Crystal structure of the carboxy-terminal region of the bacteriophage T4 proximal long tail fiber protein Gp34

Viruses

Volumn 9, Issue 7, 2017, Pages

  Granell, Meritxell ^a,d   Namura, Mikiyoshi ^b   Alvira, Sara ^a,c,e   Kanamaru, Shuji ^b   van Raaij, Mark J ^a,c  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^c UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^d CNRS   (France)

^e UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Bacterial viruses; Caudovirales; Crystallography; Fibrous protein; Myoviridae

Indexed keywords

LONG TAIL FIBRE PROTEIN GP34; LONG TAIL FIBRE PROTEIN GP35; LONG TAIL FIBRE PROTEIN GP36; LONG TAIL FIBRE PROTEIN GP37; UNCLASSIFIED DRUG; VIRAL PROTEIN;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BACTERIOPHAGE TYPING; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DNA HAIRPIN; ENTEROBACTERIA PHAGE T4; MOLECULAR DOCKING; NONHUMAN; PHAGE THERAPY; PROTEIN EXPRESSION; PROTEIN STABILITY; RECEPTOR BINDING; SEQUENCE ANALYSIS; TRIPLE HELIX; CHEMISTRY; MOLECULAR MODEL; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

BACTERIOPHAGE T4; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; PROTEIN CONFORMATION; VIRAL TAIL PROTEINS;

EID: 85022339941     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v9070168     Document Type: Article

References (49)

