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. 1992 Dec;66(12):6858–6867. doi: 10.1128/jvi.66.12.6858-6867.1992

Multiple amino acids in the capsid structure of canine parvovirus coordinately determine the canine host range and specific antigenic and hemagglutination properties.

S F Chang 1, J Y Sgro 1, C R Parrish 1
PMCID: PMC240290  PMID: 1331498

Abstract

Canine parvovirus (CPV) and feline panleukopenia virus (FPV) are over 98% similar in DNA sequence but have specific host range, antigenic, and hemagglutination (HA) properties which were located within the capsid protein gene. In vitro mutagenesis and recombination were used to prepare 16 different recombinant genomic clones, and viruses derived from those clones were analyzed for their in vitro host range, antigenic, and HA properties. The region of CPV from 59 to 91 map units determined the ability to replicate in canine cells. A complex series of interactions was observed among the individual sequence differences between 59 and 73 map units. The canine host range required that VP2 amino acids (aa) 93 and 323 both be the CPV sequence, and those two CPV sequences introduced alone into FPV greatly increased viral replication in canine cells. Changing any one of aa 93, 103, or 323 of CPV to the FPV sequence either greatly decreased replication in canine cells or resulted in an inviable plasmid. The Asn-Lys difference of aa 93 alone was responsible for the CPV-specific epitope recognized by monoclonal antibodies. An FPV-specific epitope was affected by aa 323. Amino acids 323 and 375 together determined the pH dependence of HA. Amino acids involved in the various specific properties were all around the threefold spikes of the viral particle.

