Analysis of factors that affect FlgM-dependent type III secretion for protein purification with Salmonella enterica serovar typhimurium

Journal of Bacteriology

Volumn 196, Issue 13, 2014, Pages 2333-2347

  Guo, Shukui ^a   Alshamy, Israa ^a   Hughes, Kelly T ^a   Chevance, Fabienne F V ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CHAPERONE; FLGM PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL FLAGELLUM; CONTROLLED STUDY; GENE EXPRESSION; IONIC STRENGTH; NONHUMAN; PATHOGENICITY ISLAND; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEIN SECRETION; PROTEIN STABILITY; SALMONELLA TYPHIMURIUM; TYPE III SECRETION SYSTEM;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR CHAPERONES; MUTATION; RECOMBINANT PROTEINS; SALMONELLA TYPHIMURIUM; SUBSTRATE SPECIFICITY;

EID: 84902006339     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01572-14     Document Type: Article

References (61)

1. Sourjik V, Wingreen NS. 2012. Responding to chemical gradients: bacterial chemotaxis. Curr. Opin. Cell Biol. 24:262-268. http://dx.doi.org/10 .1016/j.ceb.2011.11.008.
2. Chevance FF, Hughes KT. 2008. Coordinating assembly of a bacterial macromolecular machine. Nat. Rev. Microbiol. 6:455-465. http://dx.doi .org/10.1038/nrmicro1887.
3. 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. http://dx.doi .org/10.1016/j.jmb.2005.11.020.
4. Macnab RM. 2003. How bacteria assemble flagella. Annu. Rev. Microbiol. 57:77-100. http://dx.doi.org/10.1146/annurev.micro.57.030502.090832.
5. Macnab RM. 2004. Type III flagellar protein export and flagellar assembly. Biochim. Biophys. Acta 1694:207-217. http://dx.doi.org/10.1016/j .bbamcr.2004.04.005.
6. Ohnishi K, Kutsukake K, Suzuki H, Iino T. 1990. Gene fliA encodes an alternative sigma factor specific for flagellar operons in Salmonella typhimurium. Mol. Gen. Genet. 221:139-147.
7. Berg HC, Anderson RA. 1973. Bacteria swim by rotating their flagellar filaments. Nature 245:380-382. http://dx.doi.org/10.1038/245380a0.
8. Ohnishi K, Kutsukake K, Suzuki H, Lino T. 1992. A novel transcriptional regulation mechanism in the flagellar regulon of Salmonella typhimurium: an antisigma factor inhibits the activity of the flagellum-specific sigma factor, sigma F. Mol. Microbiol. 6:3149-3157. http://dx.doi.org/10 .1111/j.1365-2958.1992.tb01771.x.
9. 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.
10. Kutsukake K. 1994. Excretion of the anti-sigma factor through a flagellar substructure couples flagellar gene expression with flagellar assembly in Salmonella typhimurium. Mol. Gen. Genet. 243:605-612.
11. Namba K. 2001. Roles of partly unfolded conformations in macromolecular self-assembly. Genes Cells 6:1-12. http://dx.doi.org/10.1046/j.1365-2443.2001.00384.x.
12. Fattori J, Prando A, Martins AM, Rodrigues FH, Tasic L. 2011. Bacterial secretion chaperones. Protein Pept. Lett. 18:158-166. http://dx.doi.org /10.2174/092986611794475048.
13. 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 antisigma28 factor FlgM. Genes Dev. 20:2315-2326. http://dx.doi.org/10 .1101/gad.380406.
14. Daughdrill GW, Chadsey MS, Karlinsey JE, Hughes KT, Dahlquist FW. 1997. The C-terminal half of the anti-sigma factor, FlgM, becomes structured when bound to its target, sigma 28. Nat. Struct. Biol. 4:285-291. http://dx.doi.org/10.1038/nsb0497-285.
15. Gillen KL, Hughes KT. 1991. Molecular characterization of flgM, a gene encoding a negative regulator of flagellin synthesis in Salmonella typhimurium. J. Bacteriol. 173:6453-6459.
16. Singer HM, Erhardt M, Steiner AM, Zhang MM, Yoshikami D, Bulaj G, Olivera BM, Hughes KT. 2012. Selective purification of recombinant neuroactive peptides using the flagellar type III secretion system. mBio 3(3):e00115-12. http://dx.doi.org/10.1128/mBio.00115-12.
17. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645. http://dx.doi.org/10.1073/pnas.120163297.
18. Davis RW, Botstein D, Roth JR. 1980. Advanced bacterial genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
