Role of NtrC-regulated exopolysaccharides in the biofilm formation and pathogenic interaction of vibrio vulnificus

Molecular Microbiology

Volumn 74, Issue 2, 2009, Pages 436-453

  Kim, Han Suk ^a   Park, Soon Jung ^b   Lee, Kyu Ho ^a  

^a Hankuk University of Foreign Studies   (South Korea)

^b Yonsei University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

2 OXOGLUTARIC ACID; AMMONIUM CHLORIDE; BACTERIAL PROTEIN; CITRIC ACID; EXOPOLYSACCHARIDE; FRUCTOSE; FUMARIC ACID; GLUCOSE; GLYCEROL; LACTIC ACID; MALIC ACID; MALTOSE; MANNITOL; MANNOSE; NTRC PROTEIN; OXALOACETIC ACID; PYRUVIC ACID; SUCCINIC ACID; TRICARBOXYLIC ACID; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL GENE; BACTERIUM ADHERENCE; BACTERIUM MUTANT; BIOFILM; CARBOHYDRATE SYNTHESIS; CARBON SOURCE; CELL ADHESION; CONTROLLED STUDY; CYTOTOXICITY; EPITHELIUM CELL; FEMALE; GENE CLUSTER; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MORTALITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; VIBRIO VULNIFICUS;

ANIMALS; BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOFILMS; CELL LINE; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GENETIC COMPLEMENTATION TEST; HUMANS; MICE; MICE, INBRED ICR; MULTIGENE FAMILY; MUTATION; POLYSACCHARIDES, BACTERIAL; TRANSCRIPTION FACTORS; VIBRIO VULNIFICUS;

MUS; VIBRIO VULNIFICUS;

EID: 70349928941     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.06875.x     Document Type: Article

References (55)

