The refined structure of human rhinovirus 16 at 2.15 Å resolution: Implications for the viral life cycle

Structure

Volumn 5, Issue 3, 1997, Pages 427-441

  Hadfield, Andrea T ^a,c   Lee, Wai Ming ^b   Zhao, Rui ^a,d   Oliveira, Marcos A ^a,e   Minor, Iwona ^a   Rueckert, Roland R ^b   Rossmann, Michael G ^a  

^a PURDUE UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c BRANDEIS UNIVERSITY   (United States)

^d UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^e UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

crystal structure; human rhinovirus 16; refinement; RNA; site directed mutagenesis

Indexed keywords

EID: 0031569393     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(97)00199-8     Document Type: Article

References (64)

1. Rueckert, R.R. (1996). Picornaviridae: the viruses and their replication. In Virology. (Fields, B.N., Knipe, D.M. & Howley, P.M., eds), pp. 609-654, Lippincott-Raven Press, New York.
2. Lee, W., Monroe, S.S. & Rueckert, R.R. (1993). Role of maturation cleavage in infectivity of picornaviruses: activation of an infectosome. J. Virol. 67, 2110-2122.
3. Oliveira, M.A., et al., & Rossmann, M.G. (1993). The structure of human rhinovirus 16. Structure 1, 51-68.
4. Rossmann, M.G., et al., & Vriend, G. (1985). Structure of a human common cold virus and functional relationship to other picornaviruses. Nature 317, 145-153.
5. Abraham, G. & Colonno, R.J. (1984). Many rhinovirus serotypes share the same cellular receptor. J. Virol. 51, 340-345.
6. Greve, J.M., et al., & McClelland, A. (1989). The major human rhinovirus receptor is ICAM-1. Cell 56, 839-847.
7. Staunton, D.E., Merluzzi, V.J., Rothlein, R., Barton, R., Marling, S.D. & Springer, T.A. (1989). A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell 56, 849-853.
8. Olson, N.H., et al., & Rossmann, M.G. (1993). Structure of a human rhinovirus complexed with its receptor molecule. Proc. Natl. Acad. Sci. USA 90, 507-511.
9. Smith, T.J., et al., & Otto, M.J. (1986). The site of attachment in human rhinovirus 14 for antiviral agents that inhibit uncoating. Science 233, 1286-1293.
10. Grant, R.A., Hiremath, C.N., Filman, D.J., Syed, R., Andries, K. & Hogle, J.M. (1994). Structures of poliovirus complexes with anti-viral drugs: implications for viral stability and drug design. Curr. Biol. 4, 784-797.
11. Kim, K.H., et al., & Pevear, D.C. (1993). A comparison of the antirhinoviral drug binding pocket in HRV14 and HRV1A. J. Mol. Biol. 230, 206-225.
12. Muckelbauer, J.K., et al., & Rossmann. M.G. (1995). The structure of coxsackievirus B3 at 3.5 Å resolution. Structure 3, 653-667.
13. McSharry, J.J., Caliguiri, L.A. & Eggers, H.J. (1979). Inhibition of uncoating of poliovirus by arildone, a new antiviral drug. Virology 97, 307-315.
14. Diana, G.D., et al., & Pancic, F. (1977). Antiviral activity of some β-diketones. 1. Aryl alkyl diketones. In vitro activity against both RNA and DNA viruses. J. Med. Chem. 20, 750-756.
15. Pevear, D.C., et al., & Dutko, F.J. (1989). Conformational change in the floor of the human rhinovirus canyon blocks adsorption to HeLa cell receptors. J. Virol. 63, 2002-2007.
16. Filman, D.J., Syed, R., Chow, M., Macadam, A.J., Minor, P.D. & Hogle, J.M. (1989). Structural factors that control conformational transitions and serotype specificity in type 3 poliovirus. EMBO J. 8, 1567-1579.
17. Hoover-Litty, H. & Greve, J.M. (1993). Formation of rhinovirus-soluble ICAM-1 complexes and conformational changes in the virion. J. Virol. 67, 390-397.
18. Fricks, C.E. & Hogle, J.M. (1990). Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding. J. Virol. 64, 1934-1945.
19. Casanovas, J.M. & Springer, T.A. (1994). Pathway of rhinovirus disruption by soluble intercellular adhesion molecule 1 (ICAM-1): an intermediate in which ICAM-1 is bound and RNA is released. J. Virol. 68, 5882-5889.
20. Moscufo, N., Yafal, A.G., Rogove, A., Hogle, J. & Chow, M. (1993). A mutation in VP4 defines a new step in the late stages of cell entry by poliovirus. J. Virol. 67, 5075-5078.
21. Zhao, R., et al., & Rossmann, M.G. (1996). Human rhinovirus 3 at 3.0 Å resolution. Structure 4, 1205-1220.
22. Harrison, S.C., Olson, A.J., Schutt, C.E., Winkler, F.K. & Bricogne, G. (1978). Tomato bushy stunt virus at 2.9 Å resolution. Nature 276, 368-373.
23. McKenna, R., et al., & Incardona, N.L. (1992). Atomic structure of single-stranded DNA bacteriophage ΦX174 and its functional implications. Nature 355, 137-143.
24. Speir, J.A., Munshi, S., Wang, G., Baker, T.S. & Johnson, J.E. (1995). Structures of the native and swollen forms of cowpea chlorotic mottle virus determined by X-ray crystallography and cryo electron microscopy. Structure 3, 63-78.
25. Zhao, R., Hadfield, A.T., Kremer, M.J. & Rossmann, M.G. (1997). Cations in human rhinoviruses. Virology, 227, 13-23.
26. Brown, E.A. & Bugg, C.E. (1980). Calcium-binding to nucleotides: structure of a hydrated calcium salt of inosine 5′-monophosphate. Acta Cryst. B 36, 2597-2604.
27. Bock, C.W., Katz, A.K. & Glusker, J.P. (1995). Hydration of zinc ions: a comparison with magnesium and beryllium ions. J. Am. Chem. Soc. 117, 3754-3765.
28. Korant, B.D., Kauer, J.C. & Butterworth, B.E. (1974). Zinc ions inhibit replication of rhinoviruses. Nature 248, 588-590.
29. Korant, B.D. & Butterworth, B.E. (1976). Inhibition by zinc of rhinovirus protein cleavage: interaction of zinc with capsid polypeptides. J. Virol. 18, 298-306.
30. Eby, G.A., Davis, D.R. & Halcomb, W.W. (1984). Reduction in duration of common colds by zinc gluconate lozenges in a double-blind study. Antimicrob. Agents Chemother. 25, 20-24.
31. Godfrey, J.C. (1988). Zinc for the common cold. Antimicrob. Agents Chemother. 32, 605-606.
32. Godfrey, J.C., Conant-Sloane, B., Smith, D.S., Turco, J.H., Mercer, N. & Godfrey, N.J. (1992). Zinc gluconate and the common cold: a controlled clinical study. J. Int. Med. Res. 20, 234-246.
33. Lee, W., Wang, W. & Rueckert, R.R. (1994). Complete sequence of the RNA genome of human rhinovirus 16, a clinically useful common cold virus belonging to the ICAM-1 receptor group. Virus Genes 9, 177-181.
34. Lea, S., et al., & Mateu, M.G (1994). The structure and antigenicity of a type C foot-and-mouth disease virus. Structure 2, 123-139.
35. Koch, F. & Koch, G. (1985). The Molecular Biology of Poliovirus. Springer-Verlag, New York.
36. Arnold, E. & Rossmann, M.G. (1990). Analysis of the structure of a common cold virus, human rhinovirus 14, refined at a resolution of 3.0 Å. J. Mol. Biol. 211, 763-801.
37. Flore, O., Fricks, C.E., Filman, D.J. & Hogle, J.M. (1990). Conformational changes in poliovirus assembly and cell entry. Semin. Virol. 1, 429-438.
38. Basavappa, R., Syed, R., Flore, O., Icenogle, J.P., Filman, D.J. & Hogle, J.M. (1994). Role and mechanism of the maturation cleavage of VPO in poliovirus assembly: structure of the empty capsid assembly intermediate at 2.9 Å resolution. Protein Sci. 3, 1651-1669.
39. Yeates, T.O., et al., & Hogle, J.M. (1991). Three-dimensional structure of a mouse-adapted type 2/type 1 poliovirus chimera. EMBO J. 10, 2331-2341.
40. Smyth, M., Tate, J., Hoey, E., Lyons, C., Martin, S. & Stuart, D. (1995). Implications for viral uncoating from the structure of bovine enterovirus. Nat. Struct. Biol. 2, 224-231.
41. Hadfield, A.T., et al., & Rossmann, M.G. (1995). Structural studies on human rhinovirus 14 drug-resistant compensation mutants. J. Mol. Biol. 253, 61-73.
42. Rossmann, M.G. (1994). Viral cell recognition and entry. Protein Sci. 3, 1712-1725.
43. Mosser, A.G., Sgro, J.-Y. & Rueckert, R.R. (1995). WIN51711-resistant mutants of poliovirus type 3: capsid residues important in uncoating functions. Acta Cryst. D 51, 490-495.
44. Giranda, V.L., et al., & Rueckert, R.R. (1992). Acid-induced structural changes in human rhinovirus 1 4: possible role in uncoating. Proc. Natl. Acad. Sci. USA 89, 10213-10217.
45. Cheng, R.H., Reddy, V.S., Olson, N.H., Fisher, A.J., Baker, T.S. & Johnson, J.E. (1994). Functional implications of quasi-equivalence in a T= 3 icosahedral animal virus established by cryo-electron microscopy and X-ray crystallography. Structure 2, 271-282.
46. Munshi, S., et al., & Johnson, J. (1996). The 2.8 Å structure of a T = 4 animal virus and its implications for membrane translocation of RNA. J. Mol. Biol. 261, 1-10.
47. Robinson, I.K. & Harrison, S.C. (1982). Structure of the expanded state of tomato bushy stunt virus. Nature 297, 563-568.
48. Lonberg-Holm, K. & Korant, B.D. (1972). Early interaction of rhinoviruses with host cells. J. Virol. 9, 29-40.
49. Everaert, L., Vrijsen, R. & Boeyé, A. (1989). Eclipse products of poliovirus after cold-synchronized infection of HeLa cells. Virology 171, 76-82.
50. Nugent, C.I. & Kirkegaard, K. (1995). RNA binding properties of poliovirus subviral particles. J. Virol. 69, 13-22.
51. Kunkel, T.A. (1987). Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154, 367-382.
52. Rossmann, M.G. (1979). Processing oscillation diffraction data for very large unit cells with an automatic convolution technique and profile fitting. J. Appl. Cryst. 12, 225-238.
53. Rossmann, M.G., Leslie, A.G.W., Abdel-Meguid, S.S. & Tsukihara, T. (1979). Processing and post-refinement of oscillation camera data. J. Appl. Cryst. 12, 570-581.
54. Otwinowski, Z. (1993). Oscillation data reduction program. In Proceedings of the CCP4 Study Weekend: Data Collection and Processing. (Sawyer, L., Isaacs, N. & Bailey, S., eds), pp. 59-62, SERC Daresbury Laboratory, Warrington, UK.
55. Muckelbauer, J.K., et al., & Rossmann. M.G. (1995). Structure determination of coxsackievirus B3 to 3.5 Å resolution. Acta Cryst. D 51, 871-887.
56. Cornea-Hasegan, M.A., et al., & Rossmann. M.G. (1995). Phase refinement and extension by means of non-crystallographic symmetry averaging using parallel computers. Acta Cryst. D51, 749-759.
57. Arnold, E. & Rossmann, M.G. (1988). The use of molecular-replacement phases for the refinement of the human rhinovirus 14 structure. Acta Cryst. A 44, 270-282.
58. Jones, T.A., Zou, J.-Y., Cowan, S.W. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron-density maps and the location of errors in these models. Acta Cryst. A 47, 110-119.
59. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. (1993). PROCHECK: a program to check the stereochemistry quality of protein structures. J. Appl. Cryst. 26, 283-291.
60. Brünger, A.T. (1992). X-PLOR, Version 3.1 Manual: A System for X-ray Crystallography and NMR. Yale University Press, New Haven.
61. Weis, W.I., Brünger, A.T., Skehel, J.J. & Wiley, D.C. (1990). Refining influenza virus haemagglutinin. J. Mol. Biol. 212, 737-761.
62. Engh, R.A. & Huber, R. (1991). Accurate bond and angle parameters for X-ray protein structure refinement. Acta Cryst. A 47, 392-400.
63. Brooks, B.R., Bruccoleri, R.E., Olafson, B.D., States, D.J., Swaminathan, S. & Karplus, M. (1983). CHARMm: a program for macromolecular energy, minimization and dynamics calculations. J. Comput. Chem. 4, 187-217.
64. Kraulis, P. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 24, 946-950.