19. Karlinsey JE. 2007. lambda-Red genetic engineering in Salmonella enterica serovar Typhimurium. Methods Enzymol. 421:199-209. http://dx .doi.org/10.1016/S0076-6879(06)21016-4.
20. 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.
21. 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.
22. Wozniak CE, Lee C, Hughes KT. 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.
23. Francez-Charlot A, Laugel B, Van Gemert A, Dubarry N, Wiorowski F, Castanie-Cornet MP, Gutierrez C, Cam K. 2004. RcsCDB His-Asp phosphorelay system negatively regulates the flhDC operon in Escherichia coli. Mol. Microbiol. 49:823-832. http://dx.doi.org/10.1046/j.1365-2958.2003 .03601.x.
24. 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.
25. 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. http: //dx.doi.org/10.1046/j.1365-2958.2002.03032.x.
26. Yokoseki T, Kutsukake K, Ohnishi K, Iino T. 1995. Functional analysis of the flagellar genes in the fliD operon of Salmonella typhimurium. Microbiology 141:1715-1722. http://dx.doi.org/10.1099/13500872-141-7-1715.
27. 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. http://dx.doi.org /10.1111/j.1365-2958.2010.07415.x.
28. Yamamoto S, Kutsukake K. 2006. FliT acts as an anti-FlhD2C2 factor in the transcriptional control of the flagellar regulon in Salmonella enterica serovar Typhimurium. J. Bacteriol. 188:6703-6708. http://dx.doi.org/10 .1128/JB.00799-06.
29. 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. http://dx.doi.org/10.1046 /j.1365-2958.1999.01372.x.
30. Lemke JJ, Durfee T, Gourse RL. 2009. DksA and ppGpp directly regulate transcription of the Escherichia coli flagellar cascade. Mol. Microbiol. 74: 1368-1379. http://dx.doi.org/10.1111/j.1365-2958.2009.06939.x.
31. Osterberg S, del Peso-Santos T, Shingler V. 2011. Regulation of alternative sigma factor use. Annu. Rev. Microbiol. 65:37-55. http://dx.doi.org /10.1146/annurev.micro.112408.134219.
32. 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.
33. 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.
34. Wei BL, Brun-Zinkernagel AM, Simecka JW, Pruss BM, Babitzke P, Romeo T. 2001. Positive regulation of motility and flhDC expression by the RNA-binding protein CsrA of Escherichia coli. Mol. Microbiol. 40: 245-256. http://dx.doi.org/10.1046/j.1365-2958.2001.02380.x.
35. Auvray F, Thomas J, Fraser GM, Hughes C. 2001. Flagellin polymerisation control by a cytosolic export chaperone. J. Mol. Biol. 308:221-229. http://dx.doi.org/10.1006/jmbi.2001.4597.
36. Bange G, Kummerer N, Engel C, Bozkurt G, Wild K, Sinning I. 2010. FlhA provides the adaptor for coordinated delivery of late flagella building blocks to the type III secretion system. Proc. Natl. Acad. Sci. U. S. A. 107:11295-11300. http://dx.doi.org/10.1073/pnas.1001383107.
37. Kinoshita M, Hara N, Imada K, Namba K, Minamino T. 2013. Interactions of bacterial flagellar chaperone-substrate complexes with FlhA contribute to co-ordinating assembly of the flagellar filament. Mol. Microbiol. 90:1249-1261. http://dx.doi.org/10.1111/mmi.12430.
38. Minamino T, Kinoshita M, Hara N, Takeuchi S, Hida A, Koya S, Glenwright H, Imada K, Aldridge PD, Namba K. 2012. Interaction of a bacterial flagellar chaperone FlgN with FlhA is required for efficient export of its cognate substrates. Mol. Microbiol. 83:775-788. http://dx.doi.org/10 .1111/j.1365-2958.2011.07964.x.
39. Barembruch C, Hengge R. 2007. Cellular levels and activity of the flagellar sigma factor FliA of Escherichia coli are controlled by FlgM-modulated proteolysis. Mol. Microbiol. 65:76-89. http://dx.doi.org/10.1111/j.1365-2958.2007.05770.x.
40. Tomoyasu T, Ohkishi T, Ukyo Y, Tokumitsu A, Takaya A, Suzuki M, Sekiya K, Matsui H, Kutsukake K, Yamamoto T. 2002. The ClpXP ATP-dependent protease regulates flagellum synthesis in Salmonella enterica serovar Typhimurium. J. Bacteriol. 184:645-653. http://dx.doi.org /10.1128/JB.184.3.645-653.2002.
