Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1996 Jan;70(1):305–312. doi: 10.1128/jvi.70.1.305-312.1996

Mouse adaptation determinants of poliovirus type 1 enhance viral uncoating.

T Couderc 1, F Delpeyroux 1, H Le Blay 1, B Blondel 1
PMCID: PMC189818  PMID: 8523541

Abstract

Most poliovirus (PV) strains, such as PV type 1/Mahoney, cannot infect the mouse central nervous system. We previously identified two determinants of mouse adaptation of PV type 1/Mahoney at positions 22 and 31 of the viral capsid proteins VP1 and VP2, respectively (T. Couderc, J. Hogle, H. Le Blay, F. Horaud, and B. Blondel, J. Virol. 67:3808-3817, 1993). These residues are located on the interior surface of the capsid. In an attempt to understand the molecular mechanisms of adaptation of PV to mice, we investigated the effects of these two determinants on the viral multiplication cycle in a human cell line. Both determinants enhanced receptor-mediated conformational changes leading to altered particles of 135S, one of the first steps of uncoating, and viral internalization. Furthermore, the residue at position 22 of VP1 appears to facilitate RNA release. These results strongly suggest that these determinants could also facilitate conformational changes mediated by the PV murine receptor and internalization in the mouse nerve cell, thus allowing PV to overcome its host range restriction. Moreover, both mouse adaptation determinants are responsible for defects in the assembly of virions in human cells and affect the thermostability of the viral particles. Thus, these mouse adaptation determinants appear to control the balance between the viral capsid plasticity needed for the conformational changes in the early steps of infection and the structural requirements which are involved in the assembly and the stability of virions.

Full Text

The Full Text of this article is available as a PDF (286.7 KB).

