Phage pierces the host cell membrane with the iron-loaded spike

Structure

Volumn 20, Issue 2, 2012, Pages 326-339

  Browning, Christopher ^a   Shneider, Mikhail M ^a,b   Bowman, Valorie D ^c   Schwarzer, David ^a   Leiman, Petr G ^a  

^a EPFL   (Switzerland)

^b SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^c PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANE PROTEIN; HISTIDINE; IRON; OLIGONUCLEOTIDE; OLIGOSACCHARIDE;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIOPHAGE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; ESCHERICHIA COLI; HOST CELL; LIPID BILAYER; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN STRUCTURE; SPIKE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BACTERIOPHAGE P2; BINDING SITES; COORDINATION COMPLEXES; CRYSTALLOGRAPHY, X-RAY; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; IRON; IRON-BINDING PROTEINS; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; SEQUENCE HOMOLOGY, AMINO ACID; VIRAL STRUCTURAL PROTEINS;

BACTERIA (MICROORGANISMS);

EID: 84856753664     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2011.12.009     Document Type: Article

References (52)

1. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, N. Echols, J.J. Headd, L.W. Hung, S. Jain, G.J. Kapral, and R.W. Grosse Kunstleve The Phenix software for automated determination of macromolecular structures Methods 55 2011 94 106
2. 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
3. T.S. Baker, and R. Henderson Electron cryomicroscopy M.G. Rossmann, E. Arnold, International Tables for Crystallography Volume F. Crystallography of biological macromolecules 2006 Kluwer Academic Publishers Dordrecht, the Netherlands 451 463
4. S.G. Bartual, J.M. Otero, C. Garcia-Doval, A.L. Llamas-Saiz, R. Kahn, G.C. Fox, and M.J. van Raaij Structure of the bacteriophage T4 long tail fiber receptor-binding tip Proc. Natl. Acad. Sci. USA 107 2010 20287 20292
5. G. Bönemann, A. Pietrosiuk, and A. Mogk Tubules and donuts: a type VI secretion story Mol. Microbiol. 76 2010 815 821
6. B. Chen, and J. King Thermal unfolding pathway for the thermostable P22 tailspike endorhamnosidase Biochemistry 30 1991 6260 6269
7. K. Cowtan Recent developments in classical density modification Acta Crystallogr. D Biol. Crystallogr. 66 2010 470 478
8. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132 (Pubitemid 41742764)
9. A. Fokine, A.J. Battisti, V.D. Bowman, A.V. Efimov, L.P. Kurochkina, P.R. Chipman, V.V. Mesyanzhinov, and M.G. Rossmann Cryo-EM study of the Pseudomonas bacteriophage phiKZ Structure 15 2007 1099 1104 (Pubitemid 47362690)
10. 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 (Pubitemid 26093143)
11. R. Gerardy-Schahn, A. Bethe, T. Brennecke, M. Mühlenhoff, M. Eckhardt, S. Ziesing, F. Lottspeich, and M. Frosch Molecular cloning and functional expression of bacteriophage PK1E-encoded endoneuraminidase Endo NE Mol. Microbiol. 16 1995 441 450
12. E. Haggrd-Ljungquist, E. Jacobsen, S. Rishovd, E.W. Six, O. Nilssen, M.G. Sunshine, B.H. Lindqvist, K.J. Kim, V. Barreiro, E.V. Koonin, and R. Calendar Bacteriophage P2: genes involved in baseplate assembly Virology 213 1995 109 121
13. J.V. Israel, T.F. Anderson, and M. Levine in vitro MORPHOGENESIS OF PHAGE P22 FROM HEADS AND BASE-PLATE PARTS Proc. Natl. Acad. Sci. USA 57 1967 284 291
14. W. Kabsch XDS Acta Crystallogr. D Biol. Crystallogr. 66 2010 125 132
