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. 1997 Dec;71(12):9214–9222. doi: 10.1128/jvi.71.12.9214-9222.1997

Canine parvovirus host range is determined by the specific conformation of an additional region of the capsid.

J S Parker 1, C R Parrish 1
PMCID: PMC230224  PMID: 9371580

Abstract

We analyzed a region of the capsid of canine parvovirus (CPV) which determines the ability of the virus to infect canine cells. This region is distinct from those previously shown to determine the canine host range differences between CPV and feline panleukopenia virus. It lies on a ridge of the threefold spike of the capsid and is comprised of five interacting loops from three capsid protein monomers. We analyzed 12 mutants of CPV which contained amino acid changes in two adjacent loops exposed on the surface of this region. Nine mutants infected and grew in feline cells but were restricted in replication in one or the other of two canine cell lines tested. Three other mutants whose genomes contain mutations which affect one probable interchain bond were nonviable and could not be propagated in either canine or feline cells, although the VP1 and VP2 proteins from those mutants produced empty capsids when expressed from a plasmid vector. Although wild-type and mutant capsids bound to canine and feline cells in similar amounts, infection or viral DNA replication was greatly reduced after inoculation of canine cells with most of the mutants. The viral genomes of two host range-restricted mutants and two nonviable mutants replicated to wild-type levels in both feline and canine cells upon transfection with plasmid clones. The capsids of wild-type CPV and two mutants were similar in susceptibility to heat inactivation, but one of those mutants and one other were more stable against urea denaturation. Most mutations in this structural region altered the ability of monoclonal antibodies to recognize epitopes within a major neutralizing antigenic site, and that site could be subdivided into a number of distinct epitopes. These results argue that a specific structure of this region is required for CPV to retain its canine host range.

