A regulatory checkpoint during flagellar biogenesis in campylobacter jejuni initiates signal transduction to activate transcription of flagellar genes

mBio

Volumn 4, Issue 5, 2013, Pages

  Boll, Joseph M ^a,b   Hendrixson, David R ^a  

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

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN FLGS; PROTEIN FLHA; PROTEIN FLIF; PROTEIN FLIG; PROTEIN FLIG C; PROTEIN HISTIDINE KINASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL GENE; BIOGENESIS; CAMPYLOBACTER; CAMPYLOBACTER JEJUNI; CELL CYCLE CHECKPOINT; CELL CYCLE REGULATION; CELL STRUCTURE; COMPLEX FORMATION; CYTOPLASM; FLAGELLATE; GENE ACTIVATION; GENE EXPRESSION; GENE INTERACTION; GENETIC CONSERVATION; GENETIC ORGANIZATION; GENETIC STABILITY; GENETIC TRANSCRIPTION; HELICOBACTER; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PSEUDOMONAS; TRANSCRIPTION INITIATION; TYPE III SECRETION SYSTEM; VIBRIO;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CAMPYLOBACTER JEJUNI; FLAGELLA; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS; SIGMA FACTOR; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84887166776     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00432-13     Document Type: Article

References (43)

1. Gao R, Stock AM. 2009. Biological insights from structures of twocomponent proteins. Annu. Rev. Microbiol. 63:133-154.
2. 28-dependent flagellar genes in Campylobacter jejuni is associated with formation of the flagellar secretory apparatus. Mol. Microbiol. 50: 687-702.
3. Niehus E, Gressmann H, Ye F, Schlapbach R, Dehio M, Dehio C, Stack A, Meyer TF, Suerbaum S, Josenhans C. 2004. Genome-wide analysis of transcriptional hierarchy and feedback regulation in the flagellar system of Helicobacter pylori. Mol. Microbiol. 52:947-961.
4. 28-dependent flagellar gene transcription hierarchy of Vibrio cholerae. Mol. Microbiol. 39:1595-1609.
5. Dasgupta N, Wolfgang MC, Goodman AL, Arora SK, Jyot J, Lory S, Ramphal R. 2003. A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa. Mol. Microbiol. 50: 809-824.
6. Correa NE, Lauriano CM, McGee R, Klose KE. 2000. Phosphorylation of the flagellar regulatory protein FlrC is necessary for Vibrio cholerae motility and enhanced colonization. Mol. Microbiol. 35:743-755.
7. Spohn G, Scarlato V. 1999. Motility of Helicobacter pylori is coordinately regulated by the transcriptional activator FlgR, an NtrC homolog. J. Bacteriol. 181:593-599.
8. Wösten MM, Wagenaar JA, van Putten JP. 2004. The FlgS/FlgR twocomponent signal transduction system regulates the fla regulon in Campylobacter jejuni. J. Biol. Chem. 279:16214-16222.
9. 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. 190:2422-2433.
10. Joslin SN, Hendrixson DR. 2009. Activation of the Campylobacter jejuni FlgSR two-component system is linked to the flagellar export apparatus. J. Bacteriol. 191:2656-2667.
11. Boll JM, Hendrixson DR. 2011. A specificity determinant for phosphorylation in a response regulator prevents in vivo cross-talk and modification by acetyl phosphate. Proc. Natl. Acad. Sci. U. S. A. 108:20160-20165.
12. 54-dependent transcription. Microbiol. Mol. Biol. Rev. 76:497-529.
13. Barrero-Tobon AM, Hendrixson DR. 2012. Identification and analysis of flagellar coexpressed determinants (Feds) of Campylobacter jejuni involved in colonization. Mol. Microbiol. 84:352-369.
14. Buelow DR, Christensen JE, Neal-McKinney JM, Konkel ME. 2011. Campylobacter jejuni survival within human epithelial cells is enhanced by the secreted protein CiaI. Mol. Microbiol. 80:1296-1312.
15. Balaban M, Hendrixson DR. 2011. Polar flagellar biosynthesis and a regulator of flagellar number influence spatial parameters of cell division in Campylobacter jejuni. PLoS Pathog. 7:e1002420.
16. 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. 191:6602-6611.
17. Kazmierczak BI, Hendrixson DR. 2013. Spatial and numerical regulation of flagellar biosynthesis in polarly flagellated bacteria. Mol. Microbiol. 88:655-663.
18. Green JC, Kahramanoglou C, Rahman A, Pender AM, Charbonnel N, Fraser GM. 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: 679-690.
19. Murray TS, Kazmierczak BI. 2006. FlhF is required for swimming and swarming in Pseudomonas aeruginosa. J. Bacteriol. 188:6995-7004.
20. Lertsethtakarn P, Ottemann KM, Hendrixson DR. 2011. Motility and chemotaxis in Campylobacter and Helicobacter. Annu. Rev. Microbiol. 65: 389-410.
21. Minamino T, Macnab RM. 2000. Domain structure of Salmonella FlhB, a flagellar export component responsible for substrate specificity switching. J. Bacteriol. 182:4906-4914.
22. Kubori T, Yamaguchi S, Aizawa S. 1997. Assembly of the switch complex onto the MS ring complex of Salmonella typhimurium does not require any other flagellar proteins. J. Bacteriol. 179:813-817.
23. Wagner S, Königsmaier L, Lara-Tejero M, Lefebre M, Marlovits TC, Galán JE. 2010. Organization and coordinated assembly of the type III secretion export apparatus. Proc. Natl. Acad. Sci. U. S. A. 107: 17745-17750.
24. Li H, Sourjik V. 2011. Assembly and stability of flagellar motor in Escherichia coli. Mol. Microbiol. 80:886-899.
25. Diepold A, Wiesand U, Cornelis GR. 2011. The assembly of the export apparatus (YscR,S,T,U,V) of the Yersinia type III secretion apparatus occurs independently of other structural components and involves the formation of an YscV oligomer. Mol. Microbiol. 82:502-514.
26. McMurry JL, Van Arnam JS, Kihara M, Macnab RM. 2004. Analysis of the cytoplasmic domains of Salmonella FlhA and interactions with components of the flagellar export machinery. J. Bacteriol. 186:7586-7592.
27. Francis NR, Irikura VM, Yamaguchi S, DeRosier DJ, Macnab RM. 1992. Localization of the Salmonella typhimurium flagellar switch protein FliG to the cytoplasmic M-ring face of the basal body. Proc. Natl. Acad. Sci. U. S. A. 89:6304-6308.
28. Kihara M, Miller GU, Macnab RM. 2000. Deletion analysis of the flagellar switch protein FliG of Salmonella. J. Bacteriol. 182:3022-3028.
29. Paul K, Gonzalez-Bonet G, Bilwes AM, Crane BR, Blair D. 2011. Architecture of the flagellar rotor. EMBO J. 30:2962-2971.
30. Lee LK, Ginsburg MA, Crovace C, Donohoe M, Stock D. 2010. Structure of the torque ring of the flagellar motor and the molecular basis for rotational switching. Nature 466:996-1000.
31. Kihara M, Minamino T, Yamaguchi S, Macnab RM. 2001. Intergenic suppression between the flagellar MS ring protein FliF of Salmonella and FlhA, a membrane component of its export apparatus. J. Bacteriol. 183: 1655-1662.
32. Chen S, Beeby M, Murphy GE, Leadbetter JR, Hendrixson DR, Briegel A, Li Z, Shi J, Tocheva EI, Müller A, Dobro MJ, Jensen GJ. 2011. Structural diversity of bacterial flagellar motors. EMBO J. 30:2972-2981.
33. Chevance FF, Hughes KT. 2008. Coordinating assembly of a bacterial macromolecular machine. Nat. Rev. Microbiol. 6:455-465.
34. Karlinsey JE, Tanaka S, Bettenworth V, Yamaguchi S, Boos W, Aizawa SI, Hughes KT. 2000. Completion of the hook-basal body complex of the Salmonella typhimurium flagellum is coupled to FlgM secretion and fliC transcription. Mol. Microbiol. 37:1220-1231.
35. Hughes KT, Gillen KL, Semon MJ, Karlinsey JE. 1993. Sensing structural intermediates in bacterial flagellar assembly by export of a negative regulator. Science 262:1277-1280.
36. Wösten 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. 75:1577-1591.
37. Minamino T, Yamaguchi S, Macnab RM. 2000. Interaction between FliE and FlgB, a proximal rod component of the flagellar basal body of Salmonella. J. Bacteriol. 182:3029-3036.
38. Hirano T, Minamino T, Namba K, Macnab RM. 2003. Substrate specificity classes and the recognition signal for Salmonella type III flagellar export. J. Bacteriol. 185:2485-2492.
39. Henderson MJ, Milazzo FH. 1979. Arylsulfatase in Salmonella typhimurium: detection and influence of carbon source and tyramine on its synthesis. J. Bacteriol. 139:80-87.
40. Yao R, Guerry P. 1996. Molecular cloning and site-specific mutagenesis of a gene involved in arylsulfatase production in Campylobacter jejuni. J. Bacteriol. 178:3335-3338.
41. Hendrixson DR. 2006. A phase-variable mechanism controlling the Campylobacter jejuni FlgR response regulator influences commensalism. Mol. Microbiol. 61:1646-1659.
42. Sham LT, Barendt SM, Kopecky KE, Winkler ME. 2011. Essential PcsB putative peptidoglycan hydrolase interacts with the essential FtsXSpn cell division protein in Streptococcus pneumoniae D39. Proc. Natl. Acad. Sci. U. S. A. 108:E1061-E1069.
43. Johnson TL, Scott ME, Sandkvist M. 2007. Mapping critical interactive sites within the periplasmic domain of the Vibrio cholerae type II secretion protein EpsM. J. Bacteriol. 189:9082-9089.