The Campylobacter jejuni dccRS two-component system is required for optimal in vivo colonization but is dispensable for in vitro growth

Molecular Microbiology

Volumn 54, Issue 5, 2004, Pages 1269-1286

  MacKichan, Joanna K ^a,e   Gaynor, Erin C ^a,b   Chang, Christopher ^c   Cawthraw, Shaun ^d   Newell, Diane G ^d   Miller, Jeff F ^c   Falkow, Stanley ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d VETERINARY LABORATORIES AGENCY   (United Kingdom)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HISTIDINE; MEMBRANE PROTEIN; PERIPLASMIC PROTEIN; PHOSPHOTRANSFERASE; PROTEIN DCCR; PROTEIN DCCS; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; CAMPYLOBACTER JEJUNI; CHICKEN; CONTROLLED STUDY; DCCRS GENE; DIARRHEA; DNA MICROARRAY; DNA SEQUENCE; FEMALE; HELICOBACTER; HEMOLYSIS; HISTOPATHOLOGY; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DNA INTERACTION; SCID MOUSE; SIGNAL TRANSDUCTION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BACTERIAL PROTEINS; CAMPYLOBACTER INFECTIONS; CAMPYLOBACTER JEJUNI; CHICKENS; CONSERVED SEQUENCE; DNA-BINDING PROTEINS; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HELICOBACTER; MEMBRANE PROTEINS; MICE; MICE, SCID; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PERIPLASMIC PROTEINS; PHENOTYPE; PROMOTER REGIONS (GENETICS); REGULON; SIGNAL TRANSDUCTION; VIRULENCE; VIRULENCE FACTORS;

ANIMALIA; BACTERIA (MICROORGANISMS); CAMPYLOBACTER; CAMPYLOBACTER JEJUNI; GALLUS GALLUS; HELICOBACTER;

EID: 9644277148     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2004.04371.x     Document Type: Article

References (49)

