High-resolution structure of a polyomavirus VP1-oligosaccharide complex: Implications for assembly and receptor binding

EMBO Journal

Volumn 16, Issue 16, 1997, Pages 5139-5148

  Stehle, Thilo ^a   Harrison, Stephen C ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

Carbohydrate recognition; Polyomavirus; Sialic acid; Viral assembly; Virus receptor interaction

Indexed keywords

OLIGOSACCHARIDE; RECEPTOR; SIALIC ACID; VIRUS PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; NONHUMAN; POLYOMA VIRUS; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STRUCTURE; RECEPTOR BINDING; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS PARTICLE; VIRUS RECOMBINANT;

AMINO ACID SEQUENCE; BINDING SITES; CAPSID; CAPSID PROTEINS; CRYSTALLOGRAPHY, X-RAY; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; N-ACETYLNEURAMINIC ACID; OLIGOSACCHARIDES; POLYOMAVIRUS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, VIRUS; RECOMBINANT PROTEINS; VIRUS ASSEMBLY;

MIRIDAE; POLYOMAVIRUS;

EID: 0030839256     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.16.5139     Document Type: Article

References (40)

1. Bauer, P.H., Bronson, R.T., Fung, S.C., Freund, R., Stehle, T., Harrison, S.C. and Benjamin, T.L. (1995) Genetic and structural analysis of a virulence determinant in polyoma VP1. J. Virol., 69, 7925-7931.
2. Bourne, Y., Mazurier, J., Legrand, D., Rouge, P., Montreuil, J., Spik, G. and Cambillau, C. (1994) Structures of a legume lectin complexed with the human lactoferrin N2 fragment, and with an isolated biantennary glycopeptide: role of the fucose moiety. Structure, 2, 209-219.
3. Breg, J., Kroon-Batenburg, L.M.J., Strecker, G., Montreuil, J. and Vliegenthart, J.F.G. (1989) Conformational analysis of the sialyl α(2-3/6) N-acetyllactosamine structural element occurring in glycoproteins, by two-dimensional NOE 1H-NMR spectroscopy in combination with energy calculations by hard sphere exo-anomeric and molecular mechanics force field with hydrogen-bonding potential. Eur. J. Biochem., 178, 727-739.
4. Brünger, A.T. (1992) Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature, 355, 472-475.
5. Brünger, A.T., Kuriyan, J. and Karplus, M. (1987) Crystallographic R factor refinement by molecular dynamics. Science, 235, 458-460.
6. Cahan, L.D., Singh, R. and Paulson, J.C. (1983) Sialyloligosaccharide receptors of binding variants of polyomavirus. Virology, 130, 281-289.
7. Carson, M. (1987) Ribbon models of macromolecules. J. Mol. Graphics, 5, 103-106.
8. Caspar, D.L.D. (1976) Switching in the self-control of self-assembly. In The Proceedings of !he Third Annual John Innes Symposium. pp. 85-99.
9. CCP4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr., D50, 760-763.
10. Connolly, M.S. (1983) Analytical molecular surface calculation. J. Appl. Crystallogr., 16, 548-558.
11. Eckhart, W. (1990) Polyomavirinae and their replication. In Fields, B.N. and Knipe, D.M. (eds). Virology. 2nd edn, Raven Press Ltd., New York, USA, pp. 1593-1607.
12. Eisen, M.B., Sabesan, S., Skehel, J.J. and Wiley, D.C. (1997) Binding of the influenza A virus to cell-surface receptors: structures of five hemagglutinin-sialyloligosaccharide complexes determined by X-ray crystallography. Virology, 232, 19-31.
13. Freund, R., Calderone, A., Dawe, C.J. and Benjamin, T.L. (1991) Polyomavirus tumor induction in mice: effects of polymorphisms of VP1 and large T antigen. J. Virol., 65, 335-341.
14. Fried, H., Cahan, L.D. and Paulson, J.C. (1981) Polyomavirus recognizes specific sialyloligosaccharide receptors on host cells. Virology, 109, 188-192.
15. Garcea, R.L., Ballmer-Hofer, K. and Benjamin, T.L. (1985) Virion assembly defect of polyomavirus hr-t mutants: underphosphorylation of major capsid protein VP1 before viral encapsidation. J. Virol., 54, 311-316.
16. Garcea, R.L., Salunke, D.M. and Caspar, D.L.D. (1987) Site-directed mutation affecting polyomavirus capsid self-assembly in vitro. Nature, 329, 86-87.
17. Jones, T.A., Zhou, J.-Y., Cowan, S.W. and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr., A47, 110-119.
18. Kawano, T., Koyama, S., Takematsu, H., Kozutsumi, Y., Kawasaki, H., Kawashima, S., Kawasaki, T. and Suzuki, A. (1995) Molecular cloning of cytidine monophospho-N-acetylneuraminic acid hydroxylase. Regulation of species-and tissue-specific expression of N-glycolyl neuraminic acid. J. Biol. Chem., 270, 16458-16463.
19. Kraulis, P.J. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr., 24, 946-950.
20. Lamzin, V.S. and Wilson, K.S. (1993) Automated refinement of protein models. Acta Crystallogr., D49, 129-147.
21. Leavitt, A.D., Roberts, T.M. and Garcea, R.L. (1985) Polyomavirus major capsid protein, VP1. J. Biol. Chem., 260, 12803-12809.
22. Liddington, R.C., Yan, Y., Moulai, J., Sahli, R., Benjamin, T.L. and Harrison, S.C. (1991) Structure of simian virus 40 at 3.8 Å resolution. Nature, 354, 278-284.
23. Luzzati, V. (1952) Traitement statistique des erreurs dans la determination des structures cristallines. Acta Crystallogr., 5, 802-810.
24. M1 pentasaccharide. Protein Sci., 3, 166-175.
25. Navaza, J. (1994) AMoRe: an automated package for molecular replacement. Acta Crystallogr., A50, 157-163.
26. Otwinowski, Z. (1993) Oscillation data reduction program. In Sawyer, L., Isaacs, N. and Burley, S. (eds). Proceedings of the Daresbury Study Weekend: Data Collection and Processing. Daresbury Laboratory, Warrington, UK, pp. 56-62.
27. M4) and its NeuNAc(α2,3) Galβ sugar component. Eur. J. Biochem., 180, 337-342.
28. Poppe, L., Stuike-Prill, R., Meyer, B. and Haalbeek, H.V. (1992) The solution conformation of sialyl-α(2,6)-lactose. Studies by modern NMR techniques and Monte Carlo simulations. J. Biomol. NMR, 2, 109-136.
29. Ramachandran, G.N. and Sasisekharan, V. (1968) Conformation of polypeptides and proteins. Adv. Protein Chem., 23, 283-437.
30. Sabesan, S., Bock, K. and Paulson, J.C. (1991) Conformational analysis of sialyloligosaccharides. Carbohydrate Res., 218, 27-54.
31. Salunke, D.M., Caspar, D.L.D. and Garcea, R.L. (1986) Self-assembly of purified polyomavirus capsid protein VP1. Cell, 46, 895-904.
32. Salunke, D.M., Caspar, D.L.D. and Garcea, R.L. (1989) Polymorphism in the assembly of polyomavirus capsid protein VP1. Biophys. J., 56, 887-900.
33. Sauter, N.S., Hanson, J.E., Glick, G.D., Brown, J.H., Crowther, R.L., Park, S.J., Skehel, J.J. and Wiley, D.C. (1992) Binding of influenza virus hemagglutinin to analogs of its cell-surface receptor, sialic acid: analysis by proton nuclear magnetic resonance spectroscopy and X-ray crystallography. Biochemistry, 31, 9609-9621.
34. Stehle, T. and Harrison, S.C. (1996) Crystal structures of murine polyomavirus in complex with straight-chain and branched-chain sialyloligosaccharide receptor fragments. Structure, 4, 183-194.
35. Stehle, T., Gamblin, S.J., Yan, Y. and Harrison, S.C. (1996) The structure of simian virus 40 refined at 3.1 Å resolution. Structure, 4, 165-182.
36. Stehle, T., Yan, Y., Benjamin, T.L. and Harrison, S.C. (1994) Structure of murine polyomavirus complexed with an oligosaccharide receptor fragment. Nature, 369, 160-163.
37. Stein, P.E., Boodhoo, A., Armstrong, G.D., Heerze, L.D., Cockle, S.A., Klein, M.H. and Read, R.J. (1994) Structure of a pertussis toxin-sugar complex as a model for receptor binding. Nature Struct. Biol., 1, 591-596.
38. Tooze, J. (1981) DNA Tumor Viruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA.
39. Wright, C.S. (1990) 2.2 Å resolution structure analysis of two refined N-acetylneuraminyl-lactose-wheat germ agglutinin isolectin complexes. J. Mol. Biol., 215, 635-651.
40. Wright, C.S. and Jaeger, J. (1993) Crystallographic refinement and structure analysis of the complex of wheat germ agglutinin with a bivalent sialoglycopeptide from glycophorin A. J. Mol. Biol., 232, 620-638.