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. 1987 Aug;61(8):2581–2588. doi: 10.1128/jvi.61.8.2581-2588.1987

Human papillomavirus types 6 and 11 mRNAs from genital condylomata acuminata.

L T Chow, M Nasseri, S M Wolinsky, T R Broker
PMCID: PMC255705  PMID: 3037118

Abstract

We have identified and mapped a number of RNA species of human papillomavirus types 6 and 11 from condylomata acuminata by the electron microscopic R-loop technique. Each of the early (E)- and late (L)-region open reading frames (ORFs) deduced from the DNA sequences was represented in one or more transcripts. In addition, RNA species that could encode the modulator of DNA replication and the repressor of transcription, functions recently identified in the genetically similar bovine papillomavirus type 1, were also detected. Some ORFs were 5' proximal in one or more transcripts, whereas others were not 5' proximal in any species, suggesting that internal initiation of translation might be required to gain access to these latter ORFs. Virtually all transcripts had their 5' ends located in the E region and were polyadenylated at one of two sites, i.e., at the end of the E region or at the end of the L region. The great majority of the RNAs were derived from the E region of the genome, with one species approximately 50 to 100 times more abundant than the others. For most of the RNAs, the 5' end mapped near nucleotide 700; minor populations had 5' ends near nucleotide 100 or 1200. By correlating our mapping data with the genomic DNA sequences as well as available RNA structures and cDNA sequences of several papillomaviruses, we predict a number of mRNA splice donor and acceptor sites and suggest that the papillomaviruses have sophisticated usage of ORFs through alternative promoters, mRNA splice sites, and polyadenylation sites.

