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. 1989 Oct;63(10):4129–4135. doi: 10.1128/jvi.63.10.4129-4135.1989

Loss of Marek's disease virus tumorigenicity is associated with truncation of RNAs transcribed within BamHI-H.

G Bradley 1, G Lancz 1, A Tanaka 1, M Nonoyama 1
PMCID: PMC251026  PMID: 2550661

Abstract

The attenuation of Marek's disease virus (MDV) is associated with loss of pathogenicity and tumorigenicity. Previous studies have demonstrated a strong correlation between attenuation and amplification of a specific sequence located within the MDV terminal and internal repeats. We recently reported that the regions containing the amplified sequences, the BamHI D and H fragments, were transcriptionally active. However, differential transcription activity was observed to exist between attenuated and pathogenic MDV strains. Specifically, a major transcript of 1.8 kilobases was found to be produced by pathogenic MDV and not by attenuated MDV. We now report that the disappearance of this transcript is concomitant with the production of a 0.4-kilobase RNA, an RNA resulting from the truncation of the tumorigenicity-related transcript.

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Selected References

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

  1. Adhya S., Gottesman M. Control of transcription termination. Annu Rev Biochem. 1978;47:967–996. doi: 10.1146/annurev.bi.47.070178.004535. [DOI] [PubMed] [Google Scholar]
  2. Aloni Y., Hay N. Attenuation may regulate gene expression in animal viruses and cells. CRC Crit Rev Biochem. 1985;18(4):327–383. doi: 10.3109/10409238509086785. [DOI] [PubMed] [Google Scholar]
  3. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bentley D. L., Groudine M. A block to elongation is largely responsible for decreased transcription of c-myc in differentiated HL60 cells. Nature. 1986 Jun 12;321(6071):702–706. doi: 10.1038/321702a0. [DOI] [PubMed] [Google Scholar]
  5. Bentley D. L., Groudine M. Sequence requirements for premature termination of transcription in the human c-myc gene. Cell. 1988 Apr 22;53(2):245–256. doi: 10.1016/0092-8674(88)90386-8. [DOI] [PubMed] [Google Scholar]
  6. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  7. Birnstiel M. L., Busslinger M., Strub K. Transcription termination and 3' processing: the end is in site! Cell. 1985 Jun;41(2):349–359. doi: 10.1016/s0092-8674(85)80007-6. [DOI] [PubMed] [Google Scholar]
  8. Bradley G., Hayashi M., Lancz G., Tanaka A., Nonoyama M. Structure of the Marek's disease virus BamHI-H gene family: genes of putative importance for tumor induction. J Virol. 1989 Jun;63(6):2534–2542. doi: 10.1128/jvi.63.6.2534-2542.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  10. Churchill A. E., Chubb R. C., Baxendale W. The attenuation, with loss of oncogenicity, of the herpes-type virus of Marek's disease (strain HPRS-16) on passage in cell culture. J Gen Virol. 1969 Jun;4(4):557–564. doi: 10.1099/0022-1317-4-4-557. [DOI] [PubMed] [Google Scholar]
  11. Connelly S., Manley J. L. A functional mRNA polyadenylation signal is required for transcription termination by RNA polymerase II. Genes Dev. 1988 Apr;2(4):440–452. doi: 10.1101/gad.2.4.440. [DOI] [PubMed] [Google Scholar]
  12. Denhardt D. T. A membrane-filter technique for the detection of complementary DNA. Biochem Biophys Res Commun. 1966 Jun 13;23(5):641–646. doi: 10.1016/0006-291x(66)90447-5. [DOI] [PubMed] [Google Scholar]
  13. Eick D., Bornkamm G. W. Transcriptional arrest within the first exon is a fast control mechanism in c-myc gene expression. Nucleic Acids Res. 1986 Nov 11;14(21):8331–8346. doi: 10.1093/nar/14.21.8331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Eidson C. S., Anderson D. P. Immunization against Marek's disease. Avian Dis. 1971 Jan-Mar;15(1):68–81. [PubMed] [Google Scholar]
  15. Eidson C. S., Schmittle S. C. Studies on acute Marek's disease. I. Characteristics of isolate GA in chickens. Avian Dis. 1968 Aug;12(3):467–476. [PubMed] [Google Scholar]
  16. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  17. Friedman D. I., Imperiale M. J., Adhya S. L. RNA 3' end formation in the control of gene expression. Annu Rev Genet. 1987;21:453–488. doi: 10.1146/annurev.ge.21.120187.002321. [DOI] [PubMed] [Google Scholar]
