Architecture of the major component of the type III secretion system export apparatus

Nature Structural and Molecular Biology

Volumn 20, Issue 1, 2013, Pages 99-104

  Abrusci, Patrizia ^a,e   Vergara Irigaray, Marta ^a,b   Johnson, Steven ^a   Beeby, Morgan D ^b,c   Hendrixson, David R ^d   Roversi, Pietro ^a,b   Friede, Miriam E ^e   Deane, Janet E ^a,b,f   Jensen, Grant J ^c   Tang, Christoph M ^a   Lea, Susan M ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e CIC BIOGUNE   (Spain)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MXIA PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL SIZE; CELL STRUCTURE; CONTROLLED STUDY; ELECTRON TOMOGRAPHY; FLAGELLUM; IN VIVO STUDY; MEMBRANE STRUCTURE; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; SHIGELLA FLEXNERI; STRUCTURAL HOMOLOGY; TYPE III SECRETION SYSTEM;

AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL SECRETION SYSTEMS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; SHIGELLA FLEXNERI;

BACTERIA (MICROORGANISMS); SHIGELLA FLEXNERI;

EID: 84872007514     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2452     Document Type: Article

References (63)

1. Cornelis, G. R. The type III secretion injectisome, a complex nanomachine for intracellular 'toxin' delivery. Biol. Chem. 391, 745-751 (2010).
2. Patel, J. C. & Galan, J. E. Manipulation of the host actin cytoskeleton by Salmonella-all in the name of entry. Curr. Opin. Microbiol. 8, 10-15 (2005).
3. Blocker, A. J. et al. What's the point of the type III secretion system needle? Proc. Natl. Acad. Sci. USA 105, 6507-6513 (2008).
4. Erhardt, M., Namba, K. & Hughes, K. T. Bacterial nanomachines: the flagellum and type III injectisome. Cold Spring Harb. Perspect. Biol. 2, a000299 (2010).
5. Marlovits, T. C. & Stebbins, C. E. Type III secretion systems shape up as they ship out. Curr. Opin. Microbiol. 13, 47-52 (2010).
6. Deane, J. E., Abrusci, P., Johnson, S. & Lea, S. M. Timing is everything: the regulation of type III secretion. Cell. Mol. Life Sci. 67, 1065-1075 (2010).
7. Diepold, A., Wiesand, U. & Cornelis, G. R. 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 (2011).
8. Wagner, S. et al. Organization and coordinated assembly of the type III secretion export apparatus. Proc. Natl. Acad. Sci. USA 107, 17745-17750 (2010).
9. Li, H. & Sourjik, V. Assembly and stability of flagellar motor in Escherichia coli. Mol. Microbiol. 80, 886-899 (2011).
10. Minamino, T., Imada, K. & Namba, K. Mechanisms of type III protein export for bacterial flagellar assembly. Mol. Biosyst. 4, 1105-1115 (2008).
11. Minamino, T., Imada, K. & Namba, K. Molecular motors of the bacterial flagella. Curr. Opin. Struct. Biol. 18, 693-701 (2008).
12. Diepold, A. et al. Deciphering the assembly of the Yersinia type III secretion injectisome. EMBO J. 29, 1928-1940 (2010).
13. Zhu, K., Gonzalez-Pedrajo, B. & Macnab, R. M. Interactions among membrane and soluble components of the flagellar export apparatus of Salmonella. Biochemistry 41, 9516-9524 (2002).
14. McMurry, J. L., Van Arnam, J. S., Kihara, M. & Macnab, R. M. Analysis of the cytoplasmic domains of Salmonella FlhA and interactions with components of the flagellar export machinery. J. Bacteriol. 186, 7586-7592 (2004).
15. Bange, G. et al. FlhA provides the adaptor for coordinated delivery of late flagella building blocks to the type III secretion system. Proc. Natl. Acad. Sci. USA 107, 11295-11300 (2010).
16. Minamino, T. et al. Interaction of a bacterial flagellar chaperone FlgN with FlhA is required for efficient export of its cognate substrates. Mol. Microbiol. 83, 775-788 (2012).