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Selected References

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  1. Androphy E. J., Hubbert N. L., Schiller J. T., Lowy D. R. Identification of the HPV-16 E6 protein from transformed mouse cells and human cervical carcinoma cell lines. EMBO J. 1987 Apr;6(4):989–992. doi: 10.1002/j.1460-2075.1987.tb04849.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baker C. C., Howley P. M. Differential promoter utilization by the bovine papillomavirus in transformed cells and productively infected wart tissues. EMBO J. 1987 Apr;6(4):1027–1035. doi: 10.1002/j.1460-2075.1987.tb04855.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beaudenon S., Kremsdorf D., Croissant O., Jablonska S., Wain-Hobson S., Orth G. A novel type of human papillomavirus associated with genital neoplasias. Nature. 1986 May 15;321(6067):246–249. doi: 10.1038/321246a0. [DOI] [PubMed] [Google Scholar]
  4. Berg L., Lusky M., Stenlund A., Botchan M. R. Repression of bovine papilloma virus replication is mediated by a virally encoded trans-acting factor. Cell. 1986 Aug 29;46(5):753–762. doi: 10.1016/0092-8674(86)90351-x. [DOI] [PubMed] [Google Scholar]
  5. Boshart M., Gissmann L., Ikenberg H., Kleinheinz A., Scheurlen W., zur Hausen H. A new type of papillomavirus DNA, its presence in genital cancer biopsies and in cell lines derived from cervical cancer. EMBO J. 1984 May;3(5):1151–1157. doi: 10.1002/j.1460-2075.1984.tb01944.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  7. Chow L. T., Reilly S. S., Broker T. R., Taichman L. B. Identification and mapping of human papillomavirus type 1 RNA transcripts recovered from plantar warts and infected epithelial cell cultures. J Virol. 1987 Jun;61(6):1913–1918. doi: 10.1128/jvi.61.6.1913-1918.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cole S. T., Danos O. Nucleotide sequence and comparative analysis of the human papillomavirus type 18 genome. Phylogeny of papillomaviruses and repeated structure of the E6 and E7 gene products. J Mol Biol. 1987 Feb 20;193(4):599–608. doi: 10.1016/0022-2836(87)90343-3. [DOI] [PubMed] [Google Scholar]
  9. Cole S. T., Streeck R. E. Genome organization and nucleotide sequence of human papillomavirus type 33, which is associated with cervical cancer. J Virol. 1986 Jun;58(3):991–995. doi: 10.1128/jvi.58.3.991-995.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Danos O., Engel L. W., Chen E. Y., Yaniv M., Howley P. M. Comparative analysis of the human type 1a and bovine type 1 papillomavirus genomes. J Virol. 1983 May;46(2):557–566. doi: 10.1128/jvi.46.2.557-566.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Danos O., Georges E., Orth G., Yaniv M. Fine structure of the cottontail rabbit papillomavirus mRNAs expressed in the transplantable VX2 carcinoma. J Virol. 1985 Mar;53(3):735–741. doi: 10.1128/jvi.53.3.735-741.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Danos O., Mulligan R. C., Yaniv M. Production of spliced DNA copies of the cottontail rabbit papillomavirus genome in a retroviral vector. Ciba Found Symp. 1986;120:68–82. doi: 10.1002/9780470513309.ch6. [DOI] [PubMed] [Google Scholar]
  13. Dartmann K., Schwarz E., Gissmann L., zur Hausen H. The nucleotide sequence and genome organization of human papilloma virus type 11. Virology. 1986 May;151(1):124–130. doi: 10.1016/0042-6822(86)90110-8. [DOI] [PubMed] [Google Scholar]
  14. Doorbar J., Campbell D., Grand R. J., Gallimore P. H. Identification of the human papilloma virus-1a E4 gene products. EMBO J. 1986 Feb;5(2):355–362. doi: 10.1002/j.1460-2075.1986.tb04219.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dvoretzky I., Shober R., Chattopadhyay S. K., Lowy D. R. A quantitative in vitro focus assay for bovine papilloma virus. Virology. 1980 Jun;103(2):369–375. doi: 10.1016/0042-6822(80)90195-6. [DOI] [PubMed] [Google Scholar]
  16. Dürst M., Gissmann L., Ikenberg H., zur Hausen H. A papillomavirus DNA from a cervical carcinoma and its prevalence in cancer biopsy samples from different geographic regions. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3812–3815. doi: 10.1073/pnas.80.12.3812. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dürst M., Kleinheinz A., Hotz M., Gissmann L. The physical state of human papillomavirus type 16 DNA in benign and malignant genital tumours. J Gen Virol. 1985 Jul;66(Pt 7):1515–1522. doi: 10.1099/0022-1317-66-7-1515. [DOI] [PubMed] [Google Scholar]
  18. Gissmann L., Diehl V., Schultz-Coulon H. J., zur Hausen H. Molecular cloning and characterization of human papilloma virus DNA derived from a laryngeal papilloma. J Virol. 1982 Oct;44(1):393–400. doi: 10.1128/jvi.44.1.393-400.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hirochika H., Broker T. R., Chow L. T. Enhancers and trans-acting E2 transcriptional factors of papillomaviruses. J Virol. 1987 Aug;61(8):2599–2606. doi: 10.1128/jvi.61.8.2599-2606.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kaback D. B., Angerer L. M., Davidson N. Improved methods for the formation and stabilization of R-loops. Nucleic Acids Res. 1979 Jun 11;6(7):2499–2317. doi: 10.1093/nar/6.7.2499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Komly C. A., Breitburd F., Croissant O., Streeck R. E. The L2 open reading frame of human papillomavirus type 1a encodes a minor structural protein carrying type-specific antigens. J Virol. 1986 Nov;60(2):813–816. doi: 10.1128/jvi.60.2.813-816.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Krieg P., Amtmann E., Sauer G. The simultaneous extraction of high-molecular-weight DNA and of RNA from solid tumors. Anal Biochem. 1983 Oct 15;134(2):288–294. doi: 10.1016/0003-2697(83)90299-3. [DOI] [PubMed] [Google Scholar]
