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. 1990 May;64(5):1934–1945. doi: 10.1128/jvi.64.5.1934-1945.1990

Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding.

C E Fricks 1, J M Hogle 1
PMCID: PMC249347  PMID: 2157861

Abstract

Upon attachment to susceptible cells, poliovirus and a number of other picornaviruses undergo conformational transitions which result in changes in antigenicity, increased protease sensitivity, the loss of the internal capsid protein VP4, and a loss of the ability to attach to cells. These conformationally altered particles have been characterized by using a number of sequence-specific probes, including two proteases, a panel of antiviral monoclonal antibodies, and a panel of antisera against synthetic peptides which correspond to sequences from the capsid protein VP1. With these probes, cell-altered virus is clearly distinguishable from native and heat-inactivated virions. The probes also demonstrate that the cell-induced conformational change alters the accessibility of several regions of the virus. In particular, the amino terminus of VP1, which is entirely internal in the native virion, becomes externalized. Unlike native and heat-inactivated virus, cell-altered virions are able to attach to liposomes. The exposed amino terminus of VP1 is shown to be responsible for liposome attachment. We propose that during infection the amino terminus of VP1 inserts into endosomal membranes and thus plays a role in the mechanism of cell entry.

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Selected References

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  1. Acharya R., Fry E., Stuart D., Fox G., Rowlands D., Brown F. The three-dimensional structure of foot-and-mouth disease virus at 2.9 A resolution. Nature. 1989 Feb 23;337(6209):709–716. doi: 10.1038/337709a0. [DOI] [PubMed] [Google Scholar]
  2. Caliguiri L. A., McSharry J. J., Lawrence G. W. Effect of arildone on modifications of poliovirus in vitro. Virology. 1980 Aug;105(1):86–93. doi: 10.1016/0042-6822(80)90158-0. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Chow M., Yabrov R., Bittle J., Hogle J., Baltimore D. Synthetic peptides from four separate regions of the poliovirus type 1 capsid protein VP1 induce neutralizing antibodies. Proc Natl Acad Sci U S A. 1985 Feb;82(3):910–914. doi: 10.1073/pnas.82.3.910. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Crowell R. L., Landau B. J., Philipson L. The early interaction of coxsackievirus B3 with HeLa cells. Proc Soc Exp Biol Med. 1971 Jul;137(3):1082–1088. doi: 10.3181/00379727-137-35732. [DOI] [PubMed] [Google Scholar]
  6. Crowell R. L., Philipson L. Specific alterations of coxsackievirus B3 eluted from HeLa cells. J Virol. 1971 Oct;8(4):509–515. doi: 10.1128/jvi.8.4.509-515.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. De Sena J., Mandel B. Studies on the in vitro uncoating of poliovirus. I. Characterization of the modifying factor and the modifying reaction. Virology. 1976 Apr;70(2):470–483. doi: 10.1016/0042-6822(76)90288-9. [DOI] [PubMed] [Google Scholar]
  8. De Sena J., Mandel B. Studies on the in vitro uncoating of poliovirus. II. Characteristics of the membrane-modified particle. Virology. 1977 May 15;78(2):554–566. doi: 10.1016/0042-6822(77)90130-1. [DOI] [PubMed] [Google Scholar]
  9. Doms R. W., Helenius A., White J. Membrane fusion activity of the influenza virus hemagglutinin. The low pH-induced conformational change. J Biol Chem. 1985 Mar 10;260(5):2973–2981. [PubMed] [Google Scholar]
  10. Everaert L., Vrijsen R., Boeyé A. Eclipse products of poliovirus after cold-synchronized infection of HeLa cells. Virology. 1989 Jul;171(1):76–82. doi: 10.1016/0042-6822(89)90512-6. [DOI] [PubMed] [Google Scholar]
