Composition, Formation, and Regulation of the Cytosolic C-ring, a Dynamic Component of the Type III Secretion Injectisome

PLoS Biology

Volumn 13, Issue 1, 2015, Pages

  Diepold, Andreas ^a   Kudryashev, Mikhail ^b   Delalez, Nicolas J ^a   Berry, Richard M ^c   Armitage, Judith P ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; BETA LACTAMASE; EFFECTOR CASPASE; PROTEIN BINDING; PROTEIN SUBUNIT; TYPE III SECRETION SYSTEM;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM CULTURE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CULTURE MEDIUM; CYTOSOL; FLUORESCENCE MICROSCOPY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GRAM NEGATIVE BACTERIUM; IMMUNOBLOTTING; INJECTISOME; NONHUMAN; PHOTOACTIVATION; PLASMID; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE; STOICHIOMETRY; TRANSCRIPTION INITIATION SITE; TRANSLATION INITIATION; TYPE III SECRETION SYSTEM; YERSINIA ENTEROCOLITICA; METABOLISM; PROTEIN SUBUNIT; PROTEIN TRANSPORT; ULTRASTRUCTURE;

EUKARYOTA; NEGIBACTERIA; YERSINIA ENTEROCOLITICA;

ADENOSINE TRIPHOSPHATASES; BACTERIAL PROTEINS; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN SUBUNITS; PROTEIN TRANSPORT; TYPE III SECRETION SYSTEMS; YERSINIA ENTEROCOLITICA;

EID: 84922260211     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1002039     Document Type: Article

References (86)

1. Cornelis GR, Wolf-Watz H, (1997) The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol Microbiol 23: 861–867. doi: 10.1046/j.1365-2958.1997.2731623.x 9076724
2. Galán JE, Collmer A, (1999) Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284: 1322–1328. doi: 10.1126/science.284.5418.1322 10334981
3. Hueck CJ, (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62: 379–433. 9618447
4. Coburn B, Sekirov I, Finlay BB, (2007) Type III secretion systems and disease. Clin Microbiol Rev 20: 535–549. doi: 10.1128/CMR.00013-07 17934073
5. Büttner 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. doi: 10.1128/MMBR.05017-11 22688814
6. Viprey V, Del Greco A, Golinowski W, Broughton WJ, Perret X, (1998) Symbiotic implications of type III protein secretion machinery in Rhizobium. Mol Microbiol 28: 1381–1389. doi: 10.1046/j.1365-2958.1998.00920.x 9680225
7. Cusano AM, Burlinson P, Deveau A, Vion P, Uroz S, et al. (2011) Pseudomonas fluorescens BBc6R8 type III secretion mutants no longer promote ectomycorrhizal symbiosis. Environ Microbiol Rep 3: 203–210. doi: 10.1111/j.1758-2229.2010.00209.x 23761252
8. Galán JE, (2009) Common themes in the design and function of bacterial effectors. Cell Host Microbe 5: 571–579. doi: 10.1016/j.chom.2009.04.008 19527884
9. Van der Heijden J, Finlay BB, Heijden J, (2012) Type III effector-mediated processes in Salmonella infection. Future Microbiol 7: 685–703. doi: 10.2217/fmb.12.49 22702524
10. Cornelis GR, (2006) The type III secretion injectisome. Nat Rev Microbiol 4: 811–825. doi: 10.1038/nrmicro1526 17041629
11. Galán JE, Wolf-Watz H, (2006) Protein delivery into eukaryotic cells by type III secretion machines. Nature 444: 567–573. doi: 10.1038/nature05272 17136086
12. Schraidt O, Marlovits TC, (2011) Three-dimensional model of Salmonella’s needle complex at subnanometer resolution. Science 331: 1192–1195. doi: 10.1126/science.1199358 21385715
13. Bergeron JRC, Worrall LJ, Sgourakis NG, DiMaio F, Pfuetzner RA, et al. (2013) A refined model of the prototypical Salmonella SPI-1 T3SS basal body reveals the molecular basis for its assembly. PLoS Pathog 9: e1003307. doi: 10.1371/journal.ppat.1003307 23633951
14. Akeda Y, Galán JE, (2005) Chaperone release and unfolding of substrates in type III secretion. Nature 437: 911–915. doi: 10.1038/nature03992 16208377
