Motility and chemotaxis in campylobacter and helicobacter

Annual Review of Microbiology

Volumn 65, Issue , 2011, Pages 389-410

  Lertsethtakarn, Paphavee ^a   Ottemann, Karen M ^a   Hendrixson, David R ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

CheZ; Epsilonproteobacteria; Flagella; FlgR; FlgS; Gene expression

Indexed keywords

BACTERIAL COLONIZATION; BACTERIAL FLAGELLUM; BIOSYNTHESIS; CAMPYLOBACTER JEJUNI; CELL ORGANELLE; CHEMORECEPTOR; CHEMOTAXIS; GENE EXPRESSION; GENE EXPRESSION REGULATION; HELICOBACTER PYLORI; LIGAND BINDING; METHYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION;

BACTERIAL PROTEINS; CAMPYLOBACTER JEJUNI; CHEMOTAXIS; FLAGELLA; GENE EXPRESSION REGULATION, BACTERIAL; HELICOBACTER PYLORI;

CAMPYLOBACTER; CAMPYLOBACTER JEJUNI; EPSILONPROTEOBACTERIA; HELICOBACTER; HELICOBACTER PYLORI;

EID: 80053238890     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-090110-102908     Document Type: Review

References (130)

1. Alexander RP, Lowenthal AC,Harshey RM,Ottemann KM. 2010. CheV: CheW-like coupling proteins at the core of the chemotaxis signaling network. Trends Microbiol. 18:494-503
2. Allan E, Dorrell N, Foynes S, Anyim M, Wren BW. 2000. Mutational analysis of genes encoding the early flagellar components of Helicobacter pylori: evidence for transcriptional regulation of flagellin A biosynthesis. J. Bacteriol. 182:5274-77
3. Andermann TM, Chen YT, Ottemann KM. 2002. Two predicted chemoreceptors of Helicobacter pylori promote stomach infection. Infect. Immun. 70:5877-81
4. Andersen-Nissen E, Smith KD, Strobe KL, Barrett SL, Cookson BT, et al. 2005. Evasion of Toll-like receptor 5 by flagellated bacteria. Proc. Natl. Acad. Sci. USA 102:9247-52 (Pubitemid 40923549)
5. Balaban M, Joslin SN, Hendrixson DR. 2009. FlhF and its GTPase activity are required for distinct processes in flagellar gene regulation and biosynthesis in Campylobacter jejuni. J. Bacteriol. 191:6602-11
6. Beery JT, Hugdahl MB, Doyle MP. 1988. Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni. Appl. Environ. Microbiol. 54:2365-70
7. Beier D, Spohn G, Rappuoli R, Scarlato V. 1997. Identification and characterization of an operon of Helicobacter pylori that is involved in motility and stress adaptation. J. Bacteriol. 179:4676-83 (Pubitemid 27339710)
8. Berg HC, Turner L. 1979. Movement of microorganisms in viscous environments. Nature. 278: 349-51 (Pubitemid 9124374)
9. BonisM, Ecobichon C, Guadagnini S, Prevost MC, Boneca IG. 2010. AM23B family metallopeptidase of Helicobacter pylori required for cell shape, pole formation and virulence. Mol. Microbiol. 78:809-19
10. Bray D. 2002. Bacterial chemotaxis and the question of gain. Proc. Natl. Acad. Sci. USA 99:7-9 (Pubitemid 34060305)
11. Caly DL, O'Toole PW, Moore SA. 2010. The 2.2-'A structure of the HP0958 protein from Helicobacter pylori reveals a kinked anti-parallel coiled-coil hairpin domain and a highly conserved ZN-ribbon domain. J. Mol. Biol. 403:405-19
12. Carrillo CD, Taboada E, Nash JH, Lanthier P, Kelly J, et al. 2004. Genome-wide expression analyses of Campylobacter jejuni NCTC11168 reveals coordinate regulation of motility and virulence by flhA. J. Biol. Chem. 279:20327-38 (Pubitemid 38623478)