Selected References

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

  1. Barnert R. H., Zeichhardt H., Habermehl K. O. Identification of 50- and 23-/25-kDa HeLa cell membrane glycoproteins involved in poliovirus infection: occurrence of poliovirus specific binding sites on susceptible and nonsusceptible cells. Virology. 1992 Feb;186(2):533–542. doi: 10.1016/0042-6822(92)90019-l. [DOI] [PubMed] [Google Scholar]
  2. Blondel B., Akacem O., Crainic R., Couillin P., Horodniceanu F. Detection by monoclonal antibodies of an antigenic determinant critical for poliovirus neutralization present on VP1 and on heat-inactivated virions. Virology. 1983 Apr 30;126(2):707–710. doi: 10.1016/s0042-6822(83)80027-0. [DOI] [PubMed] [Google Scholar]
  3. Blondel B., Crainic R., Fichot O., Dufraisse G., Candrea A., Diamond D., Girard M., Horaud F. Mutations conferring resistance to neutralization with monoclonal antibodies in type 1 poliovirus can be located outside or inside the antibody-binding site. J Virol. 1986 Jan;57(1):81–90. doi: 10.1128/jvi.57.1.81-90.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Colonno R. J., Condra J. H., Mizutani S., Callahan P. L., Davies M. E., Murcko M. A. Evidence for the direct involvement of the rhinovirus canyon in receptor binding. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5449–5453. doi: 10.1073/pnas.85.15.5449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Colston E. M., Racaniello V. R. Poliovirus variants selected on mutant receptor-expressing cells identify capsid residues that expand receptor recognition. J Virol. 1995 Aug;69(8):4823–4829. doi: 10.1128/jvi.69.8.4823-4829.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Colston E., Racaniello V. R. Soluble receptor-resistant poliovirus mutants identify surface and internal capsid residues that control interaction with the cell receptor. EMBO J. 1994 Dec 15;13(24):5855–5862. doi: 10.1002/j.1460-2075.1994.tb06930.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Couderc T., Barzu T., Horaud F., Crainic R. Poliovirus permissivity and specific receptor expression on human endothelial cells. Virology. 1990 Jan;174(1):95–102. doi: 10.1016/0042-6822(90)90058-y. [DOI] [PubMed] [Google Scholar]
  8. Couderc T., Guédo N., Calvez V., Pelletier I., Hogle J., Colbère-Garapin F., Blondel B. Substitutions in the capsids of poliovirus mutants selected in human neuroblastoma cells confer on the Mahoney type 1 strain a phenotype neurovirulent in mice. J Virol. 1994 Dec;68(12):8386–8391. doi: 10.1128/jvi.68.12.8386-8391.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Couderc T., Hogle J., Le Blay H., Horaud F., Blondel B. Molecular characterization of mouse-virulent poliovirus type 1 Mahoney mutants: involvement of residues of polypeptides VP1 and VP2 located on the inner surface of the capsid protein shell. J Virol. 1993 Jul;67(7):3808–3817. doi: 10.1128/jvi.67.7.3808-3817.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dietzschold B., Wiktor T. J., Trojanowski J. Q., Macfarlan R. I., Wunner W. H., Torres-Anjel M. J., Koprowski H. Differences in cell-to-cell spread of pathogenic and apathogenic rabies virus in vivo and in vitro. J Virol. 1985 Oct;56(1):12–18. doi: 10.1128/jvi.56.1.12-18.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. 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]
  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. Fricks C. E., Hogle J. M. Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding. J Virol. 1990 May;64(5):1934–1945. doi: 10.1128/jvi.64.5.1934-1945.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gómez Yafal A., Kaplan G., Racaniello V. R., Hogle J. M. Characterization of poliovirus conformational alteration mediated by soluble cell receptors. Virology. 1993 Nov;197(1):501–505. doi: 10.1006/viro.1993.1621. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. 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]
  18. 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]
  19. Kaplan G., Freistadt M. S., Racaniello V. R. Neutralization of poliovirus by cell receptors expressed in insect cells. J Virol. 1990 Oct;64(10):4697–4702. doi: 10.1128/jvi.64.10.4697-4702.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Koike S., Horie H., Ise I., Okitsu A., Yoshida M., Iizuka N., Takeuchi K., Takegami T., Nomoto A. The poliovirus receptor protein is produced both as membrane-bound and secreted forms. EMBO J. 1990 Oct;9(10):3217–3224. doi: 10.1002/j.1460-2075.1990.tb07520.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Koike S., Taya C., Kurata T., Abe S., Ise I., Yonekawa H., Nomoto A. Transgenic mice susceptible to poliovirus. Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):951–955. doi: 10.1073/pnas.88.3.951. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. 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]
  25. Lu H. H., Yang C. F., Murdin A. D., Klein M. H., Harber J. J., Kew O. M., Wimmer E. Mouse neurovirulence determinants of poliovirus type 1 strain LS-a map to the coding regions of capsid protein VP1 and proteinase 2Apro. J Virol. 1994 Nov;68(11):7507–7515. doi: 10.1128/jvi.68.11.7507-7515.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Martin A., Wychowski C., Couderc T., Crainic R., Hogle J., Girard M. Engineering a poliovirus type 2 antigenic site on a type 1 capsid results in a chimaeric virus which is neurovirulent for mice. EMBO J. 1988 Sep;7(9):2839–2847. doi: 10.1002/j.1460-2075.1988.tb03140.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Mason P. W., Baxt B., Brown F., Harber J., Murdin A., Wimmer E. Antibody-complexed foot-and-mouth disease virus, but not poliovirus, can infect normally insusceptible cells via the Fc receptor. Virology. 1993 Feb;192(2):568–577. doi: 10.1006/viro.1993.1073. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Mendelsohn C., Johnson B., Lionetti K. A., Nobis P., Wimmer E., Racaniello V. R. Transformation of a human poliovirus receptor gene into mouse cells. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7845–7849. doi: 10.1073/pnas.83.20.7845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Morrison M. E., Racaniello V. R. Molecular cloning and expression of a murine homolog of the human poliovirus receptor gene. J Virol. 1992 May;66(5):2807–2813. doi: 10.1128/jvi.66.5.2807-2813.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Moscufo N., Yafal A. G., Rogove A., Hogle J., Chow M. A mutation in VP4 defines a new step in the late stages of cell entry by poliovirus. J Virol. 1993 Aug;67(8):5075–5078. doi: 10.1128/jvi.67.8.5075-5078.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Moss E. G., Racaniello V. R. Host range determinants located on the interior of the poliovirus capsid. EMBO J. 1991 May;10(5):1067–1074. doi: 10.1002/j.1460-2075.1991.tb08046.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Mosser A. G., Rueckert R. R. WIN 51711-dependent mutants of poliovirus type 3: evidence that virions decay after release from cells unless drug is present. J Virol. 1993 Mar;67(3):1246–1254. doi: 10.1128/jvi.67.3.1246-1254.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Mosser A. G., Sgro J. Y., Rueckert R. R. Distribution of drug resistance mutations in type 3 poliovirus identifies three regions involved in uncoating functions. J Virol. 1994 Dec;68(12):8193–8201. doi: 10.1128/jvi.68.12.8193-8201.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Murray M. G., Bradley J., Yang X. F., Wimmer E., Moss E. G., Racaniello V. R. Poliovirus host range is determined by a short amino acid sequence in neutralization antigenic site I. Science. 1988 Jul 8;241(4862):213–215. doi: 10.1126/science.2838906. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Olson N. H., Kolatkar P. R., Oliveira M. A., Cheng R. H., Greve J. M., McClelland A., Baker T. S., Rossmann M. G. Structure of a human rhinovirus complexed with its receptor molecule. Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):507–511. doi: 10.1073/pnas.90.2.507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Ren R. B., Costantini F., Gorgacz E. J., Lee J. J., Racaniello V. R. Transgenic mice expressing a human poliovirus receptor: a new model for poliomyelitis. Cell. 1990 Oct 19;63(2):353–362. doi: 10.1016/0092-8674(90)90168-e. [DOI] [PubMed] [Google Scholar]
  38. Shepley M. P., Racaniello V. R. A monoclonal antibody that blocks poliovirus attachment recognizes the lymphocyte homing receptor CD44. J Virol. 1994 Mar;68(3):1301–1308. doi: 10.1128/jvi.68.3.1301-1308.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES