Contribution of six flagellin genes to the flagellum biogenesis of Vibrio vulnificus and in vivo invasion

Infection and Immunity

Volumn 82, Issue 1, 2014, Pages 29-42

  Kim, Soo Young ^a   Thanh, Xuan Tran Thi ^a   Jeong, Kwangjoon ^a,b   Kim, Seong Bin ^a   Pan, Sang O ^c   Jung, Che Hun ^c   Hong, Seol Hee ^a,c   Lee, Shee Eun ^a,c   Rhee, Joon Haeng ^a,b  

^a Chonnam National University Research Institute of Medical Sciences   (South Korea)

^b Chonnam National University Medical School   (South Korea)

^c Chonnam National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; FLAGELLIN; GLUTATHIONE TRANSFERASE; RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM ADHERENCE; BACTERIUM CULTURE; BIOGENESIS; COLONY FORMING UNIT; CULTURE MEDIUM; CYTOTOXICITY; DELETION MUTANT; ESCHERICHIA COLI; FLAA GENE; FLAB GENE; FLAC GENE; FLAD GENE; FLAE GENE; FLAF GENE; GENE LOCUS; GENE SEQUENCE; GENOTYPE; HELA CELL; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IN VIVO STUDY; LD 50; MOUSE; NONHUMAN; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; TWO DIMENSIONAL GEL ELECTROPHORESIS; VIBRIO VULNIFICUS;

EID: 84890820924     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00654-13     Document Type: Article

References (45)