  18. Fukuchi K., Tanaka A., Schierman L. W., Witter R. L., Nonoyama M. The structure of Marek disease virus DNA: the presence of unique expansion in nonpathogenic viral DNA. Proc Natl Acad Sci U S A. 1985 Feb;82(3):751–754. doi: 10.1073/pnas.82.3.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hay N., Aloni Y. Attenuation of late simian virus 40 mRNA synthesis is enhanced by the agnoprotein and is temporally regulated in isolated nuclear systems. Mol Cell Biol. 1985 Jun;5(6):1327–1334. doi: 10.1128/mcb.5.6.1327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hay N., Skolnik-David H., Aloni Y. Attenuation in the control of SV40 gene expression. Cell. 1982 May;29(1):183–193. doi: 10.1016/0092-8674(82)90102-7. [DOI] [PubMed] [Google Scholar]
  21. Kenzy S. G., Cho B. R. Transmission of classical Marek's disease by affected and carrier birds. Avian Dis. 1969 Feb;13(1):211–214. [PubMed] [Google Scholar]
  22. Klein P., Kanehisa M., DeLisi C. The detection and classification of membrane-spanning proteins. Biochim Biophys Acta. 1985 May 28;815(3):468–476. doi: 10.1016/0005-2736(85)90375-x. [DOI] [PubMed] [Google Scholar]
  23. Lai E. C., Stein J. P., Catterall J. F., Woo S. L., Mace M. L., Means A. R., O'Malley B. W. Molecular structure and flanking nucleotide sequences of the natural chicken ovomucoid gene. Cell. 1979 Nov;18(3):829–842. doi: 10.1016/0092-8674(79)90135-1. [DOI] [PubMed] [Google Scholar]
  24. Lee F., Yanofsky C. Transcription termination at the trp operon attenuators of Escherichia coli and Salmonella typhimurium: RNA secondary structure and regulation of termination. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4365–4369. doi: 10.1073/pnas.74.10.4365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Maotani K., Kanamori A., Ikuta K., Ueda S., Kato S., Hirai K. Amplification of a tandem direct repeat within inverted repeats of Marek's disease virus DNA during serial in vitro passage. J Virol. 1986 May;58(2):657–660. doi: 10.1128/jvi.58.2.657-660.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. McLauchlan J., Gaffney D., Whitton J. L., Clements J. B. The consensus sequence YGTGTTYY located downstream from the AATAAA signal is required for efficient formation of mRNA 3' termini. Nucleic Acids Res. 1985 Feb 25;13(4):1347–1368. doi: 10.1093/nar/13.4.1347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. McMaster G. K., Carmichael G. G. Analysis of single- and double-stranded nucleic acids on polyacrylamide and agarose gels by using glyoxal and acridine orange. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4835–4838. doi: 10.1073/pnas.74.11.4835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Nazerian K. Attenuation of Marek's disease virus and study of its properties in two different cell cultures. J Natl Cancer Inst. 1970 Jun;44(6):1257–1267. [PubMed] [Google Scholar]
  29. Nepveu A., Marcu K. B. Intragenic pausing and anti-sense transcription within the murine c-myc locus. EMBO J. 1986 Nov;5(11):2859–2865. doi: 10.1002/j.1460-2075.1986.tb04580.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Okazaki W., Purchase H. G., Burmester B. R. Protection against Marek's disease by vaccination with a herpesvirus of turkeys. Avian Dis. 1970 May;14(2):413–429. [PubMed] [Google Scholar]
  31. Platt T. Transcription termination and the regulation of gene expression. Annu Rev Biochem. 1986;55:339–372. doi: 10.1146/annurev.bi.55.070186.002011. [DOI] [PubMed] [Google Scholar]
  32. Rispens B. H., van Vloten H., Mastenbroek N., Maas H. J., Schat K. A. Control of Marek's disease in the Netherlands. I. Isolation of an avirulent Marek's disease virus (strain CVI 988) and its use in laboratory vaccination trials. Avian Dis. 1972 Apr;16(1):108–125. [PubMed] [Google Scholar]
  33. Silva R. F., Witter R. L. Genomic expansion of Marek's disease virus DNA is associated with serial in vitro passage. J Virol. 1985 Jun;54(3):690–696. doi: 10.1128/jvi.54.3.690-696.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sklar J., Yot P., Weissman S. M. Determination of genes, restriction sites, and DNA sequences surrounding the 6S RNA template of bacteriophage lambda. Proc Natl Acad Sci U S A. 1975 May;72(5):1817–1821. doi: 10.1073/pnas.72.5.1817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wright S., Bishop J. M. DNA sequences that mediate attenuation of transcription from the mouse protooncogene myc. Proc Natl Acad Sci U S A. 1989 Jan;86(2):505–509. doi: 10.1073/pnas.86.2.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Yanofsky C. Transcription attenuation. J Biol Chem. 1988 Jan 15;263(2):609–612. [PubMed] [Google Scholar]

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