13. Celli JP, Turner BS, Afdhal NH, Keates S, Ghiran I, et al. 2009. Helicobacter pylori moves through mucus by reducing mucin viscoelasticity. Proc. Natl. Acad. Sci. USA 106:14321-26
14. Center forDisease Control. 2010. PreliminaryFoodNet data on the incidence of infectionwith pathogens transmitted commonly through food - 10 states, 2009. MMWR Morb. Mortal. Wkly Rep. 59:418-22
15. Cerda O, Rivas A, Toledo H. 2003. Helicobacter pylori strain ATCC700392 encodes a methyl-accepting chemotaxis receptor protein (MCP) for arginine and sodium bicarbonate. FEMS Microbiol. Lett. 224:175-81 (Pubitemid 36929822)
16. Chang C, Miller JF. 2006. Campylobacter jejuni colonization of mice with limited enteric flora. Infect. Immun. 74:5261-71 (Pubitemid 44300445)
17. Chevance FF, Hughes KT. 2008. Coordinating assembly of a bacterial macromolecular machine. Nat. Rev. Microbiol. 6:455-65 (Pubitemid 351696439)
18. Chilcott GS,Hughes KT. 2000. Coupling of flagellar gene expression to flagellar assembly in Salmonella enterica serovar typhimurium and Escherichia coli. Microbiol. Mol. Biol. Rev. 64:694-708 (Pubitemid 32475927)
19. Colland F,Rain JC,Gounon P, LabigneA,Legrain P, De ReuseH. 2001. Identification of the Helicobacter pylori anti-28 factor. Mol. Microbiol. 41:477-87 (Pubitemid 32730545)
20. Correa NE, Peng F, Klose KE. 2005. Roles of the regulatory proteins FlhF and FlhG in the Vibrio cholerae flagellar transcription hierarchy. J. Bacteriol. 187:6324-32 (Pubitemid 41318391)
21. Cover TL, Blaser MJ. 2009. Helicobacter pylori in health and disease. Gastroenterology 136:1863-73
22. Croxen MA, Sisson G, Melano R, Hoffman PS. 2006. The Helicobacter pylori chemotaxis receptor TlpB (HP0103) is required for pH taxis and for colonization of the gastric mucosa. J. Bacteriol. 188:2656-65
23. Dasgupta N, Arora SK, Ramphal R. 2000. fleN, a gene that regulates flagellar number in Pseudomonas aeruginosa. J. Bacteriol. 182:357-64 (Pubitemid 30030118)
24. Dasgupta N, Ramphal R. 2001. Interaction of the antiactivator FleN with the transcriptional activator FleQ regulates flagellar number in Pseudomonas aeruginosa. J. Bacteriol. 183:6636-44 (Pubitemid 33026755)
25. Delany I, Spohn G, Rappuoli R, Scarlato V. 2002. Growth phase-dependent regulation of target gene promoters for binding of the essential orphan response regulator HP1043 of Helicobacter pylori. J. Bacteriol. 184:4800-10
26. Doig P, Kinsella N, Guerry P, Trust TJ. 1996. Characterization of a post-translational modification of Campylobacter flagellin: identification of a sero-specific glycosyl moiety. Mol. Microbiol. 19:379-87 (Pubitemid 26036117)
27. Douillard FP, Ryan KA, Caly DL, Hinds J, Witney AA, et al. 2008. Posttranscriptional regulation of flagellin synthesis in Helicobacter pylori by the RpoN chaperone HP0958. J. Bacteriol. 190:7975-84
28. Elliott KT, Dirita VJ. 2008. Characterization of CetA and CetB, a bipartite energy taxis system in Campylobacter jejuni. Mol. Microbiol. 69:1091-103
29. Erhardt M, Hirano T, Su Y, Paul K, Wee DH, et al. 2010. The role of the FliK molecular ruler in hook-length control in Salmonella enterica. Mol. Microbiol. 75:1272-84
30. Ewing CP, Andreishcheva E, Guerry P. 2009. Functional characterization of flagellin glycosylation in Campylobacter jejuni 81-176. J. Bacteriol. 191:7086-93
