Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1990 Jan;64(1):387–396. doi: 10.1128/jvi.64.1.387-396.1990

Nonstructural protein of parvoviruses B19 and minute virus of mice controls transcription.

C Doerig 1, B Hirt 1, J P Antonietti 1, P Beard 1
PMCID: PMC249113  PMID: 2293668

Abstract

The genome of the human parvovirus B19 contains a transcriptional promoter (BP06) at map position 6, upstream from the nonstructural protein genes. By cotransfecting HeLa cells with this promoter cloned before the chloramphenicol acetyltransferase (CAT) gene together with a plasmid containing almost the whole B19 genome, we showed that BP06 is transactivated by a B19 gene product. The transactivating viral protein was identified as the nonstructural protein NS-1. NS-1 synthesized in a wheat germ extract specifically stimulates transcription from BP06 in vitro. NS-1 of the minute virus of mice (MVM) activates the analogous MVM promoter, MP04. NS-1, therefore, has a positive feedback effect on the activity of its own promoter. Moreover, NS-1 of MVM activates the human BP06. We have identified, in the genome of B19, a second transcriptional promoter activity at map position 44, before the capsid protein genes. This promoter, BP44, was identified by cloning fragments of B19 DNA upstream of the CAT gene, transfecting the DNA into HeLa cells, and measuring CAT expression. The strength of the BP44 promoter is similar to that of the capsid gene promoter, MP39, of MVM. In (nonpermissive) HeLa cells, the BP44 promoter is not activated by NS-1. Thus, the BP06 promoter apparently does not determine the tissue specificity of B19 virus but BP44 could do so.

Full text

PDF
387

Images in this article

390Image
on p.390
391Image
on p.391
392Image
on p.392
393Image
on p.393
393Image
on p.393