1. Albright, L.M., Huala, E., and Ausubel, F.M. (1989) Prokaryotic signal transduction mediated by sensor and regulator protein pairs. Annu Rev Genet 23: 311-336.
2. Alm, R.A., Ling, L.S., Moir, D.T., King, B.L, Brown, E.D., Doig, P.C., et al. (1999) Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397: 176-180.
3. Andersen, C., Hughes, C., and Koronakis, V. (2000) Chunnel vision. Export and efflux through bacterial channel-tunnels. EMBO Rep 1: 313-318.
4. Andersen, C., Hughes, C., and Koronakis, V. (2001) Protein export and drug efflux through bacterial channel-tunnels. Curr Opin Cell Biol 13: 412-416.
5. Barrett, J.P., and Hoch, J.A. (1998) Two-component signal transduction as a target for microbial anti-infective therapy. Antimicrob Agents Chemother 42: 1529-1536.
6. Beier, D., and Frank, R. (2000) Molecular characterization of two-component systems of Helicobacter pylori. J Bacteriol 182: 2068-2076.
7. Bereswill, S., and Kist, M. (2003) Recent developments in Campylobacter pathogenesis. Curr Opin Infect Dis 16: 487-491.
8. Black, R.E., Levine, M.M., Clements, M.L, Hughes, T.P., and Blaser, M.J. (1988) Experimental Campylobacter jejuni infection in humans. J Infect Dis 157: 472-479.
9. Brás, A.M., Chatterjee, S., Wren, B.W., Newell, D.G., and Ketley, J.M. (1999) A novel Campylobacter jejuni two-component regulatory system important for temperature-dependent growth and colonization. J Bacteriol 181: 3298-3302.
10. Braun, V., Schonherr, R., and Hobbie, S. (1993) Enterobacterial hemolysins: activation, secretion and pore formation. Trends Microbiol 1: 211-216.
11. Cawthraw, S., Ayling, R., Nuijten, P., Wassenaar, T., and Newell, D.G. (1994) Isotype, specificity, and kinetics of systemic and mucosal antibodies to Campylobacter jejuni antigens, including flagellin, during experimental oral infections of chickens. Avian Diseases 38: 341-349.
12. Eisen, M.B., Spellman, P.T., Brown, P.O., and Botstein, D. (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95: 14863-14868.
13. Gaynor, E.G., Cawthraw, S., Manning, G., MacKichan, J.K., Falkow, S., and Newell, D.G. (2004) The genome-sequenced variant of Campylobacter jejuni NCTC 11168 and the original clonal clinical isolate differ markedly in colonization, gene expression, and virulence-associated phenotypes. J Bacteriol 186: 503-517.
14. Grant, K.A., Belandia, I.U., Dekker, N., Richardson, P.T., and Park, S.F. (1997) Molecular characterization of pldA, the structural gene for a phospholipase A from Campylobacter coli, and its contribution to cell-associated hemolysis. Infect Immun 65: 1172-1180.
15. Hagihara, B., Matsubara, H., Nakai, M., and Okunuki, K. (1958) Crystalline bacterial proteinase. J Biochem (Tokyo) 45: 185-194.
16. Higgins, D.G., and Sharp, P.M. (1988) CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 73: 237-244.
17. Hitchcock, P.J., and Brown, T.M. (1983) Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J Bacteriol 154: 269-277.
18. Karlyshev, A.V., and Wren, B.W. (2001) Detection and initial characterization of novel capsular polysaccharide among diverse Campylobacter jejuni strains using alcian blue dye. J Clin Microbiol 39: 279-284.
19. Karlyshev, A.V., Linton, D., Gregson, N.A., Lastovica, A.J., and Wren, B.W. (2000) Genetic and biochemical evidence of a Campylobacter jejuni capsular polysaccharide that accounts for Penner serotype specificity. Mol Microbiol 35: 529-541.
20. Korlath, J.A., Osterholm, M.T., Judy, L.A., Forfang, J.C., and Robinson, R.A. (1985) A point-source outbreak of campylobacteriosis associated with consumption of raw milk. J Infect Dis 152: 592-596.
21. Koronakis, V., Sharff, A., Koronakis, E., Luisi, B., and Hughes, C. (2000) Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405: 914-919.
22. Leonard, E.E., 2nd, Takata, T., Blaser, M.J., Falkow, S., Tompkins, L.S., and Gaynor, E.G. (2003) Use of an open-reading frame-specific Campylobacter jejuni DNA microarray as a new genotyping tool for studying epidemiologically related isolates. J Infect Dis 187: 691-694.
23. Merrell, D.S., Thompson, L.J., Kim, C.C., Mitchell, H., Tompkins, L.S., Lee, A., et al. (2003) Growth phase-dependent response of Helicobacter pylori to iron starvation. Infect Immun 71: 6510-6525.
24. Misawa, N., Hirayama, K., Itoh, K., and Takahashi, E. (1995) Detection of alpha- and beta-hemolytic-like activity from Campylobacter jejuni. J Clin Microbiol 33: 729-731.