41. Bonifield HR, Hughes KT. 2003. Flagellar phase variation in Salmonella enterica serovar Typhimurium is mediated by a posttranscriptional control mechanism. J. Bacteriol. 185:3567-3574. http://dx.doi.org/10.1128 /JB.185.12.3567-3574.2003.
42. Enomoto M, Stocker BA. 1975. Integration, at hag or elsewhere, of H2 (phase-2 flagellin) genes transduced from Salmonella to Escherichia coli. Genetics 81:595-614.
43. Karlinsey JE, Lonner J, Brown KL, Hughes KT. 2000. Translation/secretion coupling by type III secretion systems. Cell 102:487-497. http: //dx.doi.org/10.1016/S0092-8674(00)00053-2.
44. Galeva A, Moroz N, Yoon YH, Hughes KT, Samatey FA, Kostyukova AS. 2014. Bacterial flagellin-specific chaperone FliS interacts with antisigma factor FlgM. J. Bacteriol. 196:1215-1221. http://dx.doi.org/10.1128 /JB.01278-13.
45. Xu S, Peng Z, Cui B, Wang T, Song Y, Zhang L, Wei G, Wang Y, Shen X. 2013. FliS modulates FlgM activity by acting as a non-canonical chaperone to control late flagellar gene expression, motility and biofilm formation in Yersinia pseudotuberculosis. Environ. Microbiol. http://dx.doi.org /10.1111/1462-2920.12222.
46. Iyoda S, Kamidoi T, Hirose K, Kutsukake K, Watanabe H. 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.
47. Lucas RL, Lostroh CP, DiRusso CC, Spector MP, Wanner BL, Lee CA. 2000. Multiple factors independently regulate hilA and invasion gene expression in Salmonella enterica serovar Typhimurium. J. Bacteriol. 182: 1872-1882. http://dx.doi.org/10.1128/JB.182.7.1872-1882.2000.
48. Chubiz JE, 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.
49. 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.
50. Mouslim C, Hughes KT. 2014. The effect of cell growth phase on the regulatory cross-talk between flagellar and Spi1 virulence gene expression. PLoS Pathog. 10:e1003987. http://dx.doi.org/10.1371/journal.ppat .1003987.
51. Singer HM, Kuhne C, Deditius JA, Hughes KT, Erhardt M. 2014. The Salmonella Spi1 virulence regulatory protein HilD directly activates transcription of the flagellar master operon flhDC. J. Bacteriol. 196:1448-1457. http://dx.doi.org/10.1128/JB.01438-13.
52. Baneyx F, Georgiuo G. 1990. In vivo degradation of secreted fusion proteins by the Escherichia coli outer membrane protease OmpT. J. Bacteriol. 172:491-494.
53. Hughes KT, Dessen A, Gray JP, Grubmeyer C. 1993. The Salmonella typhimurium nadC gene: sequence determination by use of Mud-P22 and purification of quinolinate phosphoribosyltransferase. J. Bacteriol. 175: 479-486.
54. Flynn JM, Neher SB, Kim YI, Sauer RT, Baker TA. 2003. Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals. Mol. Cell 11:671-683. http://dx.doi.org/10 .1016/S1097-2765(03)00060-1.
55. Dorel C, Lejeune P, Rodrigue A. 2006. The Cpx system of Escherichia coli, a strategic signaling pathway for confronting adverse conditions and for settling biofilm communities? Res. Microbiol. 157:306-314. http://dx.doi .org/10.1016/j.resmic.2005.12.003.
56. Merdanovic M, Clausen T, Kaiser M, Huber R, Ehrmann M. 2011. Protein quality control in the bacterial periplasm. Annu. Rev. Microbiol. 65:149-168. http://dx.doi.org/10.1146/annurev-micro-090110-102925.
57. Galán JE, Curtiss R, III. 1990. Expression of Salmonella typhimurium genes required for invasion is regulated by changes in DNA supercoiling. Infect. Immun. 58:1879-1885.
58. Minamino T, Namba K. 2008. Distinct roles of the ATPase and proton motive force in bacterial flagellar protein export. Nature 451:485-488. http://dx.doi.org/10.1038/nature06449.
59. Paul K, Erhardt M, Hirano T, Blair DF, Hughes KT. 2008. Energy source of flagellar type III secretion. Nature 451:489-492. http://dx.doi.org/10 .1038/nature06497.
60. Erhardt M, Singer HM, Wee DH, Keener JP, Hughes KT. 2011. An infrequent molecular ruler controls flagellar hook length in Salmonella enterica. EMBO J. 30:2948-2961. http://dx.doi.org/10.1038/emboj.2011 .185.
61. Uchida K, Aizawa SI. 21 February 2014. The flagellar soluble protein FliK determines the minimal length of the hook in Salmonella enterica serovar Typhimurium. J. Bacteriol. http://dx.doi.org/10.1128/JB.00050-14.