1887

Abstract

Porcine parvovirus (PPV) is a small DNA virus with restricted coding capacity. The 5 kb genome expresses three major non-structural proteins (NS1, NS2 and SAT), and two structural proteins (VP1 and VP2). These few viral proteins are pleiotropic and interact with cellular components throughout viral replication. In this regard, very few cell lines have been shown to replicate the virus efficiently. Cell lines were established from a primary culture of bovine cells that allowed allotropic variants of PPV to be distinguished. Three cell lines were differentially sensitive to infection by two prototype PPV strains, NADL-2 and Kresse. In the first cell line (D10), infection was restricted early in the infectious cycle and was not productive. Infection of the second cell line (G11) was 1000 times less efficient with the NADL-2 strain compared with porcine cells, while production of infectious virus of the Kresse strain was barely detectable. Restriction points in these cells were the initial generation of DNA replication intermediates and NS1 production. Infection with chimeras between NADL-2 and Kresse showed that residues outside the previously described allotropic determinant were also partially responsible for the restriction to Kresse replication in G11 cells. F4 cells were permissive to both strains, although genome replication and infectious virus production were lower than in the porcine cells used for comparison. These results highlight the dependent nature of parvovirus tropism on host factors and suggest that cells from a non-host origin can fully support a productive infection by both strains.

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2014-04-01
2024-04-20
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References

  1. Anouja F., Wattiez R., Mousset S., Caillet-Fauquet P. 1997; The cytotoxicity of the parvovirus minute virus of mice nonstructural protein NS1 is related to changes in the synthesis and phosphorylation of cell proteins. J Virol 71:4671–4678[PubMed]
    [Google Scholar]
  2. Ball-Goodrich L. J., Tattersall P. 1992; 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 66:3415–3423[PubMed]
    [Google Scholar]
  3. Barrett L. W., Fletcher S., Wilton S. D. 2012; Regulation of eukaryotic gene expression by the untranslated gene regions and other non-coding elements. Cell Mol Life Sci 69:3613–3634 [View Article][PubMed]
    [Google Scholar]
  4. Bashir T., Horlein R., Rommelaere J., Willwand K. 2000; Cyclin A activates the DNA polymerase delta-dependent elongation machinery in vitro: a parvovirus DNA replication model. Proc Natl Acad Sci U S A 97:5522–5527 [View Article][PubMed]
    [Google Scholar]
  5. Bergeron J., Menezes J., Tijssen P. 1993; Genomic organization and mapping of transcription and translation products of the NADL-2 strain of porcine parvovirus. Virology 197:86–98 [View Article][PubMed]
    [Google Scholar]
  6. Bergeron J., Hébert B., Tijssen P. 1996; 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 70:2508–2515[PubMed]
    [Google Scholar]
  7. Boisvert M., Fernandes S., Tijssen P. 2010; Multiple pathways involved in porcine parvovirus cellular entry and trafficking toward the nucleus. J Virol 84:7782–7792 [View Article][PubMed]
    [Google Scholar]
  8. Brandenburger A., Legendre D., Avalosse B., Rommelaere J. 1990; NS-1 and NS-2 proteins may act synergistically in the cytopathogenicity of parvovirus MVMp. Virology 174:576–584 [View Article][PubMed]
    [Google Scholar]
  9. Christensen J., Tattersall P. 2002; Parvovirus initiator protein NS1 and RPA coordinate replication fork progression in a reconstituted DNA replication system. J Virol 76:6518–6531 [View Article][PubMed]
    [Google Scholar]
  10. Cossons N., Faust E. A., Zannis-Hadjopoulos M. 1996; DNA polymerase delta-dependent formation of a hairpin structure at the 5′ terminal palindrome of the minute virus of mice genome. Virology 216:258–264 [View Article][PubMed]
    [Google Scholar]
  11. Cotmore S. F., Tattersall P. 2005; Encapsidation of minute virus of mice DNA: aspects of the translocation mechanism revealed by the structure of partially packaged genomes. Virology 336:100–112 [View Article][PubMed]
    [Google Scholar]
  12. Deleu L., Pujol A., Faisst S., Rommelaere J. 1999; Activation of promoter P4 of the autonomous parvovirus minute virus of mice at early S phase is required for productive infection. J Virol 73:3877–3885[PubMed]
    [Google Scholar]
  13. Eichwald V., Daeffler L., Klein M., Rommelaere J., Salomé N. 2002; The NS2 proteins of parvovirus minute virus of mice are required for efficient nuclear egress of progeny virions in mouse cells. J Virol 76:10307–10319 [View Article][PubMed]
    [Google Scholar]
  14. Engelsma D., Valle N., Fish A., Salomé N., Almendral J. M., Fornerod M. 2008; A supraphysiological nuclear export signal is required for parvovirus nuclear export. Mol Biol Cell 19:2544–2552 [View Article][PubMed]
    [Google Scholar]
  15. Farr G. A., Zhang L. G., Tattersall P. 2005; Parvoviral virions deploy a capsid-tethered lipolytic enzyme to breach the endosomal membrane during cell entry. Proc Natl Acad Sci U S A 102:17148–17153 [View Article][PubMed]
    [Google Scholar]
  16. Fernandes S., Boisvert M., Tijssen P. 2011; Genetic elements in the VP region of porcine parvovirus are critical to replication efficiency in cell culture. J Virol 85:3025–3029 [View Article][PubMed]
    [Google Scholar]
  17. Gardiner E. M., Tattersall P. 1988; Evidence that developmentally regulated control of gene expression by a parvoviral allotropic determinant is particle mediated. J Virol 62:1713–1722[PubMed]
    [Google Scholar]
  18. Hansen J., Qing K., Srivastava A. 2001; Adeno-associated virus type 2-mediated gene transfer: altered endocytic processing enhances transduction efficiency in murine fibroblasts. J Virol 75:4080–4090 [View Article][PubMed]
    [Google Scholar]
  19. Harbison C. E., Chiorini J. A., Parrish C. R. 2008; The parvovirus capsid odyssey: from the cell surface to the nucleus. Trends Microbiol 16:208–214 [View Article][PubMed]
    [Google Scholar]
  20. Hoelzer K., Parrish C. R. 2010; The emergence of parvoviruses of carnivores. Vet Res 41:39 [View Article][PubMed]
    [Google Scholar]
  21. Hoelzer K., Shackelton L. A., Parrish C. R., Holmes E. C. 2008; Phylogenetic analysis reveals the emergence, evolution and dispersal of carnivore parvoviruses. J Gen Virol 89:2280–2289 [View Article][PubMed]
    [Google Scholar]
  22. Jóźwik A., Manteufel J., Selbitz H. J., Truyen U. 2009; Vaccination against porcine parvovirus protects against disease, but does not prevent infection and virus shedding after challenge infection with a heterologous virus strain. J Gen Virol 90:2437–2441 [View Article][PubMed]
    [Google Scholar]
  23. Kang B. Y., You H., Bandyopadhyay S., Agrawal N., Melchert R. B., Basnakian A. G., Liu Y., Hermonat P. L. 2009; Cervical cancer isolate PT3, super-permissive for adeno-associated virus replication, over-expresses DNA polymerase delta, PCNA, RFC and RPA. BMC Microbiol 9:79 [View Article][PubMed]
    [Google Scholar]
  24. Lombardo E., Ramírez J. C., Agbandje-McKenna M., Almendral J. M. 2000; A beta-stranded motif drives capsid protein oligomers of the parvovirus minute virus of mice into the nucleus for viral assembly. J Virol 74:3804–3814 [View Article][PubMed]
    [Google Scholar]
  25. Mani B., Baltzer C., Valle N., Almendral J. M., Kempf C., Ros C. 2006; Low pH-dependent endosomal processing of the incoming parvovirus minute virus of mice virion leads to externalization of the VP1 N-terminal sequence (N-VP1), N-VP2 cleavage, and uncoating of the full-length genome. J Virol 80:1015–1024 [View Article][PubMed]
    [Google Scholar]
  26. Meier O., Greber U. F. 2004; Adenovirus endocytosis. J Gene Med 6:Suppl 1S152–S163 [View Article][PubMed]
    [Google Scholar]
  27. Miller C. L., Pintel D. J. 2002; Interaction between parvovirus NS2 protein and nuclear export factor Crm1 is important for viral egress from the nucleus of murine cells. J Virol 76:3257–3266 [View Article][PubMed]
    [Google Scholar]
  28. Nüesch J. P., Rommelaere J. 2006; NS1 interaction with CKII alpha: novel protein complex mediating parvovirus-induced cytotoxicity. J Virol 80:4729–4739 [View Article][PubMed]
    [Google Scholar]
  29. Nüesch J. P., Bär S., Lachmann S., Rommelaere J. 2009; Ezrin-radixin-moesin family proteins are involved in parvovirus replication and spreading. J Virol 83:5854–5863 [View Article][PubMed]
    [Google Scholar]
  30. Oraveerakul K., Choi C. S., Molitor T. W. 1992; Restriction of porcine parvovirus replication in nonpermissive cells. J Virol 66:715–722[PubMed]
    [Google Scholar]
  31. Parker J. S., Parrish C. R. 2000; Cellular uptake and infection by canine parvovirus involves rapid dynamin-regulated clathrin-mediated endocytosis, followed by slower intracellular trafficking. J Virol 74:1919–1930 [View Article][PubMed]
    [Google Scholar]
  32. Parrish C. R. 2010; Structures and functions of parvovirus capsids and the process of cell infection. Curr Top Microbiol Immunol 343:149–176[PubMed]
    [Google Scholar]
  33. Porwal M., Cohen S., Snoussi K., Popa-Wagner R., Anderson F., Dugot-Senant N., Wodrich H., Dinsart C., Kleinschmidt J. A.other authors 2013; Parvoviruses cause nuclear envelope breakdown by activating key enzymes of mitosis. PLoS Pathog 9:e1003671 [View Article][PubMed]
    [Google Scholar]
  34. Previsani N., Fontana S., Hirt B., Beard P. 1997; Growth of the parvovirus minute virus of mice MVMp3 in EL4 lymphocytes is restricted after cell entry and before viral DNA amplification: cell-specific differences in virus uncoating in vitro. J Virol 71:7769–7780[PubMed]
    [Google Scholar]
  35. Rhode S. L. III 1985; Trans-activation of parvovirus P38 promoter by the 76K noncapsid protein. J Virol 55:886–889[PubMed]
    [Google Scholar]
  36. Rhode S. L. III 1989; Both excision and replication of cloned autonomous parvovirus DNA require the NS1 (rep) protein. J Virol 63:4249–4256[PubMed]
    [Google Scholar]
  37. Ridpath J. F., Mengeling W. L. 1988; Uptake of porcine parvovirus into host and nonhost cells suggests host specificity is determined by intracellular factors. Virus Res 10:17–27 [View Article][PubMed]
    [Google Scholar]
  38. Rodeffer H. E., Leman A. D., Dunne H. W., Cropper M., Sprecher D. J. 1975; Reproductive failure in swine associated with maternal seroconversion for porcine parvovirus. J Am Vet Med Assoc 166:991–992[PubMed]
    [Google Scholar]
  39. Rubio M. P., Guerra S., Almendral J. M. 2001; Genome replication and postencapsidation functions mapping to the nonstructural gene restrict the host range of a murine parvovirus in human cells. J Virol 75:11573–11582 [View Article][PubMed]
    [Google Scholar]
  40. Simpson A. A., Hébert B., Sullivan G. M., Parrish C. R., Zádori Z., Tijssen P., Rossmann M. G. 2002; The structure of porcine parvovirus: comparison with related viruses. J Mol Biol 315:1189–1198 [View Article][PubMed]
    [Google Scholar]
  41. Streck A. F., Bonatto S. L., Homeier T., Souza C. K., Gonçalves K. R., Gava D., Canal C. W., Truyen U. 2011; High rate of viral evolution in the capsid protein of porcine parvovirus. J Gen Virol 92:2628–2636 [View Article][PubMed]
    [Google Scholar]
  42. Tattersall P. 1972; Replication of the parvovirus MVM. I. Dependence of virus multiplication and plaque formation on cell growth. J Virol 10:586–590[PubMed]
    [Google Scholar]
  43. Tattersall P. 2006; The evolution of parvovirus taxonomy. In Parvoviruses pp. 5–14 Edited by Kerr J. R., Cotmore S. F., Bloom M. E., Linden M. R., Parrish C. R. London, UK: Hodder Arnold;
    [Google Scholar]
  44. Tattersall P., Ward D. C. 1976; Rolling hairpin model for replication of parvovirus and linear chromosomal DNA. Nature 263:106–109 [View Article][PubMed]
    [Google Scholar]
  45. Truyen U., Gruenberg A., Chang S. F., Obermaier B., Veijalainen P., Parrish C. R. 1995; Evolution of the feline-subgroup parvoviruses and the control of canine host range in vivo. J Virol 69:4702–4710[PubMed]
    [Google Scholar]
  46. Vasudevacharya J., Compans R. W. 1992; The NS and capsid genes determine the host range of porcine parvovirus. Virology 187:515–524 [View Article][PubMed]
    [Google Scholar]
  47. Weichert W. S., Parker J. S., Wahid A. T., Chang S. F., Meier E., Parrish C. R. 1998; Assaying for structural variation in the parvovirus capsid and its role in infection. Virology 250:106–117 [View Article][PubMed]
    [Google Scholar]
  48. Willwand K., Mumtsidu E., Kuntz-Simon G., Rommelaere J. 1998; Initiation of DNA replication at palindromic telomeres is mediated by a duplex-to-hairpin transition induced by the minute virus of mice nonstructural protein NS1. J Biol Chem 273:1165–1174 [View Article][PubMed]
    [Google Scholar]
  49. Yeung D. E., Brown G. W., Tam P., Russnak R. H., Wilson G., Clark-Lewis I., Astell C. R. 1991; Monoclonal antibodies to the major nonstructural nuclear protein of minute virus of mice. Virology 181:35–45 [View Article][PubMed]
    [Google Scholar]
  50. Zádori Z., Szelei J., Lacoste M. C., Li Y., Gariépy S., Raymond P., Allaire M., Nabi I. R., Tijssen P. 2001; A viral phospholipase A2 is required for parvovirus infectivity. Dev Cell 1:291–302 [View Article][PubMed]
    [Google Scholar]
  51. Zádori Z., Szelei J., Tijssen P. 2005; SAT: a late NS protein of porcine parvovirus. J Virol 79:13129–13138 [View Article][PubMed]
    [Google Scholar]
  52. Zeeuw E. J., Leinecker N., Herwig V., Selbitz H. J., Truyen U. 2007; Study of the virulence and cross-neutralization capability of recent porcine parvovirus field isolates and vaccine viruses in experimentally infected pregnant gilts. J Gen Virol 88:420–427 [View Article][PubMed]
    [Google Scholar]
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