Structure and biophysical properties of a triple-stranded beta-helix comprising the central spike of bacteriophage T4

Viruses

Volumn 7, Issue 8, 2015, Pages 4676-4706

  Buth, Sergey A ^a   Menin, Laure ^a   Shneider, Mikhail M ^a,b   Engel, Jürgen ^c   Boudko, Sergei P ^c,d,e,f,g   Leiman, Petr G ^a,d  

^a EPFL   (Switzerland)

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

^c UNIVERSITY OF BASEL   (Switzerland)

^d PURDUE UNIVERSITY   (United States)

^e SHRINERS HOSPITAL FOR CHILDREN   (United States)

^f OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^g VANDERBILT UNIVERSITY   (United States)

Author keywords

Amyloid like structure; Fatty acid; Fibrous proteins; Intrinsic protein fluorescence; Low complexity amino acid sequence; Mass spectrometry; Protein folding; Protein stability; X ray crystallography; Helical proteins

Indexed keywords

AMINO ACID SEQUENCE; ARTICLE; BIOPHYSICS; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; ELECTROSPRAY MASS SPECTROMETRY; ENTEROBACTERIA PHAGE T4; FLUORESCENCE ANALYSIS; GENE EXPRESSION; MASS FRAGMENTOGRAPHY; MASS SPECTROMETRY; MOLECULAR CLONING; NONHUMAN; PROTEIN FOLDING; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; TRIPLE STRANDED BETA HELIX; ULTRACENTRIFUGATION; X RAY CRYSTALLOGRAPHY; CHEMISTRY; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION;

FATTY ACID; GENE 5 PROTEIN, ENTEROBACTERIA PHAGE T4; PROTEIN BINDING; VIRAL PROTEIN;

BACTERIOPHAGE T4; BIOPHYSICAL PHENOMENA; CRYSTALLOGRAPHY, X-RAY; FATTY ACIDS; MASS SPECTROMETRY; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; VIRAL PROTEINS;

EID: 84941065962     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v7082839     Document Type: Article

References (63)