17. Worrall, L. J., Vuckovic, M. & Strynadka, N. C. Crystal structure of the C-terminal domain of the Salmonella type III secretion system export apparatus protein InvA. Prot. Sci. 19, 1091-1096 (2010).
18. Saijo-Hamano, Y. et al. Structure of the cytoplasmic domain of FlhA and implication for flagellar type III protein export. Mol. Microbiol. 76, 260-268 (2010).
19. Moore, S. A. & Jia, Y. Structure of the cytoplasmic domain of the flagellar secretion apparatus component FlhA from Helicobacter pylori. J. Biol. Chem. 285, 21060-21069 (2010).
20. Lilic, M., Quezada, C. M. & Stebbins, C. E. 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 (2010).
21. Andrews, G. P. & Maurelli, A. T. mxiA of Shigella flexneri 2a, which facilitates export of invasion plasmid antigens, encodes a homolog of the low-calcium-response protein, LcrD, of Yersinia pestis. Infect. Immun. 60, 3287-3295 (1992).
22. Ashida, H. et al. Shigella deploy multiple countermeasures against host innate immune responses. Curr. Opin. Microbiol. 14, 16-23 (2011).
23. Spreter, T. et al. A conserved structural motif mediates formation of the periplasmic rings in the type III secretion system. Nat. Struct. Mol. Biol. 16, 468-476 (2009).
24. Worrall, L. J., Lameignere, E. & Strynadka, N. C. Structural overview of the bacterial injectisome. Curr. Opin. Microbiol. 14, 3-8 (2011).
25. Yip, C. K. et al. Structural characterization of the molecular platform for type III secretion system assembly. Nature 435, 702-707 (2005).
26. Sanowar, S. et al. Interactions of the transmembrane polymeric rings of the Salmonella enterica serovar Typhimurium type III secretion system. mBio 1, e00158-10 (2010).
27. Lee, L. K., Ginsburg, M. A., Crovace, C., Donohoe, M. & Stock, D. Structure of the torque ring of the flagellar motor and the molecular basis for rotational switching. Nature 466, 996-1000 (2010).
28. Schraidt, O. & Marlovits, T. C. Three-dimensional model of Salmonella's needle complex at subnanometer resolution. Science 331, 1192-1195 (2011).
29. 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).
30. Goodsell, D. S. & Olson, A. J. Structural symmetry and protein function. Annu. Rev. Biophys. Biomol. Struct. 29, 105-153 (2000).
31. 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).
32. Chen, S. et al. Structural diversity of bacterial flagellar motors. EMBO J. 30, 2972-2981 (2011).
33. Liu, J. et al. Intact flagellar motor of Borrelia burgdorferi revealed by cryo-electron tomography: evidence for stator ring curvature and rotor/C-ring assembly flexion. J. Bacteriol. 191, 5026-5036 (2009).
34. Minamino, T. et al. Roles of the extreme N-terminal region of FliH for efficient localization of the FliH-FliI complex to the bacterial flagellar type III export apparatus. Mol. Microbiol. 74, 1471-1483 (2009).
35. 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 (2011).
36. Pallen, M. J., Bailey, C. M. & Beatson, S. A. Evolutionary links between FliH/YscL-like proteins from bacterial type III secretion systems and second-stalk components of the FoF1 and vacuolar ATPases. Prot. Sci. 15, 935-941 (2006).
37. Imada, K., Minamino, T., Tahara, A. & Namba, K. Structural similarity between the flagellar type III ATPase FliI and F1-ATPase subunits. Proc. Natl. Acad. Sci. USA 104, 485-490 (2007).
38. Zarivach, R., Vuckovic, M., Deng, W., Finlay, B. B. & Strynadka, N. C. Structural analysis of a prototypical ATPase from the type III secretion system. Nat. Struct. Mol. Biol. 14, 131-137 (2007).
39. Minamino, T., Morimoto, Y. V., Hara, N. & Namba, K. An energy transduction mechanism used in bacterial flagellar type III protein export. Nature Commun. 2, 475 (2011).