15. Y. Kageyama, M. Murayama, T. Onodera, S. Yamada, H. Fukada, M. Kudou, K. Tsumoto, Y. Toyama, S. Kado, K. Kubota, and S. Takeda Observation of the membrane binding activity and domain structure of gpV, which comprises the tail spike of bacteriophage P2 Biochemistry 48 2009 10129 10135
16. A.V. Kajava, and A.C. Steven Beta-rolls, beta-helices, and other beta-solenoid proteins Adv. Protein Chem. 73 2006 55 96 (Pubitemid 44960401)
17. S. Kanamaru, P.G. Leiman, V.A. Kostyuchenko, P.R. Chipman, V.V. Mesyanzhinov, F. Arisaka, and M.G. Rossmann Structure of the cell-puncturing device of bacteriophage T4 Nature 415 2002 553 557 (Pubitemid 34130613)
18. S. Kanamaru, Y. Ishiwata, T. Suzuki, M.G. Rossmann, and F. Arisaka Control of bacteriophage T4 tail lysozyme activity during the infection process J. Mol. Biol. 346 2005 1013 1020 (Pubitemid 40215526)
19. Y. Kondou, D. Kitazawa, S. Takeda, Y. Tsuchiya, E. Yamashita, M. Mizuguchi, K. Kawano, and T. Tsukihara Structure of the central hub of bacteriophage Mu baseplate determined by X-ray crystallography of gp44 J. Mol. Biol. 352 2005 976 985 (Pubitemid 41267082)
20. V.A. Kostyuchenko, P.G. Leiman, P.R. Chipman, S. Kanamaru, M.J. van Raaij, F. Arisaka, V.V. Mesyanzhinov, and M.G. Rossmann Three-dimensional structure of bacteriophage T4 baseplate Nat. Struct. Biol. 10 2003 688 693 (Pubitemid 37052405)
21. 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 (Pubitemid 43086256)
22. B. Kwiatkowski, B. Boschek, H. Thiele, and S. Stirm Endo-N- acetylneuraminidase associated with bacteriophage particles J. Virol. 43 1982 697 704 (Pubitemid 12096341)
23. P.G. Leiman, and I.J. Molineux Evolution of a new enzyme activity from the same motif fold Mol. Microbiol. 69 2008 287 290 (Pubitemid 351988006)
24. P.G. Leiman, and M.M. Shneider Contractile tail machines of bacteriophages M.G. Rossmann, V.B. Rao, Viral Molecular Machines 2012 Springer New York in press
25. 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 (Pubitemid 39485662)
26. 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
27. P.G. Leiman, F. Arisaka, M.J. van Raaij, V.A. Kostyuchenko, A.A. Aksyuk, S. Kanamaru, and M.G. Rossmann Morphogenesis of the T4 tail and tail fibers Virol. J. 7 2010 355
28. A.G. Leslie The integration of macromolecular diffraction data Acta Crystallogr. D Biol. Crystallogr. 62 2006 48 57
29. J. Liu, C.Y. Chen, D. Shiomi, H. Niki, and W. Margolin Visualization of bacteriophage P1 infection by cryo-electron tomography of tiny Escherichia coli Virology 417 2011 304 311
30. S.J. Ludtke, P.R. Baldwin, and W. Chiu EMAN: semiautomated software for high-resolution single-particle reconstructions J. Struct. Biol. 128 1999 82 97 (Pubitemid 30013436)
31. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Cryst. 40 2007 658 674 (Pubitemid 47080256)
32. L.J. McGuffin, K. Bryson, and D.T. Jones The PSIPRED protein structure prediction server Bioinformatics 16 2000 404 405 (Pubitemid 30417087)
33. R.J. Morris, A. Perrakis, and V.S. Lamzin ARP/wARP and automatic interpretation of protein electron density maps Methods Enzymol. 374 2003 229 244 (Pubitemid 37531812)
34. A.G. Murzin, and C. Chothia Protein architecture: new superfamilies Curr. Opin. Struct. Biol. 2 1992 895 903
35. K. Nakayama, K. Takashima, H. Ishihara, T. Shinomiya, M. Kageyama, S. Kanaya, M. Ohnishi, T. Murata, H. Mori, and T. Hayashi The R-type pyocin of Pseudomonas aeruginosa is related to P2 phage, and the F-type is related to lambda phage Mol. Microbiol. 38 2000 213 231