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Selected References

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  1. Ball-Goodrich L. J., Moir R. D., Tattersall P. Parvoviral target cell specificity: acquisition of fibrotropism by a mutant of the lymphotropic strain of minute virus of mice involves multiple amino acid substitutions within the capsid. Virology. 1991 Sep;184(1):175–186. doi: 10.1016/0042-6822(91)90834-x. [DOI] [PubMed] [Google Scholar]
  2. Ball-Goodrich L. J., Tattersall P. Two amino acid substitutions within the capsid are coordinately required for acquisition of fibrotropism by the lymphotropic strain of minute virus of mice. J Virol. 1992 Jun;66(6):3415–3423. doi: 10.1128/jvi.66.6.3415-3423.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barbis D. P., Chang S. F., Parrish C. R. Mutations adjacent to the dimple of the canine parvovirus capsid structure affect sialic acid binding. Virology. 1992 Nov;191(1):301–308. doi: 10.1016/0042-6822(92)90192-r. [DOI] [PubMed] [Google Scholar]
  4. Basak S., Turner H. Infectious entry pathway for canine parvovirus. Virology. 1992 Feb;186(2):368–376. doi: 10.1016/0042-6822(92)90002-7. [DOI] [PubMed] [Google Scholar]
  5. Bergeron J., Hébert B., Tijssen P. Genome organization of the Kresse strain of porcine parvovirus: identification of the allotropic determinant and comparison with those of NADL-2 and field isolates. J Virol. 1996 Apr;70(4):2508–2515. doi: 10.1128/jvi.70.4.2508-2515.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Binn L. N., Marchwicki R. H., Stephenson E. H. Establishment of a canine cell line: derivation, characterization, and viral spectrum. Am J Vet Res. 1980 Jun;41(6):855–860. [PubMed] [Google Scholar]
  7. Bloom M. E., Berry B. D., Wei W., Perryman S., Wolfinbarger J. B. Characterization of chimeric full-length molecular clones of Aleutian mink disease parvovirus (ADV): identification of a determinant governing replication of ADV in cell culture. J Virol. 1993 Oct;67(10):5976–5988. doi: 10.1128/jvi.67.10.5976-5988.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chang S. F., Sgro J. Y., Parrish C. R. Multiple amino acids in the capsid structure of canine parvovirus coordinately determine the canine host range and specific antigenic and hemagglutination properties. J Virol. 1992 Dec;66(12):6858–6867. doi: 10.1128/jvi.66.12.6858-6867.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chapman M. S., Rossmann M. G. Structure, sequence, and function correlations among parvoviruses. Virology. 1993 Jun;194(2):491–508. doi: 10.1006/viro.1993.1288. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. 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]
  12. Cotmore S. F., Tattersall P. The autonomously replicating parvoviruses of vertebrates. Adv Virus Res. 1987;33:91–174. doi: 10.1016/s0065-3527(08)60317-6. [DOI] [PubMed] [Google Scholar]
  13. Couderc T., Delpeyroux F., Le Blay H., Blondel B. Mouse adaptation determinants of poliovirus type 1 enhance viral uncoating. J Virol. 1996 Jan;70(1):305–312. doi: 10.1128/jvi.70.1.305-312.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Crandell R. A., Fabricant C. G., Nelson-Rees W. A. Development, characterization, and viral susceptibility of a feline (Felis catus) renal cell line (CRFK). In Vitro. 1973 Nov-Dec;9(3):176–185. doi: 10.1007/BF02618435. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Gardiner E. M., Tattersall P. Evidence that developmentally regulated control of gene expression by a parvoviral allotropic determinant is particle mediated. J Virol. 1988 May;62(5):1713–1722. doi: 10.1128/jvi.62.5.1713-1722.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gardiner E. M., Tattersall P. Mapping of the fibrotropic and lymphotropic host range determinants of the parvovirus minute virus of mice. J Virol. 1988 Aug;62(8):2605–2613. doi: 10.1128/jvi.62.8.2605-2613.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Giranda V. L., Heinz B. A., Oliveira M. A., Minor I., Kim K. H., Kolatkar P. R., Rossmann M. G., Rueckert R. R. Acid-induced structural changes in human rhinovirus 14: possible role in uncoating. Proc Natl Acad Sci U S A. 1992 Nov 1;89(21):10213–10217. doi: 10.1073/pnas.89.21.10213. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Greber U. F., Willetts M., Webster P., Helenius A. Stepwise dismantling of adenovirus 2 during entry into cells. Cell. 1993 Nov 5;75(3):477–486. doi: 10.1016/0092-8674(93)90382-z. [DOI] [PubMed] [Google Scholar]
  21. Horiuchi M., Goto H., Ishiguro N., Shinagawa M. Mapping of determinants of the host range for canine cells in the genome of canine parvovirus using canine parvovirus/mink enteritis virus chimeric viruses. J Gen Virol. 1994 Jun;75(Pt 6):1319–1328. doi: 10.1099/0022-1317-75-6-1319. [DOI] [PubMed] [Google Scholar]
  22. Horiuchi M., Ishiguro N., Goto H., Shinagawa M. Characterization of the stage(s) in the virus replication cycle at which the host-cell specificity of the feline parvovirus subgroup is regulated in canine cells. Virology. 1992 Aug;189(2):600–608. doi: 10.1016/0042-6822(92)90583-b. [DOI] [PubMed] [Google Scholar]
  23. Kim S., Boege U., Krishnaswamy S., Minor I., Smith T. J., Luo M., Scraba D. G., Rossmann M. G. Conformational variability of a picornavirus capsid: pH-dependent structural changes of Mengo virus related to its host receptor attachment site and disassembly. Virology. 1990 Mar;175(1):176–190. doi: 10.1016/0042-6822(90)90198-z. [DOI] [PubMed] [Google Scholar]
