The Campylobacter jejuni stringent response controls specific stress survival and virulence-associated phenotypes

Molecular Microbiology

Volumn 56, Issue 1, 2005, Pages 8-27

  Gaynor, Erin C ^a,b   Wells, Derek H ^a   MacKichan, Joanna K ^a   Falkow, Stanley ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; CARBON DIOXIDE; CHLORAMPHENICOL; COMPLEMENTARY DNA; GENOMIC DNA; KANAMYCIN; OXYGEN; RIFAMPICIN; RNA; RNA POLYMERASE; TRIMETHOPRIM; VANCOMYCIN;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BACTERIUM CULTURE; BACTERIUM MUTANT; CAMPYLOBACTER JEJUNI; CELL STRAIN CACO 2; DIARRHEA; GRAM NEGATIVE INFECTION; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; LIQUID CULTURE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING; STRESS; SURVIVAL; ZOONOSIS;

BACTERIAL PROTEINS; CAMPYLOBACTER INFECTIONS; CAMPYLOBACTER JEJUNI; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HEAT-SHOCK RESPONSE; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; VIRULENCE;

EID: 16244417460     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2005.04525.x     Document Type: Article

References (113)

1. Abu Kwaik, Y. (1998) Induced expression of the Legionella pneumophila gene encoding a 20-kilodalton protein during intracellular infection. Infect Immun 66: 203-212.
2. Aleksandrova, N.Z., Minaev, V.I., and Gorelov, A.V. (1990) [Antibiotic resistance of Campylobacter and its epidemiologic significance]. Antibiot Khimioter 35: 34-36.
3. Allaoui, A., Schulte, R., and Cornelis, G.R. (1995) Mutational analysis of the Yersinia enterocolitica virC operon: characterization of yscE, F, G, I, J, K required for Yop secretion and yscH encoding YopR. Mol Microbiol 18: 343-355.
4. 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.
5. Baar, C., Eppinger, M., Raddatz, G., Simon, J., Lanz, C., Klimmek, O., et al. (2003) Complete genome sequence and analysis of Wolinella succinogenes. Proc Natl Acad Sci USA 100: 11690-11695.
6. Babakhani, F.K., and Joens, L.A. (1993) Primary swine intestinal cells as a model for studying Campylobacter jejuni invasiveness. Infect Immun 61: 2723-2726.
7. Babakhani, F.K., Bradley, G.A., and Joens, L.A. (1993) Newborn piglet model for campylobacteriosis. Infect Immun 61: 3466-3475.
8. Bacon, D.J., Alm, R.A., Burr, D.H., Hu, L., Kopecko, D.J., Ewing, C.P., et al. (2000) Involvement of a plasmid in virulence of Campylobacter jejuni 81-176. Infect Immun 68: 4384-4390.
9. Bacon, D.J., Szymanski, C.M., Burr, D.H., Silver, R.P., Alm, R.A., and Guerry, P. (2001) A phase-variable capsule is involved in virulence of Campylobacter jejuni 81-176. Mol Microbiol 40: 769-777.
10. Bacon, D.J., Alm, R.A., Hu, L., Hickey, T.E., Ewing, C.P., Batchelor, R.A., et al. (2002) DNA sequence and mutational analyses of the pVir plasmid of Campylobacter jejuni 81-176. Infect Immun 70: 6242-6250.
11. Bartlett, M.S., Gaal, T., Ross, W., and Course, R.L. (1998) RNA polymerase mutants that destabilize RNA polymerase-promoter complexes alter NTP-sensing by rrn P1 promoters. J Mol Biol 279: 331-345.
12. 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.
13. Blaser, M.J., Wells, J.G., Feldman, R.A., Pollard, R.A., and Allen, J.R. (1983) Campylobacter enteritis in the United States. A multicenter study. Ann Intern Med 98: 360-365.
14. Butzler, J.P., and Skirrow, M.B. (1979) Campylobacter enteritis. Clin Gastroenterol 8: 737-765.
15. Carvalho, A.C., Ruiz-Palacios, G.M., Ramos-Cervantes, P., Cervantes, L.E., Jiang, X., and Pickering, L.K. (2001) Molecular characterization of invasive and noninvasive Campylobacter jejuni and Campylobacter coli isolates. J Clin Microbiol 39: 1353-1359.