31. Ferrero RL, Lee A. 1988. Motility of Campylobacter jejuni in a viscous environment: comparison with conventional rod-shaped bacteria. J. Gen. Microbiol. 134:53-59
32. Foynes S, Dorrell N, Ward SJ, Stabler RA, McColm AA, et al. 2000. Helicobacter pylori possesses two CheY response regulators and a histidine kinase sensor, CheA, which are essential for chemotaxis and colonization of the gastric mucosa. Infect. Immun. 68:2016-23 (Pubitemid 30164832)
33. Geis G, Leying H, Suerbaum S, Mai U, Opferkuch W. 1989. Ultrastructure and chemical analysis of Campylobacter pylori flagella. J. Clin. Microbiol. 27:436-41 (Pubitemid 19072350)
34. Goodwin CS,McCulloch RK, Armstrong JA, Wee SH. 1985. Unusual cellular fatty acids and distinctive ultrastructure in a new spiral bacterium (Campylobacter pyloridis) from the human gastric mucosa. J. Med. Microbiol. 19:257-67 (Pubitemid 15086850)
35. Goon S, Ewing CP, Lorenzo M, Pattarini D, Majam G, Guerry P. 2006. A '28-regulated nonflagella gene contributes to virulence of Campylobacter jejuni 81-176. Infect. Immun. 74:769-72 (Pubitemid 43023136)
36. Goon S, Kelly JF, Logan SM, Ewing CP, Guerry P. 2003. Pseudaminic acid, the major modification on Campylobacter flagellin, is synthesized via the Cj1293 gene. Mol. Microbiol. 50:659-71 (Pubitemid 37297142)
37. Green JC, Kahramanoglou C, Rahman A, Pender AM,CharbonnelN, FraserGM. 2009. Recruitment of the earliest component of the bacterial flagellum to the old cell division pole by a membrane-associated signal recognition particle family GTP-binding protein. J. Mol. Biol. 391:679-90
38. Guerry P, Ewing CP, Schirm M, Lorenzo M, Kelly J, et al. 2006. Changes in flagellin glycosylation affect Campylobacter autoagglutination and virulence. Mol. Microbiol. 60:299-311
39. Guruge JL, Falk PG, Lorenz RG, Dans M, Wirth HP, et al. 1998. Epithelial attachment alters the outcome of Helicobacter pylori infection. Proc. Natl. Acad. Sci. USA 95:3925-30 (Pubitemid 28173230)
40. Hartley-Tassell LE, Shewell LK, Day CJ, Wilson JC, Sandhu R, et al. 2010. Identification and characterization of the aspartate chemosensory receptor of Campylobacter jejuni. Mol. Microbiol. 75:710-30
41. Hazell SL, Lee A, Brady L, Hennessy W. 1986. Campylobacter pyloridis and gastritis: association with intercellular spaces and adaptation to an environment of mucus as important factors in colonization of the gastric epithelium. J. Infect. Dis. 153:658-63 (Pubitemid 16133745)
42. Hendrixson DR. 2006. A phase-variable mechanism controlling the Campylobacter jejuni FlgR response regulator influences commensalism. Mol. Microbiol. 61:1646-59 (Pubitemid 44359390)
43. Hendrixson DR. 2008. Restoration of flagellar biosynthesis by varied mutational events in Campylobacter jejuni. Mol. Microbiol. 70:519-36
44. Hendrixson DR, Akerley BJ, DiRita VJ. 2001. Transposon mutagenesis of Campylobacter jejuni identifies a bipartite energy taxis system required for motility. Mol. Microbiol. 40:214-24 (Pubitemid 32322874)
45. Hendrixson DR,DiRita VJ. 2003. Transcription of 54-dependent but not 28-dependent flagellar genes in Campylobacter jejuni is associated with formation of the flagellar secretory apparatus. Mol. Microbiol. 50:687-702 (Pubitemid 37297144)
46. Hendrixson DR, DiRita VJ. 2004. Identification of Campylobacter jejuni genes involved in commensal colonization of the chick gastrointestinal tract. Mol. Microbiol. 52:471-84 (Pubitemid 38520716)