1. Jones MK, Oliver JD. 2009. Vibrio vulnificus: disease and pathogenesis. Infect. Immun. 77:1723-1733. http://dx.doi.org/10.1128/IAI.01046-08.
2. Wright AC, Powell JL, Tanner MK, Ensor LA, Karpas AB, Morris JG, Jr, Sztein MB. 1999. Differential expression of Vibrio vulnificus capsular polysaccharide. Infect. Immun. 67:2250-2257.
3. Kim YR, Kim BU, Kim SY, Kim CM, Na HS, Koh JT, Choy HE, Rhee JH, Lee SE. 2010. Outer membrane vesicles of Vibrio vulnificus deliver cytolysinhemolysin VvhA into epithelial cells to induce cytotoxicity. Biochem. Biophys. Res. Commun. 399:607-612. http://dx.doi.org/10.1016/j.bbrc.2010.07.122.
4. Kim YR, Lee SE, Kang IC, Nam KI, Choy HE, Rhee JH. 2013. A bacterial RTX toxin causes programmed necrotic cell death through calciummediated mitochondrial dysfunction. J. Infect. Dis. 207:1406-1415. http://dx.doi.org/10.1093/infdis/jis746.
5. Kim YR, Lee SE, Kook H, Yeom JA, Na HS, Kim SY, Chung SS, Choy HE, Rhee JH. 2008. Vibrio vulnificus RTX toxin kills host cells only after contact of the bacteria with host cells. Cell. Microbiol. 10:848-862. http://dx.doi.org/10.1111/j.1462-5822.2007.01088.x.
6. Kim YR, Rhee JH. 2003. Flagellar basal body flg operon as a virulence determinant of Vibrio vulnificus. Biochem. Biophys. Res. Commun. 304: 405-410. http://dx.doi.org/10.1016/S0006-291X(03)00613-2.
7. Lee JH, Rho JB, Park KJ, Kim CB, Han YS, Choi SH, Lee KH, Park SJ. 2004. Role of flagellumandmotility in pathogenesis of Vibrio vulnificus. Infect.Immun. 72:4905-4910. http://dx.doi.org/10.1128/IAI.72.8.4905-4910.2004.
8. Doetsch RN, Sjoblad RD. 1980. Flagellar structure and function in eubacteria. Annu. Rev. Microbiol. 34:69-108. http://dx.doi.org/10.1146/annurev.mi.34.100180.000441.
9. McCarter LL. 2006. Regulation of flagella. Curr. Opin. Microbiol. 9:180-186. http://dx.doi.org/10.1016/j.mib.2006.02.001.
10. Samatey FA, Imada K, Nagashima S, Vonderviszt F, Kumasaka T, Yamamoto M, Namba K. 2001. Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature 410:331-337. http://dx.doi.org/10.1038/35066504.
11. Namba K, Yamashita I, Vonderviszt F. 1989. Structure of the core and central channel of bacterial flagella. Nature 342:648-654. http://dx.doi.org/10.1038/342648a0.
12. Alley MR, Maddock JR, Shapiro L. 1992. Polar localization of a bacterial chemoreceptor. Genes Dev. 6:825-836. http://dx.doi.org/10.1101/gad.6.5.825.
13. Arora SK, Ritchings BW, Almira EC, Lory S, Ramphal R. 1997. A transcriptional activator, FleQ, regulates mucin adhesion and flagellar gene expression in Pseudomonas aeruginosa in a cascade manner. J. Bacteriol. 179:5574-5581.
14. Konkel ME, Klena JD, Rivera-Amill V, Monteville MR, Biswas D, Raphael B, Mickelson J. 2004. Secretion of virulence proteins from Campylobacter jejuni is dependent on a functional flagellar export apparatus. J. Bacteriol. 186:3296-3303. http://dx.doi.org/10.1128/JB.186.11.3296-3303.2004.
15. Young GM, Schmiel DH, Miller VL. 1999. A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system. Proc. Natl. Acad. Sci. U.S.A. 96:6456-6461. http://dx.doi.org/10.1073/pnas.96.11.6456.
16. Ramos HC, Rumbo M, Sirard JC. 2004. Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol. 12:509-517. http://dx.doi.org/10.1016/j.tim.2004.09.002.
17. Arora SK, Ritchings BW, Almira EC, Lory S, Ramphal R. 1998. The Pseudomonas aeruginosa flagellar cap protein, FliD, is responsible for mucin adhesion. Infect. Immun. 66:1000-1007.
18. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, Goodlett DR, Eng Akira JKS, Underhill DM, Aderem A. 2001. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410:1099-1103. http://dx.doi.org/10.1038/35074106.
19. Lee SE, Kim SY, Jeong BC, Kim YR, Bae SJ, Ahn OS, Lee JJ, Song HC, Kim JM, Choy HE, Chung SS, Kweon MN, Rhee JH. 2006. A bacterial flagellin, Vibrio vulnificus FlaB, has a strong mucosal adjuvant activity to induce protective immunity. Infect. Immun. 74:694-702. http://dx.doi.org/10.1128/IAI.74.1.694-702.2006.
20. Wallich R, Moter SE, Simon MM, Ebnet K, Heiberger A, Kramer MD. 1990. The Borrelia burgdorferi flagellum-associated 41-kilodalton antigen (flagellin): molecular cloning, expression, and amplification of the gene. Infect. Immun. 58:1711-1719.
21. Kuwajima G, Asaka J, Fujiwara T, Node K, Kondo E. 1986. Nucleotide sequence of the hag gene encoding flagellin of Escherichia coli. J. Bacteriol. 168:1479-1483.
22. Lövgren A, Zhang MY, Engstrom A, Landen R. 1993. Identification of two expressed flagellin genes in the insect pathogen Bacillus thuringiensis subsp. alesti. J. Gen. Microbiol. 139:21-30. http://dx.doi.org/10.1099/00221287-139-1-21.