16. Cashel, M., Gentry, D.R., Hernandez, V.J., and Vinella, D. (1996) The stringent response. In Escherichia coli and Salmonella; Cellular and Molecular Biology. Washington, DC: American Society for Microbiology.
17. Chatterji, D., and Ojha, A.K. (2001) Revisiting the stringent response, ppGpp and starvation signaling. Curr Opin Microbiol 4: 160-165.
18. CPHLS (2000) Common gastrointestinal infections, England and Wales. Commun Dis Rep 10: 9-12.
19. Dahl, J.L., Kraus, C.N., Boshoff, H.I., Doan, B., Foley, K., Avarbock, D., et al. (2003) The role of RelMtb-mediated adaptation to stationary phase in long-term persistence of Mycobacterium tuberculosis in mice. Proc Natl Acad Sci USA 1100: 10026-10031.
20. Day, W.A., Jr, Sajecki, J.L., Pitts, T.M., and Joens, L.A. (2000) Role of catalase in Campylobacter jejuni intracellular survival. Infect Immun 68: 6337-6345.
21. 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.
22. Elzer, P.H., Phillips, R.W., Robertson, G.T., and Roop, R.M., II (1996) The HtrA stress response protease contributes to resistance of Brucella abortus to killing by murine phagocytes. Infect Immun 64: 4838-4841.
23. Everest, P.M., Goossens, H., Butzler, J.P., Lloyd, D., Knutton, S., Ketley, J.M., and Williams, P.H. (1992) Differentiated Caco-2 cells as a model for enteric invasion by Campylobacter jejuni and C. coli. J Med Microbiol 37: 319-325.
24. Figurski, D.H., and Helinski, D.R. (1979) Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci USA 76: 1648-1652.
25. Friedman, C.R., Neimann, J., Wegener, H.C., and Tauxe, R. (2001) Epidemiology of Campylobacter jejuni infection in the United States and other industrialized nations. In Campylobacter. Nachamkin, I., and Blaser, M.J. (eds). Washington, DC: American Society for Microbiology Press, pp. 121-138.
26. Gaal, T., Bartlett, M.S., Ross, W., Turnbough, C.L., Jr, and Course, R.L. (1997) Transcription regulation by initiating NTP concentration: rRNA synthesis in bacteria. Science 278: 2092-2097.
27. Gaynor, E.G., Ghori, N., and Falkow, S. (2001) Bile-induced 'pili' in Campylobacter jejuni are bacteria-independent artifacts of the culture medium. Mol Microbiol 39: 1546-1549.
28. 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.
29. Godfrey, H.P., Bugrysheva, J.V., and Cabello, F.C. (2002) The role of the stringent response in the pathogenesis of bacterial infections. Trends Microbiol 10: 349-351.
30. Guerry, P., Szymanski, C.M., Prendergast, M.M., Mickey, T.E., Ewing, C.P., Pattarini, D.L., and Moran, A.P. (2002) Phase variation of Campylobacter jejuni 81-176 lipooligosaccharide affects ganglioside mimicry and invasiveness in vitro. Infect Immun 70: 787-793.
31. Hammer, B.K., and Swanson, M.S. (1999) Co-ordination of legionella pneumophila virulence with entry into stationary phase by ppGpp. Mol Microbiol 33: 721-731.
32. Haralalka, S., Nandi, S., and Bhadra, R.K. (2003) Mutation in the relA gene of Vibrio cholerae affects in vitro and in vivo expression of virulence factors. J Bacteriol 185: 4672-4682.
33. Hendrixson, D.R., Akerley, B.J., and DiRita, V.J. (2001) Transposon mutagenesis of Campylobacter jejuni identifies a bipartite energy taxis system required for motility. Mol Microbiol 40: 214-224.
34. Hernandez, V.J., and Cashel, M. (1995) Changes in conserved region 3 of Escherichia coli sigma 70 mediate ppGpp-dependent functions in vivo. J Mol Biol 252: 536-549.