47. Hoffman PS, Vats N, Hutchison D, Butler J, Chisholm K, et al. 2003. Development of an interleukin- 12-deficient mouse model that is permissive for colonization by a motile KE26695 strain of Helicobacter pylori. Infect. Immun. 71:2534-41 (Pubitemid 36519866)
48. Hugdahl MB, Beery JT, Doyle MP. 1988. Chemotactic behavior of Campylobacter jejuni. Infect. Immun. 56:1560-66
49. Jahreis K, Morrison TB, Garzon A, Parkinson JS. 2004. Chemotactic signaling by an Escherichia coli CheA mutant that lacks the binding domain for phosphoacceptor partners. J. Bacteriol. 186:2664-72 (Pubitemid 38525920)
50. Jimenez-PearsonMA, Delany I, Scarlato V, Beier D. 2005. Phosphate flow in the chemotactic response system of Helicobacter pylori. Microbiology 151:3299-311 (Pubitemid 41488913)
51. Josenhans C, Eaton KA, Thevenot T, Suerbaum S. 2000. Switching of flagellar motility in Helicobacter pylori by reversible length variation of a short homopolymeric sequence repeat in fliP, a gene encoding a basal body protein. Infect. Immun. 68:4598-603 (Pubitemid 30497729)
52. Josenhans C, Labigne A, Suerbaum S. 1995. Comparative ultrastructural and functional studies of Helicobacter pylori and Helicobacter mustelae flagellin mutants: both flagellin subunits, FlaA and FlaB, are necessary for full motility in Helicobacter species. J. Bacteriol. 177:3010-20
53. Josenhans C, Niehus E, Amersbach S, Horster A, Betz C, et al. 2002. Functional characterization of the antagonistic flagellar late regulators FliA and FlgM of Helicobacter pylori and their effects on the H. pylori transcriptome. Mol. Microbiol. 43:307-22 (Pubitemid 34146724)
54. Josenhans C, Vossebein L, Friedrich S, Suerbaum S. 2002. The neuA/flmD gene cluster of Helicobacter pylori is involved in flagellar biosynthesis and flagellin glycosylation. FEMS Microbiol. Lett. 210:165-72 (Pubitemid 34607181)
55. Joslin SN, Hendrixson DR. 2008. Analysis of the Campylobacter jejuni FlgR response regulator suggests integration of diverse mechanisms to activate an NtrC-like protein. J. Bacteriol. 190:2422-33 (Pubitemid 351466337)
56. Joslin SN, Hendrixson DR. 2009. Activation of the Campylobacter jejuni FlgSR two component system is linked to the flagellar export apparatus. J. Bacteriol. 191:2656-67
57. KamalN,Dorrell N, Jagannathan A, Turner SM, Constantinidou C, et al. 2007. Deletion of a previously uncharacterized flagellar-hook-length control gene fliK modulates the sigma54 -dependent regulon in Campylobacter jejuni. Microbiology 153:3099-111 (Pubitemid 47517070)
58. Kanungpean D, Kakuda T, Takai S. 2011. False positive responses of Campylobacter jejuni when using the chemical-in-plug chemotaxis assay. J. Vet. Med. Sci. 73:389-91
59. Kanungpean D, Kakuda T, Takai S. 2011. Participation ofCheR and CheB in the chemosensory response of Campylobacter jejuni. Microbiology 157:1279-89
60. Karim QN, Logan RP, Puels J, Karnholz A, Worku ML. 1998. Measurement of motility of Helicobacter pylori, Campylobacter jejuni, and Escherichia coli by real time computer tracking using the Hobson BacTracker. J. Clin. Pathol. 51:623-28 (Pubitemid 28394259)
