The Architecture of the Cytoplasmic Region of Type III Secretion Systems

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Makino, Fumiaki ^a,b   Shen, Dakang ^a   Kajimura, Naoko ^a,b   Kawamoto, Akihiro ^b   Pissaridou, Panayiota ^a,c   Oswin, Henry ^a   Pain, Maria ^a,d   Murillo, Isabel ^a   Namba, Keiichi ^b   Blocker, Ariel J ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b OSAKA UNIVERSITY   (Japan)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF TROMSØ   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84989811783     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep33341     Document Type: Article

References (42)

1. Burkinshaw, B. J. & Strynadka, N. C. Assembly and structure of the T3SS. Biochim Biophys Acta 1843, 1649-1663, doi: 10. 1016/j. bbamcr. 2014. 01. 035 (2014)
2. Abrusci, P. et al. Architecture of the major component of the type III secretion system export apparatus. Nat Struct Mol Biol 20, 99-104, doi: 10. 1038/nsmb. 2452 (2013)
3. Chen, S. et al. Structural diversity of bacterial flagellar motors. Embo J 30, 2972-2981, doi: 10. 1038/emboj. 2011. 186 (2011)
4. Hu, B. et al. Visualization of the type III secretion sorting platform of Shigella flexneri. Proc Natl Acad Sci USA 112, 1047-1052, doi: 10. 1073/pnas. 1411610112 (2015)
5. Zhao, X., Norris, S. J. & Liu, J. Molecular architecture of the bacterial flagellar motor in cells. Biochemistry 53, 4323-4333, doi: 10. 1021/bi500059y (2014)
6. Thomas, D. R., Francis, N. R., Xu, C. & DeRosier, D. J. The three-dimensional structure of the flagellar rotor from a clockwise-locked mutant of Salmonella enterica serovar Typhimurium. J Bacteriol 188, 7039-7048 (2006)
7. Ibuki, T. et al. Common architecture of the flagellar type III protein export apparatus and F-and V-type ATPases. Nat Struct Mol Biol 18, 277-282, doi: nsmb. 1977 10. 1038/nsmb. 1977 (2011)
8. Jouihri, N. et al. MxiK and MxiN interact with the Spa47 ATPase and are required for transit of the needle components MxiH and MxiI, but not of Ipa proteins, through the type III secretion apparatus of Shigella flexneri. Mol Microbiol 49, 755-767 (2003)
9. Brown, P. N., Mathews, M. A., Joss, L. A., Hill, C. P. & Blair, D. F. Crystal structure of the flagellar rotor protein FliN from Thermotoga maritima. J Bacteriol 187, 2890-2902, doi: 10. 1128/JB. 187. 8. 2890-2902. 2005 (2005)
10. Park, S. Y., Lowder, B., Bilwes, A. M., Blair, D. F. & Crane, B. R. Structure of FliM provides insight into assembly of the switch complex in the bacterial flagella motor. Proc Natl Acad Sci USA 103, 11886-11891, doi: 10. 1073/pnas. 0602811103 (2006)
11. Notti, R. Q., Bhattacharya, S., Lilic, M. & Stebbins, C. E. A common assembly module in injectisome and flagellar type III secretion sorting platforms. Nat Commun 6, 7125, doi: 10. 1038/ncomms8125 (2015)
12. Yu, X. J., Liu, M., Matthews, S. & Holden, D. W. Tandem translation generates a chaperone for the Salmonella type III secretion system protein SsaQ. J Biol Chem 286, 36098-36107, doi: 10. 1074/jbc. M111. 278663 (2011)
13. Bzymek, K. P., Hamaoka, B. Y. & Ghosh, P. Two translation products of Yersinia yscQ assemble to form a complex essential to type III secretion. Biochemistry 51, 1669-1677, doi: 10. 1021/bi201792p (2012)
14. McDowell, M. A. et al. Characterisation of Shigella Spa33 and Thermotoga FliM/N reveals a new model for C-ring assembly in T3SS. Mol Microbiol 99, 749-766, doi: 10. 1111/mmi. 13267 (2016)
15. Zhao, R., Pathak, N., Jaffe, H., Reese, T. S. & Khan, S. FliN is a major structural protein of the C-ring in the Salmonella typhimurium flagellar basal body. J Mol Biol 261, 195-208, doi: 10. 1006/jmbi. 1996. 0452 (1996)
16. Diepold, A., Kudryashev, M., Delalez, N. J., Berry, R. M. & Armitage, J. P. Composition, formation, and regulation of the cytosolic c-ring, a dynamic component of the type III secretion injectisome. PLoS Biol 13, e1002039, doi: 10. 1371/journal. pbio. 1002039 (2015)
17. Kawamoto, A. et al. Common and distinct structural features of Salmonella injectisome and flagellar basal body. Scientific reports 3, 3369, doi: 10. 1038/srep03369 (2013)
18. Kudryashev, M. et al. In situ structural analysis of the Yersinia enterocolitica injectisome. eLife 2, e00792, doi: 10. 7554/eLife. 00792 (2013)
19. Castano-Diez, D., Kudryashev, M., Arheit, M. & Stahlberg, H. Dynamo: A flexible, user-friendly development tool for subtomogram averaging of cryo-EM data in high-performance computing environments. J Struct Biol 178, 139-151, doi: 10. 1016/j. jsb. 2011. 12. 017 (2012)