25. Panthel, K., Dietz, P., Haas, R., and Beier, D. (2003) Two-component systems of Helicobacter pylori contribute to virulence in a mouse infection model. Infect Immun 71: 5381-5385.
26. Park, S.F. (2002) The physiology of Campylobacter species and its relevance to their role as foodborne pathogens. Int J Food Microbiol 74: 177-188.
27. Parkhill, J., Wren, B.W., Mungall, K., Ketley, J.M., Churcher, C., Basham, D., et al. (2000) The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403: 665-668.
28. Richardson, P.T., and Park, S.F. (1995) Enterochelin acquisition in Campylobacter coli: characterization of components of a binding-protein- dependent transport system. Microbiology 141: 3181-3191.
29. Rutherford, K., Parkhill, J., Crook, J., Horsnell, T., Rice, P., Rajandream, M.A., et al. (2000) Artemis: sequence visualization and annotation. Bioinformatics 16: 944-945.
30. Salama, N., Guillemin, K., McDaniel, T.K., Sherlock, G., Tompkins, L., and Falkow, S. (2000) A whole-genome microarray reveals genetic diversity among Helicobacter pylori strains. Proc Natl Acad Sci USA 97: 14668-14673.
31. Schultz, J., Copley, R.R., Doerks, T., Porting, C.P., and Bork, P. (2000) SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res 28: 231-234.
32. Sharff, A., Fanutti, C., Shi, J., Calladine, C., and Luisi, B. (2001) The role of the TolC family in protein transport and multidrug efflux. From stereochemical certainty to mechanistic hypothesis. Eur J Biochem 268: 5011-5026.
33. Stock, A.M., Robinson, V.L., and Goudreau, P.M. (2000) Two-component signal transduction. Annu Rev Biochem 69: 183-215.
34. Suerbaum, S., Josenhans, C., Sterzenbach, T., Drescher, B., Brandt, P., Bell, M., et al. (2003) The complete genome sequence of the carcinogenic bacterium Helicobacter hepaticus. Proc Natl Acad Sci USA 100: 7901-7906.
35. Throup, J.P., Koretke, K.K., Bryant, A.P., Ingraham, K.A., Chalker, A.F., Ge, Y., et al. (2000) A genomic analysis of two-component signal transduction in Streptococcus pneumoniae. Mol Microbiol 35: 566-576.
36. Tomb, J.F., White, O., Kerlavage, A.R., Clayton, R.A., Sutton, G.G., Fleischmann, R.D., et al. (1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388: 539-547.
37. Tsai, C.M., and Frasch, C.E. (1982) A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem 119: 115-119.
38. Tsang, R.S. (2002) The relationship of Campylobacter jejuni infection and the development of Guillain-Barre syndrome. Curr Opin Infect Dis 15: 221-228.
39. Tusher, V.G., Tibshirani, R., and Chu, G. (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116-5121.
40. Valdivia, R.H., and Falkow, S. (1996) Bacterial genetics by flow cytometry: rapid isolation of Salmonella typhimurium acid-inducible promoters by differential fluorescence induction. Mol Microbiol 22: 367-378.
41. Valdivia, R.H., and Falkow, S. (1997) Fluorescence-based isolation of bacterial genes expressed within host cells. Science 277: 2007-2011.
42. Van Vliet, A.M., Wood, A., Henderson, J., Wooldridge, K., and Ketley, J.M. (1997) Genetic manipulation of enteric Campylobacter species. Method Microbiol 27: 407-419.
43. Wassenaar, T.M. (1997) Toxin production by Campylobacter spp. Clin Microbiol Rev 10: 466-476.
44. Wassenaar, T.M., and Blaser, M.J. (1999) Pathophysiology of Campylobacter jejuni infections of humans. Microbes Infect 1: 1023-1033.
45. Wassenaar, T.M., van der Zeijst, B.A., Ayling, R., and Newell, D.G. (1993) Colonization of chicks by motility mutants of Campylobacter jejuni demonstrates the importance of flagellin A expression. J Gen Microbiol 139: 1171-1175.
46. Wosten, M.M., Boeve, M., Koot, M.G., van Nuene, A.C., and van der Zeijst, B.A. (1998) Identification of Campylobacter jejuni promoter sequences. J Bacteriol 180: 594-599.
47. Wren, B.W., Stabler, R.A., Das, S.S., Butcher, P.D., Mangan, J.A., Clarke, J.D., et al. (1998) Characterization of a haemolysin from Mycobacterium tuberculosis with homology to a virulence factor of Serpulina hyodysenteriae. Microbiology 144: 1205-1211.
48. Yao, R., Alm, R.A., Trust, T.J., and Guerry, P. (1993) Construction of new Campylobacter cloning vectors and a new mutational cat cassette. Gene 130: 127-130.
49. Ziprin, R.L., Young, C.R., Byrd, J.A., Stanker, L.H., Hume, M.E., Gray, S.A., et al. (2001) Role of Campylobacter jejuni potential virulence genes in cecal colonization. Avian Diseases 45: 549-557.