  11. FENWICK M. L., COOPER P. D. Early interactions between poliovirus and ERK cells: some observations on the nature and significance of the rejected particles. Virology. 1962 Oct;18:212–223. doi: 10.1016/0042-6822(62)90007-7. [DOI] [PubMed] [Google Scholar]
  12. Fenwick M. L., Wall M. J. Factors determining the site of synthesis of poliovirus proteins: the early attachment of virus particles to endoplasmic membranes. J Cell Sci. 1973 Sep;13(2):403–413. doi: 10.1242/jcs.13.2.403. [DOI] [PubMed] [Google Scholar]
  13. Filman D. J., Syed R., Chow M., Macadam A. J., Minor P. D., Hogle J. M. Structural factors that control conformational transitions and serotype specificity in type 3 poliovirus. EMBO J. 1989 May;8(5):1567–1579. doi: 10.1002/j.1460-2075.1989.tb03541.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fox M. P., Otto M. J., McKinlay M. A. Prevention of rhinovirus and poliovirus uncoating by WIN 51711, a new antiviral drug. Antimicrob Agents Chemother. 1986 Jul;30(1):110–116. doi: 10.1128/aac.30.1.110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fricks C. E., Icenogle J. P., Hogle J. M. Trypsin sensitivity of the Sabin strain of type 1 poliovirus: cleavage sites in virions and related particles. J Virol. 1985 Jun;54(3):856–859. doi: 10.1128/jvi.54.3.856-859.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Greve J. M., Davis G., Meyer A. M., Forte C. P., Yost S. C., Marlor C. W., Kamarck M. E., McClelland A. The major human rhinovirus receptor is ICAM-1. Cell. 1989 Mar 10;56(5):839–847. doi: 10.1016/0092-8674(89)90688-0. [DOI] [PubMed] [Google Scholar]
  17. Guttman N., Baltimore D. A plasma membrane component able to bind and alter virions of poliovirus type 1: studies on cell-free alteration using a simplified assay. Virology. 1977 Oct 1;82(1):25–36. doi: 10.1016/0042-6822(77)90029-0. [DOI] [PubMed] [Google Scholar]
  18. HOLLAND J. J., HOYER B. H. Early stages of enterovirus infection. Cold Spring Harb Symp Quant Biol. 1962;27:101–112. doi: 10.1101/sqb.1962.027.001.013. [DOI] [PubMed] [Google Scholar]
  19. HOLLAND J. J. Receptor affinities as major determinants of enterovirus tissue tropisms in humans. Virology. 1961 Nov;15:312–326. doi: 10.1016/0042-6822(61)90363-4. [DOI] [PubMed] [Google Scholar]
  20. Hall L., Rueckert R. R. Infection of mouse fibroblasts by cardioviruses: premature uncoating and its prevention by elevated pH and magnesium chloride. Virology. 1971 Jan;43(1):152–165. doi: 10.1016/0042-6822(71)90233-9. [DOI] [PubMed] [Google Scholar]
  21. Helenius A., Kartenbeck J., Simons K., Fries E. On the entry of Semliki forest virus into BHK-21 cells. J Cell Biol. 1980 Feb;84(2):404–420. doi: 10.1083/jcb.84.2.404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hogle J. M., Chow M., Filman D. J. Three-dimensional structure of poliovirus at 2.9 A resolution. Science. 1985 Sep 27;229(4720):1358–1365. doi: 10.1126/science.2994218. [DOI] [PubMed] [Google Scholar]
  23. Hogle J., Kirchhausen T., Harrison S. C. Divalent cation sites in tomato bushy stunt virus. Difference maps at 2-9 A resolution. J Mol Biol. 1983 Nov 25;171(1):95–100. doi: 10.1016/s0022-2836(83)80315-5. [DOI] [PubMed] [Google Scholar]
  24. INCARDONA N. L., KAESBERG P. A PH-INDUCED STRUCTURAL CHANGE IN BROMEGRASS MOSAIC VIRUS. Biophys J. 1964 Jan;4:11–21. doi: 10.1016/s0006-3495(64)86766-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. JOKLIK W. K., DARNELL J. E., Jr The adsorption and early fate of purified poliovirus in HeLa cells. Virology. 1961 Apr;13:439–447. doi: 10.1016/0042-6822(61)90275-6. [DOI] [PubMed] [Google Scholar]
  26. Kew O. M., Pallansch M. A., Omilianowski D. R., Rueckert R. R. Changes in three of the four coat proteins of oral polio vaccine strain derived from type 1 poliovirus. J Virol. 1980 Jan;33(1):256–263. doi: 10.1128/jvi.33.1.256-263.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kirkegaard K. Mutations in VP1 of poliovirus specifically affect both encapsidation and release of viral RNA. J Virol. 1990 Jan;64(1):195–206. doi: 10.1128/jvi.64.1.195-206.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Kitamura N., Semler B. L., Rothberg P. G., Larsen G. R., Adler C. J., Dorner A. J., Emini E. A., Hanecak R., Lee J. J., van der Werf S. Primary structure, gene organization and polypeptide expression of poliovirus RNA. Nature. 1981 Jun 18;291(5816):547–553. doi: 10.1038/291547a0. [DOI] [PubMed] [Google Scholar]
  29. Krüse J., Krüse K. M., Witz J., Chauvin C., Jacrot B., Tardieu A. Divalent ion-dependent reversible swelling of tomato bushy stunt virus and organization of the expanded virion. J Mol Biol. 1982 Dec 5;162(2):393–414. doi: 10.1016/0022-2836(82)90534-4. [DOI] [PubMed] [Google Scholar]
  30. Lonberg-Holm K., Gosser L. B., Kauer J. C. Early alteration of poliovirus in infected cells and its specific inhibition. J Gen Virol. 1975 Jun;27(3):329–342. doi: 10.1099/0022-1317-27-3-329. [DOI] [PubMed] [Google Scholar]
  31. Lonberg-Holm K., Gosser L. B., Shimshick E. J. Interaction of liposomes with subviral particles of poliovirus type 2 and rhinovirus type 2. J Virol. 1976 Aug;19(2):746–749. doi: 10.1128/jvi.19.2.746-749.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lonberg-Holm K., Korant B. D. Early interaction of rhinoviruses with host cells. J Virol. 1972 Jan;9(1):29–40. doi: 10.1128/jvi.9.1.29-40.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Luo M., Vriend G., Kamer G., Minor I., Arnold E., Rossmann M. G., Boege U., Scraba D. G., Duke G. M., Palmenberg A. C. The atomic structure of Mengo virus at 3.0 A resolution. Science. 1987 Jan 9;235(4785):182–191. doi: 10.1126/science.3026048. [DOI] [PubMed] [Google Scholar]
  34. Madshus I. H., Olsnes S., Sandvig K. Requirements for entry of poliovirus RNA into cells at low pH. EMBO J. 1984 Sep;3(9):1945–1950. doi: 10.1002/j.1460-2075.1984.tb02074.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. McSharry J. J., Caliguiri L. A., Eggers H. J. Inhibition of uncoating of poliovirus by arildone, a new antiviral drug. Virology. 1979 Sep;97(2):307–315. doi: 10.1016/0042-6822(79)90342-8. [DOI] [PubMed] [Google Scholar]
  36. Mendelsohn C. L., Wimmer E., Racaniello V. R. Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily. Cell. 1989 Mar 10;56(5):855–865. doi: 10.1016/0092-8674(89)90690-9. [DOI] [PubMed] [Google Scholar]
  37. Minor P. D., Dunn G., Evans D. M., Magrath D. I., John A., Howlett J., Phillips A., Westrop G., Wareham K., Almond J. W. The temperature sensitivity of the Sabin type 3 vaccine strain of poliovirus: molecular and structural effects of a mutation in the capsid protein VP3. J Gen Virol. 1989 May;70(Pt 5):1117–1123. doi: 10.1099/0022-1317-70-5-1117. [DOI] [PubMed] [Google Scholar]
  38. Niman H. L., Houghten R. A., Walker L. E., Reisfeld R. A., Wilson I. A., Hogle J. M., Lerner R. A. Generation of protein-reactive antibodies by short peptides is an event of high frequency: implications for the structural basis of immune recognition. Proc Natl Acad Sci U S A. 1983 Aug;80(16):4949–4953. doi: 10.1073/pnas.80.16.4949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Noble J., Lonberg-Holm K. Interactions of components of human rhinovirus type 2 with Hela cells. Virology. 1973 Feb;51(2):270–278. doi: 10.1016/0042-6822(73)90427-3. [DOI] [PubMed] [Google Scholar]