15. Blaylock B, Riordan K, Missiakas D, Schneewind O, (2006) Characterization of the Yersinia enterocolitica type III secretion ATPase YscN and its regulator, YscL. J Bacteriol 188: 3525–3534. doi: 10.1128/JB.188.10.3525-3534.2006 16672607
16. Pallen MJ, Bailey CM, Beatson SA, (2006) Evolutionary links between FliH/YscL-like proteins from bacterial type III secretion systems and second-stalk components of the FoF1 and vacuolar ATPases. Protein Sci 15: 935–941. doi: 10.1110/ps.051958806 16522800
17. Ibuki T, Imada K, Minamino T, Kato T, Miyata T, et al. (2011) Common architecture of the flagellar type III protein export apparatus and F- and V-type ATPases. Nat Struct Mol Biol 18: 277–282. doi: 10.1038/nsmb.1977 21278755
18. Evans LDB, Hughes C, (2009) Selective binding of virulence type III export chaperones by FliJ escort orthologues InvI and YscO. FEMS Microbiol Lett 293: 292–297. doi: 10.1111/j.1574-6968.2009.01535.x 19260965
19. Romo-Castillo M, Andrade A, Espinosa N, Monjarás Feria J, Soto E, et al. (2014) EscO, a functional and structural analog of the flagellar FliJ protein, is a positive regulator of EscN ATPase activity of the enteropathogenic Escherichia coli injectisome. J Bacteriol 196: 2227–2241. doi: 10.1128/JB.01551-14 24706741
20. Morita-ishihara T, Ogawa M, Sagara H, Yoshida M, Katayama E, et al. (2005) Shigella Spa33 is an essential C-ring component of type III secretion machinery. J Biol Chem 281: 599–607. doi: 10.1074/jbc.M509644200 16246841
21. Johnson S, Blocker AJ, (2008) Characterization of soluble complexes of the Shigella flexneri type III secretion system ATPase. FEMS Microbiol Lett 286: 274–278. doi: 10.1111/j.1574-6968.2008.01284.x 18657109
22. Jackson M, Plano G V, (2000) Interactions between type III secretion apparatus components from Yersinia pestis detected using the yeast two-hybrid system. FEMS Microbiol Lett 186: 85–90. doi: 10.1111/j.1574-6968.2000.tb09086.x 10779717
23. Spaeth K, Chen Y-S, Valdivia R, (2009) The Chlamydia type III secretion system C-ring engages a chaperone-effector protein complex. PLoS Pathog 5: e1000579. doi: 10.1371/journal.ppat.1000579 19750218
24. Cherradi Y, Hachani A, Allaoui A, (2014) Spa13 of Shigella flexneri has a dual role: chaperone escort and export gate-activator switch of the type III secretion system. Microbiology 160: 130–141. doi: 10.1099/mic.0.071712-0 24126350
25. Diepold A, Amstutz M, Abel S, Sorg I, Jenal U, et al. (2010) Deciphering the assembly of the Yersinia type III secretion injectisome. EMBO J 29: 1928–1940. doi: 10.1038/emboj.2010.84 20453832
26. Lara-Tejero M, Kato J, Wagner S, Liu X, Galán JE, (2011) A Sorting Platform Determines the Order of Protein Secretion in Bacterial Type III Systems. Science 331: 1188–1191. doi: 10.1126/science.1201476 21292939
27. Wilharm G, Lehmann V, Krauss K, Lehnert B, Richter S, et al. (2004) 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. doi: 10.1128/IAI.72.7.4004-4009.2004 15213145
28. Gophna U, Ron E, Graur D, (2003) Bacterial type III secretion systems are ancient and evolved by multiple horizontal-transfer events. Gene 312: 151–163. doi: 10.1016/S0378-1119(03)00612-7 12909351
29. Abby SS, Rocha EPC, (2012) The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems. PLoS Genet 8: e1002983. doi: 10.1371/journal.pgen.1002983 23028376
30. Blocker AJ, Komoriya K, Aizawa S-I, (2003) Type III secretion systems and bacterial flagella: insights into their function from structural similarities. Proc Natl Acad Sci U S A 100: 3027–3030. doi: 10.1073/pnas.0535335100 12631703
31. Erhardt M, Namba K, Hughes KT, (2010) Bacterial nanomachines: the flagellum and type III injectisome. Cold Spring Harb Perspect Biol 2: a000299. doi: 10.1101/cshperspect.a000299 20926516
32. Yu X-J, Liu M, Matthews S, Holden DW, (2011) 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 21878641
33. Bzymek KP, Hamaoka BY, Ghosh P, (2012) Two translation products of Yersinia yscQ assemble to form a complex essential to type III secretion. Biochemistry 51: 1669–1677. doi: 10.1021/bi201792p 22320351
34. Driks A, DeRosier D, (1990) Additional structures associated with bacterial flagellar basal body. J Mol Biol 211: 669–672. doi: 10.1016/0022-2836(90)90063-R 2179562
35. Khan I, Reese T, Khan S, (1992) The cytoplasmic component of the bacterial flagellar motor. Proc Natl Acad Sci U S A 89: 5956–5960. doi: 10.1073/pnas.89.13.5956 1631080
36. Irikura VM, Kihara M, Yamaguchi S, Sockett H, Macnab RM, (1993) Salmonella typhimurium fliG and fliN mutations causing defects in assembly, rotation, and switching of the flagellar motor. J Bacteriol 175: 802–810. 8423152
37. Bren A, Eisenbach M, (1998) The N terminus of the flagellar switch protein, FliM, is the binding domain for the chemotactic response regulator, CheY. J Mol Biol 278: 507–514. doi: 10.1006/jmbi.1998.1730 9600834
38. Welch M, Oosawa K, Aizawa S-I, Eisenbach M, (1993) Phosphorylation-dependent binding of a signal molecule to the flagellar switch of bacteria. Proc Natl Acad Sci U S A 90: 8787–8791. doi: 10.1073/pnas.90.19.8787 8415608
39. Erhardt M, Hughes KT, (2009) C-ring requirement in flagellar type III secretion is bypassed by FlhDC upregulation. Mol Microbiol 75: 376–393. doi: 10.1111/j.1365-2958.2009.06973.x 19919668
40. Konishi M, Kanbe M, McMurry J, Aizawa S-I, (2009) Flagellar formation in C-ring defective mutants by overproduction of FliI, the ATPase specific for the flagellar type III secretion. J Bacteriol 191: 6186–6191. doi: 10.1128/JB.00601-09 19648242
41. Kudryashev M, Stenta M, Schmelz S, Amstutz M, Wiesand U, et al. (2013) In situ structural analysis of the Yersinia enterocolitica injectisome. Elife 2: e00792. doi: 10.7554/eLife.00792 23908767
42. Kawamoto A, Morimoto Y V, Miyata T, Minamino T, Hughes KT, et al. (2013) Common and distinct structural features of Salmonella injectisome and flagellar basal body. Sci Rep 3: 3369. doi: 10.1038/srep03369 24284544
43. Francis NR, Sosinsky GE, Thomas D, DeRosier D, (1994) Isolation, characterization and structure of bacterial flagellar motors containing the switch complex. J Mol Biol 235: 1261–1270. doi: 10.1006/jmbi.1994.1079 8308888
44. Spreter T, Yip CK, Sanowar S, André I, Kimbrough TG, et al. (2009) A conserved structural motif mediates formation of the periplasmic rings in the type III secretion system. Nat Struct Mol Biol 16: 468–476. doi: 10.1038/nsmb.1603 19396170
45. Schraidt O, Lefebre MD, Brunner MJ, Schmied WH, Schmidt A, et al. (2010) Topology and organization of the Salmonella typhimurium type III secretion needle complex components. PLoS Pathog 6: e1000824. doi: 10.1371/journal.ppat.1000824 20368966
46. McDowell MA, Johnson S, Deane JE, Cheung M, Roehrich AD, et al. (2011) Structural and functional studies on the N-terminal domain of the Shigella type III secretion protein MxiG. J Biol Chem 286: 30606–30614. doi: 10.1074/jbc.M111.243865 21733840
47. Hodgkinson J, Horsley A, Stabat D, Simon M, Johnson S, et al. (2009) Three-dimensional reconstruction of the Shigella T3SS transmembrane regions reveals 12-fold symmetry and novel features throughout. Nat Struct Mol Biol 16: 477–485. doi: 10.1038/nsmb.1599 19396171
48. Sani M, Allaoui A, Fusetti F, Oostergetel GT, Keegstra W, et al. (2006) Structural organization of the needle complex of the type III secretion apparatus of Shigella flexneri. Micron 38: 291–301. doi: 10.1016/j.micron.2006.04.007 16920362
49. 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. doi: 10.1111/j.1365-2958.2011.07830.x 21923772
50. Marketon MM, DePaolo RW, DeBord KL, Jabri B, Schneewind O, (2005) Plague bacteria target immune cells during infection. Science 309: 1739–1741. doi: 10.1126/science.1114580 16051750
51. Charpentier X, Oswald E, (2004) Identification of the secretion and translocation domain of the enteropathogenic and enterohemorrhagic Escherichia coli effector Cif, using TEM-1 beta-lactamase as a new fluorescence-based reporter. J Bacteriol 186: 5486–5495. doi: 10.1128/JB.186.16.5486-5495.2004 15292151
52. Sory M-P, Boland A, Lambermont I, Cornelis GR, (1995) Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach. Proc Natl Acad Sci U S A 92: 11998–12002. doi: 10.1073/pnas.92.26.11998 8618831
53. Uphoff S, Reyes-Lamothe R, Garza de Leon F, Sherratt DJ, Kapanidis AN, (2013) Single-molecule DNA repair in live bacteria. Proc Natl Acad Sci U S A 110: 8063–8068. doi: 10.1073/pnas.1301804110 23630273
54. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, et al. (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313: 1642–1645. doi: 10.1126/science.1127344 16902090
55. Manley S, Gillette JM, Patterson GH, Shroff H, Hess HF, et al. (2008) High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat Methods 5: 155–157. doi: 10.1038/nmeth.1176 18193054
56. Subach F V, Patterson GH, Manley S, Gillette JM, Lippincott-Schwartz J, et al. (2009) Photoactivatable mCherry for high-resolution two-color fluorescence microscopy. Nat Methods 6: 153–159. doi: 10.1038/nmeth.1298 19169259
57. Eichelberg K, Ginocchio CC, Galán JE, (1994) Molecular and functional characterization of the Salmonella typhimurium invasion genes invB and invC: homology of InvC to the F0F1 ATPase family of proteins. J Bacteriol 176: 4501–4510. 8045880
58. Akeda Y, Galán JE, (2004) Genetic analysis of the Salmonella enterica type III secretion-associated ATPase InvC defines discrete functional domains. J Bacteriol 186: 2402–2412. doi: 10.1128/JB.186.8.2402-2412.2004 15060043
59. Li H, Sourjik V, (2011) Assembly and stability of flagellar motor in Escherichia coli. Mol Microbiol 80: 886–899. doi: 10.1111/j.1365-2958.2011.07557.x 21244534
60. Sourjik V, Berg HC, (2000) Localization of components of the chemotaxis machinery of Escherichia coli using fluorescent protein fusions. Mol Microbiol 37: 740–751. doi: 10.1046/j.1365-2958.2000.02044.x 10972797
61. Delalez NJ, Berry RM, Armitage JP, (2014) Stoichiometry and turnover of the bacterial flagellar switch protein FliN. MBio 5: e01216–e01214. doi: 10.1128/mBio.01216-14 24987089
62. Thomas DR, Francis N, Xu C, DeRosier D, (2006) The three-dimensional structure of the flagellar rotor from a clockwise-locked mutant of Salmonella enterica serovar Typhimurium. J Bacteriol 188: 7039–7048. doi: 10.1128/JB.00552-06 17015643
63. Yuan J, Branch RW, Hosu BG, Berg HC, (2012) Adaptation at the output of the chemotaxis signalling pathway. Nature 484: 233–236. doi: 10.1038/nature10964 22498629
64. Chen S, Beeby MD, Murphy GE, Leadbetter JR, Hendrixson DR, et al. (2011) Structural diversity of bacterial flagellar motors. EMBO J 30: 2972–2981. doi: 10.1038/emboj.2011.186 21673657
65. Koster M, Bitter W, de Cock H, Allaoui A, Cornelis GR, et al. (1997) The outer membrane component, YscC, of the Yop secretion machinery of Yersinia enterocolitica forms a ring-shaped multimeric complex. Mol Microbiol 26: 789–797. doi: 10.1046/j.1365-2958.1997.6141981.x 9427408
66. Morimoto Y V, Ito M, Hiraoka KD, Che Y-S, Bai F, et al. (2014) Assembly and stoichiometry of FliF and FlhA in Salmonella flagellar basal body. Mol Microbiol 91: 1214–1226. doi: 10.1111/mmi.12529 24450479
67. Wagner S, Königsmaier L, Lara-Tejero M, Lefebre MD, Marlovits TC, et al. (2010) Organization and coordinated assembly of the type III secretion export apparatus. Proc Natl Acad Sci U S A 107: 17745–17750. doi: 10.1073/pnas.1008053107 20876096
68. Leake MC, Chandler J, Wadhams GH, Bai F, Berry RM, et al. (2006) Stoichiometry and turnover in single, functioning membrane protein complexes. Nature 443: 355–358. doi: 10.1038/nature05135 16971952
