Structure of the Type VI secretion system contractile sheath

Cell

Volumn 160, Issue 5, 2015, Pages 952-962

  Kudryashev, Mikhail ^a   Wang, Ray Yu Ruei ^b,c   Brackmann, Maximilian ^a   Scherer, Sebastian ^a   Maier, Timm ^a   Baker, David ^b   Dimaio, Frank ^b   Stahlberg, Henning ^a   Egelman, Edward H ^d   Basler, Marek ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CLPV PROTEIN; UNCLASSIFIED DRUG; VIPA PROTEIN; VIPB PROTEIN; BACTERIAL SECRETION SYSTEM;

ARTICLE; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL SHEATH; BACTERIAL STRUCTURES; BACTERIOPHAGE; CELL MEMBRANE; ELECTRON TOMOGRAPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STRUCTURE; TYPE IV SECRETION SYSTEM; TYPE VI SECRETION SYSTEM; VIBRIO CHOLERAE; AMINO ACID SEQUENCE; BACTERIAL SECRETION SYSTEM; CHEMICAL STRUCTURE; CHEMISTRY; CRYOELECTRON MICROSCOPY; CYTOLOGY; METABOLISM; MOLECULAR GENETICS; SEQUENCE ALIGNMENT; ULTRASTRUCTURE;

BACTERIA (MICROORGANISMS); VIBRIO CHOLERAE;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CRYOELECTRON MICROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; VIBRIO CHOLERAE;

EID: 84923345050     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.01.037     Document Type: Article

References (62)

1. A.A. Aksyuk, P.G. Leiman, L.P. Kurochkina, M.M. Shneider, V.A. Kostyuchenko, V.V. Mesyanzhinov, and M.G. Rossmann The tail sheath structure of bacteriophage T4: a molecular machine for infecting bacteria EMBO J. 28 2009 821 829
2. A.A. Aksyuk, P.G. Leiman, M.M. Shneider, V.V. Mesyanzhinov, and M.G. Rossmann The structure of gene product 6 of bacteriophage T4, the hinge-pin of the baseplate Structure 17 2009 800 808
3. A.A. Aksyuk, L.P. Kurochkina, A. Fokine, F. Forouhar, V.V. Mesyanzhinov, L. Tong, and M.G. Rossmann Structural conservation of the myoviridae phage tail sheath protein fold Structure 19 2011 1885 1894
4. G.M. Alushin, G.C. Lander, E.H. Kellogg, R. Zhang, D. Baker, and E. Nogales High-resolution microtubule structures reveal the structural transitions in αβ-tubulin upon GTP hydrolysis Cell 157 2014 1117 1129
5. A. Amunts, A. Brown, X.C. Bai, J.L. Llácer, T. Hussain, P. Emsley, F. Long, G. Murshudov, S.H.W. Scheres, and V. Ramakrishnan Structure of the yeast mitochondrial large ribosomal subunit Science 343 2014 1485 1489
6. M. Basler, and J.J. Mekalanos Type 6 secretion dynamics within and between bacterial cells Science 337 2012 815
7. M. Basler, M. Pilhofer, G.P. Henderson, G.J. Jensen, and J.J. Mekalanos Type VI secretion requires a dynamic contractile phage tail-like structure Nature 483 2012 182 186
8. M. Basler, B.T. Ho, and J.J. Mekalanos Tit-for-tat: type VI secretion system counterattack during bacterial cell-cell interactions Cell 152 2013 884 894
9. J.E. Bina, and J.J. Mekalanos Vibrio cholerae tolC is required for bile resistance and colonization Infect. Immun. 69 2001 4681 4685
10. G. Bönemann, A. Pietrosiuk, A. Diemand, H. Zentgraf, and A. Mogk Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion EMBO J. 28 2009 315 325
11. Y.R. Brunet, L. Espinosa, S. Harchouni, T. Mignot, and E. Cascales Imaging type VI secretion-mediated bacterial killing Cell Rep. 3 2013 36 41
12. Y.R. Brunet, J. Hénin, H. Celia, and E. Cascales Type VI secretion and bacteriophage tail tubes share a common assembly pathway EMBO Rep. 15 2014 315 321
13. D. Castaño-Díez, M. Kudryashev, M. Arheit, and H. Stahlberg Dynamo: a flexible, user-friendly development tool for subtomogram averaging of cryo-EM data in high-performance computing environments J. Struct. Biol. 178 2012 139 151
14. M. Castelain, S. Ehlers, J. Klinth, S. Lindberg, M. Andersson, B.E. Uhlin, and O. Axner Fast uncoiling kinetics of F1C pili expressed by uropathogenic Escherichia coli are revealed on a single pilus level using force-measuring optical tweezers Eur. Biophys. J. 40 2011 305 316
15. V.B. Chen, W.B. Arendall 3rd, J.J. Headd, D.A. Keedy, R.M. Immormino, G.J. Kapral, L.W. Murray, J.S. Richardson, and D.C. Richardson MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr. D Biol. Crystallogr. 66 2010 12 21
16. C. Cole, J.D. Barber, and G.J. Barton The Jpred 3 secondary structure prediction server Nucleic Acids Res. 36 2008 W197 W201
17. K. Cowtan The Buccaneer software for automated model building. 1. Tracing protein chains Acta Crystallogr. D Biol. Crystallogr. 62 2006 1002 1011
18. L. Craig, N. Volkmann, A.S. Arvai, M.E. Pique, M. Yeager, E.H. Egelman, and J.A. Tainer Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions Mol. Cell 23 2006 651 662
19. A. Desfosses, R. Ciuffa, I. Gutsche, and C. Sachse SPRING - an image processing package for single-particle based helical reconstruction from electron cryomicrographs J. Struct. Biol. 185 2014 15 26
20. F. DiMaio, Y. Song, X. Li, M.J. Brunner, C. Xu, V. Conticello, E. Egelman, T. Marlovits, Y. Cheng, and D. Baker Atomic- accuracy models from 4.5-Å cryo-electron microscopy data with density-guided iterative local refinement Nat. Methods 2015 10.1038/NMETH.3286 Published online February 23, 2015
21. E.H. Egelman A robust algorithm for the reconstruction of helical filaments using single-particle methods Ultramicroscopy 85 2000 225 234
22. E.H. Egelman Reconstruction of helical filaments and tubes Methods Enzymol. 482 2010 167 183
23. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
24. A.R. Faruqi, D.M. Cattermole, R. Henderson, B. Mikulec, and C. Raeburn Evaluation of a hybrid pixel detector for electron microscopy Ultramicroscopy 94 2003 263 276
25. A. Fokine, Z. Zhang, S. Kanamaru, V.D. Bowman, A.A. Aksyuk, F. Arisaka, V.B. Rao, and M.G. Rossmann The molecular architecture of the bacteriophage T4 neck J. Mol. Biol. 425 2013 1731 1744
26. J. Frank, M. Radermacher, P. Penczek, J. Zhu, Y. Li, M. Ladjadj, and A. Leith SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields J. Struct. Biol. 116 1996 190 199
27. V.E. Galkin, A. Orlova, M.R. Vos, G.F. Schröder, and E.H. Egelman Near-atomic resolution for one state of f-actin Structure 23 2015 173 182
28. L.M. Guzman, D. Belin, M.J. Carson, and J. Beckwith Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter J. Bacteriol. 177 1995 4121 4130
29. L. Kaján, T.A. Hopf, M. Kalaš, D.S. Marks, and B. Rost FreeContact: fast and free software for protein contact prediction from residue co-evolution BMC Bioinformatics 15 2014 85
30. N. Kapitein, G. Bönemann, A. Pietrosiuk, F. Seyffer, I. Hausser, J.K. Locker, and A. Mogk ClpV recycles VipA/VipB tubules and prevents non-productive tubule formation to ensure efficient type VI protein secretion Mol. Microbiol. 87 2013 1013 1028
31. V.A. Kostyuchenko, P.R. Chipman, P.G. Leiman, F. Arisaka, V.V. Mesyanzhinov, and M.G. Rossmann The tail structure of bacteriophage T4 and its mechanism of contraction Nat. Struct. Mol. Biol. 12 2005 810 813
32. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797
33. S. Kube, N. Kapitein, T. Zimniak, F. Herzog, A. Mogk, and P. Wendler Structure of the VipA/B type VI Secretion complex suggests a contraction-state-specific recycling mechanism Cell Rep. 8 2014 20 30
34. W. Kühlbrandt Biochemistry. The resolution revolution Science 343 2014 1443 1444
35. P.G. Leiman, and M.M. Shneider Contractile tail machines of bacteriophages Adv. Exp. Med. Biol. 726 2012 93 114
36. P.G. Leiman, P.R. Chipman, V.A. Kostyuchenko, V.V. Mesyanzhinov, and M.G. Rossmann Three-dimensional rearrangement of proteins in the tail of bacteriophage T4 on infection of its host Cell 118 2004 419 429
37. P.G. Leiman, M. Basler, U.A. Ramagopal, J.B. Bonanno, J.M. Sauder, S. Pukatzki, S.K. Burley, S.C. Almo, and J.J. Mekalanos Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin Proc. Natl. Acad. Sci. USA 106 2009 4154 4159
38. X. Li, P. Mooney, S. Zheng, C.R. Booth, M.B. Braunfeld, S. Gubbens, D.A. Agard, and Y. Cheng Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM Nat. Methods 10 2013 584 590
39. N.S. Lossi, R. Dajani, P. Freemont, and A. Filloux Structure-function analysis of HsiF, a gp25-like component of the type VI secretion system, in Pseudomonas aeruginosa Microbiology 157 2011 3292 3305
40. N.S. Lossi, E. Manoli, A. Förster, R. Dajani, T. Pape, P. Freemont, and A. Filloux The HsiB1C1 (TssB-TssC) complex of the Pseudomonas aeruginosa type VI secretion system forms a bacteriophage tail sheathlike structure J. Biol. Chem. 288 2013 7536 7548
41. A. Lu, V.G. Magupalli, J. Ruan, Q. Yin, M.K. Atianand, M.R. Vos, G.F. Schröder, K.A. Fitzgerald, H. Wu, and E.H. Egelman Unified polymerization mechanism for the assembly of ASC-dependent inflammasomes Cell 156 2014 1193 1206
42. W.W. Metcalf, W. Jiang, L.L. Daniels, S.K. Kim, A. Haldimann, and B.L. Wanner Conditionally replicative and conjugative plasmids carrying lacZ alpha for cloning, mutagenesis, and allele replacement in bacteria Plasmid 35 1996 1 13
43. S. Miller, A.M. Lesk, J. Janin, and C. Chothia The accessible surface area and stability of oligomeric proteins Nature 328 1987 834 836
44. E. Miller, T. Garcia, S. Hultgren, and A.F. Oberhauser The mechanical properties of E. coli type 1 pili measured by atomic force microscopy techniques Biophys. J. 91 2006 3848 3856
45. J.A. Mindell, and N. Grigorieff Accurate determination of local defocus and specimen tilt in electron microscopy J. Struct. Biol. 142 2003 334 347
46. S. Ovchinnikov, H. Kamisetty, and D. Baker Robust and accurate prediction of residue-residue interactions across protein interfaces using evolutionary information eLife 3 2014 e02030
47. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
48. A. Pietrosiuk, E.D. Lenherr, S. Falk, G. Bönemann, J. Kopp, H. Zentgraf, I. Sinning, and A. Mogk Molecular basis for the unique role of the AAA+ chaperone ClpV in type VI protein secretion J. Biol. Chem. 286 2011 30010 30021
49. S. Pukatzki, A.T. Ma, A.T. Revel, D. Sturtevant, and J.J. Mekalanos Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin Proc. Natl. Acad. Sci. USA 104 2007 15508 15513
50. S. Scherer, J. Kowal, M. Chami, V. Dandey, M. Arheit, P. Ringler, and H. Stahlberg 2dx-automator: implementation of a semiautomatic high-throughput high-resolution cryo-electron crystallography pipeline J. Struct. Biol. 186 2014 302 307
51. J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, and B. Schmid Fiji: an open-source platform for biological-image analysis Nat. Methods 9 2012 676 682
52. M.M. Shneider, S.A. Buth, B.T. Ho, M. Basler, J.J. Mekalanos, and P.G. Leiman PAAR-repeat proteins sharpen and diversify the type VI secretion system spike Nature 500 2013 350 353
53. Y. Song, F. DiMaio, R.Y.-R. Wang, D. Kim, C. Miles, T. Brunette, J. Thompson, and D. Baker High-resolution comparative modeling with RosettaCM Structure 21 2013 1735 1742
54. G. Tang, L. Peng, P.R. Baldwin, D.S. Mann, W. Jiang, I. Rees, and S.J. Ludtke EMAN2: an extensible image processing suite for electron microscopy J. Struct. Biol. 157 2007 38 46
55. J. von der Ecken, M. Müller, W. Lehman, D.J. Manstein, P.A. Penczek, and S. Raunser Structure of the F-actin - tropomyosin complex Nature 2014 10.1038/nature14033 Published online December 1, 2014
56. R.M. Voorhees, I.S. Fernández, S.H.W. Scheres, and R.S. Hegde Structure of the mammalian ribosome-Sec61 complex to 3.4 Å resolution Cell 157 2014 1632 1643
57. G. Waksman, and S.J. Hultgren Structural biology of the chaperone-usher pathway of pilus biogenesis Nat. Rev. Microbiol. 7 2009 765 774
58. S. Wang, J. Ma, J. Peng, and J. Xu Protein structure alignment beyond spatial proximity Sci. Rep. 3 2013 1448
59. R.Y.-R. Wang, M. Kudryashev, X. Li, E.H. Egelman, M. Basler, Y. Cheng, D. Baker, and F. DiMaio De novo protein structure determination from near-atomic-resolution cryo-EM maps Nat. Methods 2015 10.1038/NMETH.3287 Published online February 23, 2015
60. K. Yonekura, S. Maki-Yonekura, and K. Namba Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy Nature 424 2003 643 650
61. D.A. Zacharias, J.D. Violin, A.C. Newton, and R.Y. Tsien Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells Science 296 2002 913 916
62. A. Zoued, E. Durand, C. Bebeacua, Y.R. Brunet, B. Douzi, C. Cambillau, E. Cascales, and L. Journet TssK is a trimeric cytoplasmic protein interacting with components of both phage-like and membrane anchoring complexes of the type VI secretion system J. Biol. Chem. 288 2013 27031 27041