Structure of the herpesvirus major capsid protein

EMBO Journal

Volumn 22, Issue 4, 2003, Pages 757-765

  Bowman, Brian R ^a   Baker, Matthew L ^a   Rixon, Frazer J ^b   Chiu, Wah ^a   Quiocho, Florante A ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b INSTITUTE OF VIROLOGY   (United Kingdom)

Author keywords

Assembly; Capsid protein; Crystal structure; Folding nucleus; Herpesviruses

Indexed keywords

CAPSID PROTEIN; PROTEIN SUBUNIT; PROTEIN VP5; UNCLASSIFIED DRUG;

ARTICLE; BINDING KINETICS; CELL NUCLEUS; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; ELECTRICITY; HERPES SIMPLEX VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; VIRION;

CAPSID PROTEINS; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; HERPESVIRUS 1, HUMAN; PROTEIN STRUCTURE, TERTIARY;

DNA VIRUSES; HERPESVIRIDAE; HUMAN HERPESVIRUS 1; SIMPLEXVIRUS;

EID: 0037450631     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg086     Document Type: Article

References (49)

1. Batterson, W., Furlong, D. and Roizman, B. (1983) Molecular genetics of herpes simplex virus. VIII. Further characterization of a temperature-sensitive mutant defective in release of viral DNA and in other stages of the viral reproductive cycle. J. Virol., 45, 397-407.
2. Benson, S.D., Bamford, J.K., Bamford, D.H. and Burnett, R.M. (1999) Viral evolution revealed by bacteriophages PRD1 and human adenovirus coat protein structures. Cell, 98, 825-833.
3. Böttcher, B., Wynne, S.A. and Crowther, R.A. (1997) Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature, 386, 88-91.
4. Brünger, A.T. et al. (1998) Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D, 54, 905-921.
5. Carson, M. (1997) Ribbons. Methods Enzymol., 277, 493-505.
6. Caspar, D.L. and Klug, A. (1962) Physical principles in the construction of regular viruses. Cold Spring Harbor Symp. Quant. Biol., 48, 1-24.
7. Cepko, C.L. and Sharp, P.A. (1983) Analysis of Ad5 hexon and 100K ts mutants using conformation-specific monoclonal antibodies. Virology, 129, 137-154.
8. Chen, D.H., Jakana, J., McNab, D., Mitchell, J., Zhou, Z.H., Dougherty, M., Chiu, W. and Rixon, F.J. (2001) The pattern of tegument - capsid interaction in the herpes simplex virus type 1 virion is not influenced by the small hexon-associated protein VP26. J. Virol., 75, 11863-11867.
9. Conway, J.F., Cheng, N., Zlotnick, A., Wingfield, P.T., Stahl, S.J. and Steven, A.C. (1997) Visualization of a 4-helix bundle in the hepatitis B virus capsid by cryo-electron microscopy. Nature, 386, 91-94.
10. Coulter, L.J., Moss, H.W., Lang, J. and McGeoch, D.J. (1993) A mutant of herpes simplex virus type 1 in which the UL13 protein kinase gene is disrupted. J. Gen. Virol., 74, 387-395.
11. Desai, P.J. (2000) A null mutation in the UL36 gene of herpes simplex virus type 1 results in accumulation of unveloped DNA-filled capsids in the cytoplasm of infected cells. J. Virol., 74, 11608-11618.
12. Dokland, T., McKenna, R., Ilag, L.L., Bowman, B.R., Incardona, N.L., Fane, B.A. and Rossmann, M.G. (1997) Structure of a viral procapsid with molecular scaffolding. Nature, 389, 308-313.
13. Fenwick, M.L. and Everett, R.D. (1990) Inactivation of the shutoff gene (UL41) of herpes simplex virus types 1 and 2. J. Gen. Virol., 71, 2961-2967.
14. Grimes, J.M., Burroughs, J.N., Gouet, P., Diprose, J.M., Malby, R., Zientara, S., Mertens, P.P. and Stuart, D.I. (1998) The atomic structure of the bluetongue virus core. Nature, 395, 470-478.