69. Delalez NJ, Wadhams GH, Rosser G, Xue Q, Brown M, et al. (2010) Signal-dependent turnover of the bacterial flagellar switch protein FliM. Proc Natl Acad Sci U S A 107: 11347–11351. doi: 10.1073/pnas.1000284107 20498085
70. Fukuoka H, Inoue Y, Terasawa S, Takahashi H, Ishijima A, (2010) Exchange of rotor components in functioning bacterial flagellar motor. Biochem Biophys Res Commun 394: 130–135. doi: 10.1016/j.bbrc.2010.02.129 20184859
71. Lele PP, Branch RW, Nathan VSJ, Berg HC, (2012) Mechanism for adaptive remodeling of the bacterial flagellar switch. Proc Natl Acad Sci U S A 109: 20018–20022. doi: 10.1073/pnas.1212327109 23169659
72. Minamino T, Imada K, Namba K, (2008) Mechanisms of type III protein export for bacterial flagellar assembly. Mol Biosyst 4: 1105–1115. doi: 10.1039/b808065h 18931786
73. Enninga J, Mounier J, Sansonetti P, Tran Van Nhieu G, Nhieu GT Van, (2005) Secretion of type III effectors into host cells in real time. Nat Methods 2: 959–965. doi: 10.1038/nmeth804 16299482
74. Schlumberger MC, Müller A, Ehrbar K, Winnen B, Duss I, et al. (2005) Real-time imaging of type III secretion: Salmonella SipA injection into host cells. Proc Natl Acad Sci U S A 102: 12548–12553. doi: 10.1073/pnas.0503407102 16107539
75. Minamino T, Yoshimura SDJ, Morimoto Y V, González-Pedrajo B, Kami-Ike N, et al. (2009) 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. doi: 10.1111/j.1365-2958.2009.06946.x 19889085
76. Hara N, Morimoto Y V, Kawamoto A, Namba K, Minamino T, (2012) Interaction of the extreme N-terminal region of FliH with FlhA is required for efficient bacterial flagellar protein export. J Bacteriol 194: 5353–5360. doi: 10.1128/JB.01028-12 22843851
77. Tran EJ, Wente SR, (2006) Dynamic nuclear pore complexes: life on the edge. Cell 125: 1041–1053. doi: 10.1016/j.cell.2006.05.027 16777596
78. Marteyn B, West NP, Browning DF, Cole JA, Shaw JG, et al. (2010) Modulation of Shigella virulence in response to available oxygen in vivo. Nature 465: 355–358. doi: 10.1038/nature08970 20436458
79. Schüller S, Phillips A, (2010) Microaerobic conditions enhance type III secretion and adherence of enterohaemorrhagic Escherichia coli to polarized human intestinal epithelial cells. Environ Microbiol 12: 2426–2435. doi: 10.1111/j.1462-2920.2010.02216.x 20406285
80. Yu X-J, McGourty K, Liu M, Unsworth KE, Holden DW, (2010) pH sensing by intracellular Salmonella induces effector translocation. Science 328: 1040–1043. doi: 10.1126/science.1189000 20395475
81. Diepold A, Wagner S, (2014) Assembly of the bacterial type III secretion machinery. FEMS Microbiol Rev 38: 802–822. doi: 10.1111/1574-6976.12061 24484471
82. Kaniga K, Delor I, Cornelis GR, (1991) A wide-host-range suicide vector for improving reverse genetics in gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica. Gene 109: 137–141. doi: 10.1016/0378-1119(91)90599-7 1756974
83. Plank M, Wadhams GH, Leake MC, (2009) Millisecond timescale slimfield imaging and automated quantification of single fluorescent protein molecules for use in probing complex biological processes. Integr Biol (Camb) 1: 602–612. doi: 10.1039/b907837a
84. Castaño-Díez D, Kudryashev M, Arheit M, Stahlberg H, (2012) 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 22245546
85. Sliusarenko O, Heinritz J, Emonet T, Jacobs-Wagner C, (2011) High-throughput, subpixel precision analysis of bacterial morphogenesis and intracellular spatio-temporal dynamics. Mol Microbiol 80: 612–627. doi: 10.1111/j.1365-2958.2011.07579.x 21414037
86. Wallace IM, O’Sullivan O, Higgins DG, Notredame C, (2006) M-Coffee: combining multiple sequence alignment methods with T-Coffee. Nucleic Acids Res 34: 1692–1699. doi: 10.1093/nar/gkl091 16556910