  40. Nomoto A., Omata T., Toyoda H., Kuge S., Horie H., Kataoka Y., Genba Y., Nakano Y., Imura N. Complete nucleotide sequence of the attenuated poliovirus Sabin 1 strain genome. Proc Natl Acad Sci U S A. 1982 Oct;79(19):5793–5797. doi: 10.1073/pnas.79.19.5793. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Page G. S., Mosser A. G., Hogle J. M., Filman D. J., Rueckert R. R., Chow M. Three-dimensional structure of poliovirus serotype 1 neutralizing determinants. J Virol. 1988 May;62(5):1781–1794. doi: 10.1128/jvi.62.5.1781-1794.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Racaniello V. R., Baltimore D. Molecular cloning of poliovirus cDNA and determination of the complete nucleotide sequence of the viral genome. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4887–4891. doi: 10.1073/pnas.78.8.4887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Rossmann M. G., Arnold E., Erickson J. W., Frankenberger E. A., Griffith J. P., Hecht H. J., Johnson J. E., Kamer G., Luo M., Mosser A. G. Structure of a human common cold virus and functional relationship to other picornaviruses. Nature. 1985 Sep 12;317(6033):145–153. doi: 10.1038/317145a0. [DOI] [PubMed] [Google Scholar]
  44. Rueckert R. R., Pallansch M. A. Preparation and characterization of encephalomyocarditis (EMC) virus. Methods Enzymol. 1981;78(Pt A):315–325. [PubMed] [Google Scholar]
  45. Skehel J. J., Bayley P. M., Brown E. B., Martin S. R., Waterfield M. D., White J. M., Wilson I. A., Wiley D. C. Changes in the conformation of influenza virus hemagglutinin at the pH optimum of virus-mediated membrane fusion. Proc Natl Acad Sci U S A. 1982 Feb;79(4):968–972. doi: 10.1073/pnas.79.4.968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Staunton D. E., Merluzzi V. J., Rothlein R., Barton R., Marlin S. D., Springer T. A. A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses. Cell. 1989 Mar 10;56(5):849–853. doi: 10.1016/0092-8674(89)90689-2. [DOI] [PubMed] [Google Scholar]
  47. Talbot P., Brown F. A model for foot-and-mouth disease virus. J Gen Virol. 1972 May;15(2):163–169. doi: 10.1099/0022-1317-15-2-163. [DOI] [PubMed] [Google Scholar]
  48. Tomassini J. E., Graham D., DeWitt C. M., Lineberger D. W., Rodkey J. A., Colonno R. J. cDNA cloning reveals that the major group rhinovirus receptor on HeLa cells is intercellular adhesion molecule 1. Proc Natl Acad Sci U S A. 1989 Jul;86(13):4907–4911. doi: 10.1073/pnas.86.13.4907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. White J. M., Wilson I. A. Anti-peptide antibodies detect steps in a protein conformational change: low-pH activation of the influenza virus hemagglutinin. J Cell Biol. 1987 Dec;105(6 Pt 2):2887–2896. doi: 10.1083/jcb.105.6.2887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. White J., Helenius A. pH-dependent fusion between the Semliki Forest virus membrane and liposomes. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3273–3277. doi: 10.1073/pnas.77.6.3273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Wilson I. A., Skehel J. J., Wiley D. C. Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature. 1981 Jan 29;289(5796):366–373. doi: 10.1038/289366a0. [DOI] [PubMed] [Google Scholar]
  52. Wray W., Boulikas T., Wray V. P., Hancock R. Silver staining of proteins in polyacrylamide gels. Anal Biochem. 1981 Nov 15;118(1):197–203. doi: 10.1016/0003-2697(81)90179-2. [DOI] [PubMed] [Google Scholar]
  53. Wychowski C., van der Werf S., Siffert O., Crainic R., Bruneau P., Girard M. A poliovirus type 1 neutralization epitope is located within amino acid residues 93 to 104 of viral capsid polypeptide VP1. EMBO J. 1983;2(11):2019–2024. doi: 10.1002/j.1460-2075.1983.tb01694.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. van der Werf S., Wychowski C., Bruneau P., Blondel B., Crainic R., Horodniceanu F., Girard M. Localization of a poliovirus type 1 neutralization epitope in viral capsid polypeptide VP1. Proc Natl Acad Sci U S A. 1983 Aug;80(16):5080–5084. doi: 10.1073/pnas.80.16.5080. [DOI] [PMC free article] [PubMed] [Google Scholar]

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