Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1992 Jun;66(6):3415–3423. doi: 10.1128/jvi.66.6.3415-3423.1992

Two amino acid substitutions within the capsid are coordinately required for acquisition of fibrotropism by the lymphotropic strain of minute virus of mice.

L J Ball-Goodrich 1, P Tattersall 1
PMCID: PMC241122  PMID: 1316457

Abstract

Nucleotide changes at both codons 317 and 321 in the VP2 capsid gene of the immunosuppressive strain of the murine parvovirus minute virus of mice, MVM(i), are required to create a virus capable of growing in A9 fibroblasts. This double mutant virus, ILB1, has growth characteristics very similar to those of the prototype fibrotropic strain MVM(p) in both single- and multiple-round infections of fibroblasts and is about 100-fold better at infecting fibroblasts than MVM(i). When only one nucleotide position is changed, either in codon 317 (as in ILB2) or in codon 321 (as in ILB3), the resulting viruses are less than twice as efficient as their parent MVM(i) at infecting fibroblasts. In the restrictive infection of A9 cells by the single mutants and MVM(i), gene expression and DNA replication were markedly reduced compared with ILB1 infection of the same cells or compared with infections of permissive hybrid cells by each of the viruses. This suggests that restriction acts predominantly at an early step in the infection. Since the phenotypes of ILB2 and ILB3 are essentially indistinguishable in restrictive infections, it is most likely that the individual loci affect the same step in the viral life cycle. The dramatic increase in fibroblast infectivity shown by ILB1 indicates a synergistic interaction between these two amino acid residues in the same rate-limiting process in fibroblast infection.

Full text

PDF
3415

Images in this article

3419Image
on p.3419
3420Image
on p.3420
3420Image
on p.3420
3421Image
on p.3421

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. Astell C. R., Gardiner E. M., Tattersall P. DNA sequence of the lymphotropic variant of minute virus of mice, MVM(i), and comparison with the DNA sequence of the fibrotropic prototype strain. J Virol. 1986 Feb;57(2):656–669. doi: 10.1128/jvi.57.2.656-669.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Astell C. R., Thomson M., Merchlinsky M., Ward D. C. The complete DNA sequence of minute virus of mice, an autonomous parvovirus. Nucleic Acids Res. 1983 Feb 25;11(4):999–1018. doi: 10.1093/nar/11.4.999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Brownstein D. G., Smith A. L., Jacoby R. O., Johnson E. A., Hansen G., Tattersall P. Pathogenesis of infection with a virulent allotropic variant of minute virus of mice and regulation by host genotype. Lab Invest. 1991 Sep;65(3):357–364. [PubMed] [Google Scholar]
  6. Cann A. J., Zack J. A., Go A. S., Arrigo S. J., Koyanagi Y., Green P. L., Koyanagi Y., Pang S., Chen I. S. Human immunodeficiency virus type 1 T-cell tropism is determined by events prior to provirus formation. J Virol. 1990 Oct;64(10):4735–4742. doi: 10.1128/jvi.64.10.4735-4742.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cotmore S. F., Tattersall P. Alternate splicing in a parvoviral nonstructural gene links a common amino-terminal sequence to downstream domains which confer radically different localization and turnover characteristics. Virology. 1990 Aug;177(2):477–487. doi: 10.1016/0042-6822(90)90512-p. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Engers H. D., Louis J. A., Zubler R. H., Hirt B. Inhibition of T cell-mediated functions by MVM(i), a parvovirus closely related to minute virus of mice. J Immunol. 1981 Dec;127(6):2280–2285. [PubMed] [Google Scholar]
  10. 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]
  11. 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]
  12. Kim S., Ikeuchi K., Groopman J., Baltimore D. Factors affecting cellular tropism of human immunodeficiency virus. J Virol. 1990 Nov;64(11):5600–5604. doi: 10.1128/jvi.64.11.5600-5604.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kimsey P. B., Engers H. D., Hirt B., Jongeneel C. V. Pathogenicity of fibroblast- and lymphocyte-specific variants of minute virus of mice. J Virol. 1986 Jul;59(1):8–13. doi: 10.1128/jvi.59.1.8-13.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kunkel T. A., Roberts J. D., Zakour R. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 1987;154:367–382. doi: 10.1016/0076-6879(87)54085-x. [DOI] [PubMed] [Google Scholar]
  15. Miller R. A., Ward D. C., Ruddle F. H. Embryonal carcinoma cells (and their somatic cell hybrids) are resistant to infection by the murine parvovirus MVM, which does infect other teratocarcinoma-derived cell lines. J Cell Physiol. 1977 Jun;91(3):393–401. doi: 10.1002/jcp.1040910309. [DOI] [PubMed] [Google Scholar]
  16. O'Brien W. A., Koyanagi Y., Namazie A., Zhao J. Q., Diagne A., Idler K., Zack J. A., Chen I. S. HIV-1 tropism for mononuclear phagocytes can be determined by regions of gp120 outside the CD4-binding domain. Nature. 1990 Nov 1;348(6296):69–73. doi: 10.1038/348069a0. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. 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]
  20. Pintel D., Dadachanji D., Astell C. R., Ward D. C. The genome of minute virus of mice, an autonomous parvovirus, encodes two overlapping transcription units. Nucleic Acids Res. 1983 Feb 25;11(4):1019–1038. doi: 10.1093/nar/11.4.1019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Segovia J. C., Real A., Bueren J. A., Almendral J. M. In vitro myelosuppressive effects of the parvovirus minute virus of mice (MVMi) on hematopoietic stem and committed progenitor cells. Blood. 1991 Mar 1;77(5):980–988. [PubMed] [Google Scholar]
  22. Shioda T., Levy J. A., Cheng-Mayer C. Macrophage and T cell-line tropisms of HIV-1 are determined by specific regions of the envelope gp120 gene. Nature. 1991 Jan 10;349(6305):167–169. doi: 10.1038/349167a0. [DOI] [PubMed] [Google Scholar]
  23. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Srivastava K. K., Fernandez-Larsson R., Zinkus D. M., Robinson H. L. Human immunodeficiency virus type 1 NL4-3 replication in four T-cell lines: rate and efficiency of entry, a major determinant of permissiveness. J Virol. 1991 Jul;65(7):3900–3902. doi: 10.1128/jvi.65.7.3900-3902.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Takeuchi Y., Akutsu M., Murayama K., Shimizu N., Hoshino H. Host range mutant of human immunodeficiency virus type 1: modification of cell tropism by a single point mutation at the neutralization epitope in the env gene. J Virol. 1991 Apr;65(4):1710–1718. doi: 10.1128/jvi.65.4.1710-1718.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Tattersall P. Replication of the parvovirus MVM. I. Dependence of virus multiplication and plaque formation on cell growth. J Virol. 1972 Oct;10(4):586–590. doi: 10.1128/jvi.10.4.586-590.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Yen T. S., Webster R. E. Bacteriophage f1 gene II and X proteins. Isolation and characterization of the products of two overlapping genes. J Biol Chem. 1981 Nov 10;256(21):11259–11265. [PubMed] [Google Scholar]
  31. de la Roche Saint André C., Harper F., Feunteun J. Analysis of the hamster polyomavirus infection in vitro: host-restricted productive cycle. Virology. 1990 Aug;177(2):532–540. doi: 10.1016/0042-6822(90)90518-v. [DOI] [PubMed] [Google Scholar]

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

RESOURCES