1. Aslam, S.N., Newman, M.A., Erbs, G., Morrissey, K.L., Chinchilla, D., Boller, T., et al. (2008) Bacterial polysaccharides suppress induced innate immunity by calcium chelation. Curr Biol 18 : 1078 1083.
2. Casper-Lindley, C. Yildiz, F.H. (2004) VpsT is a transcriptional regulator required for expression of vps biosynthesis genes and the development of rugose colonial morphology in Vibrio cholerae O1 El Tor. J Bacteriol 186 : 1574 1578.
3. Chatzidaki-Livanis, M., Jones, M.K. Wright, A.C. (2006) Genetic variation in the Vibrio vulnificus group 1 capsular polysaccharide operon. J Bacteriol 188 : 1987 1998.
4. Chen, C.-Y., Wu, K.-M., Chang, Y.-C., Chang. C.-H., Tsai, H.-C., Liao, T.-L., et al. (2003) Comparative genome analysis of Vibrio vulnificus, a marine pathogen. Genome Res 13 : 2577 2587.
5. Costerton, J.W., Lewandowski, Z., Caldwell, D.E., Korber, D.R. Lappin-Scott, H.M. (1995) Microbial biofilms. Annu Rev Microbiol 49 : 711 745.
6. Cowman, M.K., Slahetka, M.F., Hittner, D.M., Kim, J., Forino, M. Gadelrab, G. (1984) Polyacrylamide-gel electrophoresis and Alcian Blue staining of sulphated glycosaminoglycan oligosaccharides. Biochem J 221 : 707 716.
7. Darnell, C.L., Hussa, E.A. Visick, K.L. (2008) The putative hybrid sensor kinase SypF coordinates biofilm formation in Vibrio fischeri by acting upstream of two response regulators, SypG and VpsR. J Bacteriol 190 : 4941 4950.
8. Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A. Smith, F. (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28 : 350 356.
9. Enos-Berlage, J.L. McCarter, L.L. (2000) Relation of capsular polysaccharide production and colonial cell organization to colony morphology in Vibrio parahaemolyticus. J Bacteriol 182 : 5513 5520.
10. Enos-Berlage, J.L., Guvener, Z.T., Keenan, C.E. McCaeter, L.L. (2005) Genetic determinants of biofilm development of opaque and translucent Vibrio parahaemolyticus. Mol Microbiol 55 : 1160 1182.
11. Friedman, L. Kolter, R. (2004) Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J Bacteriol 186 : 4457 4465.
12. Gilbert, P., Das, J. Foley, I. (1997) Biofilm susceptibility to antimicrobials. Adv Dent Res 11 : 160 167.
13. Goo, S.Y., Lee, H.-J., Kim, W.H., Han, K.-L., Park, D.-K., Lee, H., et al. (2006) Identification of OmpU of Vibrio vulnificus as a fibronectin-binding protein and its role in bacterial pathogenesis. Infect Immun 74 : 5586 5594.
14. Grau, B.L., Henk, M.C. Pettis, G.S. (2005) High-frequency phase variation of Vibrio vulnificus 1003: isolation and characterization of a rugose phenotypic variant. J Bacteriol 187 : 2519 2525.
15. Grau, B.L., Henk, M.C., Garrison, K.L., Olivier, B.J., Schulz, R.M., O'Reilly, K.L. Pettis, G.S. (2008) Further characterization of Vibrio vulnificus rugose exopolysaccharide gene cluster. Infect Immun 76 : 1485 1497.
16. Greenberg, E.P., Hastings, J.W. Ulitzur, S. (1979) Induction of luciferase synthesis in Beneckea harveyi by other marine bacteria. Arch Microbiol 120 : 87 91.
17. Hammer, B.K. Bassler, B.L. (2003) Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol 50 : 101 104.
18. Hayat, U., Reddy, G.P., Bush, C.A., Johnson, J.A., Wright, A.C. Morris, J.G. Jr. (1993) Capsular types of Vibrio vulnificus: an analysis of strains from clinical and environmental sources. J Infect Dis 168 : 758 762.
19. Hickman, J.W. Harwood, C.S. (2008) Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol 69 : 376 389.
20. Jones, M.K., Warner, E.B. Oliver, J.D. (2008) csrA inhibits the formation of biofilms by Vibrio vulnificus. Appl Environ Microbiol 74 : 7064 7066.
21. Joseph, L.A. Wright, A.C. (2004) Expression of Vibrio vulnificus capsular polysaccharide inhibits biofilm formation. J Bacteriol 186 : 889 893.
22. Kim, H.-S., Lee, M.-A., Chun, S.-J., Park, S.-J. Lee, K.-H. (2007) Role of NtrC in biofilm formation via controlling expression of the gene encoding an ADP-glycero-manno-heptose-6-epimerase in the pathogenic bacterium, Vibrio vulnificus. Mol Microbiol 63 : 559 574.
23. Kim, W.H., Goo, S.Y., Shin, M.H., Chun, S.-J., Lee, H., Lee, K.-H. Park, S.-J. (2008) Vibrio vulnificus-induced death of Jurkat T-cells requires activation of p38 mitogen-activated protein kinase by NADPH oxidase-derived reactive oxygen species. Cell Immunol 253 : 81 91.
24. Ledeboer, N.A. Jones, B.D. (2005) Exopolysaccharide sugars contribute to biofilm formation by Salmonella enterica serovar typhimurium on HEp-2 cells and chicken intestinal epithelium. J Bacteriol 187 : 3214 3226.
25. Lee, J.H., Rho, J.-B., Park, K.-J., Kim, C.-B., Han, Y.-S., Choi, S.H., et al. (2004) Role of flagellum and motility in pathogenesis of Vibrio vulnificus. Infect Immun 72 : 4905 4910.
26. Lee, J.H., Rhee, J.E., Park, U., Ju, H.M., Lee, B.C., Kim, T.S., et al. (2007) Identification and functional analysis of Vibrio vulnificus SmcR, a novel global regulator. J Microbiol Biotechnol 17 : 325 334.