61. Kim JS, Chang JH, Chung SI, Yum JS. 1999. Molecular cloning and characterization of the Helicobacter pylori fliD gene, an essential factor in flagellar structure and motility. J. Bacteriol. 181:6969-76 (Pubitemid 29536509)
62. Kostrzynska M, Betts JD, Austin JW, Trust TJ. 1991. Identification, characterization, and spatial localization of two flagellin species in Helicobacter pylori flagella. J. Bacteriol. 173:937-46
63. Kusumoto A, Shinohara A, Terashima H, Kojima S, Yakushi T, Homma M. 2008. Collaboration of FlhF and FlhG to regulate polar-flagella number and localization in Vibrio alginolyticus. Microbiology 154:1390-99
64. Lam KH, Ling TK, Au SW. 2010. Crystal structure of activated CheY1 from Helicobacter pylori. J. Bacteriol. 192:2324-34
65. Lee A,O'Rourke JL, Barrington PJ, TrustTJ. 1986. Mucus colonization as a determinant of pathogenicity in intestinal infection by Campylobacter jejuni: a mouse cecal model. Infect. Immun. 51:536-46 (Pubitemid 16212132)
66. Lertsethtakarn P, Ottemann KM. 2010. A remote CheZ orthologue retains phosphatase function. Mol. Microbiol. 77:225-35
67. Leying H, Suerbaum S, Geis G, Haas R. 1992. Cloning and genetic characterization of a Helicobacter pylori flagellin gene. Mol. Microbiol. 6:2863-74
68. Li J, Go AC,WardMJ, Ottemann KM. 2010. The chemical-in-plug bacterial chemotaxis assay is prone to false positive responses. BMC Res. Notes 3:77
69. Logan SM, Harris LA, Trust TJ. 1987. Isolation and characterization of Campylobacter flagellins. J. Bacteriol. 169:5072-77
70. Logan SM, Kelly JF, Thibault P, Ewing CP, Guerry P. 2002. Structural heterogeneity of carbohydrate modifications affects serospecificity of Campylobacter flagellins. Mol. Microbiol. 46:587-97 (Pubitemid 35340966)
71. Lowenthal AC,Hill M, Sycuro LK,Mehmood K, Salama NR, Ottemann KM. 2009. Functional analysis of the Helicobacter pylori flagellar switch proteins. J. Bacteriol. 191:7147-56
72. Lowenthal AC, Simon C, Fair AS, Mehmood K, Terry K, et al. 2009. A fixed-time diffusion analysis method determines that the three cheV genes of Helicobacter pylori differentially affect motility. Microbiology 155:1181-91
73. Macnab RM. 2003. How bacteria assemble flagella. Annu. Rev. Microbiol. 57:77-100
74. Marchant J, Wren B, Ketley J. 2002. Exploiting genome sequence: predictions formechanisms of Campylobacter chemotaxis. Trends Microbiol. 10:155-59 (Pubitemid 34242945)
75. McGee DJ, Langford ML, Watson EL, Carter JE, Chen YT, Ottemann KM. 2005. Colonization and inflammation deficiencies inMongolian gerbils infected by Helicobacter pylori chemotaxis mutants. Infect. Immun. 73:1820-27 (Pubitemid 40470771)
76. McNally DJ, Aubry AJ, Hui JP, Khieu NH, Whitfield D, et al. 2007. Targeted metabolomics analysis of Campylobacter coli VC167 reveals legionaminic acid derivatives as novel flagellar glycans. J. Biol. Chem. 282:14463-75 (Pubitemid 47100450)
77. Minamino T, Imada K, Namba K. 2008. Molecular motors of the bacterial flagella. Curr. Opin. Struct. Biol. 18:693-701
78. Mizote T, Yoshiyama H, Nakazawa T. 1997. Urease-independent chemotactic responses of Helicobacter pylori to urea, urease inhibitors, and sodium bicarbonate. Infect. Immun. 65:1519-21 (Pubitemid 27146647)
79. Molbak K, Havelaar A. 2008. Burden of illness of campylobacteriosis and sequelae. In Campylobacter, ed. I Nachamkin, CM Szymanski, MJ Blaser, pp. 151-62. Washington, DC: ASM Press
80. Muff TJ,OrdalGW.2008. The diverse CheC-type phosphatases: chemotaxis and beyond. Mol. Microbiol. 70:1054-61
81. Murray TS, Kazmierczak BI. 2006. FlhF is required for swimming and swarming in Pseudomonas aeruginosa. J. Bacteriol. 188:6995-7004 (Pubitemid 44497912)
82. Niehus E, Gressmann H, Ye F, Schlapbach R, Dehio M, et al. 2004. Genome-wide analysis of transcriptional hierarchy and feedback regulation in the flagellar system of Helicobacter pylori. Mol. Microbiol. 52:947-61 (Pubitemid 38916167)
83. Ottemann KM, Lowenthal AC. 2002. Helicobacter pylori uses motility for initial colonization and to attain robust infection. Infect. Immun. 70:1984-90 (Pubitemid 34242199)
84. Ottemann KM,Miller JF. 1997. Roles for motility in bacterial-host interactions. Mol. Microbiol. 24:1109-17 (Pubitemid 27293786)
85. Pandza S, Baetens M, Park CH, Au T, Keyhan M, Matin A. 2000. The G-protein FlhF has a role in polar flagellar placement and general stress response induction in Pseudomonas putida. Mol. Microbiol. 36:414-23 (Pubitemid 30229486)
86. Park SF, Purdy D, Leach S. 2000. Localized reversible frameshift mutation in the flhA gene confers phase variability to flagellin gene expression in Campylobacter coli. J. Bacteriol. 182:207-10 (Pubitemid 30004577)
87. Parkhill J, Wren BW, Mungall K, Ketley JM, Churcher C, et al. 2000. The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665-68 (Pubitemid 30104008)
88. Pereira L, Hoover TR. 2005. Stable accumulation of sigma54 in Helicobacter pylori requires the novel protein HP0958. J. Bacteriol. 187:4463-69 (Pubitemid 40880957)
89. Pittman MS, Goodwin M, Kelly DJ. 2001. Chemotaxis in the human gastric pathogen Helicobacter pylori: different roles for CheW and the three CheV paralogues, and evidence for CheV2 phosphorylation. Microbiology 147:2493-504 (Pubitemid 32899245)
90. Poly F, Ewing C, Goon S, Hickey TE, Rockabrand D, et al. 2007. Heterogeneity of a Campylobacter jejuni protein that is secreted through the flagellar filament. Infect. Immun. 75:3859-67 (Pubitemid 47206283)
91. Rain JC, Selig L, De Reuse H, Battaglia V, Reverdy C, et al. 2001. The protein-protein interaction map of Helicobacter pylori. Nature 409:211-15 (Pubitemid 32144288)
92. Rust M, Borchert S, Niehus E, Kuehne SA, Gripp E, et al. 2009. The Helicobacter pylori anti-sigma factor FlgM is predominantly cytoplasmic and cooperates with the flagellar basal body protein FlhA. J. Bacteriol. 191:4824-34
93. Ryan KA, Karim N, Worku M, Moore SA, Penn CW, O'Toole PW. 2005. HP0958 is an essential motility gene in Helicobacter pylori. FEMS Microbiol. Lett. 248:47-55 (Pubitemid 40834313)
94. Ryan KA, Karim N, WorkuM, Penn CW, O'Toole PW. 2005. Helicobacter pylori flagellar hook-filament transition is controlled by a FliK functional homolog encoded by the gene HP0906. J. Bacteriol. 187:5742-50 (Pubitemid 41134311)
95. Sarkar MK, Paul K, Blair D. 2010. Chemotaxis signaling protein CheY binds to the rotor protein FliN to control the direction of flagellar rotation in Escherichia coli. Proc. Natl. Acad. Sci. USA 107:9370-75
96. Schirm M, Schoenhofen IC, Logan SM, Waldron KC, Thibault P. 2005. Identification of unusual bacterial glycosylation by tandemmass spectrometry analyses of intact proteins. Anal. Chem. 77:7774-82 (Pubitemid 41746246)
