Skip to main content
SpringerLink
Log in

Transcriptional analysis of the bovine herpesvirus 1 Cooper isolate

Temporal analysis and characterization of immediate-early, early, and late RNA

  • Original Papers
  • Published:
Archives of Virology Aims and scope Submit manuscript

Summary

Blot hybridization analysis of infected bovine herpesvirus 1 (BHV-1) cellular RNA isolated at various times post infection and after treatment with specific metabolic inhibitors was used to characterize transcription of the BHV-1 Cooper isolate. Synthesis of BHV-1 RNA was detected as early as 3 h post infection and reached a maximum at six to eight hours post infection. The most transcriptionally active area of the genome was between map units 0.110 to 0.195, within theHindIII I fragment. From the entire genome a total of 59 transcripts ranging in size from approximately 0.6 to 10 kilobases were characterized as belonging to one of three distinct classes. Using the protein synthesis inhibitor cycloheximide, three immediate-early transcripts were identified as originating from the internal inverted repeat region between map units 0.734 and 0.842, corresponding to theHindIII D fragment. Using phosphonoacetic acid to prevent virus DNA synthesis by inhibition of the BHV-1 DNA polymerase, 28 early transcripts were recognized. The remaining 28 transcripts, classified as late RNA, were detected without the use of metabolic inhibitors at 6 to 8 h post infection. Transcription of early and late RNA was not restricted to any specific area of the genome. Eighty percent of the transcripts from both theHindIII A fragment, between map units 0.381 to 0.537 within the unique long segment, and theHindIII K fragment, between map units 0.840 to 0.907 of the unique short segment, were designated as belonging to the early class.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Babiuk LA, Acres SD, Misra V, Stockdale PHG, DeClerq E (1983) Susceptibility of bovine herpesvirus 1 to antiviral drugs: In vitro versus in vivo efficacy of (E)-5-(2-bromoviny1)-2′-deoxyuridine. Antimicrob Agents Chemother 23: 715–720

    Google Scholar 

  2. Bandyopadhyay SK, Mittal SK, Field HJ (1990) Identification of the gene homologous to HSV major DNA binding protein in the BHV-1 genome. Vet Microbiol 22: 203–212

    Google Scholar 

  3. Bello LJ, Whitbeck JC, Lawrence WC (1987) Map location of the thymidine kinase gene of bovine herpesvirus 1. J Virol 61: 4023–4025

    Google Scholar 

  4. Bolton DC, Zee YC, Ardans AA (1983) Identification of envelope and nucleocapsid proteins of infectious bovine rhinotracheitis virus by SDS-PAGE. Vet Microbiol 8: 57–68

    Google Scholar 

  5. Caughman GB, Staczek J, O'Callaghan DJ (1985) Equine herpesvirus type 1 infected cell polypeptides: evidence for immediate early/early/late regulation of viral gene expression. Virology 145: 49–61

    Google Scholar 

  6. Chirgwin JM, Przybyla AE, MacDonald RJ, Rutter WJ (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18: 5294–5299

    Google Scholar 

  7. Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81: 1991–1995

    Google Scholar 

  8. Engels M, Gelderblom H, Darai G, Ludwig H (1983) Goat herpesvirus: biological and physicochemical properties. J Gen Virol 64: 2237–2247

    Google Scholar 

  9. Engels M, Giuliani C, Wild P, Beck TM, Leopfe E, Wyler R (1986) The genome of BHV 1 strains exhibiting a neuropathogenic potential compared to known BHV-1 strains by restriction site mapping and cross hybridization. Virus Res 6: 57–73

    Google Scholar 

  10. Feinberg AP, Vogelstein B (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132: 6–13

    Google Scholar 

  11. Feinberg AP, Vogelstein B (1984) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Addendum. Anal Biochem 137: 266–267

    Google Scholar 

  12. Fitzpatrick DR, Babiuk LA, Zamb TJ (1989) Nucleotide sequence of bovine herpesvirus type 1 glycoprotein gIII, a structural model for gIII as a new member of the immunoglobulin superfamily, and implications for the homologous glycoproteins of other herpesviruses. Virology 173: 46–57

    Google Scholar 

  13. Fitzpatrick DR, Zamb T, Parker MD, van Drunen Littel-van den Hurk S, Babiuk LA, Lawman MJP (1988) Expression of bovine herpesvirus 1 glycoprotein gI and gIII in transfected murine cells. J Virol 62: 4239–4248

    Google Scholar 

  14. Glisin V, Crkvenjakov R, Byers C (1974) Ribonucleic acid isolated by cesium chloride centrifugation. Biochemistry 13: 2633–2637

    Google Scholar 

  15. Graham BJ, Ludwig H, Bronson DL, Benyesh-Melnick M, Biswal N (1972) Physicochemical properties of the DNA of herpesviruses. Biochem Biophys Acta 259: 13–23

    Google Scholar 

  16. Gray WL, Bauman RP, Robertson AT, O'Callaghan DJ, Staczek J (1987) Characterization and mapping of equine herpesvirus type 1 immediate early, early and late transcripts. Virus Res 8: 233–244