23. Nuijten PJ, van Asten FJ, Gaastra W, van der Zeijst BA. 1990. Structural and functional analysis of two Campylobacter jejuni flagellin genes. J. Biol. Chem. 265:17798-17804.
24. McCarter LL. 2001. Polar flagellar motility of the Vibrionaceae. Microbiol. Mol. Biol. Rev. 65:445-462. http://dx.doi.org/10.1128/MMBR.65.3.445-462.2001.
25. Wilson DR, Beveridge TJ. 1993. Bacterial flagellar filaments and their component flagellins. Can. J. Microbiol. 39:451-472.
26. Kim HU, Kim SY, Jeong H, Kim TY, Kim JJ, Choy HE, Yi KY, Rhee JH, Lee SY. 2011. Integrative genome-scale metabolic analysis of Vibrio vulnificus for drug targeting and discovery. Mol. Syst. Biol. 7:460. http://dx.doi.org/10.1038/msb.2010.115.
27. Morrison SS, Williams T, Cain A, Froelich B, Taylor C, Baker-Austin C, Verner-Jeffreys D, Hartnell R, Oliver JD, Gibas CJ. 2012. Pyrosequencing-based comparative genome analysis of Vibrio vulnificus environmental isolates. PLoS One 7:e37553. http://dx.doi.org/10.1371/journal.pone.0037553.
28. Jeong BC, Kim SY, Choi BH, Park MS, Lee JJ, Rhee JH, Lee SE. 2005. A bacterial flagellin, Vibrio vulnificus FlaB, induces human dendritic cell maturation. J. Bacteriol. Virol. 35:209-216.
29. Brett PJ, Mah DC, Woods DE. 1994. Isolation and characterization of Pseudomonas pseudomallei flagellin proteins. Infect. Immun. 62:1914-1919.
30. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408. http://dx.doi.org/10.1006/meth.2001.1262.
31. Kim YR, Lee SE, Kim CM, Kim SY, Shin EK, Shin DH, Chung SS, Choy HE, Progulske-Fox A, Hillman JD, Handfield M, Rhee JH. 2003. Characterization and pathogenic significance of Vibrio vulnificus antigens preferentially expressed in septicemic patients. Infect. Immun. 71:5461-5471. http://dx.doi.org/10.1128/IAI.71.10.5461-5471.2003.
32. Milton DL, O'Toole R, Horstedt P, Wolf-Watz H. 1996. Flagellin A is essential for the virulence of Vibrio anguillarum. J. Bacteriol. 178:1310-1319.
33. Kim SY, Lee SE, Kim YR, Kim CM, Ryu PY, Choy HE, Chung SS, Rhee JH. 2003. Regulation of Vibrio vulnificus virulence by the LuxS quorumsensing system. Mol. Microbiol. 48:1647-1664. http://dx.doi.org/10.1046/j.1365-2958.2003.03536.x.
34. Kokotek W, Lotz W. 1989. Construction of a lacZ-kanamycin-resistance cassette, useful for site-directed mutagenesis and as a promoter probe. Gene 84:467-471. http://dx.doi.org/10.1016/0378-1119(89)90522-2.
35. Miller JH. 1992. A short course in bacterial genetics; a laboratory manual and handbook for Escherichia coli and related bacteria. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
36. Ditta G, Stanfield S, Corbin D, Helinski DR. 1980. Broad host range DNA cloning system for gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proc. Natl. Acad. Sci. U.S.A. 77:7347-7351. http://dx.doi.org/10.1073/pnas.77.12.7347.
37. Lee J, Mo JH, Katakura K, Alkalay I, Rucker AN, Liu YT, Lee HK, Shen C, Cojocaru G, Shenouda S, Kagnoff M, Eckmann L, Ben-Neriah Y, RazE. 2006. Maintenance of colonic homeostasis by distinctive apical TLR9 signalling in intestinal epithelial cells. Nat. Cell Biol. 8:1327-1336. http://dx.doi.org/10.1038/ncb1500.
38. Kim YK, McCarter LL. 2000. Analysis of the polar flagellar gene system of Vibrio parahaemolyticus. J. Bacteriol. 182:3693-3704. http://dx.doi.org/10.1128/JB.182.13.3693-3704.2000.
39. Klose KE, Mekalanos JJ. 1998. Differential regulation of multiple flagellins in Vibrio cholerae. J. Bacteriol. 180:303-316.
40. McGee K, Horstedt P, Milton DL. 1996. Identification and characterization of additional flagellin genes from Vibrio anguillarum. J. Bacteriol. 178:5188-5198.
41. Millikan DS, Ruby EG. 2004. Vibrio fischeri flagellin A is essential for normal motility and for symbiotic competence during initial squid light organ colonization. J. Bacteriol. 186:4315-4325. http://dx.doi.org/10.1128/JB.186.13.4315-4325.2004.
42. Gulig PA, Tucker MS, Thiaville PC, Joseph JL, Brown RN. 2009. USER friendly cloning coupled with chitin-based natural transformation enables rapid mutagenesis of Vibrio vulnificus. Appl. Environ. Microbiol. 75: 4936-4949. http://dx.doi.org/10.1128/AEM.02564-08.
43. Poole MD, Oliver JD. 1978. Experimental pathogenicity and mortality in ligated ileal loop studies of the newly reported halophilic lactose-positive Vibrio sp. Infect. Immun. 20:126-129.
44. Chung KJ, Cho EJ, Kim MK, Kim YR, Kim SH, Yang HY, Chung KC, Lee SE, Rhee JH, Choy HE, Lee TH. 2010. RtxA1-induced expression of the small GTPase Rac2 plays a key role in the pathogenicity of Vibrio vulnificus. J. Infect. Dis. 201:97-105. http://dx.doi.org/10.1086/648612.
45. Miller VL, Mekalanos JJ. 1988. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170:2575-2583.