  23. Law M. F., Lowy D. R., Dvoretzky I., Howley P. M. Mouse cells transformed by bovine papillomavirus contain only extrachromosomal viral DNA sequences. Proc Natl Acad Sci U S A. 1981 May;78(5):2727–2731. doi: 10.1073/pnas.78.5.2727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Lehn H., Ernst T. M., Sauer G. Transcription of episomal papillomavirus DNA in human condylomata acuminata and Buschke-Löwenstein tumours. J Gen Virol. 1984 Nov;65(Pt 11):2003–2010. doi: 10.1099/0022-1317-65-11-2003. [DOI] [PubMed] [Google Scholar]
  25. Lehn H., Krieg P., Sauer G. Papillomavirus genomes in human cervical tumors: analysis of their transcriptional activity. Proc Natl Acad Sci U S A. 1985 Aug;82(16):5540–5544. doi: 10.1073/pnas.82.16.5540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lorincz A. T., Lancaster W. D., Temple G. F. Cloning and characterization of the DNA of a new human papillomavirus from a woman with dysplasia of the uterine cervix. J Virol. 1986 Apr;58(1):225–229. doi: 10.1128/jvi.58.1.225-229.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Lusky M., Botchan M. R. A bovine papillomavirus type 1-encoded modulator function is dispensable for transient viral replication but is required for establishment of the stable plasmid state. J Virol. 1986 Nov;60(2):729–742. doi: 10.1128/jvi.60.2.729-742.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Nasseri M., Wettstein F. O. Differences exist between viral transcripts in cottontail rabbit papillomavirus-induced benign and malignant tumors as well as non-virus-producing and virus-producing tumors. J Virol. 1984 Sep;51(3):706–712. doi: 10.1128/jvi.51.3.706-712.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Neary K., Horwitz B. H., DiMaio D. Mutational analysis of open reading frame E4 of bovine papillomavirus type 1. J Virol. 1987 Apr;61(4):1248–1252. doi: 10.1128/jvi.61.4.1248-1252.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Pelham H. R. A regulatory upstream promoter element in the Drosophila hsp 70 heat-shock gene. Cell. 1982 Sep;30(2):517–528. doi: 10.1016/0092-8674(82)90249-5. [DOI] [PubMed] [Google Scholar]
  31. Phelps W. C., Leary S. L., Faras A. J. Shope papillomavirus transcription in benign and malignant rabbit tumors. Virology. 1985 Oct 15;146(1):120–129. doi: 10.1016/0042-6822(85)90058-3. [DOI] [PubMed] [Google Scholar]
  32. Przybyla A. E., MacDonald R. J., Harding J. D., Pictet R. L., Rutter W. J. Accumulation of the predominant pancreatic mRNAs during embryonic development. J Biol Chem. 1979 Mar 25;254(6):2154–2159. [PubMed] [Google Scholar]
  33. Roberts J. M., Weintraub H. Negative control of DNA replication in composite SV40-bovine papilloma virus plasmids. Cell. 1986 Aug 29;46(5):741–752. doi: 10.1016/0092-8674(86)90350-8. [DOI] [PubMed] [Google Scholar]
  34. Schiller J. T., Vass W. C., Vousden K. H., Lowy D. R. E5 open reading frame of bovine papillomavirus type 1 encodes a transforming gene. J Virol. 1986 Jan;57(1):1–6. doi: 10.1128/jvi.57.1.1-6.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Schneider-Gädicke A., Schwarz E. Different human cervical carcinoma cell lines show similar transcription patterns of human papillomavirus type 18 early genes. EMBO J. 1986 Sep;5(9):2285–2292. doi: 10.1002/j.1460-2075.1986.tb04496.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Schwarz E., Dürst M., Demankowski C., Lattermann O., Zech R., Wolfsperger E., Suhai S., zur Hausen H. DNA sequence and genome organization of genital human papillomavirus type 6b. EMBO J. 1983;2(12):2341–2348. doi: 10.1002/j.1460-2075.1983.tb01744.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Seedorf K., Krämmer G., Dürst M., Suhai S., Röwekamp W. G. Human papillomavirus type 16 DNA sequence. Virology. 1985 Aug;145(1):181–185. doi: 10.1016/0042-6822(85)90214-4. [DOI] [PubMed] [Google Scholar]
  38. Smotkin D., Wettstein F. O. Transcription of human papillomavirus type 16 early genes in a cervical cancer and a cancer-derived cell line and identification of the E7 protein. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4680–4684. doi: 10.1073/pnas.83.13.4680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Stenlund A., Zabielski J., Ahola H., Moreno-Lopez J., Pettersson U. Messenger RNAs from the transforming region of bovine papilloma virus type I. J Mol Biol. 1985 Apr 20;182(4):541–554. doi: 10.1016/0022-2836(85)90240-2. [DOI] [PubMed] [Google Scholar]
  40. Tsunokawa Y., Takebe N., Nozawa S., Kasamatsu T., Gissmann L., zur Hausen H., Terada M., Sugimura T. Presence of human papillomavirus type-16 and type-18 DNA sequences and their expression in cervical cancers and cell lines from Japanese patients. Int J Cancer. 1986 Apr 15;37(4):499–503. doi: 10.1002/ijc.2910370405. [DOI] [PubMed] [Google Scholar]
  41. Yang Y. C., Okayama H., Howley P. M. Bovine papillomavirus contains multiple transforming genes. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1030–1034. doi: 10.1073/pnas.82.4.1030. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. de Villiers E. M., Gissmann L., zur Hausen H. Molecular cloning of viral DNA from human genital warts. J Virol. 1981 Dec;40(3):932–935. doi: 10.1128/jvi.40.3.932-935.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]

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