35. Humphrey, T.J., and Cruickshank, J.G. (1985) Antibiotic and deoxycholate resistance in Campylobacter jejuni following freezing or heating. J Appl Bacteriol 59: 65-71.
36. Ishihama, A. (2000) Functional modulation of Escherichia coli RNA polymerase. Annu Rev Microbiol 54: 499-518.
37. Jones, D.M., Sutcliffe, E.M., Rios, R., Fox, A.J., and Curry, A. (1993) Campylobacter jejuni adapts to aerobic metabolism in the environment. J Med Microbiol 38: 145-150.
38. Jones, C.H., Bolken, T.C., Jones, K.F., Zeller, G.O., and Hruby, D.E. (2001) Conserved DegP protease in Gram-positive bacteria is essential for thermal and oxidative tolerance and full virulence in Streptococcus pyogenes. Infect Immun 69: 5538-5545.
39. Kaneko, T., Nakamura, Y., Sato, S., Minamisawa, K., Uchiumi, T., Sasamoto, S., et al. (2002) Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res 9: 189-197.
40. Karlinger, K., Gyorke, T., Mako, E., Mester, A., and Tarjan, Z. (2000) The epidemiology and the pathogenesis of inflammatory bowel disease. Eur J Radiol 35: 154-167.
41. Kelly, A.F., Park, S.F., Bovill, R., and Mackey, B.M. (2001) Survival of Campylobacter jejuni during stationary phase: evidence for the absence of a phenotypic stationary-phase response. Appl Environ Microbiol 67: 2248-2254.
42. Ketley, J.M. (1997) Pathogenesis of enteric infection by Campylobacter. Microbiology 143: 5-21.
43. Konkel, M.E., and Cieplak, W., Jr (1992) Altered synthetic response of Campylobacter jejuni to cocultivation with human epithelial cells is associated with enhanced internalization. Infect Immun 60: 4945-4949.
44. Konkel, M.E., Hayes, S.F., Joens, L.A., and Cieplak, W., Jr (1992a) Characteristics of the internalization and intracellular survival of Campylobacter jejuni in human epithelial cell cultures. Microb Pathog 13: 357-370.
45. Konkel, M.E., Mead, D.J., Hayes, S.F., and Cieplak, W., Jr (1992b) Translocation of Campylobacter jejuni across human polarized epithelial cell monolayer cultures. J Infect Dis 166: 308-315.
46. Konkel, M.E., Corwin, M.D., Joens, L.A., and Cieplak, W. (1992c) Factors that influence the interaction of Campylobacter jejuni with cultured mammalian cells. J Med Microbiol 37: 30-37.
47. 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.
48. Lastovica, A.J. (1996) Campylobacter/Helicobacter bacteraemia in Cape Town, South Africa, 1977-95. In Campylobacters, Helicobacters and Related Organisms. Newell, D.G., Ketley, J.M., and Feldman, R.A. (eds). New York: Plenum Press, pp. 475-479.
49. Leach, S., Harvey, P., and Wali, R. (1997) Changes with growth rate in the membrane lipid composition of and amino acid utilization by continuous cultures of Campylobacter jejuni. J Appl Microbiol 82: 631-640.
50. Leonard, E.E., II, 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.
51. Li, S.R., Dorrell, N., Everest, P.H., Dougan, G., and Wren, B.W. (1996) Construction and characterization of a Yersinia enterocolitica O:8 high-temperature requirement (htrA) isogenic mutant. Infect Immun 64: 2088-2094.
52. Little, R., Ryals, J., and Bremer, H. (1983) rpoB mutation in Escherichia coli alters control of ribosome synthesis by guanosine tetraphosphate. J Bacteriol 154: 787-792.
53. McQuigge, M. (2000) The investigative report on the Walkerton outbreak of waterborne gastroenteritis: May-June 2000. In Bruce-Grey-Owen Sound Health Unit, Vol. 2000.
54. Markaryan, A., Zaborina, O., Punj, V., and Chakrabarty, A.M. (2001) Adenylate kinase as a virulence factor of Pseudomonas aeruginosa. J Bacteriol 183: 3345-3352.
55. Martin, D.W., and Mohr, C.D. (2000) Invasion and intracellular survival of Burkholderia cepacia. Infect Immun 68: 24-29.
56. Martinez-Rodriguez, A., Kelly, A.F., Park, S.F., and Mackey, B.M. (2004) Emergence of variants with altered survival properties in stationary phase cultures of Campylobacter jejuni. Int J Food Microbiol 90: 321-329.
57. Mason, M.J., Humphrey, T.J., and Martin, K.W. (1999) Isolation of sublethally injured campylobacters from poultry and water sources. Br J Biomed Sci 56: 2-5.
58. Masuda, S., and Bauer, C.E. (2004) Null mutation of HvrA compensates for loss of an essential relA/spoT-like gene in Rhodobacter capsulatus. J Bacteriol 186: 235-239.
59. Menard, R., Sansonetti, P.J., and Parsot, C. (1993) Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J Bacteriol 175: 5899-5906.
60. Mendrygal, K.E., and Gonzalez, J.E. (2000) Environmental regulation of exopolysaccharide production in Sinorhizobium meliloti. J Bacteriol 182: 599-606.
61. Mittenhuber, G. (2001) Comparative genomics and evolution of genes encoding bacterial (p)ppGpp synthetases/hydrolases (the Rel, RelA and SpoT proteins). J Mol Microbiol Biotechnol 3: 585-600.
62. Monteville, M.R., Yoon, J.E., and Konkel, M.E. (2003) Maximal adherence and invasion of INT 407 cells by Campylobacter jejuni requires the CadF outer-membrane protein and microfilament reorganization. Microbiology 49: 153-165.
63. Munier-Lehmann, H., Chenal-Francisque, V., Ionescu, M., Chrisova, P., Foulon, J., Carniel, E., and Barzu, O. (2003) Relationship between bacterial virulence and nucleotide metabolism: a mutation in the adenylate kinase gene renders Yersinia pestis avirulent. Biochem J 373: 515-522.
64. Murphy, H., and Cashel, M. (2003) Isolation of RNA polymerase suppressors of a (p)ppGpp deficiency. Meth Enzymol 371: 596-601.
65. Murphy, C., Carroll, C., and Jordan, K.N. (2003a) Identification of a novel stress resistance mechanism in Campylobacter jejuni. J Appl Microbiol 95: 704-708.
66. Murphy, C., Carroll, C., and Jordan, K.N. (2003b) Induction of an adaptive tolerance response in the foodborne pathogen, Campylobacter jejuni. FEMS Microbiol Lett 223: 89-93.
67. Nachamkin, I., Liu, J., Li, M., Ung, H., Moran, A.P., Prendergast, M.M., and Sheikh, K. (2002a) Campylobacter jejuni from patients with Guillain-Barre syndrome preferentially expresses a GD(1a)-like epitope. Infect Immun 70: 5299-5303.
68. Nachamkin, I., Ung, H., and Li, M. (2002b) Increasing fluoroquinolone resistance in Campylobacter jejuni, Pennsylvania, USA, 1982-2001. Emerg Infect Dis 8: 1501-1503.
69. Newell, D.G., and Fearnley, C. (2003) Sources of Campylobacter colonization in broiler chickens. Appl Environ Microbiol 69: 4343-4351.
70. Ng, L.K., Sherburne, R., Taylor, D.E., and Stiles, M.E. (1985) Morphological forms and viability of Campylobacter species studied by electron microscopy. J Bacteriol 164: 338-343.
71. Nierman, W.C., Feldblyum, T.V., Laub, M.T., Paulsen, I.T., Nelson, K.E., Eisen, J.A., et al. (2001) Complete genome sequence of Caulobacter crescentus. Proc Natl Acad Sci USA 98: 4136-4141.
72. Okada, Y., Makino, S., Tobe, T., Okada, N., and Yamazaki, S. (2002) Cloning of rel from Listeria monocytogenes as an osmotolerance involvement gene. Appl Environ Microbiol 68: 1541-1547.
73. 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.
74. 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.
75. Pesci, E.G., Cottle, D.L., and Pickett, C.L. (1994) Genetic, enzymatic, and pathogenic studies of the iron Superoxide dismutase of Campylobacter jejuni Infect Immun 62: 2687-2694.
76. Pozhalostina, L.V., Solodovnikova, A.V., and Avakov, A.A. (1992) [Sensitivity of the pathogen of Campylobacter infection to various antibiotics]. Antibiot Khimioter 37: 34-35.
77. Primm, T.P., Anderson, S.J., Mizrahi, V., Avarbock, D., Rubin, H., and Barry, C.E., III (2000) The stringent response of Mycobacterium tuberculosis is required for long-term survival. J Bacteriol 182: 4889-4898.
78. Pruss, B.M., Nelms, J.M., Park, C., and Wolfe, A.J. (1994) Mutations in NADH: ubiquinone oxidoreductase of Escherichia coli affect growth on mixed amino acids. J Bacteriol 176: 2143-2150.
79. Reddy, P.S., Raghavan, A., and Chatterji, D. (1995) Evidence for a ppGpp-binding site on Escherichia coli RNA polymerase: proximity relationship with the rifampicin-binding domain. Mol Microbiol 15: 255-265.
80. Russell, R.G., O'Donnoghue, M., Blake, D.C., Jr, Zulty, J., and DeTolla, L.J. (1993) Early colonic damage and invasion of Campylobacter jejuni in experimentally challenged infant Macaca mulatta. J Infect Dis 168: 210-215.
81. Schreiber, G., Metzger, S., Aizenman, E., Roza, S., Cashel, M., and Glaser, G, (1991) Overexpression of the relA gene in Escherichia coli. J Biol Chem 266: 3760-3767.
82. Scoarughi, G.L., Cimmino, C., and Donini, P. (1999) Helicobacter pylori: a eubacterium lacking the stringent response. J Bacteriol 181: 552-555.
83. Sicinschi, L. (1996) [The antibiotic susceptibility of Campylobacter strains isolated in Moldova. The possibilities for estimation and the results]. Bacteriol Virusol Parazitol Epidemiol 41: 123-129.
84. Skirrow, M.B. (1990) Campylobacter, Helicobacter and other mobile curved Gram-negative rods. In Topley and Wilson's Principles of Bacteriology, Virology and Immunity. Parker, M.T., and Collier, L.H. (eds). London: Edward Arnold.
85. Skirrow, M.B., and Blaser, M.J. (1992) Clinical and epidemiological considerations. In Campylobacter Jejuni: Current Status and Future Trends. Nachamkin, I., Blaser, M.J., and Tompkins, L.S. (eds). Washington, DC: American Society for Microbiology, pp. 3-8.
86. Skouloubris, S., Thiberge, J.M., Labigne, A., and De Reuse, H. (1998) The Helicobacter pylori Urel protein is not involved in urease activity but is essential for bacterial survival in vivo. Infect Immun 66: 4517-4521.
87. Srinivasa Rao, P.S., Lim, T.M., and Leung, K.Y. (2003) Functional genomics approach to the identification of virulence genes involved in Edwardsiella tarda pathogenesis. Infect Immun 71: 1343-1351.
88. St Michael, F., Szymanski, C.M., Li, J., Chan, K.H., Khieu, N.H., Larocque, S., et al. (2002) The structures of the lipooligosaccharide and capsule polysaccharide of Campylobacter jejuni genome sequenced strain NCTC 11168. Eur J Biochem 269: 5119-5136.
89. Stead, D., and Park, S.F. (2000) Roles of Fe Superoxide dismutase and catalase in resistance of Campylobacter coli to freeze-thaw stress. Appl Environ Microbiol 66: 3110-3112.
90. Steiner, K., and Malke, H. (2001) relA-Independent amino acid starvation response network of Streptococcus pyogenes. J Bacteriol 183: 7354-7364.
91. 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.
92. Tauxe, R.V. (1992) Epidemiology of Campylobacter jejuni infections in the United States and other industrialized nations. In Campylobacter jejuni: Current Status and Future Trends. Nachamkin, I., Blaser, M.J., and Tompkins, L.S. (eds). Washington, DC: American Society for Microbiology, pp. 9-20.
93. Taylor, C.M., Beresford, M., Epton, H.A., Sigee, D.C., Shama, G., Andrew, P.W., and Roberts, I.S. (2002) Listeria monocytogenes relA and hpt mutants are impaired in surface-attached growth and virulence. J Bacteriol 184: 621-628.
94. Tholozan, J.L., Cappelier, J.M., Tissier, J.P., Delattre, G., and Federighi, M. (1999) Physiological characterization of viable-but-nonculturable Campylobacter jejuni cells. Appl Environ Microbiol 65: 1110-1116.
95. Thornley, J.P., Jenkins, D., Neal, K., Wright, T., Brough, J., and Spiller, R.C. (2001) Relationship of Campylobacter toxigenicity in vitro to the development of postinfectious irritable bowel syndrome. J Infect Dis 184: 606-609.
96. 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.
97. Toulokhonov, I.I., Shulgina, I., and Hernandez, V.J. (2001) Binding of the transcription effector ppGpp to Escherichia coli RNA polymerase is allosteric, modular, and occurs near the N terminus of the beta′-subunit. J Biol Chem 276: 1220-1225.
98. Trieu-Cuot, P., Gerbaud, G., Lambert, T., and Courvalin, P. (1985) In vivo transfer of genetic information between Gram-positive and Gram-negative bacteria. EMBO J 4: 3583-3587.
99. 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.
100. Venturi, V. (2003) Control of rpoS transcription in Escherichia coli and Pseudomonas: why so different? Mol Microbiol 49: 1-9.
101. van Vliet, A.M., Wooldridge, K.G., and Ketley, J.M. (1998) Iron-responsive gene regulation in a Campylobacter jejuni fur mutant. J Bacteriol 180: 5291-5298.
102. Wackwitz, B., Bongaerts, J., Goodman, S.D., and Unden, G. (1999) Growth phase-dependent regulation of nuoA-N expression in Escherichia coli K-12 by the Fis protein: upstream binding sites and bioenergetic significance. Mol General Genet 262: 876-883.
103. Walker, R.I., Caldwell, M.B., Lee, E.G., Guerry, P., Trust, T.J., and Ruiz-Palacios, G.M. (1986) Pathophysiology of Campylobacter enteritis. Microbiol Rev 50: 81-94.
104. Wanner, B.L. (1993) Gene regulation by phosphate in enteric bacteria. J Cell Biochem 51: 47-54.
105. Wassenaar, T.M., Engelskirchen, M., Park, S., and Lastovica, A. (1997) Differential uptake and killing potential of Campylobacter jejuni by human peripheral monocytes/macrophages. Med Microbiol Immunol (Berl) 186: 139-144.
106. Wells, D.H., and Long, S.R. (2002) The Sinorhizobium meliloti stringent response affects multiple aspects of symbiosis. Mol Microbiol 43: 1115-1127.
107. Wells, D.H., and Long, S.R. (2003) Mutations in rpoBC suppress the defects of a Sinorhizobium meliloti relA mutant. J Bacteriol 185: 5602-5610.
108. WHO (2000) The Increasing Incidence of Human Campylobacteriosis. Reports and proceedings of a WHO consulation of experts. Denmark: Copenhagen, p. 137.
109. Wooldridge, K.G., and Ketley, J.M. (1997) Campylobacter-host cell interactions. Trends Microbiol 5: 96-102.
110. 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.
111. Yao, R., Aim, 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.
112. Zhou, Y.N., and Jin, D.J. (1998) The rpoB mutants destabilizing initiation complexes at stringently controlled promoters behave like 'stringent' RNA polymerases in Escherichia coli. Proc Natl Acad Sci USA 95: 2908-2913.
113. Zillig, W., Zechel, K., Rabussay, D., Schachner, M., Sethi, V.S., Palm, P., etal. (1970) On the role of different subunits of DNA-dependent RNA polymerase from E. coli In the transcription process. Cold Spring Harb Symp Quant Biol 35: 47-58.