1. Cairns, J.; Stent, G.S.; Watson, J.D. Phage and the Origins of Molecular Biology, the Centennial Edition; Cold Spring Harbor laboratory Press: New York, NY, USA, 2007; ISBN 9780879698003.
2. Canchaya, C.; Fournous, G.; Chibani-Chennoufi, S.; Dillmann, M.L.; Brüssow, H. Phage as agents of lateral gene transfer. Curr. Opin. Microbiol. 2003, 6, 417–424. [CrossRef]
3. Brüssow, H.; Canchaya, C.; Hardt, W.D. Phages and the evolution of bacterial pathogens: From genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 2004, 68, 560–602. [CrossRef] [PubMed]
4. Clark, J.R.; March, J.B. Bacteriophages and biotechnology: Vaccines, gene therapy and antibacterials. Trends Biotechnol. 2006, 24, 212–218. [CrossRef] [PubMed]
5. Ackermann, H.W. Bacteriophage observations and evolution. Res. Microbiol. 2003, 154, 245–251. [CrossRef]
6. Ackermann, H.W.; Prangishvili, D. Prokaryote viruses studied by electron microscopy. Arch. Virol. 2012, 157, 1843–1849. [CrossRef] [PubMed]
7. Karam, J.D.; Drake, J.W.; Kreuzer, K.N.; Mosig, G.; Hall, D.H.; Eiserling, F.A.; Black, L.W.; Spicer, E.K.; Kutter, E.; Carlson, K. et al. Molecular Biology of Bacteriophage T4; American Society for Microbiology: Washington, DC, USA, 1994; ISBN 9781555810641.
8. Leiman, P.G.; Arisaka, F.; van Raaij, M.J.; Kostyuchenko, V.A.; Aksyuk, A.A.; Kanamaru, S.; Rossmann, M.G. Morphogenesis of the T4 tail and tail fibers. Virol. J. 2010, 7, 355. [CrossRef] [PubMed]
9. Taylor, N.M.I.; Prokhorov, N.S.; Guerrero-Ferreira, R.C.; Shneider, M.M.; Browning, C.; Goldie, K.N.; Stahlberg, H.; Leiman, P.G. Structure of the T4 baseplate and its function in triggering sheath contraction. Nature 2016, 533, 346–352. [CrossRef] [PubMed]
10. Hu, B.; Margolin, W.; Molineux, I.J.; Liu, J. Structural remodeling of bacteriophage T4 and host membranes during infection initiation. Proc. Natl. Acad. Sci. USA 2015, 112, E4919–E4928. [CrossRef] [PubMed]
11. Riede, I. Receptor specificity of the short tail fibres (gp12) of T-even type Escherichia coli phages. Mol. Gen. Genet. 1987, 206, 110–115. [CrossRef] [PubMed]
12. Kostyuchenko, V.A.; Leiman, P.G.; Chipman, P.R.; Kanamaru, S.; van Raaij, M.J.; Arisaka, F.; Mesyanzhinov, V.V.; Rossmann, M.G. Three-dimensional structure of bacteriophage T4 baseplate. Nat. Struct. Biol. 2003, 10, 688–693. [CrossRef] [PubMed]
13. Cerritelli, M.E.; Wall, J.S.; Simon, M.N.; Conway, J.F.; Steven, A.C. Stoichiometry and domainal organization of the long tail-fiber of bacteriophage T4 A hinged viral adhesin. J. Mol. Biol. 1996, 260, 767–780. [CrossRef] [PubMed]
14. Granell, M.; Namura, M.; Alvira, S.; Garcia-Doval, C.; Singh, A.K.; Gutsche, I.; van Raaij, M.J.; Kanamaru, S. Crystallization of the carboxy-terminal region of the bacteriophage T4 proximal long tail fibre protein gp34. Acta Cryst. Sect. F 2014, 70, 970–975. [CrossRef] [PubMed]
15. Bartual, S.G.; Otero, J.M.; Garcia-Doval, C.; Llamas-Saiz, A.L.; Kahn, R.; Fox, G.C.; van Raaij, M.J. Structure of the bacteriophage T4 long tail fiber receptor-binding tip. Proc. Natl. Acad. Sci. USA 2010, 107, 20287–20292. [CrossRef] [PubMed]
16. Hashemolhosseini, S.; Stierhof, Y.D.; Hindennach, I.; Henning, U. Characterization of the helper proteins for the assembly of tail fibers of coliphages T4 and λ. J. Bacteriol. 1996, 178, 6258–6265. [CrossRef] [PubMed]
17. Ali, S.A.; Iwabuchi, N.; Matsui, T.; Hirota, K.; Kidokoro, S.; Arai, M.; Kuwajima, K.; Schuck, P.; Arisaka, F. Reversible and fast association equilibria of a molecular chaperone, gp57A, of bacteriophage T4. Biophys. J. 2003, 85, 2606–2618. [CrossRef]
18. Bartual, S.G.; Garcia-Doval, C.; Alonso, J.; Schoehn, G.; van Raaij, M.J. Two-chaperone assisted soluble expression and purification of the bacteriophage T4 long tail fibre protein gp37. Protein Expr. Purif. 2010, 70, 116–121. [CrossRef] [PubMed]
19. Van Raaij, M.J.; Schoehn, G.; Burda, M.R.; Miller, S. Crystal structure of a heat and protease-stable part of the bacteriophage T4 short tail fibre. J. Mol. Biol. 2001, 314, 1137–1146. [CrossRef] [PubMed]
20. Thomassen, E.; Gielen, G.; Schütz, M.; Schoehn, G.; Abrahams, J.P.; Miller, S.; van Raaij, M.J. The structure of the receptor-binding domain of the bacteriophage T4 short tail fibre reveals a knitted trimeric metal-binding fold. J. Mol. Biol. 2003, 331, 361–373. [CrossRef]
21. Sheldrick, G.M. A short history of SHELX. Acta Cryst. Sect. A 2008, 64, 112–122. [CrossRef] [PubMed]
22. Vonrhein, C.; Blanc, E.; Roversi, R.; Bricogne, G. Automated structure solution with Autosharp. Methods Mol. Biol. 2007, 364, 215–230. [CrossRef] [PubMed]
23. Abrahams, J.P.; Leslie, A.G.W. Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Cryst. Sect. D 1996, 52, 30–42. [CrossRef] [PubMed]
24. Langer, G.; Cohen, S.X.; Lamzin, V.S.; Perrakis, A. Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7. Nat. Protoc. 2008, 3, 1171–1179. [CrossRef] [PubMed]
25. McCoy, A.J.; Grosse-Kunstleve, R.W.; Adams, P.D.; Winn, M.D.; Storoni, L.C.; Read, R.J. Phaser crystallographic software. J. Appl. Crystallogr. 2007, 40, 658–674. [CrossRef] [PubMed]