  24. Kunkel T. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc Natl Acad Sci U S A. 1985 Jan;82(2):488–492. doi: 10.1073/pnas.82.2.488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Llamas-Saiz A. L., Agbandje-McKenna M., Parker J. S., Wahid A. T., Parrish C. R., Rossmann M. G. Structural analysis of a mutation in canine parvovirus which controls antigenicity and host range. Virology. 1996 Nov 1;225(1):65–71. doi: 10.1006/viro.1996.0575. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. Nichols G. E., Lovejoy J. C., Borgman C. A., Sanders J. M., Young W. W., Jr Isolation and characterization of two types of MDCK epithelial cell clones based on glycosphingolipid pattern. Biochim Biophys Acta. 1986 Jun 16;887(1):1–12. doi: 10.1016/0167-4889(86)90115-1. [DOI] [PubMed] [Google Scholar]
  29. Paradiso P. R., Rhode S. L., 3rd, Singer I. I. Canine parvovirus: a biochemical and ultrastructural characterization. J Gen Virol. 1982 Sep;62(Pt 1):113–125. doi: 10.1099/0022-1317-62-1-113. [DOI] [PubMed] [Google Scholar]
  30. Parrish C. R., Aquadro C. F., Strassheim M. L., Evermann J. F., Sgro J. Y., Mohammed H. O. Rapid antigenic-type replacement and DNA sequence evolution of canine parvovirus. J Virol. 1991 Dec;65(12):6544–6552. doi: 10.1128/jvi.65.12.6544-6552.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Parrish C. R., Carmichael L. E. Antigenic structure and variation of canine parvovirus type-2, feline panleukopenia virus, and mink enteritis virus. Virology. 1983 Sep;129(2):401–414. doi: 10.1016/0042-6822(83)90179-4. [DOI] [PubMed] [Google Scholar]
  32. Parrish C. R., Carmichael L. E. Characterization and recombination mapping of an antigenic and host range mutation of canine parvovirus. Virology. 1986 Jan 15;148(1):121–132. doi: 10.1016/0042-6822(86)90408-3. [DOI] [PubMed] [Google Scholar]
  33. Parrish C. R. Emergence, natural history, and variation of canine, mink, and feline parvoviruses. Adv Virus Res. 1990;38:403–450. doi: 10.1016/S0065-3527(08)60867-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Parrish C. R. Mapping specific functions in the capsid structure of canine parvovirus and feline panleukopenia virus using infectious plasmid clones. Virology. 1991 Jul;183(1):195–205. doi: 10.1016/0042-6822(91)90132-u. [DOI] [PubMed] [Google Scholar]
  35. Parrish C. R., O'Connell P. H., Evermann J. F., Carmichael L. E. Natural variation of canine parvovirus. Science. 1985 Nov 29;230(4729):1046–1048. doi: 10.1126/science.4059921. [DOI] [PubMed] [Google Scholar]
  36. Rossmann M. G., Palmenberg A. C. Conservation of the putative receptor attachment site in picornaviruses. Virology. 1988 Jun;164(2):373–382. doi: 10.1016/0042-6822(88)90550-8. [DOI] [PubMed] [Google Scholar]
  37. Spalholz B. A., Tattersall P. Interaction of minute virus of mice with differentiated cells: strain-dependent target cell specificity is mediated by intracellular factors. J Virol. 1983 Jun;46(3):937–943. doi: 10.1128/jvi.46.3.937-943.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Strassheim M. L., Gruenberg A., Veijalainen P., Sgro J. Y., Parrish C. R. Two dominant neutralizing antigenic determinants of canine parvovirus are found on the threefold spike of the virus capsid. Virology. 1994 Jan;198(1):175–184. doi: 10.1006/viro.1994.1020. [DOI] [PubMed] [Google Scholar]
  39. Tresnan D. B., Southard L., Weichert W., Sgro J. Y., Parrish C. R. Analysis of the cell and erythrocyte binding activities of the dimple and canyon regions of the canine parvovirus capsid. Virology. 1995 Aug 1;211(1):123–132. doi: 10.1006/viro.1995.1385. [DOI] [PubMed] [Google Scholar]
  40. Truyen U., Agbandje M., Parrish C. R. Characterization of the feline host range and a specific epitope of feline panleukopenia virus. Virology. 1994 May 1;200(2):494–503. doi: 10.1006/viro.1994.1212. [DOI] [PubMed] [Google Scholar]
  41. Truyen U., Evermann J. F., Vieler E., Parrish C. R. Evolution of canine parvovirus involved loss and gain of feline host range. Virology. 1996 Jan 15;215(2):186–189. doi: 10.1006/viro.1996.0021. [DOI] [PubMed] [Google Scholar]
  42. Truyen U., Parrish C. R. Canine and feline host ranges of canine parvovirus and feline panleukopenia virus: distinct host cell tropisms of each virus in vitro and in vivo. J Virol. 1992 Sep;66(9):5399–5408. doi: 10.1128/jvi.66.9.5399-5408.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Tsao J., Chapman M. S., Agbandje M., Keller W., Smith K., Wu H., Luo M., Smith T. J., Rossmann M. G., Compans R. W. The three-dimensional structure of canine parvovirus and its functional implications. Science. 1991 Mar 22;251(5000):1456–1464. doi: 10.1126/science.2006420. [DOI] [PubMed] [Google Scholar]
  44. Tullis G. E., Labieniec-Pintel L., Clemens K. E., Pintel D. Generation and characterization of a temperature-sensitive mutation in the NS-1 gene of the autonomous parvovirus minute virus of mice. J Virol. 1988 Aug;62(8):2736–2744. doi: 10.1128/jvi.62.8.2736-2744.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Vasudevacharya J., Compans R. W. The NS and capsid genes determine the host range of porcine parvovirus. Virology. 1992 Apr;187(2):515–524. doi: 10.1016/0042-6822(92)90454-w. [DOI] [PubMed] [Google Scholar]
  46. Wikoff W. R., Wang G., Parrish C. R., Cheng R. H., Strassheim M. L., Baker T. S., Rossmann M. G. The structure of a neutralized virus: canine parvovirus complexed with neutralizing antibody fragment. Structure. 1994 Jul 15;2(7):595–607. doi: 10.1016/s0969-2126(00)00062-9. [DOI] [PMC free article] [PubMed] [Google Scholar]

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