Sequences at the capped 5'-ends of polyoma virus late region mRNAs: an example of extreme terminal heterogeneity (original) (raw)

Abstract

We have localized with respect to the genomic DNA sequence the capped 5'-termini of polyoma virus late region mRNAs. A minimum of fifteen different purine termini were found within a 94 base pair region (66.36 to 68.12 map units, nt 5075-5168) immediately preceding the sequence determining the late region mRNA leader repeat (1-3). The most common termini occur at nearly every possible purine within a 25 bp sequence proximal to the leader repeat unit. These do not bear the usual positional relationship to a sequence resembling the 'TATA' box consensus. Deletion mutants lacking minor cap sites and sequences upstream from the principal cap sites were viable. A deletion mutant lacking one of the principal cap sites formed small plaques, while a slightly larger deletion further impinging on the principal cap site region was non-viable. The principal cap sites, which we assume to be transcriptional initiation points, are included in a DNaseI hypersensitive region of polyoma virus chromatin (4).

6305

Images in this article

Selected References

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

  1. Acheson N. H., Buetti E., Scherrer K., Weil R. Transcription of the polyoma virus genome: synthesis and cleavage of giant late polyoma-specific RNA. Proc Natl Acad Sci U S A. 1971 Sep;68(9):2231–2235. doi: 10.1073/pnas.68.9.2231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Acheson N. H. Polyoma virus giant RNAs contain tandem repeats of the nucleotide sequence of the entire viral genome. Proc Natl Acad Sci U S A. 1978 Oct;75(10):4754–4758. doi: 10.1073/pnas.75.10.4754. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Arrand J. R., Soeda E., Walsh J. E., Smolar N., Griffin B. E. Polyoma virus DNA: Sequence from the late region that specifies the leader sequence for late mRNA and codes for VP2, VP3, and the N-terminus of VP1. J Virol. 1980 Feb;33(2):606–618. doi: 10.1128/jvi.33.2.606-618.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baker C. C., Ziff E. B. Promoters and heterogeneous 5' termini of the messenger RNAs of adenovirus serotype 2. J Mol Biol. 1981 Jun 25;149(2):189–221. doi: 10.1016/0022-2836(81)90298-9. [DOI] [PubMed] [Google Scholar]
  5. Benoist C., O'Hare K., Breathnach R., Chambon P. The ovalbumin gene-sequence of putative control regions. Nucleic Acids Res. 1980 Jan 11;8(1):127–142. doi: 10.1093/nar/8.1.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Birg F., Favaloro J., Kamen R. Analysis of polyoma virus nuclear RNA by mini-blot hybridization. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3138–3142. doi: 10.1073/pnas.74.8.3138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Canaani D., Kahana C., Mukamel A., Groner Y. Sequence heterogeneity at the 5' termini of late simian virus 40 19S and 16S mRNAs. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3078–3082. doi: 10.1073/pnas.76.7.3078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Contreras R., Fiers W. Initiation of transcription by RNA polymerase II in permeable, SV40-infected or noninfected, CVI cells; evidence for multiple promoters of SV40 late transcription. Nucleic Acids Res. 1981 Jan 24;9(2):215–236. doi: 10.1093/nar/9.2.215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Deininger P., Esty A., LaPorte P., Friedmann T. Nucleotide sequence and genetic organization of the polyoma late region: features common to the polyoma early region and SV40. Cell. 1979 Nov;18(3):771–779. doi: 10.1016/0092-8674(79)90130-2. [DOI] [PubMed] [Google Scholar]
  10. Donis-Keller H., Maxam A. M., Gilbert W. Mapping adenines, guanines, and pyrimidines in RNA. Nucleic Acids Res. 1977 Aug;4(8):2527–2538. doi: 10.1093/nar/4.8.2527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. FRIED M. CELL-TRANSFORMING ABILITY OF A TEMPERATURE-SENSITIVE MUTANT OF POLYOMA VIRUS. Proc Natl Acad Sci U S A. 1965 Mar;53:486–491. doi: 10.1073/pnas.53.3.486. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Favaloro J., Treisman R., Kamen R. Transcription maps of polyoma virus-specific RNA: analysis by two-dimensional nuclease S1 gel mapping. Methods Enzymol. 1980;65(1):718–749. doi: 10.1016/s0076-6879(80)65070-8. [DOI] [PubMed] [Google Scholar]
  13. Faye G., Leung D. W., Tatchell K., Hall B. D., Smith M. Deletion mapping of sequences essential for in vivo transcription of the iso-1-cytochrome c gene. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2258–2262. doi: 10.1073/pnas.78.4.2258. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fiers W., Contreras R., Haegemann G., Rogiers R., Van de Voorde A., Van Heuverswyn H., Van Herreweghe J., Volckaert G., Ysebaert M. Complete nucleotide sequence of SV40 DNA. Nature. 1978 May 11;273(5658):113–120. doi: 10.1038/273113a0. [DOI] [PubMed] [Google Scholar]
  15. Flavell A. J., Cowie A., Arrand J. R., Kamen R. Localization of three major cappe 5' ends of polyoma virus late mRNA's within a single tetranucleotide sequence in the viral genome. J Virol. 1980 Feb;33(2):902–908. doi: 10.1128/jvi.33.2.902-908.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Flavell A. J., Cowie A., Legon S., Kamen R. Multiple 5' terminal cap structures in late polyoma virus RNA. Cell. 1979 Feb;16(2):357–371. doi: 10.1016/0092-8674(79)90012-6. [DOI] [PubMed] [Google Scholar]
  17. Friedmann T., Esty A., LaPorte P., Deininger P. The nucleotide sequence and genome organization of the polyoma early region: extensive nucleotide and amino acid homology with SV40. Cell. 1979 Jul;17(3):715–724. doi: 10.1016/0092-8674(79)90278-2. [DOI] [PubMed] [Google Scholar]
  18. Ghosh P. K., Reddy V. B., Swinscoe J., Lebowitz P., Weissman S. M. Heterogeneity and 5'-terminal structures of the late RNAs of simian virus 40. J Mol Biol. 1978 Dec 25;126(4):813–846. doi: 10.1016/0022-2836(78)90022-0. [DOI] [PubMed] [Google Scholar]
  19. Gidoni D., Kahana C., Canaani D., Groner Y. Specific in vitro initiation of transcription of simian virus 40 early and late genes occurs at the various cap nucleotides including cytidine. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2174–2178. doi: 10.1073/pnas.78.4.2174. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Haegeman G., Fiers W. Characterization of the 5'-terminal cap structures of early simian virus 40 mRNA. J Virol. 1980 Sep;35(3):955–961. doi: 10.1128/jvi.35.3.955-961.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Haegeman G., van Heuverswyn H., Gheysen D., Fiers W. Heterogeneity of the 5' terminus of late mRNA induced by a viable simian virus 40 deletion mutant. J Virol. 1979 Aug;31(2):484–493. doi: 10.1128/jvi.31.2.484-493.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hagenbüchle O., Schibler U. Mouse beta-globin and adenovirus-2 major late transcripts are initiated at the cap site in vitro. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2283–2286. doi: 10.1073/pnas.78.4.2283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hashimoto S., Pursley M. H., Green M. Nucleotide sequences and mapping of novel heterogenous 5'-termini of adenovirus 2 early region 4 mRNA. Nucleic Acids Res. 1981 Apr 10;9(7):1675–1689. doi: 10.1093/nar/9.7.1675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Horowitz M., Bratosin S., Aloni Y. Polyoma infected cells contain at least three spliced late RNAs. Nucleic Acids Res. 1978 Dec;5(12):4663–4675. doi: 10.1093/nar/5.12.4663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hunter T., Gibson W. Characterization of the mRNA's for the polyoma virus capsid proteins VP1, VP2, and VP3. J Virol. 1978 Oct;28(1):240–253. doi: 10.1128/jvi.28.1.240-253.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kahana C., Gidoni D., Canaani D., Groner Y. Simian virus 40 early mRNA's in lytically infected and transformed cells contain six 5'-terminal caps. J Virol. 1981 Jan;37(1):7–16. doi: 10.1128/jvi.37.1.7-16.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kamen R., Favaloro J., Parker J. Topography of the three late mRNA's of polyoma virus which encode the virion proteins. J Virol. 1980 Feb;33(2):637–651. doi: 10.1128/jvi.33.2.637-651.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Katinka M., Yaniv M., Vasseur M., Blangy D. Expression of polyoma early functions in mouse embryonal carcinoma cells depends on sequence rearrangements in the beginning of the late region. Cell. 1980 Jun;20(2):393–399. doi: 10.1016/0092-8674(80)90625-x. [DOI] [PubMed] [Google Scholar]
  29. Legerski R. J., Hodnett J. L., Gray H. B., Jr Extracellular nucleases of pseudomonas BAL 31. III. Use of the double-strand deoxyriboexonuclease activity as the basis of a convenient method for the mapping of fragments of DNA produced by cleavage with restriction enzymes. Nucleic Acids Res. 1978 May;5(5):1445–1464. doi: 10.1093/nar/5.5.1445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Legon S., Flavell A. J., Cowie A., Kamen R. Amplification in the leader sequence of late polyoma virus mRNAs. Cell. 1979 Feb;16(2):373–388. doi: 10.1016/0092-8674(79)90013-8. [DOI] [PubMed] [Google Scholar]
  31. Lockhard R. E., Rajbhandary U. L. Nucleotide sequences at the 5'termini of rabbit alpha and beta globin mRNA. Cell. 1976 Dec;9(4 Pt 2):747–760. doi: 10.1016/0092-8674(76)90138-0. [DOI] [PubMed] [Google Scholar]
  32. Manley J. L., Fire A., Cano A., Sharp P. A., Gefter M. L. DNA-dependent transcription of adenovirus genes in a soluble whole-cell extract. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3855–3859. doi: 10.1073/pnas.77.7.3855. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Manor H., Wu M., Baran N., Davidson N. Electron microscopic mapping of RNA transcribed from the late region of polyoma virus DNA. J Virol. 1979 Oct;32(1):293–303. doi: 10.1128/jvi.32.1.293-303.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  35. McCutchan J. H., Pagano J. S. Enchancement of the infectivity of simian virus 40 deoxyribonucleic acid with diethylaminoethyl-dextran. J Natl Cancer Inst. 1968 Aug;41(2):351–357. [PubMed] [Google Scholar]
  36. Pedersen F. S., Haseltine W. A. Analysis of the genome of an endogenous, ecotropic retrovirus of the AKR strain of mice: micromethod for detailed characterization of high-molecular-weight RNA. J Virol. 1980 Jan;33(1):349–365. doi: 10.1128/jvi.33.1.349-365.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Reddy V. B., Thimmappaya B., Dhar R., Subramanian K. N., Zain B. S., Pan J., Ghosh P. K., Celma M. L., Weissman S. M. The genome of simian virus 40. Science. 1978 May 5;200(4341):494–502. doi: 10.1126/science.205947. [DOI] [PubMed] [Google Scholar]
  38. Roychoudhury R., Jay E., Wu R. Terminal labeling and addition of homopolymer tracts to duplex DNA fragments by terminal deoxynucleotidyl transferase. Nucleic Acids Res. 1976 Jan;3(1):101–116. doi: 10.1093/nar/3.1.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Silberklang M., Gillum A. M., RajBhandary U. L. Use of in vitro 32P labeling in the sequence analysis of nonradioactive tRNAs. Methods Enzymol. 1979;59:58–109. doi: 10.1016/0076-6879(79)59072-7. [DOI] [PubMed] [Google Scholar]
  40. Soeda E., Arrand J. R., Smolar N., Walsh J. E., Griffin B. E. Coding potential and regulatory signals of the polyoma virus genome. Nature. 1980 Jan 31;283(5746):445–453. doi: 10.1038/283445a0. [DOI] [PubMed] [Google Scholar]
  41. Treisman R. Characterisation of polyoma late mRNA leader sequences by molecular cloning and DNA sequence analysis. Nucleic Acids Res. 1980 Nov 11;8(21):4867–4888. doi: 10.1093/nar/8.21.4867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Treisman R., Kamen R. Structure of polyoma virus late nuclear RNA. J Mol Biol. 1981 May 25;148(3):273–301. doi: 10.1016/0022-2836(81)90539-8. [DOI] [PubMed] [Google Scholar]
  43. Twigg A. J., Sherratt D. Trans-complementable copy-number mutants of plasmid ColE1. Nature. 1980 Jan 10;283(5743):216–218. doi: 10.1038/283216a0. [DOI] [PubMed] [Google Scholar]
  44. Twigg A. J., Sherratt D. Trans-complementable copy-number mutants of plasmid ColE1. Nature. 1980 Jan 10;283(5743):216–218. doi: 10.1038/283216a0. [DOI] [PubMed] [Google Scholar]
  45. Zuckermann M., Manor H., Parker J., Kamen R. Electron microscopic demonstration of the presence of amplified sequences at the 5'-ends of the polyoma virus late mRNAs. Nucleic Acids Res. 1980 Apr 11;8(7):1505–1519. doi: 10.1093/nar/8.7.1505. [DOI] [PMC free article] [PubMed] [Google Scholar]