26. Vagin, A.; Teplyakov, A. MOLREP An automated program for molecular replacement. J. Appl. Cryst. 1997, 30, 1022–1025. [CrossRef]
27. Emsley, P.; Lohkamp, B.; Scott, W.G.; Cowtan, K. Features and development of Coot. Acta Cryst. Sect. D 2010, 66, 486–501. [CrossRef] [PubMed]
28. Murshudov, G.N.; Skubák, P.; Lebedev, A.A.; Pannu, N.S.; Steiner, R.A.; Nicholls, R.A.; Winn, M.D.; Long, F.; Vagin, A.A. REFMAC5 for the refinement of macromolecular crystal structures. Acta Cryst. Sect. D 2011, 67, 355–367. [CrossRef] [PubMed]
29. Headd, J.J.; Echols, N.; Afonine, P.V.; Grosse-Kunstleve, R.W.; Chen, V.B.; Moriarty, N.W.; Richardson, D.C.; Richardson, J.S.; Adams, P.D. Use of knowledge-based restraints in phenix.refine to improve macromolecular refinement at low resolution. Acta Cryst. Sect. D 2012, 68, 381–390. [CrossRef] [PubMed]
30. Chen, V.B.; Arendall, W.B.; Headd, J.J.; Keedy, D.A.; Immormino, R.M.; Kapral, G.J.; Murray, L.W.; Richardson, J.S.; Richardson, D.C. MolProbity: All-atom structure validation for macromolecular crystallography. Acta Cryst. Sect. D 2010, 66, 12–21. [CrossRef] [PubMed]
31. Young, J.; Westbrook, J.D.; Feng, Z.; Sala, R.; Peisach, E.; Oldfield, T.J.; Sen, S.; Gutmanas, A.; Armstrong, D.R.; Berrisford, J.M. et al. OneDep Unified wwPDB system for deposition, biocuration, and validation of macromolecular structures in the Protein Data Bank (PDB) archive. Structure 2017, 25, 536–545. [CrossRef] [PubMed]
32. The PyMOL Molecular Graphics System, Version 1.6; Schrödinger LLC: New York, NY, USA, 2013.
33. Pettersen, E.F.; Goddard, T.D.; Huang, C.C.; Couch, G.S.; Greenblatt, D.M.; Meng, E.C.; Ferrin, T.E. UCSF Chimera, a visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25, 1605–1612. [CrossRef] [PubMed]
34. Holm, L.; Rosenstrom, P. Dali server: Conservation mapping in 3D. Nucleic Acids Res. 2010, 38, W545–W549. [CrossRef] [PubMed]
35. Krissinel, E. Stock-based detection of protein oligomeric states in jsPISA. Nucleic Acids Res. 2015, 43, W314–W319. [CrossRef] [PubMed]
36. Tai, C.H.; Paul, R.; Dukka, K.C.; Shilling, J.D.; Lee, B. SymD webserver: A platform for detecting internally symmetric protein structures. Nucleic Acids Res. 2014, 42, W296–W300. [CrossRef] [PubMed]
37. Thompson, J.D.; Higgins, D.G.; Gibson, T.J. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids. Res. 1994, 22, 4673–4680. [CrossRef] [PubMed]
38. Aurora, R.; Rose, G.D. Helix capping. Protein Sci. 1998, 7, 21–38. [CrossRef] [PubMed]
39. Kanamaru, S.; Leiman, P.G.; Kostyuchenko, V.A.; Chipman, P.R.; Mesyanzhinov, V.V.; Arisaka, F.; Rossmann, M.G. Structure of the cell-puncturing device of bacteriophage T4. Nature 2002, 415, 553–557. [CrossRef] [PubMed]
40. Jabs, A.; Weiss, M.S.; Hilgenfeld, R. Non-proline cis peptide bonds in proteins. J. Mol. Biol. 1999, 286, 291–304. [CrossRef] [PubMed]
41. Steinbacher, S.; Seckler, R.; Miller, S.; Steipe, B.; Huber, R.; Reinemer, P. Crystal structure of P22 tailspike protein Interdigitated subunits in a thermostable trimer. Science 1994, 265, 383–386. [CrossRef] [PubMed]
42. Walter, M.; Fiedler, C.; Grassl, R.; Biebl, M.; Rachel, R.; Hermo-Parrado, X.L.; Llamas-Saiz, A.L.; Seckler, R.; Miller, S.; van Raaij, M.J. Structure of the receptor-binding protein of bacteriophage Det7: A podoviral tail spike in a myovirus. J. Virol. 2008, 82, 2265–2273. [CrossRef] [PubMed]
43. Garcia-Doval, C.; van Raaij, M.J. Structure of the receptor-binding carboxy-terminal domain of bacteriophage T7 tail fibers. Proc. Natl. Acad. Sci. USA 2012, 109, 9390–9395. [CrossRef] [PubMed]
44. Garcia-Doval, C.; Castón, J.R.; Luque, D.; Granell, M.; Otero, J.M.; Llamas-Saiz, A.L.; Renouard, M.; Boulanger, P.; van Raaij, M.J. Structure of the receptor-binding carboxy-terminal domain of the bacteriophage T5 L-shaped tail fibre with and without its intra-molecular chaperone. Viruses 2015, 7, 6424–6440. [CrossRef] [PubMed]
45. Schulz, E.C.; Dickmanns, A.; Urlaub, H; Schmitt, A.; Mühlenhoff, M.; Stummeyer, K.; Schwarzer, D.; Gerardy-Schahn, R.; Ficner, R. Crystal structure of an intramolecular chaperone mediating triple-β-helix folding. Nat. Struct. Mol. Biol. 2010, 17, 210–215. [CrossRef] [PubMed]
46. Xiang, Y.; Leiman, P.G.; Li, L.; Grimes, S.; Anderson, D.L.; Rossmann, M.G. Crystallographic insights into the autocatalytic assembly mechanism of a bacteriophage tail spike. Mol. Cell 2009, 34, 375–386. [CrossRef] [PubMed]
47. Kostyuchenko, V.A.; Chipman, P.R.; Leiman, P.G.; Arisaka, F.; Mesyanzhinov, V.V.; Rossmann, M.G. The tail structure of bacteriophage T4 and its mechanism of contraction. Nat. Struct. Mol. Biol. 2005, 12, 810–813. [CrossRef] [PubMed]
48. Van Raaij, M.J.; Mitraki, A. β-structured viral fibres: Assembly, structure and implications for materials design. Curr. Opin. Solid State Mater. Sci. 2004, 8, 151–156. [CrossRef]
49. Woolfson, D.N. Building fibrous biomaterials from α-helical and collagen-like coiled-coil peptides. Biopolymers 2010, 94, 118–127. [CrossRef] [PubMed]