A Salmonella type three secretion effector/chaperone complex adopts a hexameric ring-like structure

Journal of Bacteriology

Volumn 197, Issue 4, 2015, Pages 688-698

  Roblin, Pierre ^a,b   Dewitte, Frédérique ^c   Villeret, Vincent ^c   Biondi, Emanuele G ^c   Bompard, Coralie ^c  

^a INRA   (France)

^b SYNCHROTRON SOLEIL   (France)

^c UNIV LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; CHAPERONE; SIGE PROTEIN; SOPB PROTEIN; UNCLASSIFIED DRUG; BACTERIAL SECRETION SYSTEM; SIGE PROTEIN, BACTERIA; SIGMA FACTOR; SOPB PROTEIN, BACTERIA;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CHEMICAL ANALYSIS; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; SALMONELLA; TYPE III SECRETION SYSTEM; X RAY CRYSTALLOGRAPHY; BACTERIAL SECRETION SYSTEM; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; PROTEIN TERTIARY STRUCTURE; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SMALL ANGLE SCATTERING;

ANIMALIA; BACTERIA (MICROORGANISMS); EUKARYOTA; SALMONELLA;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; MODELS, MOLECULAR; MOLECULAR CHAPERONES; PROTEIN STRUCTURE, TERTIARY; SALMONELLA TYPHIMURIUM; SCATTERING, SMALL ANGLE; SIGMA FACTOR;

EID: 84921824920     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.02294-14     Document Type: Article

References (50)

1. Galan JE, 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.
2. Minamino T, Imada K, Namba K. 2008. Mechanisms of type III protein export for bacterial flagellar assembly. Mol Biosyst 4:1105-1115. http://dx.doi.org/10.1039/b808065h.
3. Erhardt M, Namba K, Hughes KT. 2010. Bacterial nanomachines: the flagellum and type III injectisome. Cold Spring Harb Perspect Biol 2:a000299. http://dx.doi.org/10.1101/cshperspect.a000299.
4. Marlovits TC, Kubori T, Sukhan A, Thomas DR, Galan JE, Unger VM. 2004. Structural insights into the assembly of the type III secretion needle complex. Science 306:1040-1042. http://dx.doi.org/10.1126/science.1102610.
5. Marlovits TC, Kubori T, Lara-Tejero M, Thomas D, Unger VM, Galan JE. 2006. Assembly of the inner rod determines needle length in the type III secretion injectisome. Nature 441:637-640. http://dx.doi.org/10.1038/nature04822.
6. Schraidt O, Marlovits TC. 2011. Three-dimensional model of Salmonella's needle complex at subnanometer resolution. Science 331:1192-1195. http://dx.doi.org/10.1126/science.1199358.
7. Buttner D. 2012. Protein export according to schedule: architecture, assembly, and regulation of type III secretion systems from plant- and animal-pathogenic bacteria. Microbiol Mol Biol Rev 76:262-310. http://dx.doi.org/10.1128/MMBR.05017-11.
8. Kawamoto A, Morimoto YV, Miyata T, Minamino T, Hughes KT, Kato T, Namba K. 2013. Common and distinct structural features of Salmonella injectisome and flagellar basal body. Sci Rep 3:3369. http://dx.doi.org/10.1038/srep03369.
9. Li H, Sourjik V. 2011. Assembly and stability of flagellar motor in Escherichia coli. Mol Microbiol 80:886-899. http://dx.doi.org/10.1111/j.1365-2958.2011.07557.x.
10. 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. http://dx.doi.org/10.1111/j.1365-2958.2011.07830.x.
11. Lilic M, Quezada CM, Stebbins CE. 2010. A conserved domain in type III secretion links the cytoplasmic domain of InvA to elements of the basal body. Acta Crystallogr D Biol Crystallogr 66:709-713. http://dx.doi.org/10.1107/S0907444910010796.
12. Worrall LJ, Vuckovic M, Strynadka NC. 2010. Crystal structure of the C-terminal domain of the Salmonella type III secretion system export apparatus protein InvA. Protein Sci 19:1091-1096. http://dx.doi.org/10.1002/pro.382.
13. Wattiau P, Cornelis GR. 1993. SycE, a chaperone-like protein of Yersinia enterocolitica involved in Ohe secretion of YopE. Mol Microbiol 8:123-131. http://dx.doi.org/10.1111/j.1365-2958.1993.tb01209.x.
14. Stebbins CE, Galan JE. 2003. Priming virulence factors for delivery into the host. Nat Rev Mol Cell Biol 4:738-743. http://dx.doi.org/10.1038/nrm1201.
15. Stebbins CE, Galan JE. 2001. Maintenance of an unfolded polypeptide by a cognate chaperone in bacterial type III secretion. Nature 414:77-81. http://dx.doi.org/10.1038/35102073.
16. Roblin P, Lebrun P, Rucktooa P, Dewitte F, Lens Z, Receveur-Brechot V, Raussens V, Villeret V, Bompard C. 2013. The structural organization of the N-terminus domain of SopB, a virulence factor of Salmonella, depends on the nature of its protein partners. Biochim Biophys Acta 1834::2564-2572. http://dx.doi.org/10.1016/j.bbapap.2013.09.014.
17. Lilic M, Vujanac M, Stebbins CE. 2006. A common structural motif in the binding of virulence factors to bacterial secretion chaperones. Mol Cell 21:653-664. http://dx.doi.org/10.1016/j.molcel.2006.01.026.
18. Remaut H, Waksman G. 2006. Protein-protein interaction through betastrand addition. Trends Biochem Sci 31:436-444. http://dx.doi.org/10.1016/j.tibs.2006.06.007.
19. Akeda Y, Galan JE. 2005. Chaperone release and unfolding of substrates in type III secretion. Nature 437:911-915. http://dx.doi.org/10.1038/nature03992.
20. Muller SA, Pozidis C, Stone R, Meesters C, Chami M, Engel A, Economou A, Stahlberg H. 2006. Double hexameric ring assembly of the type III protein translocase ATPase HrcN. Mol Microbiol 61:119-125. http://dx.doi.org/10.1111/j.1365-2958.2006.05219.x.
21. Boonyom R, Karavolos MH, Bulmer DM, Khan CM. 2010. Salmonella pathogenicity island 1 (SPI-1) type III secretion of SopD involves N- and C-terminal signals and direct binding to the InvC ATPase. Microbiology 156:1805-1814. http://dx.doi.org/10.1099/mic.0.038117-0.
22. Lorenz C, Schulz S, Wolsch T, Rossier O, Bonas U, Buttner D. 2008. HpaC controls substrate specificity of the Xanthomonas type III secretion system. PLoS Pathog 4:e1000094. http://dx.doi.org/10.1371/journal.ppat.1000094.
23. Lara-Tejero M, Kato J, Wagner S, Liu X, Galan JE. 2011. A sorting platform determines the order of protein secretion in bacterial type III systems. Science 331:1188-1191. http://dx.doi.org/10.1126/science.1201476.
24. Raffatellu M, Wilson RP, Chessa D, Andrews-Polymenis H, Tran QT, Lawhon S, Khare S, Adams LG, Baumler AJ. 2005. SipA, SopA, SopB, SopD, and SopE2 contribute to Salmonella enterica serotype Typhimurium invasion of epithelial cells. Infect Immun 73:146-154. http://dx.doi.org/10.1128/IAI.73.1.146-154.2005.
25. Steele-Mortimer O, Knodler LA, Marcus SL, Scheid MP, Goh B, Pfeifer CG, Duronio V, Finlay BB. 2000. Activation of Akt/protein kinase B in epithelial cells by the Salmonella typhimurium effector sigD. J Biol Chem 275:37718-37724. http://dx.doi.org/10.1074/jbc. M008187200.
26. Hernandez LD, Hueffer K, Wenk MR, Galan JE. 2004. Salmonella modulates vesicular traffic by altering phosphoinositide metabolism. Science 304:1805-1807. http://dx.doi.org/10.1126/science.1098188.
27. Darwin KH, Robinson LS, Miller VL. 2001. SigE is a chaperone for the Salmonella enterica serovar Typhimurium invasion protein SigD. J Bacteriol 183:1452-1454. http://dx.doi.org/10.1128/JB.183.4.1452-1454.2001.
28. Luo Y, Bertero MG, Frey EA, Pfuetzner RA, Wenk MR, Creagh L, Marcus SL, Lim D, Sicheri F, Kay C, Haynes C, Finlay BB, Strynadka NC. 2001. Structural and biochemical characterization of the type III secretion chaperones CesT and SigE. Nat Struct Biol 8:1031-1036. http://dx.doi.org/10.1038/nsb717.
29. Knodler LA, Bertero M, Yip C, Strynadka NC, Steele-Mortimer O. 2006. Structure-based mutagenesis of SigE verifies the importance of hydrophobic and electrostatic residues in type III chaperone function. Mol Microbiol 62::928-940. http://dx.doi.org/10.1111/j.1365-2958.2006.05418.x.
30. Marcus SL, Knodler LA, Finlay BB. 2002. Salmonella enterica serovar Typhimurium effector SigD/SopB is membrane-associated and ubiquitinated inside host cells. Cell Microbiol 4:435-446. http://dx.doi.org/10.1046/j.1462-5822.2002.00202.x.
31. David G, Perez J. 2009. Combined sampler robot and high-performance liquid chromatography: a fully automated system for biological small angle X-ray scattering experiments at the synchrotron SOLEIL SWING beamline. J Appl Crystallogr 42:892-900. http://dx.doi.org/10.1107/S0021889809029288.
32. Konarev PV, Volkov VV, Petoukhov MV, Svergun DI. 2006. ATSAS 2.1, a program package for small-angle scattering data analysis. J Appl Crystallogr 39:277-286. http://dx.doi.org/10.1107/S0021889806004699.
33. Fisher H, de Oliveira Neto M, Napolitano HB, Polikarpov I, Craievich AF. 2010. determination of the molecular weight of proteins in solution from a single small-angle X-ray scattering measurement on a relative scale. J Appl Crystallogr 43:101-109. http://dx.doi.org/10.1107/S0021889809043076.
34. Konarev PV, Volkov VV, Sokolova AV, Koch MHJ, Svergun DI. 2003. PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J Appl Crystallogr 36:1277-1282. http://dx.doi.org/10.1107/S0021889803012779.
35. Svergun DI. 1992. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J Appl Crystallogr 25:495-503. http://dx.doi.org/10.1107/S0021889892001663.
36. Hura GL, Budworth H, Dyer KN, Rambo RP, Hammel M, McMurray CT, Tainer JA. 2013. Comprehensive macromolecular conformations mapped by quantitative SAXS analyses. Nat Methods 10:453-454. http://dx.doi.org/10.1038/nmeth.2453.
37. Svergun DI, Petoukhov MV, Koch MH. 2001. Determination of domain structure of proteins from X-ray solution scattering. Biophys J 80:2946-2953. http://dx.doi.org/10.1016/S0006-3495(01)76260-1.
38. Volkov VV, Svergun DI. 2003. Uniqueness of ab initio shape determination in small angle scattering. J Appl Crystallogr 36:860-864. http://dx.doi.org/10.1107/S0021889803000268.
39. Kozin MB, Svergun DI. 2001. Automated matching of high- and lowresolution structural models. J Appl Crystallogr 34:33-41. http://dx.doi.org/10.1107/S0021889800014126.
40. Zhang Y. 2008. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9:40. http://dx.doi.org/10.1186/1471-2105-9-40.
41. Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363-371. http://dx.doi.org/10.1038/nprot.2009.2.
42. Evrard G, Mareuil F, Bontems F, Sizun C, Perez J. 2011. DADIMODO: a program for refining the structure of multidomain proteins and complexes against small-angle scattering data and NMR-derived restraints. J Appl Crystallogr 44:1264-1271. http://dx.doi.org/10.1107/S0021889811035758.
43. Petoukhov MV, Svergun DI. 2005. Global rigid body modeling of macromolecular complexes against small-angle scattering data. Biophys J 89::1237-1250. http://dx.doi.org/10.1529/biophysj.105.064154.
44. Petoukhov MV, Billas IM, Takacs M, Graewert MA, Moras D, Svergun DI. 2013. Reconstruction of quaternary structure from X-ray scattering by equilibrium mixtures of biological macromolecules. Biochemistry 52::6844-6855. http://dx.doi.org/10.1021/bi400731u.
45. Zarivach R, Vuckovic M, Deng W, Finlay BB, Strynadka NC. 2007. Structural analysis of a prototypical ATPase from the type III secretion system. Nat Struct Mol Biol 14:131-137. http://dx.doi.org/10.1038/nsmb1196.
46. Buchko GW, Niemann G, Baker ES, Belov ME, Smith RD, Heffron F, Adkins JN, McDermott JE. 2010. A multi-pronged search for a common structural motif in the secretion signal of Salmonella enterica serovar Typhimurium type III effector proteins. Mol Biosyst 6:2448-2458. http://dx.doi.org/10.1039/c0mb00097c.
47. Cherradi Y, Schiavolin L, Moussa S, Meghraoui A, Meksem A, Biskri L, Azarkan M, Allaoui A, Botteaux A. 2013. Interplay between predicted inner-rod and gatekeeper in controlling substrate specificity of the type III secretion system. Mol Microbiol 87:1183-1199. http://dx.doi.org/10.1111/mmi.12158.
48. Kim BH, Kim HG, Kim JS, Jang JI, Park YK. 2007. Analysis of functional domains present in the N-terminus of the SipB protein. Microbiology 153:2998-3008. http://dx.doi.org/10.1099/mic.0.2007/007872-0.
49. Trcek J, Wilharm G, Jacobi CA, Heesemann J. 2002. Yersinia enterocolitica YopQ: strain-dependent cytosolic accumulation and posttranslational secretion. Microbiology 148:1457-1465.
50. Abrusci P, Vergara-Irigaray M, Johnson S, Beeby MD, Hendrixson DR, Roversi P, Friede ME, Deane JE, Jensen GJ, Tang CM, Lea SM. 2013. Architecture of the major component of the type III secretion system export apparatus. Nat Struct Mol Biol 20:99-104. http://dx.doi.org/10.1038/nsmb.2452.