36. A.S. Nilsson, and E. Haggrd-Ljungquist Evolution of P2-like phages and their impact on bacterial evolution Res. Microbiol. 158 2007 311 317 (Pubitemid 46810204)
37. Z. Otwinowski, and W. Minor DENZO and SCALEPACK M.G. Rossmann, E. Arnold, International Tables for Crystallography. Volume F: Crystallography of Biological Macromolecules 2006 Kluwer Academic Publishers Dordrecht, the Netherlands 226 235
38. 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
39. 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 (Pubitemid 47502947)
40. M.G. Rossmann, V.V. Mesyanzhinov, F. Arisaka, and P.G. Leiman The bacteriophage T4 DNA injection machine Curr. Opin. Struct. Biol. 14 2004 171 180 (Pubitemid 38490783)
41. S.B. Santos, A.M. Kropinski, P.J. Ceyssens, H.W. Ackermann, A. Villegas, R. Lavigne, V.N. Krylov, C.M. Carvalho, E.C. Ferreira, and J. Azeredo Genomic and proteomic characterization of the broad-host-range Salmonella phage PVP-SE1: creation of a new phage genus J. Virol. 85 2011 11265 11273
42. G. Sciara, C. Bebeacua, P. Bron, D. Tremblay, M. Ortiz-Lombardia, J. Lichire, M. van Heel, V. Campanacci, S. Moineau, and C. Cambillau Structure of lactococcal phage p2 baseplate and its mechanism of activation Proc. Natl. Acad. Sci. USA 107 2010 6852 6857
43. G.M. Sheldrick A short history of SHELX Acta Crystallogr. A 64 2008 112 122
44. L.D. Simon, and T.F. Anderson The infection of Escherichia coli by T2 and T4 bacteriophages as seen in the electron microscope. I. Attachment and penetration Virology 32 1967 279 297
45. L.D. Simon, and T.F. Anderson The infection of Escherichia coli by T2 and T4 bacteriophages as seen in the electron microscope. II. Structure and function of the baseplate Virology 32 1967 298 305
46. J. Söding, A. Biegert, and A.N. Lupas The HHpred interactive server for protein homology detection and structure prediction Nucleic Acids Res. 33 Web Server issue 2005 W244-8
47. S. Steinbacher, R. Seckler, S. Miller, B. Steipe, R. Huber, and P. Reinemer Crystal structure of P22 tailspike protein: interdigitated subunits in a thermostable trimer Science 265 1994 383 386 (Pubitemid 24259969)
48. E. Thomassen, G. Gielen, M. Schütz, G. Schoehn, J.P. Abrahams, S. Miller, and M.J. van Raaij The structure of the receptor-binding domain of the bacteriophage T4 short tail fibre reveals a knitted trimeric metal-binding fold J. Mol. Biol. 331 2003 361 373 (Pubitemid 36904021)
49. J.D. Thompson, D.G. Higgins, and T.J. Gibson CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice Nucleic Acids Res. 22 1994 4673 4680 (Pubitemid 24354800)
50. M.J. van Raaij, G. Schoehn, M.R. Burda, and S. Miller Crystal structure of a heat and protease-stable part of the bacteriophage T4 short tail fibre J. Mol. Biol. 314 2001 1137 1146 (Pubitemid 34073076)
51. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, P.R. Evans, R.M. Keegan, E.B. Krissinel, A.G. Leslie, and A. McCoy Overview of the CCP4 suite and current developments Acta Crystallogr. D Biol. Crystallogr. 67 2011 235 242
52. E. Yamashita, A. Nakagawa, J. Takahashi, K.I. Tsunoda, S. Yamada, and S. Takeda The host-binding domain of the P2 phage tail spike reveals a trimeric iron-binding structure Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 67 2011 837 841