15. Harrison, S.C., Skehel, J.J. and Wiley, D.C. (1996) Virus structure. In Fields, B.N., Knipe, D.M., Howley, P.M., Chanock, R.M., Melnick, J.L., Monath, T.P., Roizman, B. and Strauss, S.E. (eds), Field's Virology. Lippincott-Raven, Philadelphia, PA, pp. 59-99.
16. Holm, L. and Sander, C. (1995) Dali: a network tool for protein structure comparison. Trends Biochem. Sci., 20, 478-480.
17. Jiang, W., Baker, M.L., Ludtke, S.J. and Chiu, W. (2001) Bridging the information gap: computational tools for intermediate resolution structure interpretation. J. Mol. Biol., 308, 1033-1044.
18. Jones, T.A., Zou, J.Y., Cowan, S.W. and Kjeldgaard, M. (1991) Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A, 47, 110-119.
19. Knipe, D.M., Batterson, W., Nosal, C., Roizman, B. and Buchan A. (1981) Molecular genetics of herpes simplex virus. VI. Characterization of a temperature-sensitive mutant defective in the expression of all early viral gene products. J. Virol., 38, 539-547.
20. Kraulis, P. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr., 24, 946-950.
21. Lemaster, S. and Roizman, B. (1980) Herpes simplex virus phosphoproteins. II. Characterization of the virion protein kinase and of the polypeptides phosphorylated in the virion. J. Virol., 35, 798-811.
22. Ludtke, S.J., Baldwin, P.R. and Chiu, W. (1999) EMAN: semiautomated software for high resolution single-particle reconstructions. J. Struct. Biol., 128, 82-97.
23. Merritt, E.A. and Bacon, D.J. (1997) Raster3D version 2.0: a program for photorealistic molecular graphics. Methods Enzymol., 277, 505-524.
24. Newcomb, W.W. and Brown, J.C. (1991) Structure of the herpes simplex virus capsid: effects of extraction with guanidine hydrochloride and partial reconstitution of extracted capsids. J. Virol., 65, 613-620.
25. Newcomb, W.W. and Brown, J.C. (1994) Induced extrusion of DNA from the capsid of herpes simplex virus type 1. J. Virol., 68, 433-440.
26. Newcomb, W.W., Homa F.L., Thomsen, D.R., Booy, F.P., Trus, B.L., Steven, A.C., Spencer, J.V. and Brown, J.C. (1996) Assembly of the herpes simplex virus capsid: characterization of intermediates observed during cell-free capsid formation. J. Mol. Biol., 263, 432-446.
27. Newcomb, W.W., Homa, F.L., Thomsen D.R., Trus B.L., Cheng, N., Steven, A.C., Booy F.P. and Brown, J.C. (1999) Assembly of the herpes simplex virus procapsid from purified components and identification of small complexes of the major capsid and scaffolding proteins. J. Virol., 73, 4239-4350.
28. Newcomb, W.W., Juhas, R.M., Thomsen, D.R., Homa, F.L., Burch, A.D., Weller, S.K. and Brown, J.C. (2001) The UL6 gene product forms the portal for entry of DNA into the herpes simplex virus capsid. J. Virol., 75, 10923-10932.
29. Nicholls, A., Bharadwaj, R. and Honig, B. (1993) GRASP: graphical representation and analysis of surface properties. Biophys. J., 64, 166-170.
30. Ojala, P.M., Sodeik, B., Ebersold, M.W., Kutay, U. and Helenius, A. (2000) Herpes simplex virus type 1 entry into host cells: reconstitution of capsid binding and uncoating at the nuclear pore complex in vitro. Mol. Cell Biol., 20, 4922-4931.
31. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol., 276, 307-326.
32. Pflugrath, J.W. (1999) The finer things in X-ray diffraction data collection. Acta Crystallogr. D, 55, 1718-1725.
33. Post, L.E., Mackem, S. and Roizman, B. (1981) Regulation of α genes of herpes simplex virus: expression of chimeric genes produced by fusion of thymidine kinase with α gene promoters. Cell, 24, 555-565.
34. Reinisch, K.M., Nibert, M.L. and Harrison, S.C. (2000) Structure of the reovirus core at 3.6 A resolution. Nature, 404, 960-967.
35. Roberts, M.M., White, J.L., Grutter, M.G. and Burnett, R.M. (1986) Three dimensional structure of the adenovirus major coat protein hexon. Science, 232, 1148-1151.
36. Roizman, B.N. and Sears, A.E. (1996) Herpes simplex viruses and their replication. In Fields, B.N., Knipe, D.M., Howley, P.M., Chanock, R.M., Melnick, J.L., Monath, T.P., Roizman, B. and Strauss, S.E. (eds), Field's Virology. Lippincott-Raven, Philadelphia, PA, pp. 2231-2295.
37. Rossmann, M.G. and Johnson, J.E. (1989) Icosahedral RNA virus structure. Annu. Rev. Biochem., 58, 533-573.
38. Sharp, P.M. (2002) Origins of human virus diversity. Cell, 108, 305-312.
39. Spencer, J.V., Trus, B.L., Booy, F.P., Steven, A.C., Newcomb, W.W. and Brown, J.C. (1997) Structure of the herpes simplex virus capsid: peptide A862-H880 of the major capsid protein is displayed on the rim of the capsomer protrusions. Virology, 228, 229-235.
40. Spencer, J.V., Newcomb, W.W., Thomsen, D.R., Homa, F.L. and Brown, J.C. (1998) Assembly of the herpes simplex virus capsid: preformed triplexes bind to the nascent capsid. J. Virol., 72, 3944-3951.
41. Stehle, T., Gamblin, S.J., Yan, Y. and Harrison S.C. (1996) The structure of simian virus 40 refined at 3.1 Å. Structure, 4, 165-182.
42. Steven, A.C. and Spear, P.G. (1997) Herpesvirus capsid assembly and envelopment. In Chiu, W., Burnett, R.M. and Garcea, R.L. (eds), Structural Biology of Viruses. Oxford University Press, New York, NY, pp. 312-351.
43. Trus, B.L., Booy, F.P., Newcomb, W.W., Brown, J.C., Homa, F.L., Thomsen, D.R. and Steven, A.C. (1996) The herpes simplex virus procapsid: structure, conformational changes upon maturation and roles of the triplex proteins VP19c and VP23 in assembly. J. Mol. Biol., 263, 447-462.
44. Wikoff, W.R., Liljas, L., Duda, R.L., Tsuruta, H., Hendrix, R.H. and Johnson, J.E. (2000) Topologically linked rings in the bacteriophage HK97 capsid. Science, 289, 2129-2133.
45. Wingfield, P.T., Stahl, S.J., Thomsen, D.R., Homa, F.L., Booy, F.P. Trus, B.L. and Steven, A.C. (1997) Hexon-only binding of VP26 reflects differences between the hexon and penton conformations of VP5, the major capsid protein from herpes simplex virus. J. Virol., 71, 8955-8961.
46. Zhang, Y. and McKnight, J.L. (1993) Herpes simplex virus type 1 UL46 and UL47 deletion mutants lack VP11 and VP12 or VP13 and VP14, respectively and exhibit altered viral thymidine kinase expression. J. Virol., 67, 1482-1492.
47. Zhou, Z.H., He, J., Jakana, J., Tatman, J.D., Rixon, F.J. and Chiu, W. (1995) Assembly of VP26 in herpes simplex virus-1 inferred from structures of wild-type and recombinant capsids. Nat. Struct. Biol., 2, 1026-1030.
48. Zhou, Z.H., Chen D.H., Jakana, J., Rixon, F.J. and Chiu, W. (1999) Visualization of tegument - capsid interactions and DNA in intact herpes simplex virus type 1 virions. J. Virol., 73, 3210-3218.
49. Zhou, Z.H., Dougherty, M., Jakana, J., He, J., Rixon, F.J. and Chiu, W. (2000) Seeing the herpesvirus capsid at 8.5 Å. Science, 288, 877-880.