97. Schirm M, Soo EC, Aubry AJ, Austin J, Thibault P, Logan SM. 2003. Structural, genetic and functional characterization of the flagellin glycosylation process in Helicobacter pylori. Mol. Microbiol. 48:1579-92 (Pubitemid 36751063)
98. Schreiber S, Konradt M, Groll C, Scheid P, Hanauer G, et al. 2004. The spatial orientation of Helicobacter pylori in the gastric mucus. Proc. Natl. Acad. Sci. USA 101:5024-29 (Pubitemid 38469196)
99. Schweinitzer T,Mizote T, Ishikawa N, Dudnik A, Inatsu S, et al. 2008. Functional characterization and mutagenesis of the proposed behavioral sensor TlpD of Helicobacter pylori. J. Bacteriol. 190:3244-55 (Pubitemid 351581420)
100. Seymour FW,Doetsch RN. 1973. Chemotactic responses bymotile bacteria. J. Gen. Microbiol. 78:287-96
101. Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiss S, et al. 2010. The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464:250-55
102. ShigematsuM,UmedaA, Fujimoto S, Amako K. 1998. Spirochaete-like swimming mode of Campylobacter jejuni in a viscous environment. J. Med. Microbiol. 47:521-26 (Pubitemid 28267571)
103. Spohn G, Scarlato V. 1999. Motility of Helicobacter pylori is coordinately regulated by the transcriptional activator FlgR, an NtrC homolog. J. Bacteriol. 181:593-99 (Pubitemid 29045152)
104. Suerbaum S, Josenhans C, Labigne A. 1993. Cloning and genetic characterization of the Helicobacter pylori and Helicobacter mustelae flaB flagellin genes and construction of H. pylori flaA- and flaB-negative mutants by electroporation-mediated allelic exchange. J. Bacteriol. 175:3278-88 (Pubitemid 23163369)
105. Sycuro LK, Pincus Z,GutierrezKD, Biboy J, SternCA, et al. 2010. Peptidoglycan crosslinking relaxation promotes Helicobacter pylori's helical shape and stomach colonization. Cell 141:822-33
106. Szurmant H, Muff TJ, Ordal GW. 2004. Bacillus subtilis CheC and FliY are members of a novel class of CheY-P-hydrolyzing proteins in the chemotactic signal transduction cascade. J. Biol. Chem. 279:21787-92 (Pubitemid 38679366)
107. Szurmant H, Ordal GW. 2004. Diversity in chemotaxis mechanisms among the bacteria and archaea. Microbiol. Mol. Biol. Rev. 68:301-19 (Pubitemid 38756867)
108. Szymanski CM, King M, Haardt M, Armstrong GD. 1995. Campylobacter jejuni motility and invasion of Caco-2 cells. Infect. Immun. 63:4295-300
109. Tareen AM, Dasti JI, Zautner AE, Gross U, Lugert R. 2010. Campylobacter jejuni proteins Cj0952c and Cj0951c affect chemotactic behavior towards formic acid and are important for invasion of host cells. Microbiology 156:3123-35
110. Terry K, Go AC, Ottemann KM. 2006. Proteomic mapping of a suppressor of non-chemotactic cheW mutants reveals that Helicobacter pylori contains a new chemotaxis protein. Mol. Microbiol. 61:871-82 (Pubitemid 44134167)
111. Terry K, Williams SM,Connolly L, Ottemann KM. 2005. Chemotaxis plays multiple roles during Helicobacter pylori animal infection. Infect. Immun. 73:803-11 (Pubitemid 40165736)
112. Thibault P, Logan SM, Kelly JF, Brisson JR, Ewing CP, et al. 2001. Identification of the carbohydrate moieties and glycosylation motifs in Campylobacter jejuni flagellin. J. Biol. Chem. 276:34862-70
113. Thomas J, Stafford GP, Hughes C. 2004. Docking of cytosolic chaperone-substrate complexes at the membrane ATPase during flagellar type III protein export. Proc. Natl. Acad. Sci. USA 101:3945-50 (Pubitemid 38381082)