40. Paul, K., Erhardt, M., Hirano, T., Blair, D. F. & Hughes, K. T. Energy source of flagellar type III secretion. Nature 451, 489-492 (2008).
41. Minamino, T. & Namba, K. Distinct roles of the FliI ATPase and proton motive force in bacterial flagellar protein export. Nature 451, 485-488 (2008).
42. Wilharm, G. et al. Yersinia enterocolitica type III secretion depends on the proton motive force but not on the flagellar motor components MotA and MotB. Infect. Immun. 72, 4004-4009 (2004).
43. Galperin, M., Dibrov, P. A. & Glagolev, A. N. delta mu H+ is required for flagellar growth in Escherichia coli. FEBS Lett. 143, 319-322 (1982).
44. Hara, N., Namba, K. & Minamino, T. Genetic Characterization of Conserved Charged Residues in the Bacterial Flagellar Type III Export Protein FlhA. PLoS ONE 6, e22417 (2011).
45. Minamino, T., Kinoshita, M., Imada, K. & Namba, K. Interaction between FliI ATPase and a flagellar chaperone FliT during bacterial flagellar protein export. Mol. Microbiol. 83, 168-178 (2012).
46. Akeda, Y. & Galan, J. E. Chaperone release and unfolding of substrates in type III secretion. Nature 437, 911-915 (2005).
47. Thomas, J., Stafford, G. P. & Hughes, C. Docking of cytosolic chaperone-substrate complexes at the membrane ATPase during flagellar type III protein export. Proc. Natl. Acad. Sci. USA 101, 3945-3950 (2004).
48. Berg, H. C. The rotary motor of bacterial flagella. Annu. Rev. Biochem. 72, 19-54 (2003).
49. Murphy, G. E., Leadbetter, J. R. & Jensen, G. J. In situ structure of the complete Treponema primitia flagellar motor. Nature 442, 1062-1064 (2006).
50. Blocker, A. et al. Structure and composition of the Shigella flexneri "needle complex", a part of its type III secreton. Mol. Microbiol. 39, 652-663 (2001).
51. Wolf, S., Freier, E., Potschies, M., Hofmann, E. & Gerwert, K. Directional proton transfer in membrane proteins achieved through protonated protein-bound water molecules: a proton diode. Angew. Chem. Int. Ed. Engl. 49, 6889-6893 (2010).
52. Miroux, B. & Walker, J. E. Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260, 289-298 (1996).
53. Solano, C. et al. Genetic reductionist approach for dissecting individual roles of GGDEF proteins within the c-di-GMP signaling network in Salmonella. Proc. Natl. Acad. Sci. USA 106, 7997-8002 (2009).
54. Hendrixson, D. R. & DiRita, V. J. Transcription of sigma54-dependent but not sigma28-dependent flagellar genes in Campylobacter jejuni is associated with formation of the flagellar secretory apparatus. Mol. Microbiol. 50, 687-702 (2003).
55. Kenjale, R. et al. The needle component of the type III secreton of Shigella regulates the activity of the secretion apparatus. J. Biol. Chem. 280, 42929-42937 (2005).
56. Marteyn, B. et al. Modulation of Shigella virulence in response to available oxygen in vivo. Nature 465, 355-358 (2010).
57. Rayment, I. Reductive alkylation of lysine residues to alter crystallization properties of proteins. Methods Enzymol. 276, 171-179 (1997).
58. Winter, G. xia2: an expert system for macromolecular crystallography data reduction. J. Appl. Crystallogr. 43, 186-190 (2010).
59. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763 (1994).
60. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
61. Blanc, E. et al. Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr. D Biol. Crystallogr. 60, 2210-2221 (2004).
62. Agulleiro, J. I. & Fernandez, J. J. Fast tomographic reconstruction on multicore computers. Bioinformatics 27, 582-583 (2011).
63. Nicastro, D. et al. The molecular architecture of axonemes revealed by cryoelectron tomography. Science 313, 944-948 (2006).