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. 1998 Jun 15;17(12):3233–3240. doi: 10.1093/emboj/17.12.3233

Interaction of polyomavirus internal protein VP2 with the major capsid protein VP1 and implications for participation of VP2 in viral entry.

X S Chen 1, T Stehle 1, S C Harrison 1
PMCID: PMC1170661  PMID: 9628860

Abstract

A complex of the polyomavirus internal protein VP2/VP3 with the pentameric major capsid protein VP1 has been prepared by co-expression in Escherichia coli. A C-terminal segment of VP2/VP3 is required for tight association, and a crystal structure of this segment, complexed with a VP1 pentamer, has been determined at 2.2 A resolution. The structure shows specific contacts between a single copy of the internal protein and a pentamer of VP1. These interactions were not detected in the previously described structure of the virion, but the location of VP2 in the recombinant complex is consistent with features in the virion electron-density map. The C-terminus of VP2/VP3 inserts in an unusual, hairpin-like manner into the axial cavity of the VP1 pentamer, where it is anchored strongly by hydrophobic interactions. The remainder of the internal protein appears to have significant flexibility. This structure restricts possible models for exposure of the internal proteins during viral entry.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Barouch D. H., Harrison S. C. Interactions among the major and minor coat proteins of polyomavirus. J Virol. 1994 Jun;68(6):3982–3989. doi: 10.1128/jvi.68.6.3982-3989.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bolen J. B., Anders D. G., Trempy J., Consigli R. A. Differences in the subpopulations of the structural proteins of polyoma virions and capsids: biological functions of the multiple VP1 species. J Virol. 1981 Jan;37(1):80–91. doi: 10.1128/jvi.37.1.80-91.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bolen J. B., Consigli R. A. Differential adsorption of polyoma virions and capsids to mouse kidney cells and guinea pig erythrocytes. J Virol. 1979 Nov;32(2):679–683. doi: 10.1128/jvi.32.2.679-683.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brady J. N., Winston V. D., Consigli R. A. Dissociation of polyoma virus by the chelation of calcium ions found associated with purified virions. J Virol. 1977 Sep;23(3):717–724. doi: 10.1128/jvi.23.3.717-724.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chow M., Newman J. F., Filman D., Hogle J. M., Rowlands D. J., Brown F. Myristylation of picornavirus capsid protein VP4 and its structural significance. Nature. 1987 Jun 11;327(6122):482–486. doi: 10.1038/327482a0. [DOI] [PubMed] [Google Scholar]
  6. Clark B., Desselberger U. Myristylation of rotavirus proteins. J Gen Virol. 1988 Oct;69(Pt 10):2681–2686. doi: 10.1099/0022-1317-69-10-2681. [DOI] [PubMed] [Google Scholar]
  7. Delos S. E., Montross L., Moreland R. B., Garcea R. L. Expression of the polyomavirus VP2 and VP3 proteins in insect cells: coexpression with the major capsid protein VP1 alters VP2/VP3 subcellular localization. Virology. 1993 May;194(1):393–398. doi: 10.1006/viro.1993.1274. [DOI] [PubMed] [Google Scholar]
  8. Forstová J., Krauzewicz N., Wallace S., Street A. J., Dilworth S. M., Beard S., Griffin B. E. Cooperation of structural proteins during late events in the life cycle of polyomavirus. J Virol. 1993 Mar;67(3):1405–1413. doi: 10.1128/jvi.67.3.1405-1413.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Garcea R. L., Ballmer-Hofer K., Benjamin T. L. Virion assembly defect of polyomavirus hr-t mutants: underphosphorylation of major capsid protein VP1 before viral DNA encapsidation. J Virol. 1985 May;54(2):311–316. doi: 10.1128/jvi.54.2.311-316.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Garcea R. L., Benjamin T. L. Host range transforming gene of polyoma virus plays a role in virus assembly. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3613–3617. doi: 10.1073/pnas.80.12.3613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Griffith J. P., Griffith D. L., Rayment I., Murakami W. T., Caspar D. L. Inside polyomavirus at 25-A resolution. Nature. 1992 Feb 13;355(6361):652–654. doi: 10.1038/355652a0. [DOI] [PubMed] [Google Scholar]
  12. Kartenbeck J., Stukenbrok H., Helenius A. Endocytosis of simian virus 40 into the endoplasmic reticulum. J Cell Biol. 1989 Dec;109(6 Pt 1):2721–2729. doi: 10.1083/jcb.109.6.2721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Liddington R. C., Yan Y., Moulai J., Sahli R., Benjamin T. L., Harrison S. C. Structure of simian virus 40 at 3.8-A resolution. Nature. 1991 Nov 28;354(6351):278–284. doi: 10.1038/354278a0. [DOI] [PubMed] [Google Scholar]
  14. Merritt E. A., Sarfaty S., van den Akker F., L'Hoir C., Martial J. A., Hol W. G. Crystal structure of cholera toxin B-pentamer bound to receptor GM1 pentasaccharide. Protein Sci. 1994 Feb;3(2):166–175. doi: 10.1002/pro.5560030202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Montross L., Watkins S., Moreland R. B., Mamon H., Caspar D. L., Garcea R. L. Nuclear assembly of polyomavirus capsids in insect cells expressing the major capsid protein VP1. J Virol. 1991 Sep;65(9):4991–4998. doi: 10.1128/jvi.65.9.4991-4998.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Moreland R. B., Garcea R. L. Characterization of a nuclear localization sequence in the polyomavirus capsid protein VP1. Virology. 1991 Nov;185(1):513–518. doi: 10.1016/0042-6822(91)90811-o. [DOI] [PubMed] [Google Scholar]
  17. Moscufo N., Simons J., Chow M. Myristoylation is important at multiple stages in poliovirus assembly. J Virol. 1991 May;65(5):2372–2380. doi: 10.1128/jvi.65.5.2372-2380.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ponder B. A., Robbins A. K., Crawford L. V. Phophorylation of polyoma and SV40 virus proteins. J Gen Virol. 1977 Oct;37(1):75–83. doi: 10.1099/0022-1317-37-1-75. [DOI] [PubMed] [Google Scholar]
  19. Rayment I., Baker T. S., Caspar D. L., Murakami W. T. Polyoma virus capsid structure at 22.5 A resolution. Nature. 1982 Jan 14;295(5845):110–115. doi: 10.1038/295110a0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sahli R., Freund R., Dubensky T., Garcea R., Bronson R., Benjamin T. Defect in entry and altered pathogenicity of a polyoma virus mutant blocked in VP2 myristylation. Virology. 1993 Jan;192(1):142–153. doi: 10.1006/viro.1993.1016. [DOI] [PubMed] [Google Scholar]
  21. Sixma T. K., Pronk S. E., Kalk K. H., Wartna E. S., van Zanten B. A., Witholt B., Hol W. G. Crystal structure of a cholera toxin-related heat-labile enterotoxin from E. coli. Nature. 1991 May 30;351(6325):371–377. doi: 10.1038/351371a0. [DOI] [PubMed] [Google Scholar]
  22. Sixma T. K., Pronk S. E., Kalk K. H., van Zanten B. A., Berghuis A. M., Hol W. G. Lactose binding to heat-labile enterotoxin revealed by X-ray crystallography. Nature. 1992 Feb 6;355(6360):561–564. doi: 10.1038/355561a0. [DOI] [PubMed] [Google Scholar]
  23. Stehle T., Harrison S. C. Crystal structures of murine polyomavirus in complex with straight-chain and branched-chain sialyloligosaccharide receptor fragments. Structure. 1996 Feb 15;4(2):183–194. doi: 10.1016/s0969-2126(96)00021-4. [DOI] [PubMed] [Google Scholar]
  24. Stehle T., Harrison S. C. High-resolution structure of a polyomavirus VP1-oligosaccharide complex: implications for assembly and receptor binding. EMBO J. 1997 Aug 15;16(16):5139–5148. doi: 10.1093/emboj/16.16.5139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Stehle T., Yan Y., Benjamin T. L., Harrison S. C. Structure of murine polyomavirus complexed with an oligosaccharide receptor fragment. Nature. 1994 May 12;369(6476):160–163. doi: 10.1038/369160a0. [DOI] [PubMed] [Google Scholar]
  26. Streuli C. H., Griffin B. E. Myristic acid is coupled to a structural protein of polyoma virus and SV40. Nature. 1987 Apr 9;326(6113):619–622. doi: 10.1038/326619a0. [DOI] [PubMed] [Google Scholar]
  27. Wychowski C., Benichou D., Girard M. The intranuclear location of simian virus 40 polypeptides VP2 and VP3 depends on a specific amino acid sequence. J Virol. 1987 Dec;61(12):3862–3869. doi: 10.1128/jvi.61.12.3862-3869.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]

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