20. Hodgkinson, J. L. et al. Three-dimensional reconstruction of the Shigella T3SS transmembrane regions reveals 12-fold symmetry and novel features throughout. Nat Struct Mol Biol 16, 477-485 (2009)
21. Schuch, R. & Maurelli, A. T. MxiM and MxiJ, base elements of the Mxi-Spa type III secretion system of Shigella, interact with and stabilize the MxiD secretin in the cell envelope. J Bacteriol 183, 6991-6998 (2001)
22. Okon, M. et al. Structural characterization of the type-III pilot-secretin complex from Shigella flexneri. Structure 16, 1544-1554, doi: 10. 1016/j. str. 2008. 08. 006 (2008)
23. Johnson, S. & Blocker, A. Characterization of soluble complexes of the Shigella flexneri type III secretion system ATPase. FEMS Microbiol Lett 286, 274-278 (2008)
24. Bahrani, F. K., Sansonetti, P. J. & Parsot, C. Secretion of Ipa proteins by Shigella flexneri: inducer molecules and kinetics of activation. Infect Immun 65, 4005-4010 (1997)
25. Cherradi, Y., Hachani, A. & Allaoui, A. Spa13 of Shigella flexneri has a dual role: chaperone escort and export gate-activator switch of the type III secretion system. Microbiology, doi: 10. 1099/mic. 0. 071712-0 (2013)
26. Schuch, R. & Maurelli, A. T. Spa33, a cell surface-associated subunit of the Mxi-Spa type III secretory pathway of Shigella flexneri, regulates Ipa protein traffic. Infect Immun 69, 2180-2189 (2001)
27. Roblin, P., Dewitte, F., Villeret, V., Biondi, E. G. & Bompard, C. A Salmonella type three secretion effector/chaperone complex adopts a hexameric ring-like structure. J Bacteriol 197, 688-698, doi: 10. 1128/JB. 02294-14 (2015)
28. Minamino, T. & MacNab, R. M. FliH, a soluble component of the type III flagellar export apparatus of Salmonella, forms a complex with FliI and inhibits its ATPase activity. Mol Microbiol 37, 1494-1503, doi: mmi2106 (2000)
29. Bai, F. et al. Assembly dynamics and the roles of FliI ATPase of the bacterial flagellar export apparatus. Scientific reports 4, 6528, doi: 10. 1038/srep06528 (2014)
30. Minamino, T. & Imada, K. The bacterial flagellar motor and its structural diversity. Trends Microbiol 23, 267-274, doi: 10. 1016/j. tim. 2014. 12. 011 (2015)
31. Ibuki, T. et al. Interaction between FliJ and FlhA, components of the bacterial flagellar type III export apparatus. J Bacteriol 195, 466-473, doi: 10. 1128/JB. 01711-12 (2013)
32. Komoriya, K. et al. Flagellar proteins and type III-exported virulence factors are the predominant proteins secreted into the culture media of Salmonella typhimurium. Mol Microbiol 34, 767-779 (1999)
33. Veenendaal, A. K. et al. The type III secretion system needle tip complex mediates host cell sensing and translocon insertion. Mol Microbiol 63, 1719-1730, doi: MMI5620 10. 1111/j. 1365-2958. 2007. 05620. x (2007)
34. Kudryashev, M., Cyrklaff, M., Wallich, R., Baumeister, W. & Frischknecht, F. Distinct in situ structures of the Borrelia flagellar motor. J Struct Biol 169, 54-61, doi: 10. 1016/j. jsb. 2009. 08. 008 (2010)
35. Nans, A., Kudryashev, M., Saibil, H. R. & Hayward, R. D. Structure of a bacterial type III secretion system in contact with a host membrane in situ. Nat Commun 6, 10114, doi: 10. 1038/ncomms10114 (2015)
36. Meitert, T. et al. Correlation between Congo red binding as virulence marker in Shigella species and Sereny test. Roum Arch Microbiol Immunol 50, 45-52 (1991)
37. Martinez-Argudo, I. & Blocker, A. J. The Shigella T3SS needle transmits a signal for MxiC release, which controls secretion of effectors. Mol Microbiol 78, 1365-1378, doi: 10. 1111/j. 1365-2958. 2010. 07413. x (2010)
38. Kremer, J. R., Mastronarde, D. N. & McIntosh, J. R. Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116, 71-76, doi: 10. 1006/jsbi. 1996. 0013 (1996)
39. Fernandez, J. J., Li, S. & Crowther, R. A. CTF determination and correction in electron cryotomography. Ultramicroscopy 106, 587-596, doi: 10. 1016/j. ultramic. 2006. 02. 004 (2006)
40. Ludtke, S. J., Baldwin, P. R. & Chiu, W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128, 82-97, doi: 10. 1006/jsbi. 1999. 4174 S1047-8477(99)94174-6 (1999)
41. Shaikh, T. R. et al. SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs. Nat Protoc 3, 1941-1974, doi: 10. 1038/nprot. 2008. 156 (2008)
42. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J Struct Biol 180, 519-530, doi: 10. 1016/j. jsb. 2012. 09. 006 (2012).