27. Lee, V.T., Matewish, J.M., Kessler, J.L., Hyodo, M., Hayakawa, Y. Lory, S. (2007) A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol Microbiol 65 : 1474 1484.
28. Leigh, J.A. Dodsworth, J.A. (2007) Nitrogen regulation in bacteria and archaea. Annu Rev Microbiol 61 : 349 377.
29. Matsukawa, M. Greenberg, E.P. (2004) Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development. J Bacteriol 186 : 4449 4456.
30. Mazmanian, S.K. Kasper, D.L. (2006) The love-hate relationship between bacterial polysaccharides and the host immune system. Nat Rev Immunol 6 : 849 858.
31. Nakhamchik, A., Wilde, C. Rowe-Magnus, D.A. (2007) Identification of a Wzy polymerase required for group IV capsular polysaccharide and lipopolysaccharide biosynthesis in Vibrio vulnificus. Infect Immun 75 : 5550 5558.
32. Nakhamchik, A., Wilde, C. Rowe-Magnus, D.A. (2008) Cyclic-di-GMP regulates extracellular polysaccharide production, biofilm formation, and rugose colony development by Vibrio vulnificus. Appl Environ Microbiol 74 : 4199 4209.
33. Nesper, J., Lauriano, C.M., Klose, K.E., Kapfhammer, D., Kraiss, A. Reidl, J. (2001) Characterization of Vibrio cholerae O1 El tor galU and galE mutants: influence on lipopolysaccharide structure, colonization, and biofilm formation. Infect Immun 69 : 435 445.
34. Nishijyo, T., Haas, D. Itoh, Y. (2001) The CbrA-CbrB two-component regulatory system controls the utilization of multiple carbon and nitrogen sources in Pseudomonas aeruginosa. Mol Microbiol 40 : 917 931.
35. O'Toole, G.A. Kolter, R. (1998) The initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signaling pathways: a genetic analysis. Mol Microbiol 30 : 449 461.
36. S in survival of exponential-phase cells under oxidative stress. J Bacteriol 186 : 3304 3312.
37. Park, N.Y., Lee, J.H., Kim, M.W., Jeong, H.G., Lee, B.C., Kim, T.S. Choi, S.H. (2006) Identification of the Vibrio vulnificus wbpP gene and evaluation of its role in virulence. Infect Immun 74 : 721 728.
38. Powell, J.L., Wright, A.C., Wasserman, S.S., Hone, D.M. Morris, J.G., Jr (1997) Release of tumor necrosis factor alpha in response to Vibrio vulnificus capsular polysaccharide in in vivo and in vitro models. Infect Immun 65 : 3713 3718.
39. Rahn, A., Beis, K., Naismith, J.H. Whitfield, C. (2003) A novel outer membrane protein, Wzi, is involved in surface assembly of the Escherichia coli K30 group 1 capsule. J Bacteriol 185 : 5882 5890.
40. Ramphal, R. Pier, G.B. (1985) Role of Pseudomonas aeruginosa mucoid exopolysaccharide in adherence to tracheal cells. Infect Immun 47 : 1 4.
41. Reitzer, L. (2003) Nitrogen assimilation and global regulation in Escherichia coli. Annu Rev Microbiol 57 : 155 176.
42. Roh, J.B., Lee, M.-A., Lee, H.-J., Kim, S.-M., Cho, Y., Kim, Y.-J., et al. (2006) Transcriptional regulatory cascade for elastase production in Vibrio vulnificus: LuxO activates luxT expression and LuxT represses smcR expression. J Biol Chem 281 : 34775 34784.
43. Ruby, E.G. Lee, K.-H. (1998) The Vibrio fischeri-Euprymna scolopes light organ association: current ecological paradigms. Appl Environ Microbiol 64 : 805 812.
44. Ruby, E.G. Nealson, K.H. (1977) Pyruvate production and excretion by the luminous marine bacteria. Appl Environ Microbiol 34 : 164 169.
45. Sadykov, M.R., Olson, M.E., Halouska, S., Zhu, Y., Fey, P.D., Powers, R. Somerville, G.A. (2008) Tricarboxylic acid cycle-dependent regulation of Staphylococcus epidermidis polysaccharide intercellular adhesion synthesis. J Bacteriol 190 : 7621 7632.
46. Sakuragi, Y. Kolter, R. (2007) Quorum-sensing regulation of the biofilm matrix genes (pel) of Pseudomonas aeruginosa. J Bacteriol 189 : 5383 5386.
47. Sambrook, J. Russell, D.W. (2001) Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor : Cold Spring. Harbor Laboratory Press.
48. Strom, M.S. Paranjpye, R.N. (2000) Epidemiology and pathogenesis of Vibrio vulnificus. Microbes Infect 2 : 177 188.
49. Sutherland, I.W. (2001) Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147 : 3 9.
50. Whitfield, C. (2006) Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 75 : 39 68.
51. Whitfield, C. Paiment, A. (2003) Biosynthesis and assembly of Group 1 capsular polysaccharide in Escherichia coli and related extracellular polysaccharides in other bacteria. Carbohydr Res 338 : 2491 2502.
52. Wright, A.C., Simpson, L.M., Oliver, J.D. Morris, J.G., Jr (1990) Phenotypic evaluation of acapsular transposon mutans of Vibrio vulnificus. Infect Immun 58 : 1769 1773.
53. Yildiz, F.H. Visick, K.L. (2009) Vibrio biofilms: so much the same yet so different. Trends Microbiol 17 : 109 118.
54. ET-associated phenotypes in Vibrio cholerae O1 El Tor. J Bacteriol 183 : 1716 1726.
55. Yoshida, S., Ogawa, M. Mizuguchi, Y. (1985) Relation of capsular materials and colony opacity to virulence of Vibrio vulnificus. Infect Immun 47 : 446 451.