    Google Scholar 

  17. Hammerschmidt W, Ludwig H, Buhk H-J (1988) Specificity of cleavage in replicative-form DNA of bovine herpesvirus 1. J Virol 62: 1355–1363

    Google Scholar 

  18. Hammerschmidt W, Ludwig H, Buhk H-J (1986) Short repeats cause heterogeneity at genomic terminus of bovine herpesvirus 1. J Virol 58: 43–49

    Google Scholar 

  19. House JA (1972) Bovine herpesvirus: IBR-IPV strain differences. Cornell Vet 62: 431–453

    Google Scholar 

  20. Jones C, Delhon G, Bratanich A, Kutich G, Rock D (1990) Analysis of the transcriptional promoter which regulates the latency-related transcript of bovine herpesvirus 1. J Virol 64: 1164–1170

    Google Scholar 

  21. Kendrick JW, Gillespie JH, McEnter K (1958) Infectious pustular vulvovaginitis of cattle. Cornell Vet 48: 458–495

    Google Scholar 

  22. Kit S, Qavi H (1983) Thymidine kinase (Tk) induction after infection of Tk-deficient rabbit cell mutants with bovine herpesvirus type 1 (BHV-1): isolation of TK− BHV-1 mutants. Virology 130: 381–389

    Google Scholar 

  23. Kokles R (1967) In: Roher H (ed) Handbuch der Virusinfektionen bei Tieren, vol 2. VEB G Fischer, Jena, pp 901–960

    Google Scholar 

  24. Lawrence WC, D'Urso RC, Kundel CA, Whitbeck JC, Bello L (1986) Map location of the gene for a 130,000-dalton glycoprotein of bovine herpesvirus 1. J Virol 60: 405–414

    Google Scholar 

  25. Lehrach H, Diamond D, Wozney JM, Boedtker H (1977) RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical examination. Biochemistry 16: 4743–4751

    Google Scholar 

  26. Leinback SS, Reno JM, Lee LF, Isbell AF, Boezi JA (1976) Mechanism of phosphonoacetate inhibition of herpesvirus-induced DNA polymerase. Biochemistry 15: 426–430

    Google Scholar 

  27. Ludwig H (1983) Bovine herpesviruses. In: Roizman B (ed) The herpesviruses. Plenum, New York, pp 135–214

    Google Scholar 

  28. Madin SH, York CJ, McKercher DG (1956) Isolation of infectious bovine rhinotracheitis virus. Science 124: 721–722

    Google Scholar 

  29. Mahmoudi M, Lin VK (1989) Comparison of two different hybridization systems in Northern transfer analysis. Biotechniques 7: 331–334

    Google Scholar 

  30. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY

    Google Scholar 

  31. Marshall RL, Rodriguez LL, Letchworth GJ (1986) Characterization of envelope proteins of infectious bovine rhinotracheitis virus (bovine herpesvirus 1) by biochemical and immunological methods. J Virol 57: 745–753

    Google Scholar 

  32. Mayfield JE, Good PJ, Van Oort HJ, Campbell AR, Reed DE (1983) Cloning and cleavage site mapping of DNA from bovine herpesvirus 1 (Cooper strain). J Virol 47: 259–264

    Google Scholar 

  33. McMaster GK, Carmichael GC (1977) Analysis of single- and double-stranded nucleic acids on polyacrylamide and agarose gels by using glyoxal and acridine orange. Proc Natl Acad Sci USA 74: 4835–4838

    Google Scholar 

  34. Metzler AE, Schudel AA, Engels M (1986) BHV 1 molecular and antigenic characteristics of variant viruses isolated from calves with neurologic disease. Arch Virol 87: 205–217

    Google Scholar 

  35. Miller NJ (1955) Infectious necrotic rhinotracheitis of cattle. J Am Vet Med Assoc 126: 463–467

    Google Scholar 

  36. Misra V, Babiuk LA, Le Q Darcel C (1983) Analysis of bovine herpes virus type 1 isolates by restriction endonuclease fingerprinting. Arch Virol 76: 341–354

    Google Scholar 

  37. Misra V, Blumenthal RM, Babiuk LA (1983) Proteins specified by bovine herpesvirus 1 (infectious bovine rhinotracheitis). J Virol 40: 367–378

    Google Scholar 

  38. Misra V, Nelson R, Smith M (1988) Sequence of a bovine herpesvirus type-1 glycoprotein gene that is homologous to the Herpes simplex gene for the glycoprotein gB. Virology 166: 542–549

    Google Scholar 

  39. Mittal SK, Field HJ (1989) Analysis of the bovine herpesvirus type 1 thymidine kinase (Tk) gene from wild-type and Tk− deficient mutants. J Gen Virol 70: 901–918

    Google Scholar 

  40. Ostrove JM, Reinhold W, Fan C-M, Zorn S, Hay J, Strauss SE (1985) Transcription mapping of the varicella zoster virus genome. J Virol 56: 600–606

    Google Scholar 

  41. Owen LJ, Field HJ (1988) Genomic localization and sequence analysis of the putative bovine herpesvirus-1 DNA polymerase gene. Arch Virol 98: 27–38

    Google Scholar 

  42. Pastoret PP, Thiry E, Brochier B, Derboven G (1982) Bovid herpesvirus 1 infection of cattle: pathogenesis, latency, consequences of latency. Ann Rech Vet 13: 221–235

    Google Scholar 

  43. Reinhold WC, Strauss SE, Ostrove JM (1988) Directionality and further mapping of varicella zoster virus transcripts. Virus Res 9: 249–261

    Google Scholar 

  44. Rock DL, Beam SL, Mayfield JE (1987) Mapping BHV 1 latency-related RNA in trigerminal ganglia of latently infected rabbits. J Virol 61: 3827–3831

    Google Scholar 

  45. Sabina LR, Parker RC (1963) Studies of infectious bovine rhinotracheitis virus. I. Plaque assay and some characteristics in bovine kidney cells. Can J Microbiol 9: 567–576

    Google Scholar 

  46. Seal BS, Martinez JD, Hall MR, St Jeor SC (1988) Occurrence of bovine herpesvirus-1 DNA in nucleosomes of bovine herpesvirus-1 infected cells. Identification of a virion associated protein in chromatin of infected cells. Arch Virol 99: 221–236

    Google Scholar 

  47. Seal BS, St Jeor SC (1988) Purification and characterization of bovine herpesvirus-1 isolates and virus DNA utilizing bovine embryonic lung cells. J Tissue Cult Methods 11: 42–48

    Google Scholar 

  48. Seal BS, St Jeor SC, Taylor REL (1985) Restriction endonuclease analysis of bovine herpesvirus-1 DNA and nucleic acid homology between isolates. J Gen Virol 66: 2787

    Google Scholar 

  49. Stevens JG, Groman NB (1963) Properties of infectious bovine rhinotracheitis virus in a quantitated virus-cell culture system. Am J Vet Res 24: 1158–1163

    Google Scholar 

  50. Stevens JG, Groman NB (1964) Infectious bovine rhinotracheitis virus replication, cytopathology, and plaque formation in the presence and absence of nucleid acid analogues. J Bacteriol 87: 446–453

    Google Scholar 

  51. Struhl K (1985) A rapid method for creating recombinant DNA molecules. Biotechniques 3: 452

    Google Scholar 

  52. Studdert MJ (1990) Bovine encephalitis herpesvirus. Vet Rec 126: 21–22

    Google Scholar 

  53. Tikoo SK, Fitzpatrick DR, Babiuk LA, Zamb TJ (1990) Molecular cloning, sequencing, and expression of functional bovine herpesvirus 1 glycoprotein gIV in transfected bovine cells. J Virol 64: 5132–5142

    Google Scholar 

  54. Weinmaster GA, Misra V, McGuire R, Babiuk LA, DeClerq E (1982) Bovine herpesvirus type-1 (infectious bovine rhinotracheitis virus)-induced thymidine kinase. Virology 118: 191–201

    Google Scholar 

  55. Whetstone CA, Miller JM, Bortner DM, Van Der Maaten MJ (1989) Changes in the restriction endonuclease patterns of four modified-live infectious bovine rhinotracheitis virus (IBRV) vaccines after one passage in the host animal. Vaccine 7: 527–532

    Google Scholar 

  56. Whetstone CA, Wheeler JG, Reed DE (1985) Investigation of possible vaccine-induced epizootics of infectious bovine rhinotracheitis, using restriction endonuclease analysis of viral DNA. Am J Vet Res 47: 1789–1795

    Google Scholar 

  57. Whitbeck JC, Bello LJ, Lawrence WC (1988) Comparison of the BHV 1 gI gene and the HSV 1 gB gene. J Virol 62: 3319–3327

    Google Scholar 

  58. Wirth UV, Gunkel K, Engels M, Schwyzer M (1989) Spatial and temporal distribution of bovine herpesvirus 1 transcripts. J Virol 63: 4882–4889

    Google Scholar 

  59. Wyler R, Engels M, Schwyzer M (1989) Infectious bovine rhinotracheitis/vulvovaginitis (BHV 1). In: Wittman G (ed) Herpesvirus diseases of cattle, horses, and pigs. Kluwer, Boston, pp 1–72

    Google Scholar 

  60. Zhang Y-F, Wagner EK (1987) The kinetics of expression of individual herpes simplex type 1 transcripts. Virus Genes 1: 49–60

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Virology Cattle Research Unit, National Animal Disease Center, USDA, Agricultural Research Service, Ames, Iowa, U.S.A.

    B. S. Seal & Cecelia A. Whetstone

  2. Institute of Gerontology, University of Michigan, Ann Arbor, Michigan, U.S.A.

    J. M. Irving

Authors
  1. B. S. Seal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. M. Irving
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cecelia A. Whetstone
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Seal, B.S., Irving, J.M. & Whetstone, C.A. Transcriptional analysis of the bovine herpesvirus 1 Cooper isolate. Archives of Virology 121, 55–73 (1991). https://doi.org/10.1007/BF01316744

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01316744

Keywords

Search

Navigation