Amino-terminal residues dictate the export efficiency of the Campylobacter jejuni filament proteins via the flagellum

Molecular Microbiology

Volumn 76, Issue 4, 2010, Pages 918-931

  Neal Mckinney, Jason M ^a   Christensen, Jeffrey E ^a   Konkel, Michael E ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FILAMENT PROTEIN; FLAGELLIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR; FLAA PROTEIN, BACTERIA; FLAB FLAGELLIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL VIRULENCE; CAMPYLOBACTER JEJUNI; ESCHERICHIA COLI; GENETIC CONSERVATION; HELICOBACTER PYLORI; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN TRANSPORT; SALMONELLA TYPHIMURIUM; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; TYPE III SECRETION SYSTEM; VIBRIO CHOLERAE; YERSINIA ENTEROCOLITICA; AMINO ACID SEQUENCE; FLAGELLUM; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PROTEIN TERTIARY STRUCTURE;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI; ESCHERICHIA COLI; HELICOBACTER PYLORI; SALMONELLA TYPHIMURIUM; VIBRIO CHOLERAE; YERSINIA ENTEROCOLITICA;

AMINO ACID SEQUENCE; CAMPYLOBACTER JEJUNI; FLAGELLA; FLAGELLIN; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT;

EID: 77952184560     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07144.x     Document Type: Article

References (41)

1. Abramoff, M.D., Magelhaes, P.J. Ram, S.J. (2004) Image processing with Image J. Biophotonics Int 11 : 36 42.
2. Andersen-Nissen, E., Smith, K.D., Strobe, K.L., Barrett, S.L., Cookson, B.T., Logan, S.M. Aderem, A. (2005) Evasion of Toll-like receptor 5 by flagellated bacteria. Proc Natl Acad Sci USA 102 : 9247 9252.
3. Badea, L., Beatson, S.A., Kaparakis, M., Ferrero, R.L. Hartland, E.L. (2009) Secretion of flagellin by the LEE-encoded type III secretion system of enteropathogenic Escherichia coli. BMC Microbiol 9 : 30.
4. Brown, J.D., Saini, S., Aldridge, C., Herbert, J., Rao, C.V. Aldridge, P.D. (2008) The rate of protein secretion dictates the temporal dynamics of flagellar gene expression. Mol Microbiol 70 : 924 937.
5. Carrillo, C.D., Taboada, E., Nash, J.H., Lanthier, P., Kelly, J., Lau, P.C., et al. (2004) Genome-wide expression analyses of Campylobacter jejuni NCTC11168 reveals coordinate regulation of motility and virulence by flhA. J Biol Chem 279 : 20327 20338.
6. Christensen, J.E., Pacheco, S.A. Konkel, M.E. (2009) Identification of a Campylobacter jejuni secreted protein required for maximal invasion of host cells. Mol Microbiol 73 : 650 662.
7. Cornelis, G.R. (2006) The type III secretion injectisome. Nat Rev Microbiol 4 : 811 825.
8. Desvaux, M., Hebraud, M., Henderson, I.R. Pallen, M.J. (2006) Type III secretion: what's in a name? Trends Microbiol 14 : 157 160.
9. Galkin, V.E., Yu, X., Bielnicki, J., Heuser, J., Ewing, C.P., Guerry, P. Egelman, E.H. (2008) Divergence of quaternary structures among bacterial flagellar filaments. Science 320 : 382 385.
10. Gazi, A.D., Charova, S.N., Panopoulos, N.J. Kokkinidis, M. (2009) Coiled-coils in type III secretion systems: structural flexibility, disorder and biological implications. Cell Microbiol 11 : 719 729.
11. Grant, C.C., Konkel, M.E., Cieplak, W., Jr. Tompkins, L.S. (1993) Role of flagella in adherence, internalization, and translocation of Campylobacter jejuni in nonpolarized and polarized epithelial cell cultures. Infect Immun 61 : 1764 1771.
12. Guerry, P. (2007) Campylobacter flagella: not just for motility. Trends Microbiol 15 : 456 461.
13. Guerry, P., Alm, R.A., Power, M.E., Logan, S.M. Trust, T.J. (1991) Role of two flagellin genes in Campylobacter motility. J Bacteriol 173 : 4757 4764.
14. Gugolya, Z., Muskotal, A., Sebestyen, A., Dioszeghy, Z. Vonderviszt, F. (2003) Interaction of the disordered terminal regions of flagellin upon flagellar filament formation. FEBS Lett 535 : 66 70.
15. Jagannathan, A., Constantinidou, C. Penn, C.W. (2001) Roles of rpoN, fliA, and flgR in expression of flagella in Campylobacter jejuni. J Bacteriol 183 : 2937 2942.
16. Komoriya, K., Shibano, N., Higano, T., Azuma, N., Yamaguchi, S. Aizawa, S.I. (1999) Flagellar proteins and type III-exported virulence factors are the predominant proteins secreted into the culture media of Salmonella typhimurium. Mol Microbiol 34 : 767 779.
17. Konkel, M.E., Kim, B.J., Rivera-Amill, V. Garvis, S.G. (1999) Bacterial secreted proteins are required for the internalization of Campylobacter jejuni into cultured mammalian cells. Mol Microbiol 32 : 691 701.
18. Konkel, M.E., Monteville, M.R., Rivera-Amill, V. Joens, L.A. (2001) The pathogenesis of Campylobacter jejuni-mediated enteritis. Curr Issues Intest Microbiol 2 : 55 71.
19. Konkel, M.E., Klena, J.D., Rivera-Amill, V., Monteville, M.R., 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.
20. Kuwajima, G. (1988) Construction of a minimum-size functional flagellin of Escherichia coli. J Bacteriol 170 : 3305 3309.
21. Larson, C.L., Christensen, J.E., Pacheco, S.A., Minnich, S.A. Konkel, M. (2008) Campylobacter jejuni secretes proteins via the flagellar type III secretion system that contribute to host cell invasion and gastroenteritis. In Campylobacter. Nachamkin, I., Szymanski, C.M. Blaser, M.J. (eds).
22. Lee, S.H. Galan, J.E. (2004) Salmonella type III secretion-associated chaperones confer secretion-pathway specificity. Mol Microbiol 51 : 483 495.
23. Lloyd, S.A., Norman, M., Rosqvist, R. Wolf-Watz, H. (2001) Yersinia YopE is targeted for type III secretion by N-terminal, not mRNA, signals. Mol Microbiol 39 : 520 531.
24. Minamino, T. Namba, K. (2004) Self-assembly and type III protein export of the bacterial flagellum. J Mol Microbiol Biotechnol 7 : 5 17.
25. Muskotal, A., Kiraly, R., Sebestyen, A., Gugolya, Z., Vegh, B.M. Vonderviszt, F. (2006) Interaction of FliS flagellar chaperone with flagellin. FEBS Lett 580 : 3916 3920.
26. Namba, K., Yamashita, I. Vonderviszt, F. (1989) Structure of the core and central channel of bacterial flagella. Nature 342 : 648 654.
27. Ozin, A.J., Claret, L., Auvray, F. Hughes, C. (2003) The FliS chaperone selectively binds the disordered flagellin C-terminal D0 domain central to polymerisation. FEMS Microbiol Lett 219 : 219 224.
28. Ramamurthi, K.S. Schneewind, O. (2002) Yersinia enterocolitica type III secretion: mutational analysis of the yopQ secretion signal. J Bacteriol 184 : 3321 3328. (Pubitemid 34568942) (Pubitemid 34568942)
29. Raphael, B.H., Pereira, S., Flom, G.A., Zhang, Q., Ketley, J.M. Konkel, M.E. (2005) The Campylobacter jejuni response regulator, CbrR, modulates sodium deoxycholate resistance and chicken colonization. J Bacteriol 187 : 3662 3670.
30. Ruiz-Palacios, G.M. (2007) The health burden of Campylobacter infection and the impact of antimicrobial resistance: playing chicken. Clin Infect Dis 44 : 701 703.
31. Samatey, F.A., 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.
32. Schmiel, D.H., Wagar, E., Karamanou, L., Weeks, D. Miller, V.L. (1998) Phospholipase A of Yersinia enterocolitica contributes to pathogenesis in a mouse model. Infect Immun 66 : 3941 3951.
33. Sory, M.P., Boland, A., Lambermont, I. Cornelis, G.R. (1995) Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach. Proc Natl Acad Sci USA 92 : 11998 12002.
34. Sun, Y.H., Rolan, H.G. Tsolis, R.M. (2007) Injection of flagellin into the host cell cytosol by Salmonella enterica serotype Typhimurium. J Biol Chem 282 : 33897 33901.
35. Tascon, R.I., Rodriguez-Ferri, E.F., Gutierrez-Martin, C.B., Rodriguez-Barbosa, I., Berche, P. Vazquez-Boland, J.A. (1993) Transposon mutagenesis in Actinobacillus pleuropneumoniae with a Tn10 derivative. J Bacteriol 175 : 5717 5722.
36. Vegh, B.M., Gal, P., Dobo, J., Zavodszky, P. Vonderviszt, F. (2006) Localization of the flagellum-specific secretion signal in Salmonella flagellin. Biochem Biophys Res Commun 345 : 93 98.
37. Vonderviszt, F., Kanto, S., Aizawa, S. Namba, K. (1989) Terminal regions of flagellin are disordered in solution. J Mol Biol 209 : 127 133.
38. Wassenaar, T.M., Bleumink-Pluym, N.M. van der Zeijst, B.A. (1991) Inactivation of Campylobacter jejuni flagellin genes by homologous recombination demonstrates that flaA but not flaB is required for invasion. EMBO J 10 : 2055 2061.
39. Yao, R., Alm, R.A., Trust, T.J. Guerry, P. (1993) Construction of new Campylobacter cloning vectors and a new mutational cat cassette. Gene 130 : 127 130.
40. Yonekura, K., Maki-Yonekura, S. Namba, K. (2003) Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424 : 643 650.
41. Yoshioka, K., Aizawa, S. Yamaguchi, S. (1995) Flagellar filament structure and cell motility of Salmonella typhimurium mutants lacking part of the outer domain of flagellin. J Bacteriol 177 : 1090 1093.