1. 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, e355. [CrossRef] [PubMed]
2. Leiman, P.G.; Shneider, M.M. Contractile tail machines of bacteriophages. Adv. Exp. Med. Biol. 2012, 726, 93-114. [PubMed]
3. Kikuchi, Y.; King, J. Genetic control of bacteriophage T4 baseplate morphogenesis. II. Mutants unable to form the central part of the baseplate. J. Mol. Biol. 1975, 99, 673-694. [CrossRef]
4. Kikuchi, Y.; King, J. Genetic control of bacteriophage T4 baseplate morphogenesis. III. Formation of the central plug and overall assembly pathway. J. Mol. Biol. 1975, 99, 695-716. [CrossRef]
5. Kanamaru, S.; Gassner, N.C.; Ye, N.; Takeda, S.; Arisaka, F. The C-terminal fragment of the precursor tail lysozyme of bacteriophage T4 stays as a structural component of the baseplate after cleavage. J. Bacteriol. 1999, 181, 2739-2744. [PubMed]
6. Leiman, P.G.; Kanamaru, S.; Mesyanzhinov, V.V.; Arisaka, F.; Rossmann, M.G. Structure and morphogenesis of bacteriophage T4. Cell. Mol. Life Sci. 2003, 60, 2356-2370. [CrossRef] [PubMed]
7. 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]
8. Mishra, P.; Prem Kumar, R.; Ethayathulla, A.S.; Singh, N.; Sharma, S.; Perbandt, M.; Betzel, C.; Kaur, P.; Srinivasan, A.; Bhakuni, V.; et al. Polysaccharide binding sites in hyaluronate lyase-Crystal structures of native phage-encoded hyaluronate lyase and its complexes with ascorbic acid and lactose. FEBS J. 2009, 276, 3392-3402. [CrossRef] [PubMed]
9. Mitraki, A.; Papanikolopoulou, K.; van Raaij, M.J. Natural triple beta-stranded fibrous folds. Adv. Protein Chem. 2006, 73, 97-124. [PubMed]
10. 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]
11. Thomassen, E.; Gielen, G.; Schutz, 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]
12. 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]
13. 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]
14. 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]
15. Spinelli, S.; Campanacci, V.; Blangy, S.; Moineau, S.; Tegoni, M.; Cambillau, C. Modular structure of the receptor binding proteins of lactococcus lactis phages. The rbp structure of the temperate phage tp901-1. J. Biol. Chem. 2006, 281, 14256-14262. [CrossRef] [PubMed]
16. Spinelli, S.; Desmyter, A.; Verrips, C.T.; de Haard, H.J.; Moineau, S.; Cambillau, C. Lactococcal bacteriophage p2 receptor-binding protein structure suggests a common ancestor gene with bacterial and mammalian viruses. Nat. Struct. Mol. Biol. 2006, 13, 85-89. [CrossRef] [PubMed]
17. Ricagno, S.; Campanacci, V.; Blangy, S.; Spinelli, S.; Tremblay, D.; Moineau, S.; Tegoni, M.; Cambillau, C. Crystal structure of the receptor-binding protein head domain from Lactococcus lactis phage bil170. J. Virol. 2006, 80, 9331-9335. [CrossRef] [PubMed]
18. Kajava, A.V.; Steven, A.C. Beta-rolls, beta-helices, and other beta-solenoid proteins. Adv. Protein Chem. 2006, 73, 55-96. [PubMed]
19. Smith, N.L.; Taylor, E.J.; Lindsay, A.M.; Charnock, S.J.; Turkenburg, J.P.; Dodson, E.J.; Davies, G.J.; Black, G.W. Structure of a group a streptococcal phage-encoded virulence factor reveals a catalytically active triple-stranded beta-helix. Proc. Natl. Acad. Sci. USA 2005, 102, 17652-17657. [CrossRef] [PubMed]
20. Stummeyer, K.; Dickmanns, A.; Muhlenhoff, M.; Gerardy-Schahn, R.; Ficner, R. Crystal structure of the polysialic acid-degrading endosialidase of bacteriophage k1f. Nat. Struct. Mol. Biol. 2005, 12, 90-96. [CrossRef] [PubMed]
21. Mosig, G.; Lin, G.W.; Franklin, J.; Fan, W.H. Functional relationships and structural determinants of two bacteriophage T4 lysozymes: A soluble (gene e) and a baseplate-associated (gene 5) protein. New Biol. 1989, 1, 171-179. [PubMed]
22. Shneider, M.M.; Buth, S.A.; Ho, B.T.; Basler, M.; Mekalanos, J.J.; Leiman, P.G. Paar-repeat proteins sharpen and diversify the type vi secretion system spike. Nature 2013, 500, 350-353. [CrossRef] [PubMed]
23. Sugimoto, K.; Kanamaru, S.; Iwasaki, K.; Arisaka, F.; Yamashita, I. Construction of a ball-and-spike protein supramolecule. Angew. Chem. Int. Ed. Engl. 2006, 45, 2725-2728. [CrossRef] [PubMed]
24. Ueno, T.; Koshiyama, T.; Tsuruga, T.; Goto, T.; Kanamaru, S.; Arisaka, F.; Watanabe, Y. Bionanotube tetrapod assembly by in situ synthesis of a gold nanocluster with (gp5-his6)3 from bacteriophage T4. Angew. Chem. Int. Ed. Engl. 2006, 45, 4508-4512. [CrossRef] [PubMed]
25. Yokoi, N.; Inaba, H.; Terauchi, M.; Stieg, A.Z.; Sanghamitra, N.J.; Koshiyama, T.; Yutani, K.; Kanamaru, S.; Arisaka, F.; Hikage, T.; et al. Construction of robust bio-nanotubes using the controlled self-assembly of component proteins of bacteriophage T4. Small 2010, 6, 1873-1879. [CrossRef]
26. Yokoi, N.; Miura, Y.; Huang, C.Y.; Takatani, N.; Inaba, H.; Koshiyama, T.; Kanamaru, S.; Arisaka, F.; Watanabe, Y.; Kitagawa, S.; et al. Dual modification of a triple-stranded beta-helix nanotube with ru and re metal complexes to promote photocatalytic reduction of co2. Chem. Commun. 2011, 47, 2074-2076. [CrossRef]
27. Kammerer, R.A.; Schulthess, T.; Landwehr, R.; Lustig, A.; Fischer, D.; Engel, J. Tenascin-c hexabrachion assembly is a sequential two-step process initiated by coiled-coil alpha-helices. J. Biol. Chem. 1998, 273, 10602-10608. [CrossRef] [PubMed]
28. Van Holde, K.E. Physical Biochemistry, 2nd ed.; Prentice Hall: Englewood Cliff, NJ, USA, 1985; pp. 93-136.
29. Otwinowski, Z.; Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Meth. Enzymol. 1997, 276, 307-326.
30. Vagin, A.; Teplyakov, A. Molrep: An automated program for molecular replacement. J. Appl. Crystallogr. 1997, 30, 1022-1025. [CrossRef]
31. Winn, M.D.; Ballard, C.C.; Cowtan, K.D.; Dodson, E.J.; Emsley, P.; Evans, P.R.; Keegan, R.M.; Krissinel, E.B.; Leslie, A.G.; McCoy, A.; et al. Overview of the ccp4 suite and current developments. Acta Crystallogr. Sect. D Biol. Crystallogr. 2011, 67, 235-242. [CrossRef] [PubMed]
32. Sheldrick, G.M. A short history of shelx. Acta Crystallogr. Sect. A Found. Crystallogr. 2008, 64, 112-122. [CrossRef] [PubMed]
33. Emsley, P.; Lohkamp, B.; Scott, W.G.; Cowtan, K. Features and development of coot. Acta Crystallogr. D Biol. Crystallogr. 2010, 66, 486-501. [CrossRef] [PubMed]
34. Kabsch, W. Integration, scaling, space-group assignment and post-refinement. Acta Crystallogr. Sect. D Biol. Crystallogr. 2010, 66, 133-144. [CrossRef] [PubMed]
35. Kabsch, W. Xds. Acta Crystallogr. Sect. D Biol. Crystallogr. 2010, 66, 125-132. [CrossRef] [PubMed]
36. 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]
37. Murshudov, G.N.; Skubak, 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 Crystallogr. Sect. D Biol. Crystallogr. 2011, 67, 355-367. [CrossRef] [PubMed]
38. Folch, J.; Lees, M.; Sloane Stanley, G.H. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 1957, 226, 497-509. [PubMed]
39. Sreerama, N.; Woody, R.W. Circular dichroism of peptides and proteins. In Circular Dichroism: Principles and Applications, 2nd ed.; Berova, N., Nakanishi, K.,Woody, R.W., Eds.; JohnWiley & Sons, Inc.: New York, NY, USA, 2000.
40. Krissinel, E.; Henrick, K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 2007, 372, 774-797. [CrossRef] [PubMed]
41. Adams, P.D.; Afonine, P.V.; Bunkoczi, G.; Chen, V.B.; Echols, N.; Headd, J.J.; Hung, L.W.; Jain, S.; Kapral, G.J.; Grosse Kunstleve, R.W.; et al. The phenix software for automated determination of macromolecular structures. Methods 2011, 55, 94-106. [CrossRef] [PubMed]
42. Hsin, K.; Sheng, Y.; Harding, M.M.; Taylor, P.; Walkinshaw, M.D. Mespeus: A database of the geometry of metal sites in proteins. J. Appl. Crystallogr. 2008, 41, 963-968. [CrossRef]
43. Potier, N.; Billas, I.M.L.; Steinmetz, A.; Schaeffer, C.; van Dorsselaer, A.; Moras, D.; Renaud, J.P. Using nondenaturing mass spectrometry to detect fortuitous ligands in orphan nuclear receptors. Protein Sci. 2003, 12, 725-733. [CrossRef] [PubMed]
44. Liu, Y.; Su, B.; Wang, X. Study on the noncovalent interactions of saikosaponins and cytochrome C by electrospray ionization mass spectrometry. Rapid Commun. Mass Spectrom. 2012, 26, 719-727. [CrossRef] [PubMed]
45. Last, A.M.; Robinson, C.V. Protein folding and interactions revealed by mass spectrometry. Curr. Opin. Chem. Biol. 1999, 3, 564-570. [CrossRef]
46. Tito, M.A.; Miller, J.; Walker, N.; Griffin, K.F.; Williamson, E.D.; Despeyroux-Hill, D.; Titball, R.W.; Robinson, C.V. Probing molecular interactions in intact antibody: Antigen complexes, an electrospray time-of-flight mass spectrometry approach. Biophys. J. 2001, 81, 3503-3509. [CrossRef]
47. Kitova, E.N.; El-Hawiet, A.; Schnier, P.D.; Klassen, J.S. Reliable determinations of protein-ligand interactions by direct esi-ms measurements. Are we there yet? J. Am. Soc. Mass Spectrom. 2012, 23, 431-441. [CrossRef] [PubMed]
48. Stein, S.E. Mass Spectra by NIST Mass Spec Data Center. NIST Chemistry WebBook; NIST Standard Reference Database Number 69. Linstrom, P.J., Mallard, W.G., Eds.; National Institute of Standards and Technology: Gaithersburg, MD, USA. Available online: http://webbook.nist.gov (accessed on 12 February 2014).
49. Letarov, A.V.; Londer, Y.Y.; Boudko, S.P.; Mesyanzhinov, V.V. The carboxy-terminal domain initiates trimerization of bacteriophage T4 fibritin. Biochemistry 1999, 64, 817-823. [PubMed]
50. 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]
51. Van Raaij, M.J.; Mitraki, A.; Lavigne, G.; Cusack, S. A triple beta-spiral in the adenovirus fibre shaft reveals a new structural motif for a fibrous protein. Nature 1999, 401, 935-938. [PubMed]
52. Boudko, S.P.; Engel, J.; Bachinger, H.P. The crucial role of trimerization domains in collagen folding. Int. J. Biochem. Cell Biol. 2012, 44, 21-32. [CrossRef] [PubMed]
53. Browning, C.; Shneider, M.M.; Bowman, V.D.; Schwarzer, D.; Leiman, P.G. Phage pierces the host cell membrane with the iron-loaded spike. Structure 2012, 20, 326-339. [CrossRef] [PubMed]
54. Squeglia, F.; Bachert, B.; De Simone, A.; Lukomski, S.; Berisio, R. The crystal structure of the streptococcal collagen-like protein 2 globular domain from invasive m3-type group a streptococcus shows significant similarity to immunomodulatory hiv protein gp41. J. Biol. Chem. 2014, 289, 5122-5133. [CrossRef] [PubMed]
55. Williams, S.R.; Gebhart, D.; Martin, D.W.; Scholl, D. Retargeting r-type pyocins to generate novel bactericidal protein complexes. Appl. Environ. Microbiol. 2008, 74, 3868-3876. [CrossRef] [PubMed]
56. Schwarzer, D.; Stummeyer, K.; Haselhorst, T.; Freiberger, F.; Rode, B.; Grove, M.; Scheper, T.; von Itzstein, M.; Muhlenhoff, M.; Gerardy-Schahn, R. Proteolytic release of the intramolecular chaperone domain confers processivity to endosialidase f. J. Biol. Chem. 2009, 284, 9465-9474. [CrossRef] [PubMed]
57. Steinmetz, M.O.; Jelesarov, I.; Matousek, W.M.; Honnappa, S.; Jahnke, W.; Missimer, J.H.; Frank, S.; Alexandrescu, A.T.; Kammerer, R.A. Molecular basis of coiled-coil formation. Proc. Natl. Acad. Sci. USA 2007, 104, 7062-7067. [CrossRef] [PubMed]
58. Crooks, G.E.; Hon, G.; Chandonia, J.M.; Brenner, S.E. Weblogo: A sequence logo generator. Genome Res. 2004, 14, 1188-1190. [CrossRef] [PubMed]
59. Chenna, R.; Sugawara, H.; Koike, T.; Lopez, R.; Gibson, T.J.; Higgins, D.G.; Thompson, J.D. Multiple sequence alignment with the clustal series of programs. Nucleic Acids Res. 2003, 31, 3497-3500. [CrossRef] [PubMed]
60. Traub, W.; Piez, K.A. The chemistry and structure of collagen. Adv. Protein Chem. 1971, 25, 243-352. [PubMed]
61. Bella, J.; Eaton, M.; Brodsky, B.; Berman, H.M. Crystal and molecular structure of a collagen-like peptide at 1.9 a resolution. Science 1994, 266, 75-81. [CrossRef] [PubMed]
62. Lupas, A. Coiled coils: New structures and new functions. Trends Biochem. Sci. 1996, 21, 375-382. [CrossRef]
63. Inaba, H.; Kanamaru, S.; Arisaka, F.; Kitagawa, S.; Ueno, T. Semi-synthesis of an artificial scandium(iii) enzyme with a beta-helical bio-nanotube. Dalton Trans. 2012, 41, 11424-11427. [CrossRef] [PubMed]