The Salmonella Spi1 virulence regulatory protein HilD directly activates transcription of the flagellar master operon flhDC

Journal of Bacteriology

Volumn 196, Issue 7, 2014, Pages 1448-1457

  Singer, Hanna M ^a   Kühne, Caroline ^b   Deditius, Julia A ^b   Hughes, Kelly T ^c   Erhardt, Marc ^a,b  

^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

HILD PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; FLAGELLUM; FLHDC GENE; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; MOLECULAR INTERACTION; MUTAGENESIS; NONHUMAN; OPERON; PATHOGENICITY ISLAND; PRIORITY JOURNAL; REGULATOR GENE; REGULATORY MECHANISM; REGULON; SALMONELLA TYPHIMURIUM; TRANSCRIPTION INITIATION; TRANSPOSON;

BACTERIAL PROTEINS; BASE SEQUENCE; FLAGELLA; GENE EXPRESSION REGULATION, BACTERIAL; GENOMIC ISLANDS; MOLECULAR SEQUENCE DATA; OPERON; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SALMONELLA TYPHIMURIUM; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84895742705     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01438-13     Document Type: Article

References (72)

1. Rubin RH, Weinstein L. 1977. Salmonellosis: microbiologic, pathogenic, and clinical features. Stratton Intercontinental Medical Book Corp., New York, NY.
2. Cornelis GR, Van Gijsegem F. 2000. Assembly and function of type III secretory systems. Annu. Rev. Microbiol. 54:735-774. http://dx.doi.org/10.1146/annurev.micro.54.1.735.
3. Galán J, Collmer A. 1999. Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284:1322-1328. http://dx.doi.org/10.1126/science.284.5418.1322.
4. Hueck C. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379-433.
5. Galan JE. 1999. Interaction of Salmonella with host cells through the centisome 63 type III secretion system. Curr. Opin. Microbiol. 2:46-50. http://dx.doi.org/10.1016/S1369-5274(99)80008-3.
6. Hensel M. 2000. Salmonella pathogenicity island 2. Mol. Microbiol. 36: 1015-1023. http://dx.doi.org/10.1046/j.1365-2958.2000.01935.x.
7. Hapfelmeier S, Ehrbar K, Stecher B, Barthel M, Kremer M, Hardt WD. 2004. Role of the Salmonella pathogenicity island 1 effector proteins SipA, SopB, SopE, and SopE2 in Salmonella enterica subspecies 1 serovar Typhimurium colitis in streptomycin-pretreated mice. Infect. Immun. 72:795-809. http://dx.doi.org/10.1128/IAI.72.2.795-809.2004.
8. Muller AJ, Hoffmann C, Galle M, Van Den Broeke A, Heikenwalder M, Falter L, Misselwitz B, Kremer M, Beyaert R, Hardt WD. 2009. The S. Typhimurium effector SopE induces caspase-1 activation in stromal cells to initiate gut inflammation. Cell Host Microbe 6:125-136. http://dx.doi.org/10.1016/j.chom.2009.07.007.
9. Muller AJ, Kaiser P, Dittmar KE, Weber TC, Haueter S, Endt K, Songhet P, Zellweger C, Kremer M, Fehling HJ, Hardt WD. 2012. Salmonella gut invasion involves TTSS-2-dependent epithelial traversal, basolateral exit, and uptake by epithelium-sampling lamina propria phagocytes. Cell Host Microbe 11:19-32. http://dx.doi.org/10.1016/j.chom.2011.11.013.
10. Cirillo DM, Valdivia RH, Monack DM, Falkow S. 1998. Macrophagedependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol. Microbiol. 30: 175-188. http://dx.doi.org/10.1046/j.1365-2958.1998.01048.x.
11. Hensel M, Shea JE, Waterman SR, Mundy R, Nikolaus T, Banks G, Vazquez-Torres A, Gleeson C, Fang FC, Holden DW. 1998. Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol. Microbiol. 30:163-174. http://dx.doi.org/10.1046/j.1365-2958.1998.01047.x.
12. Ellermeier CD, Ellermeier JR, Slauch JM. 2005. HilD, HilC and RtsA constitute a feed forward loop that controls expression of the SPI1 type three secretion system regulator hilA in Salmonella enterica serovar Typhimurium. Mol. Microbiol. 57:691-705. http://dx.doi.org/10.1111/j.1365-2958.2005.04737.x.
