: 307-312.
49. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
50. Sanger, F., Nicklen, S., and Coulson, A.R. (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74: 5463-5467.
51. Schmitt, C.K., Darnell, S.C., Tesh, V.L., Stocker, B.A.D., and O'Brien, A.D. (1994) Mutation of flgM attenuates virulence of Salmonella typhimurium, and mutation of fliA represses the attenuated phenotype. J Bacteriol 176: 368-377.
52. Singer, J.T., Schmidt, K.A., and Reno, P.W. (1991) Polypeptides p40, pOM2, and pAngR are required for iron uptake and for virulence of the marine fish pathogen Vibrio anguillarum 775. J Bacteriol 173: 1347-1352.
53. Toranzo, A.E., Barja, J.L., Colwell, R.R., Hetrick, F.M., and Crosa, J.H. (1983) Haemagglutinating, haemolytic and cytotoxic activities of Vibrio anguillarum and related vibrios isolated from striped bass on the Atlantic coast. FEMS Microbiol Lett 18: 257-262.
54. Totten, P.A., Lara, J.C., and Lory, S. (1990) The rpoN gene product of Pseudomonas aeruginosa is required for expression of diverse genes, including the flagellin gene. J Bacteriol 172: 389-396.
55. Wassenaar, T.M., van der Zeijst, B.A.M., Ayling, R., and Newell, D.G. (1993) Colonisation of chicks by motility mutants of Campylobacter jejuni demonstrates the importance of flagellin A expression. J Gen Microbiol 139: 1171-1175.
56. Yao, R., Burr, D.H., Doig, P., Trust, T.J., Niu, H., and Guerry, P. (1994) Isolation of motile and non-motile insertional mutants of Campylobacter jejuni: the role of motility in adherence and invasion of eukaryotic cells. Mol Microbiol 14: 883-893.