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Selected References

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

  1. Antonietti J. P., Sahli R., Beard P., Hirt B. Characterization of the cell type-specific determinant in the genome of minute virus of mice. J Virol. 1988 Feb;62(2):552–557. doi: 10.1128/jvi.62.2.552-557.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Appel M. J., Scott F. W., Carmichael L. E. Isolation and immunisation studies of a canine parco-like virus from dogs with haemorrhagic enteritis. Vet Rec. 1979 Aug 25;105(8):156–159. doi: 10.1136/vr.105.8.156. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. 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]
  6. Brownstein D. G., Smith A. L., Johnson E. A., Pintel D. J., Naeger L. K., Tattersall P. The pathogenesis of infection with minute virus of mice depends on expression of the small nonstructural protein NS2 and on the genotype of the allotropic determinants VP1 and VP2. J Virol. 1992 May;66(5):3118–3124. doi: 10.1128/jvi.66.5.3118-3124.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Carlson J., Rushlow K., Maxwell I., Maxwell F., Winston S., Hahn W. Cloning and sequence of DNA encoding structural proteins of the autonomous parvovirus feline panleukopenia virus. J Virol. 1985 Sep;55(3):574–582. doi: 10.1128/jvi.55.3.574-582.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Carmichael L. E., Binn L. N. New enteric viruses in the dog. Adv Vet Sci Comp Med. 1981;25:1–37. [PubMed] [Google Scholar]
  9. Carmichael L. E., Joubert J. C., Pollock R. V. Hemagglutination by canine parvovirus: serologic studies and diagnostic applications. Am J Vet Res. 1980 May;41(5):784–791. [PubMed] [Google Scholar]
  10. 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]
  11. 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]
  12. Dubensky T. W., Freund R., Dawe C. J., Benjamin T. L. Polyomavirus replication in mice: influences of VP1 type and route of inoculation. J Virol. 1991 Jan;65(1):342–349. doi: 10.1128/jvi.65.1.342-349.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Freund R., Garcea R. L., Sahli R., Benjamin T. L. A single-amino-acid substitution in polyomavirus VP1 correlates with plaque size and hemagglutination behavior. J Virol. 1991 Jan;65(1):350–355. doi: 10.1128/jvi.65.1.350-355.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Frost E., Williams J. Mapping temperature-sensitive and host-range mutations of adenovirus type 5 by marker rescue. Virology. 1978 Nov;91(1):39–50. doi: 10.1016/0042-6822(78)90353-7. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Graham F. L., van der Eb A. J. A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology. 1973 Apr;52(2):456–467. doi: 10.1016/0042-6822(73)90341-3. [DOI] [PubMed] [Google Scholar]
  17. Hattori M., Sakaki Y. Dideoxy sequencing method using denatured plasmid templates. Anal Biochem. 1986 Feb 1;152(2):232–238. doi: 10.1016/0003-2697(86)90403-3. [DOI] [PubMed] [Google Scholar]
  18. Hirt B. Selective extraction of polyoma DNA from infected mouse cell cultures. J Mol Biol. 1967 Jun 14;26(2):365–369. doi: 10.1016/0022-2836(67)90307-5. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. Lemon S. M., Binn L. N., Marchwicki R. H. Radioimmunofocus assay for quantitation of hepatitis A virus in cell cultures. J Clin Microbiol. 1983 May;17(5):834–839. doi: 10.1128/jcm.17.5.834-839.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Martin A., Benichou D., Couderc T., Hogle J. M., Wychowski C., Van der Werf S., Girard M. Use of type 1/type 2 chimeric polioviruses to study determinants of poliovirus type 1 neurovirulence in a mouse model. Virology. 1991 Feb;180(2):648–658. doi: 10.1016/0042-6822(91)90078-p. [DOI] [PubMed] [Google Scholar]
  23. Martyn J. C., Davidson B. E., Studdert M. J. Nucleotide sequence of feline panleukopenia virus: comparison with canine parvovirus identifies host-specific differences. J Gen Virol. 1990 Nov;71(Pt 11):2747–2753. doi: 10.1099/0022-1317-71-11-2747. [DOI] [PubMed] [Google Scholar]
  24. McMaster G. K., Beard P., Engers H. D., Hirt B. Characterization of an immunosuppressive parvovirus related to the minute virus of mice. J Virol. 1981 Apr;38(1):317–326. doi: 10.1128/jvi.38.1.317-326.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Oraveerakul K., Choi C. S., Molitor T. W. Restriction of porcine parvovirus replication in nonpermissive cells. J Virol. 1992 Feb;66(2):715–722. doi: 10.1128/jvi.66.2.715-722.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Parrish C. R., Aquadro C. F., Carmichael L. E. Canine host range and a specific epitope map along with variant sequences in the capsid protein gene of canine parvovirus and related feline, mink, and raccoon parvoviruses. Virology. 1988 Oct;166(2):293–307. doi: 10.1016/0042-6822(88)90500-4. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Parrish C. R., Burtonboy G., Carmichael L. E. Characterization of a nonhemagglutinating mutant of canine parvovirus. Virology. 1988 Mar;163(1):230–232. doi: 10.1016/0042-6822(88)90255-3. [DOI] [PubMed] [Google Scholar]
  29. Parrish C. R., Carmichael L. E., Antczak D. F. Antigenic relationships between canine parvovirus type 2, feline panleukopenia virus and mink enteritis virus using conventional antisera and monoclonal antibodies. Arch Virol. 1982;72(4):267–278. doi: 10.1007/BF01315223. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. 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]
  33. 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]
  34. 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]
  35. Reed A. P., Jones E. V., Miller T. J. Nucleotide sequence and genome organization of canine parvovirus. J Virol. 1988 Jan;62(1):266–276. doi: 10.1128/jvi.62.1.266-276.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Rhode S. L., 3rd Nucleotide sequence of the coat protein gene of canine parvovirus. J Virol. 1985 May;54(2):630–633. doi: 10.1128/jvi.54.2.630-633.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Ridpath J. F., Mengeling W. L. Uptake of porcine parvovirus into host and nonhost cells suggests host specificity is determined by intracellular factors. Virus Res. 1988 Apr;10(1):17–27. doi: 10.1016/0168-1702(88)90054-8. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Senda M., Hirayama N., Itoh O., Yamamoto H. Canine parvovirus: strain difference in haemagglutination activity and antigenicity. J Gen Virol. 1988 Feb;69(Pt 2):349–354. doi: 10.1099/0022-1317-69-2-349. [DOI] [PubMed] [Google Scholar]
  41. Siegl G., Bates R. C., Berns K. I., Carter B. J., Kelly D. C., Kurstak E., Tattersall P. Characteristics and taxonomy of Parvoviridae. Intervirology. 1985;23(2):61–73. doi: 10.1159/000149587. [DOI] [PubMed] [Google Scholar]
  42. 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]
  43. Tattersall P., Bratton J. Reciprocal productive and restrictive virus-cell interactions of immunosuppressive and prototype strains of minute virus of mice. J Virol. 1983 Jun;46(3):944–955. doi: 10.1128/jvi.46.3.944-955.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. 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]
  45. 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]
  46. Tsao J., Chapman M. S., Wu H., Agbandje M., Keller W., Rossmann M. G. Structure determination of monoclinic canine parvovirus. Acta Crystallogr B. 1992 Feb 1;48(Pt 1):75–88. doi: 10.1107/s0108768191009539. [DOI] [PubMed] [Google Scholar]
  47. 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]
  48. Veijalainen P. Characterization of biological and antigenic properties of raccoon dog and blue fox parvoviruses: a monoclonal antibody study. Vet Microbiol. 1988 Mar;16(3):219–230. doi: 10.1016/0378-1135(88)90026-0. [DOI] [PubMed] [Google Scholar]
  49. Yeates T. O., Jacobson D. H., Martin A., Wychowski C., Girard M., Filman D. J., Hogle J. M. Three-dimensional structure of a mouse-adapted type 2/type 1 poliovirus chimera. EMBO J. 1991 Sep;10(9):2331–2341. doi: 10.1002/j.1460-2075.1991.tb07772.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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