13. 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. http://dx.doi.org/10.1371/journal.ppat.1001025.
14. Gophna U, Ron EZ, Graur D. 2003. Bacterial type III secretion systems are ancient and evolved by multiple horizontal-transfer events. Gene 312: 151-163. http://dx.doi.org/10.1016/S0378-1119(03)00612-7.
15. Van Gijsegem F, Gough C, Zischek C, Niqueux E, Arlat M, Genin S, Barberis P, German S, Castello P, Boucher C. 1995. The hrp gene locus of Pseudomonas solanacearum, which controls the production of a type III secretion system, encodes eight proteins related to components of the bacterial flagellar biogenesis complex. Mol. Microbiol. 15:1095-1114. http://dx.doi.org/10.1111/j.1365-2958.1995.tb02284.x.
16. Kubori T, Matsushima Y, Nakamura D, Uralil J, Lara-Tejero M, Sukhan A, Galán JE, Aizawa SI. 1998. Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280: 602-605. http://dx.doi.org/10.1126/science.280.5363.602.
17. Kubori T, Sukhan A, Aizawa SI, Galan JE. 2000. Molecular characterization and assembly of the needle complex of the Salmonella typhimurium type III protein secretion system. Proc. Natl. Acad. Sci. U. S. A. 97:10225-10230. http://dx.doi.org/10.1073/pnas.170128997.
18. 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. http://dx.doi.org/10.1126/science.8235660.
19. Chadsey MS, Karlinsey JE, Hughes KT. 1998. The flagellar anti-sigma factor FlgM actively dissociates Salmonella typhimurium sigma28 RNA polymerase holoenzyme. Genes Dev. 12:3123-3136. http://dx.doi.org/10.1101/gad.12.19.3123.
20. Chadsey MS, Hughes KT. 2001. A multipartite interaction between Salmonella transcription factor sigma28 and its anti-sigma factor FlgM: implications for sigma28 holoenzyme destabilization through stepwise binding. J. Mol. Biol. 306:915-929. http://dx.doi.org/10.1006/jmbi.2001.4438.
21. 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. http://dx.doi.org/10.1099/mic.0.27209-0.
22. 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.
23. 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.
24. 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. http://dx.doi.org/10.1128/JB.185.17.5096-5108.2003.
25. Erhardt M, Hughes KT. 2010. C-ring requirement in flagellar type III secretion is bypassed by FlhDC upregulation. Mol. Microbiol. 75:376-393. http://dx.doi.org/10.1111/j.1365-2958.2009.06973.x.
26. Singer HM, Erhardt M, Hughes KT. 2013. RflM functions as transcriptional repressor in the autogenous control of the Salmonella flagellar master operon flhDC. J. Bacteriol. 195:4274-4282. http://dx.doi.org/10.1128/JB.00728-13.
27. Kutsukake K. 1997. Autogenous and global control of the flagellar master operon, flhD, inSalmonella typhimurium. Mol. Gen. Genet. 254:440-448. http://dx.doi.org/10.1007/s004380050437.
28. 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. http://dx.doi.org/10.1128/JB.01177-08.
29. 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. http://dx.doi.org/10.1128/JB.01198-07.
30. Macnab RM. 1996. Flagella and motility, p 123-145. In Neidhardt FC, Curtiss R, III, Ingraham JL, Lin ECC, Low KB, Magasanik B, ReznikoffWS, Riley M, Schaechter M, Umbarger HE (ed), Escherichia coli and Sal- monella: cellular and molecular biology, 2nd ed, vol 1. ASM Press, Washington, DC.
31. 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.
32. 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.
33. 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. http://dx.doi.org/10.1093/nar/gkm456.
34. 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. http://dx.doi.org/10.1128/JB.01494-10.
35. 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.
36. Beloin C, Ghigo JM. 2005. Finding gene-expression patterns in bacterial biofilms. Trends Microbiol. 13:16-19. http://dx.doi.org/10.1016/j.tim.2004.11.008.
37. 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. http://dx.doi.org/10.1046/j.1365-2958.2003.03313.x.
38. 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. http://dx.doi.org/10.1111/j.1365-2958.2006.05271.x.
39. Hautefort I, Thompson A, Eriksson-Ygberg S, Parker ML, Lucchini S, Danino V, Bongaerts RJ, Ahmad N, Rhen M, Hinton JC. 2008. During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems. Cell. Microbiol. 10: 958-984. http://dx.doi.org/10.1111/j.1462-5822.2007.01099.x.
40. Cummings LA, Barrett SL, Wilkerson WD, Fellnerova I, Cookson BT. 2005. FliC-specific CD4+ T cell responses are restricted by bacterial regulation of antigen expression. J. Immunol. 174:7929-7938.
41. Lucas RL, Lee CA. 2001. Roles of hilC and hilD in regulation of hilA expression in Salmonella enterica serovar Typhimurium. J. Bacteriol. 183: 2733-2745. http://dx.doi.org/10.1128/JB.183.9.2733-2745.2001.
42. Iyoda S. 2001. A flagellar gene fliZ regulates the expression of invasion genes and virulence phenotype in Salmonella enterica serovar Typhimurium. Microb. Pathog. 30:81-90. http://dx.doi.org/10.1006/mpat.2000.0409.
43. Kage H, Takaya A, Ohya M, Yamamoto T. 2008. Coordinated regulation of expression of Salmonella pathogenicity island 1 and flagellar type III secretion systems by ATP-dependent ClpXP protease. J. Bacteriol. 190: 2470-2478. http://dx.doi.org/10.1128/JB.01385-07.
44. Chubiz JEC, Golubeva YA, Lin D, Miller LD, Slauch JM. 2010. FliZ regulates expression of the Salmonella pathogenicity island 1 invasion locus by controlling HilD protein activity in Salmonella enterica serovar Typhimurium. J. Bacteriol. 192:6261-6270. http://dx.doi.org/10.1128/JB.00635-10.
45. Kutsukake K, Ikebe T, Yamamoto S. 1999. Two novel regulatory genes, fliT and fliZ, in the flagellar regulon of Salmonella. Genes Genet. Syst. 74:287-292. http://dx.doi.org/10.1266/ggs.74.287.
46. 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. http://dx.doi.org/10.1128/JB.00751-10.
47. 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. http://dx.doi.org/10.1128/JB.05441-11.
48. 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. http://dx.doi.org/10.1111/j.1365-2958.2012.08007.x.
49. Stewart MK, Cummings LA, Johnson ML, Berezow AB, Cookson BT. 2011. Regulation of phenotypic heterogeneity permits Salmonella evasion of the host caspase-1 inflammatory response. Proc. Natl. Acad. Sci. U. S. A. 108:20742-20747. http://dx.doi.org/10.1073/pnas.1108963108.
50. Hisert KB, MacCoss M, Shiloh MU, Darwin KH, Singh S, Jones RA, Ehrt S, Zhang Z, Gaffney BL, Gandotra S, Holden DW, Murray D, Nathan C. 2005. A glutamate-alanine-leucine (EAL) domain protein of Salmonella controls bacterial survival in mice, antioxidant defence and killing of macrophages: role of cyclic diGMP. Mol. Microbiol. 56:1234-1245. http://dx.doi.org/10.1111/j.1365-2958.2005.04632.x.
51. Thijs IM, De Keersmaecker SC, Fadda A, Engelen K, Zhao H, Mc- Clelland M, Marchal K, Vanderleyden J. 2007. Delineation of the Salmonella enterica serovar Typhimurium HilA regulon through genomewide location and transcript analysis. J. Bacteriol. 189:4587-4596. http://dx.doi.org/10.1128/JB.00178-07.
52. Teplitski M, Goodier RI, Ahmer BMM. 2003. Pathways leading from BarA/SirA to motility and virulence gene expression in Salmonella. J. Bacteriol. 185:7257-7265. http://dx.doi.org/10.1128/JB.185.24.7257-7265.2003.
53. Bustamante VH, Martinez LC, Santana FJ, Knodler LA, Steele-Mortimer O, Puente JL. 2008. HilD-mediated transcriptional cross-talk between SPI-1 and SPI-2. Proc. Natl. Acad. Sci. U. S. A. 105:14591-14596. http://dx.doi.org/10.1073/pnas.0801205105.
54. Bertani G. 2004. Lysogeny at mid-twentieth century: P1, P2, and other experimental systems. J. Bacteriol. 186:595-600. http://dx.doi.org/10.1128/JB.186.3.595-600.2004.
55. Sanderson KE, Roth JR. 1983. Linkage map of Salmonella typhimurium, edition VI. Microbiol. Rev. 47:410-453.
56. Aldridge PD, Karlinsey JE, Aldridge C, Birchall C, Thompson D, Yagasaki J, Hughes KT. 2006. The flagellar-specific transcription factor, sigma28, is the type III secretion chaperone for the flagellar-specific anti-sigma28 factor FlgM. Genes Dev. 20:2315-2326. http://dx.doi.org/10.1101/gad.380406.
57. PfafflMW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45. http://dx.doi.org/10.1093/nar/29.9.e45.
58. Andreasson C, Fiaux J, Rampelt H, Mayer MP, Bukau B. 2008. Hsp110 is a nucleotide-activated exchange factor for Hsp70. J. Biol. Chem. 283: 8877-8884. http://dx.doi.org/10.1074/jbc. M710063200.
59. Schechter LM, Lee CA. 2001. AraC/XylS family members, HilC and HilD, directly bind and derepress the Salmonella typhimurium hilA promoter. Mol. Microbiol. 40:1289-1299. http://dx.doi.org/10.1046/j.1365-2958.2001.02462.x.
60. Olekhnovich IN, Kadner RJ. 2002. DNA-binding activities of the HilC and HilD virulence regulatory proteins of Salmonella enterica serovar Typhimurium. J. Bacteriol. 184:4148-4160. http://dx.doi.org/10.1128/JB.184.15.4148-4160.2002.
61. Sturm A, Heinemann M, Arnoldini M, Benecke A, Ackermann M, Benz M, Dormann J, Hardt W-D. 2011. The cost of virulence: retarded growth of Salmonella Typhimurium cells expressing type III secretion system 1. PLoS Pathog. 7:e1002143. http://dx.doi.org/10.1371/journal.ppat.1002143.
62. 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. http://dx.doi.org/10.1046/j.1365-2958.2000.02081.x.
63. Yanagihara S, Iyoda S, Ohnishi K, Iino T, Kutsukake K. 1999. Structure and transcriptional control of the flagellar master operon of Salmonella typhimurium. Genes Genet. Syst. 74:105-111. http://dx.doi.org/10.1266/ggs.74.105.
64. Olekhnovich IN, Kadner RJ. 2007. Role of nucleoid-associated proteins Hha and H-NS in expression of Salmonella enterica activators HilD, HilC, and RtsA required for cell invasion. J. Bacteriol. 189:6882-6890. http://dx.doi.org/10.1128/JB.00905-07.
65. Kroger C, Colgan A, Srikumar S, Handler K, Sivasankaran SK, Hammarlof DL, Canals R, Grissom JE, Conway T, Hokamp K, Hinton JC. 2013. An infection-relevant transcriptomic compendium for Salmonella enterica serovar Typhimurium. Cell Host Microbe 14:683-695. http://dx.doi.org/10.1016/j.chom.2013.11.010.
66. Lanois A, Jubelin G, Givaudan A. 2008. FliZ, a flagellar regulator, is at the crossroads between motility, haemolysin expression and virulence in the insect pathogenic bacterium Xenorhabdus. Mol. Microbiol. 68:516-533. http://dx.doi.org/10.1111/j.1365-2958.2008.06168.x.
67. Golubeva YA, Sadik AY, Ellermeier JR, Slauch JM. 2012. Integrating global regulatory input into the salmonella pathogenicity island 1 type III secretion system. Genetics 190:70-90. http://dx.doi.org/10.1534/genetics.111.132779.
68. Saini S, Slauch JM, Aldridge PD, Rao CV. 2010. Role of cross talk in regulating the dynamic expression of the flagellar Salmonella pathogenicity island 1 and type 1 fimbrial genes J. Bacteriol. 192:5767-5777. http://dx.doi.org/10.1128/JB.00624-10.
69. Sano G, Takada Y, Goto S, Maruyama K, Shindo Y, Oka K, Matsui H, Matsuo K. 2007. Flagella facilitate escape of Salmonella from oncotic macrophages. J. Bacteriol. 189:8224-8232. http://dx.doi.org/10.1128/JB.00898-07.
70. Byrne B, Swanson MS. 1998. Expression of Legionella pneumophila virulence traits in response to growth conditions. Infect. Immun. 66:3029-3034.
71. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Res. 14:1188-1190. http://dx.doi.org/10.1101/gr.849004.
72. Mouslim C, Hughes KT. The effect of cell growth phase on the regulatory cross-talk between flagellar and Spi1 virulence gene expression. PLOS Pathog., in press.