RflM functions as a transcriptional repressor in the autogenous control of the salmonella flagellar master operon flhDC

Journal of Bacteriology

Volumn 195, Issue 18, 2013, Pages 4274-4282

  Singer, Hanna M ^a   Erhardt, Marc ^a,b   Hughes, Kelly T ^c  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^c UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; RFLM PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL FLAGELLUM; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSCRIPTION; MUTAGENESIS; NONHUMAN; OPERON; PRIORITY JOURNAL; SALMONELLA ENTERICA; TRANSPOSON;

BACTERIAL PROTEINS; DNA TRANSPOSABLE ELEMENTS; DOWN-REGULATION; FLAGELLA; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REGULATOR; MUTAGENESIS, INSERTIONAL; OPERON; PROMOTER REGIONS, GENETIC; SALMONELLA TYPHIMURIUM; TRANS-ACTIVATORS;

EID: 84883305151     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00728-13     Document Type: Article

References (47)

1. Macnab RM. 1996. Flagella and motility, p 123-145. In Neidhardt FC, Curtiss R, III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (ed), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed, vol 1. American Society for Microbiology, Washington, DC.
2. Fontaine F, Stewart EJ, Lindner AB, Taddei F. 2008. Mutations in two global regulators lower individual mortality in Escherichia coli. Mol. Microbiol. 67:2-14.
3. Aldridge C, Poonchareon K, Saini S, Ewen T, Soloyva A, Rao CV, Imada K, Minamino T, Aldridge PD. 2010. The interaction dynamics of a negative feedback loop regulates flagellar number in Salmonella enterica serovar Typhimurium. Mol. Microbiol. 78:1416-1430.
4. Soutourina OA, Bertin PN. 2003. Regulation cascade of flagellar expression in Gram-negative bacteria. FEMS Microbiol. Rev. 27:505-523.
5. Yokota T, Gots JS. 1970. Requirement of adenosine 3=,5=-cyclic phosphate for flagella formation in Escherichia coli and Salmonella typhimurium. J. Bacteriol. 103:513-516.
6. Zhao K, Liu M, Burgess RR. 2007. Adaptation in bacterial flagellar and motility systems: from regulon members to 'foraging'-like behavior in E. coli. Nucleic Acids Res. 35:4441-4452.
7. Wada T, Morizane T, Abo T, Tominaga A, Inoue-Tanaka K, Kutsukake K. 2011. EAL domain protein YdiV acts as an anti-FlhD4C2 factor responsible for nutritional control of the flagellar regulon in Salmonella enterica serovar Typhimurium. J. Bacteriol. 193:1600-1611.
8. Wada T, Hatamoto Y, Kutsukake K. 2012. Functional and expressional analyses of the anti-FlhD4C2 factor gene ydiV in Escherichia coli. Microbiology 158:1533-1542.
9. Prigent-Combaret C, Vidal O, Dorel C, Lejeune P. 1999. Abiotic surface sensing and biofilm-dependent regulation of gene expression in Escherichia coli. J. Bacteriol. 181:5993-6002.
10. Beloin C, Ghigo JM. 2005. Finding gene-expression patterns in bacterial biofilms. Trends Microbiol. 13:16-19.
11. Eriksson S, Lucchini S, Thompson A, Rhen M, Hinton JC. 2003. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 47:103-118.
12. Cummings LA, Wilkerson WD, Bergsbaken T, Cookson BT. 2006. In vivo, fliC expression by Salmonella enterica serovar Typhimurium is heterogeneous, regulated by ClpX, and anatomically restricted. Mol. Microbiol. 61:795-809.
13. Kutsukake K. 1997. Autogenous and global control of the flagellar master operon, flhD, inSalmonella typhimurium. Mol. Gen. Genet. 254:440-448.
14. Komeda Y, Suzuki H, Ishidsu JI, Iino T. 1976. The role of cAMP in flagellation of Salmonella typhimurium. Mol. Gen. Genet. 142:289-298.
15. Soutourina O, Kolb A, Krin E, Laurent-Winter C, Rimsky S, Danchin A, Bertin P. 1999. Multiple control of flagellum biosynthesis in Escherichia coli: role of H-NS protein and the cyclic AMP-catabolite activator protein complex in transcription of the flhDC master operon. J. Bacteriol. 181:7500-7508.
16. Campoy S, Jara M, Busquets N, de Rozas AM, Badiola I, Barbe J. 2002. Intracellular cyclic AMP concentration is decreased in Salmonella typhimurium fur mutants. Microbiology 148:1039-1048.
17. Kelly A, Goldberg MD, Carroll RK, Danino V, Hinton JC, Dorman CJ. 2004. A global role for Fis in the transcriptional control of metabolism and type III secretion in Salmonella enterica serovar Typhimurium. Microbiology 150:2037-2053.
18. Stojiljkovic I, Baumler AJ, Hantke K. 1994. Fur regulon in gram-negative bacteria. Identification and characterization of new iron-regulated Escherichia coli genes by a Fur titration assay. J. Mol. Biol. 236:531-545.
19. Erhardt M, Hughes KT. 2010. C-ring requirement in flagellar type III secretion is bypassed by FlhDC upregulation. Mol. Microbiol. 75:376- 393.
20. Libby SJ, Goebel W, Ludwig A, Buchmeier N, Bowe F, Fang FC, Guiney DG, Songer JG, Heffron F. 1994. A cytolysin encoded by Salmonella is required for survival within macrophages. Proc. Natl. Acad. Sci. U. S. A. 91:489-493.
21. Ellermeier CD, Slauch JM. 2003. RtsA and RtsB coordinately regulate expression of the invasion and flagellar genes in Salmonella enterica serovar Typhimurium. J. Bacteriol. 185:5096-5108.
22. Lehnen D, Blumer C, Polen T, Wackwitz B, Wendisch VF, Unden G. 2002. LrhA as a new transcriptional key regulator of flagella, motility and chemotaxis genes in Escherichia coli. Mol. Microbiol. 45:521-532.
23. Wang Q, Zhao Y, McClelland M, Harshey RM. 2007. The RcsCDB signaling system and swarming motility in Salmonella enterica serovar typhimurium: dual regulation of flagellar and SPI-2 virulence genes. J. Bacteriol. 189:8447-8457.
24. Francez-Charlot A, Laugel B, Van Gemert A, Dubarry N, Wiorowski F, Castanie-Cornet MP, Gutierrez C, Cam K. 2003. RcsCDB His-Asp phosphorelay system negatively regulates the flhDC operon in Escherichia coli. Mol. Microbiol. 49:823-832.
25. Saini S, Koirala S, Floess E, Mears PJ, Chemla YR, Golding I, Aldridge C, Aldridge PD, Rao CV. 2010. FliZ induces a kinetic switch in flagellar gene expression. J. Bacteriol. 192:6477-6481.
26. Saini S, Brown JD, Aldridge PD, Rao CV. 2008. FliZ is a posttranslational activator of FlhD4C2-dependent flagellar gene expression. J. Bacteriol. 190:4979-4988.
27. Wada T, Tanabe Y, Kutsukake K. 2011. FliZ acts as a repressor of the ydiV gene, which encodes an anti-FlhD4C2 factor of the flagellar regulon in Salmonella enterica serovar typhimurium. J. Bacteriol. 193: 5191-5198.
28. Takaya A, Erhardt M, Karata K, Winterberg K, Yamamoto T, Hughes KT. 2012. YdiV: a dual function protein that targets FlhDC for ClpXPdependent degradation by promoting release of DNA-bound FlhDC complex. Mol. Microbiol. 83:1268-1284.
29. Bishop RE, Leskiw BK, Hodges RS, Kay CM, Weiner JH. 1998. The entericidin locus of Escherichia coli and its implications for programmed bacterial cell death. J. Mol. Biol. 280:583-596.
30. Wozniak C, Lee C, Hughes K. 2009. T-POP array identifies EcnR and PefI-SrgD as novel regulators of flagellar gene expression. J. Bacteriol. 191:1498-1508.
31. Sanderson KE, Roth JR. 1983. Linkage map of Salmonella typhimurium, edition VI. Microbiol. Rev. 47:410-453.
32. Saini S, Ellermeier JR, Slauch JM, Rao CV. 2010. The role of coupled positive feedback in the expression of the SPI1 type three secretion system in Salmonella. PLoS Pathog. 6:e1001025.
33. Bajaj V, Lucas RL, Hwang C, Lee CA. 1996. Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol. Microbiol. 22:703- 714.
34. 28 factor FlgM. Genes Dev. 20:2315-2326.
35. Bender J, Kleckner N. 1992. IS10 transposase mutations that specifically alter target site recognition. EMBO J. 11:741-750.
36. Zhang X, Bremer H. 1995. Control of the Escherichia coli rrnB P1 promoter strength by ppGpp. J. Biol. Chem. 270:11181-11189.
37. Miller J. 1972. Assay of beta-galactosidase, p 352-355. In Experiments in molecular genetics.. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
38. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
39. Gillen KL, Hughes KT. 1991. Molecular characterization of flgM, a geneencoding a negative regulator of flagellin synthesis in Salmonella typhimurium. J. Bacteriol. 173:6453-6459.
40. Rappleye CA, Roth JR. 1997. A Tn10 derivative (T-POP) for isolation of insertions with conditional (tetracycline-dependent) phenotypes. J. Bacteriol. 179:5827-5834.
41. Shuman HA, Silhavy TJ. 2003. The art and design of genetic screens: Escherichia coli. Nat. Rev. Genet. 4:419-431.
42. Liu X, Matsumura P. 1994. The FlhD/FlhC complex, a transcriptional activator of the Escherichia coli flagellar class II operons. J. Bacteriol. 176:7345-7351.
43. Wang S, Fleming RT, Westbrook EM, Matsumura P, McKay DB. 2006. Structure of the Escherichia coli FlhDC complex, a prokaryotic heteromeric regulator of transcription. J. Mol. Biol. 355:798-808.
44. Liu X, Fujita N, Ishihama A, Matsumura P. 1995. The C-terminal region of the _ subunit of Escherichia coli RNA polymerase is required for transcriptional activation of the flagellar level II operons by the FlhD/FlhC complex. J. Bacteriol. 177:5186-5188.
45. Fraser GM, Bennett JC, Hughes C. 1999. Substrate-specific binding of hook-associated proteins by FlgN and FliT, putative chaperones for flagellum assembly. Mol. Microbiol. 32:569-580.
46. Karlinsey JE, Lonner J, Brown KL, Hughes KT. 2000. Translation/ secretion coupling by type III secretion systems. Cell 102:487-497.
47. Aldridge P, Karlinsey J, Hughes KT. 2003. The type III secretion chaperone FlgN regulates flagellar assembly via a negative feedback loop containing its chaperone substrates FlgK and FlgL. Mol. Microbiol. 49:1333-1345.