114. Tomb JF,White O, Kerlavage AR, Clayton RA, Sutton GG, et al. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-47 (Pubitemid 27339996)
115. van Alphen LB, Bleumink-Pluym NM, Rochat KD, van Balkom BW,Wósten MM, van Putten JP. 2008. Active migration into the subcellular space precedes Campylobacter jejuni invasion of epithelial cells. Cell Microbiol. 10:53-66 (Pubitemid 350239055)
116. Vegge CS, Brondsted L, Li YP, Bang DD, Ingmer H. 2009. Energy taxis drives Campylobacter jejuni toward the most favorable conditions for growth. Appl. Environ. Microbiol. 75:5308-14
117. Wadhams GH, Armitage JP. 2004. Making sense of it all: bacterial chemotaxis. Nat. Rev. Mol. Cell Biol. 5:1024-37 (Pubitemid 39611538)
118. Wassenaar TM, Bleumink-PluymNMC,Newell DG, Nuijten PJ, van der Zeijst BAM. 1994. Differential flagellin expression in a flaA flaB+ mutant of Campylobacter jejuni. Infect. Immun. 62:3901-6 (Pubitemid 24264335)
119. Wassenaar TM, Bleumink-Pluym NMC, van der Zeijst BAM. 1991. Inactivation of Campylobacter jejuni flagellin genes by homologous recombination demonstrates that flaA but not flaB is required for invasion. EMBO J. 10:2055-61 (Pubitemid 21905676)
120. Williams SM, Chen YT, Andermann TM, Carter JE, McGee DJ, Ottemann KM. 2007. Helicobacter pylori chemotaxis modulates inflammation and bacterium-gastric epithelium interactions in infected mice. Infect. Immun. 75:3747-57 (Pubitemid 47206272)
121. Worku ML, Karim QN, Spencer J, Sidebotham RL. 2004. Chemotactic response of Helicobacter pylori to human plasma and bile. J. Med. Microbiol. 53:807-11 (Pubitemid 39433380)
122. Worku ML, Sidebotham RL, Baron JH, Misiewicz JJ, Logan RP, et al. 1999. Motility of Helicobacter pylori in a viscous environment. Eur. J. Gastroenterol. Hepatol. 11:1143-50 (Pubitemid 30433766)
123. Wö sten MM, van Dijk L, Veenendaal AK, de Zoete MR, Bleumink-Pluijm NM, van Putten JP. 2010. Temperature-dependent FlgM/FliA complex formation regulates Campylobacter jejuni flagella length. Mol. Microbiol. 75:1577-91
124. Wósten MMSM, Wagenaar JA, van Putten JPM. 2004. The FlgS/FlgR two-component signal transduction system regulates the fla regulon in Campylobacter jejuni. J. Biol. Chem. 279:16214-22 (Pubitemid 38509314)
125. Wuichet K, Alexander RP, Zhulin IB. 2007. Comparative genomic and protein sequence analyses of a complex system controlling bacterial chemotaxis. Methods Enzymol. 422:1-31
126. Wuichet K, Zhulin IB. 2010. Origins and diversification of a complex signal transduction system in prokaryotes. Sci. Signal. 3:ra50
127. Wunder C, Churin Y, Winau F,Warnecke D, Vieth M, et al. 2006. Cholesterol glucosylation promotes immune evasion by Helicobacter pylori. Nat. Med. 12:1030-38 (Pubitemid 44353384)
128. Yao R, Burr DH, Guerry P. 1997. CheY-mediated modulation of Campylobacter jejuni virulence. Mol. Microbiol. 23:1021-31 (Pubitemid 27096737)
129. Yonekura K, Maki-Yonekura S, Namba K. 2003. Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424:643-50 (Pubitemid 36987983)
130. Zhao R, Collins EJ, Bourret RB, Silversmith RE. 2002. Structure and catalytic mechanism of the E. coli chemotaxis phosphatase CheZ. Nat. Struct. Biol. 9:570-75 (Pubitemid 34816135)