Selected References

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

  1. Anderson M. J., Jones S. E., Fisher-Hoch S. P., Lewis E., Hall S. M., Bartlett C. L., Cohen B. J., Mortimer P. P., Pereira M. S. Human parvovirus, the cause of erythema infectiosum (fifth disease)? Lancet. 1983 Jun 18;1(8338):1378–1378. doi: 10.1016/s0140-6736(83)92152-9. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. 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]
  5. Blundell M. C., Beard C., Astell C. R. In vitro identification of a B19 parvovirus promoter. Virology. 1987 Apr;157(2):534–538. doi: 10.1016/0042-6822(87)90296-0. [DOI] [PubMed] [Google Scholar]
  6. Bodnar J. W. Sequence organization in regulatory regions of DNA of minute virus of mice. Virus Genes. 1989 Mar;2(2):167–182. doi: 10.1007/BF00315260. [DOI] [PubMed] [Google Scholar]
  7. Clemens K. E., Pintel D. J. The two transcription units of the autonomous parvovirus minute virus of mice are transcribed in a temporal order. J Virol. 1988 Apr;62(4):1448–1451. doi: 10.1128/jvi.62.4.1448-1451.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cossart Y. E., Field A. M., Cant B., Widdows D. Parvovirus-like particles in human sera. Lancet. 1975 Jan 11;1(7898):72–73. doi: 10.1016/s0140-6736(75)91074-0. [DOI] [PubMed] [Google Scholar]
  9. Cotmore S. F., McKie V. C., Anderson L. J., Astell C. R., Tattersall P. Identification of the major structural and nonstructural proteins encoded by human parvovirus B19 and mapping of their genes by procaryotic expression of isolated genomic fragments. J Virol. 1986 Nov;60(2):548–557. doi: 10.1128/jvi.60.2.548-557.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cotmore S. F., Tattersall P. Characterization and molecular cloning of a human parvovirus genome. Science. 1984 Dec 7;226(4679):1161–1165. doi: 10.1126/science.6095448. [DOI] [PubMed] [Google Scholar]
  11. Cotmore S. F., Tattersall P. Organization of nonstructural genes of the autonomous parvovirus minute virus of mice. J Virol. 1986 Jun;58(3):724–732. doi: 10.1128/jvi.58.3.724-732.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cotmore S. F., Tattersall P. The NS-1 polypeptide of minute virus of mice is covalently attached to the 5' termini of duplex replicative-form DNA and progeny single strands. J Virol. 1988 Mar;62(3):851–860. doi: 10.1128/jvi.62.3.851-860.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dente L., Cesareni G., Cortese R. pEMBL: a new family of single stranded plasmids. Nucleic Acids Res. 1983 Mar 25;11(6):1645–1655. doi: 10.1093/nar/11.6.1645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dignam J. D., Lebovitz R. M., Roeder R. G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983 Mar 11;11(5):1475–1489. doi: 10.1093/nar/11.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Doerig C., Beard P., Hirt B. A transcriptional promoter of the human parvovirus B19 active in vitro and in vivo. Virology. 1987 Apr;157(2):539–542. doi: 10.1016/0042-6822(87)90297-2. [DOI] [PubMed] [Google Scholar]
  16. Doerig C., Hirt B., Beard P., Antonietti J. P. Minute virus of mice non-structural protein NS-1 is necessary and sufficient for trans-activation of the viral P39 promoter. J Gen Virol. 1988 Oct;69(Pt 10):2563–2573. doi: 10.1099/0022-1317-69-10-2563. [DOI] [PubMed] [Google Scholar]
  17. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Hope I. A., Struhl K. GCN4 protein, synthesized in vitro, binds HIS3 regulatory sequences: implications for general control of amino acid biosynthetic genes in yeast. Cell. 1985 Nov;43(1):177–188. doi: 10.1016/0092-8674(85)90022-4. [DOI] [PubMed] [Google Scholar]
  20. Jongeneel C. V., Sahli R., McMaster G. K., Hirt B. A precise map of splice junctions in the mRNAs of minute virus of mice, an autonomous parvovirus. J Virol. 1986 Sep;59(3):564–573. doi: 10.1128/jvi.59.3.564-573.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Krieg P. A., Melton D. A. Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucleic Acids Res. 1984 Sep 25;12(18):7057–7070. doi: 10.1093/nar/12.18.7057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Melton D. A., Krieg P. A., Rebagliati M. R., Maniatis T., Zinn K., Green M. R. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 1984 Sep 25;12(18):7035–7056. doi: 10.1093/nar/12.18.7035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mortimer P. P., Humphries R. K., Moore J. G., Purcell R. H., Young N. S. A human parvovirus-like virus inhibits haematopoietic colony formation in vitro. 1983 Mar 31-Apr 6Nature. 302(5907):426–429. doi: 10.1038/302426a0. [DOI] [PubMed] [Google Scholar]
  24. Ozawa K., Ayub J., Hao Y. S., Kurtzman G., Shimada T., Young N. Novel transcription map for the B19 (human) pathogenic parvovirus. J Virol. 1987 Aug;61(8):2395–2406. doi: 10.1128/jvi.61.8.2395-2406.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ozawa K., Kurtzman G., Young N. Replication of the B19 parvovirus in human bone marrow cell cultures. Science. 1986 Aug 22;233(4766):883–886. doi: 10.1126/science.3738514. [DOI] [PubMed] [Google Scholar]
  26. Ozawa K., Young N. Characterization of capsid and noncapsid proteins of B19 parvovirus propagated in human erythroid bone marrow cell cultures. J Virol. 1987 Aug;61(8):2627–2630. doi: 10.1128/jvi.61.8.2627-2630.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Preston C. M. Control of herpes simplex virus type 1 mRNA synthesis in cells infected with wild-type virus or the temperature-sensitive mutant tsK. J Virol. 1979 Jan;29(1):275–284. doi: 10.1128/jvi.29.1.275-284.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rao K. R., Patel A. R., Anderson M. J., Hodgson J., Jones S. E., Pattison J. R. Infection with parvovirus-like virus and aplastic crisis in chronic hemolytic anemia. Ann Intern Med. 1983 Jun;98(6):930–932. doi: 10.7326/0003-4819-98-6-930. [DOI] [PubMed] [Google Scholar]
  30. Reed S. I., Stark G. R., Alwine J. C. Autoregulation of simian virus 40 gene A by T antigen. Proc Natl Acad Sci U S A. 1976 Sep;73(9):3083–3087. doi: 10.1073/pnas.73.9.3083. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rhode S. L., 3rd, Paradiso P. R. Parvovirus genome: nucleotide sequence of H-1 and mapping of its genes by hybrid-arrested translation. J Virol. 1983 Jan;45(1):173–184. doi: 10.1128/jvi.45.1.173-184.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Rhode S. L., 3rd, Richard S. M. Characterization of the trans-activation-responsive element of the parvovirus H-1 P38 promoter. J Virol. 1987 Sep;61(9):2807–2815. doi: 10.1128/jvi.61.9.2807-2815.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rhode S. L., 3rd trans-Activation of parvovirus P38 promoter by the 76K noncapsid protein. J Virol. 1985 Sep;55(3):886–889. doi: 10.1128/jvi.55.3.886-889.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Saarinen U. M., Chorba T. L., Tattersall P., Young N. S., Anderson L. J., Palmer E., Coccia P. F. Human parvovirus B19-induced epidemic acute red cell aplasia in patients with hereditary hemolytic anemia. Blood. 1986 May;67(5):1411–1417. [PubMed] [Google Scholar]
  35. Sahli R., McMaster G. K., Hirt B. DNA sequence comparison between two tissue-specific variants of the autonomous parvovirus, minute virus of mice. Nucleic Acids Res. 1985 May 24;13(10):3617–3633. doi: 10.1093/nar/13.10.3617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Shade R. O., Blundell M. C., Cotmore S. F., Tattersall P., Astell C. R. Nucleotide sequence and genome organization of human parvovirus B19 isolated from the serum of a child during aplastic crisis. J Virol. 1986 Jun;58(3):921–936. doi: 10.1128/jvi.58.3.921-936.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sompayrac L. M., Danna K. J. Efficient infection of monkey cells with DNA of simian virus 40. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7575–7578. doi: 10.1073/pnas.78.12.7575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. 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]
  39. Trempe J. P., Carter B. J. Regulation of adeno-associated virus gene expression in 293 cells: control of mRNA abundance and translation. J Virol. 1988 Jan;62(1):68–74. doi: 10.1128/jvi.62.1.68-74.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES