Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1988 May 11;16(9):3771–3786. doi: 10.1093/nar/16.9.3771

Replication-induced stimulation of the major late promoter of adenovirus is correlated to the binding of a factor to sequences in the first intron.

P Jansen-Durr 1, H Boeuf 1, C Kédinger 1
PMCID: PMC336555  PMID: 2836800

Abstract

The sequence requirements for transcriptional stimulation of the adenovirus major late promoter (MLP) by the products of the early transcription unit Ela and by the replication of viral DNA were analyzed by in vitro transcription. Sequences upstream of +33 are involved in the moderate Ela-responsiveness of the MLP, while sequences between +33 and +131 are required for its major replication-induced transcriptional activation. Dnase I footprinting experiments delineate a sequence component, extending from +76 to +120, which binds protein(s) only in extracts of cells where viral DNA replication occurred. Taken together, these results suggest that the replication-dependent stimulation of the MLP is mediated by the increased binding of this protein(s).

Full text

PDF
3783

Images in this article

Selected References

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

  1. Antoniou M., deBoer E., Habets G., Grosveld F. The human beta-globin gene contains multiple regulatory regions: identification of one promoter and two downstream enhancers. EMBO J. 1988 Feb;7(2):377–384. doi: 10.1002/j.1460-2075.1988.tb02824.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Banerji J., Olson L., Schaffner W. A lymphocyte-specific cellular enhancer is located downstream of the joining region in immunoglobulin heavy chain genes. Cell. 1983 Jul;33(3):729–740. doi: 10.1016/0092-8674(83)90015-6. [DOI] [PubMed] [Google Scholar]
  3. Berk A. J. Adenovirus promoters and E1A transactivation. Annu Rev Genet. 1986;20:45–79. doi: 10.1146/annurev.ge.20.120186.000401. [DOI] [PubMed] [Google Scholar]
  4. Berk A. J., Lee F., Harrison T., Williams J., Sharp P. A. Pre-early adenovirus 5 gene product regulates synthesis of early viral messenger RNAs. Cell. 1979 Aug;17(4):935–944. doi: 10.1016/0092-8674(79)90333-7. [DOI] [PubMed] [Google Scholar]
  5. Boeuf H., Zajchowski D. A., Tamura T., Hauss C., Kédinger C. Specific cellular proteins bind to critical promoter sequences of the adenovirus early EIIa promoter. Nucleic Acids Res. 1987 Jan 26;15(2):509–527. doi: 10.1093/nar/15.2.509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brunet L. J., Babiss L. E., Young C. S., Mills D. R. Mutations in the adenovirus major late promoter: effects on viability and transcription during infection. Mol Cell Biol. 1987 Mar;7(3):1091–1100. doi: 10.1128/mcb.7.3.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Charnay P., Treisman R., Mellon P., Chao M., Axel R., Maniatis T. Differences in human alpha- and beta-globin gene expression in mouse erythroleukemia cells: the role of intragenic sequences. Cell. 1984 Aug;38(1):251–263. doi: 10.1016/0092-8674(84)90547-6. [DOI] [PubMed] [Google Scholar]
  8. Chodosh L. A., Carthew R. W., Sharp P. A. A single polypeptide possesses the binding and transcription activities of the adenovirus major late transcription factor. Mol Cell Biol. 1986 Dec;6(12):4723–4733. doi: 10.1128/mcb.6.12.4723. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Concino M. F., Lee R. F., Merryweather J. P., Weinmann R. The adenovirus major late promoter TATA box and initiation site are both necessary for transcription in vitro. Nucleic Acids Res. 1984 Oct 11;12(19):7423–7433. doi: 10.1093/nar/12.19.7423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Crossland L. D., Raskas H. J. Identification of adenovirus genes that require template replication for expression. J Virol. 1983 Jun;46(3):737–748. doi: 10.1128/jvi.46.3.737-748.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Derse D., Caradonna S. J., Casey J. W. Bovine leukemia virus long terminal repeat: a cell type-specific promoter. Science. 1985 Jan 18;227(4684):317–320. doi: 10.1126/science.2981431. [DOI] [PubMed] [Google Scholar]
  12. Devaux B., Albrecht G., Kedinger C. Identical genomic footprints of the adenovirus EIIa promoter are detected before and after EIa induction. Mol Cell Biol. 1987 Dec;7(12):4560–4563. doi: 10.1128/mcb.7.12.4560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dynan W. S., Tjian R. Control of eukaryotic messenger RNA synthesis by sequence-specific DNA-binding proteins. 1985 Aug 29-Sep 4Nature. 316(6031):774–778. doi: 10.1038/316774a0. [DOI] [PubMed] [Google Scholar]
  14. Green M. R., Treisman R., Maniatis T. Transcriptional activation of cloned human beta-globin genes by viral immediate-early gene products. Cell. 1983 Nov;35(1):137–148. doi: 10.1016/0092-8674(83)90216-7. [DOI] [PubMed] [Google Scholar]
  15. Hen R., Sassone-Corsi P., Corden J., Gaub M. P., Chambon P. Sequences upstream from the T-A-T-A box are required in vivo and in vitro for efficient transcription from the adenovirus serotype 2 major late promoter. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7132–7136. doi: 10.1073/pnas.79.23.7132. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hu S. L., Manley J. L. DNA sequence required for initiation of transcription in vitro from the major late promoter of adenovirus 2. Proc Natl Acad Sci U S A. 1981 Feb;78(2):820–824. doi: 10.1073/pnas.78.2.820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jones K. A., Kadonaga J. T., Rosenfeld P. J., Kelly T. J., Tjian R. A cellular DNA-binding protein that activates eukaryotic transcription and DNA replication. Cell. 1987 Jan 16;48(1):79–89. doi: 10.1016/0092-8674(87)90358-8. [DOI] [PubMed] [Google Scholar]
  18. Jones N., Shenk T. An adenovirus type 5 early gene function regulates expression of other early viral genes. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3665–3669. doi: 10.1073/pnas.76.8.3665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Leff T., Chambon P. Sequence-specific activation of transcription by adenovirus EIa products is observed in HeLa cells but not in 293 cells. Mol Cell Biol. 1986 Jan;6(1):201–208. doi: 10.1128/mcb.6.1.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Leong K., Berk A. J. Adenovirus early region 1A protein increases the number of template molecules transcribed in cell-free extracts. Proc Natl Acad Sci U S A. 1986 Aug;83(16):5844–5848. doi: 10.1073/pnas.83.16.5844. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lewis E. D., Manley J. L. Control of adenovirus late promoter expression in two human cell lines. Mol Cell Biol. 1985 Sep;5(9):2433–2442. doi: 10.1128/mcb.5.9.2433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Logan J., Shenk T. In vivo identification of sequence elements required for normal function of the adenovirus major late transcriptional control region. Nucleic Acids Res. 1986 Aug 11;14(15):6327–6335. [PMC free article] [PubMed] [Google Scholar]
  23. Manley J. L., Fire A., Samuels M., Sharp P. A. In vitro transcription: whole-cell extract. Methods Enzymol. 1983;101:568–582. doi: 10.1016/0076-6879(83)01038-1. [DOI] [PubMed] [Google Scholar]
  24. Merrill G. F., Hauschka S. D., McKnight S. L. tk Enzyme expression in differentiating muscle cells is regulated through an internal segment of the cellular tk gene. Mol Cell Biol. 1984 Sep;4(9):1777–1784. doi: 10.1128/mcb.4.9.1777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Miyamoto N. G., Moncollin V., Egly J. M., Chambon P. Specific interaction between a transcription factor and the upstream element of the adenovirus-2 major late promoter. EMBO J. 1985 Dec 16;4(13A):3563–3570. doi: 10.1002/j.1460-2075.1985.tb04118.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Moncollin V., Miyamoto N. G., Zheng X. M., Egly J. M. Purification of a factor specific for the upstream element of the adenovirus-2 major late promoter. EMBO J. 1986 Oct;5(10):2577–2584. doi: 10.1002/j.1460-2075.1986.tb04537.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Muesing M. A., Smith D. H., Capon D. J. Regulation of mRNA accumulation by a human immunodeficiency virus trans-activator protein. Cell. 1987 Feb 27;48(4):691–701. doi: 10.1016/0092-8674(87)90247-9. [DOI] [PubMed] [Google Scholar]
  28. Natarajan V., Madden M. J., Salzman N. P. Proximal and distal domains that control in vitro transcription of the adenovirus IVa2 gene. Proc Natl Acad Sci U S A. 1984 Oct;81(20):6290–6294. doi: 10.1073/pnas.81.20.6290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ohtani K., Nakamura M., Saito S., Noda T., Ito Y., Sugamura K., Hinuma Y. Identification of two distinct elements in the long terminal repeat of HTLV-I responsible for maximum gene expression. EMBO J. 1987 Feb;6(2):389–395. doi: 10.1002/j.1460-2075.1987.tb04767.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Paek I., Axel R. Glucocorticoids enhance stability of human growth hormone mRNA. Mol Cell Biol. 1987 Apr;7(4):1496–1507. doi: 10.1128/mcb.7.4.1496. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ptashne M. Gene regulation by proteins acting nearby and at a distance. Nature. 1986 Aug 21;322(6081):697–701. doi: 10.1038/322697a0. [DOI] [PubMed] [Google Scholar]
  32. Queen C., Baltimore D. Immunoglobulin gene transcription is activated by downstream sequence elements. Cell. 1983 Jul;33(3):741–748. doi: 10.1016/0092-8674(83)90016-8. [DOI] [PubMed] [Google Scholar]
  33. Reinberg D., Horikoshi M., Roeder R. G. Factors involved in specific transcription in mammalian RNA polymerase II. Functional analysis of initiation factors IIA and IID and identification of a new factor operating at sequences downstream of the initiation site. J Biol Chem. 1987 Mar 5;262(7):3322–3330. [PubMed] [Google Scholar]
  34. Rosen C. A., Sodroski J. G., Haseltine W. A. The location of cis-acting regulatory sequences in the human T cell lymphotropic virus type III (HTLV-III/LAV) long terminal repeat. Cell. 1985 Jul;41(3):813–823. doi: 10.1016/s0092-8674(85)80062-3. [DOI] [PubMed] [Google Scholar]
  35. Rossouw C. M., Vergeer W. P., du Plooy S. J., Bernard M. P., Ramirez F., de Wet W. J. DNA sequences in the first intron of the human pro-alpha 1(I) collagen gene enhance transcription. J Biol Chem. 1987 Nov 5;262(31):15151–15157. [PubMed] [Google Scholar]
  36. Sawadogo M., Roeder R. G. Factors involved in specific transcription by human RNA polymerase II: analysis by a rapid and quantitative in vitro assay. Proc Natl Acad Sci U S A. 1985 Jul;82(13):4394–4398. doi: 10.1073/pnas.82.13.4394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sawadogo M., Roeder R. G. Interaction of a gene-specific transcription factor with the adenovirus major late promoter upstream of the TATA box region. Cell. 1985 Nov;43(1):165–175. doi: 10.1016/0092-8674(85)90021-2. [DOI] [PubMed] [Google Scholar]
  38. Shaw A. R., Ziff E. B. Transcripts from the adenovirus-2 major late promoter yield a single early family of 3' coterminal mRNAs and five late families. Cell. 1980 Dec;22(3):905–916. doi: 10.1016/0092-8674(80)90568-1. [DOI] [PubMed] [Google Scholar]
  39. Theill L. E., Wiborg O., Vuust J. Cell-specific expression of the human gastrin gene: evidence for a control element located downstream of the TATA box. Mol Cell Biol. 1987 Dec;7(12):4329–4336. doi: 10.1128/mcb.7.12.4329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Thomas G. P., Mathews M. B. DNA replication and the early to late transition in adenovirus infection. Cell. 1980 Nov;22(2 Pt 2):523–533. doi: 10.1016/0092-8674(80)90362-1. [DOI] [PubMed] [Google Scholar]
  41. Venkatesh L. K., Chinnadurai G. Activation of the adenovirus 2 protein IX promoter by DNA replication in a transient expression assay. Nucleic Acids Res. 1987 Mar 11;15(5):2235–2250. doi: 10.1093/nar/15.5.2235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wu L., Rosser D. S., Schmidt M. C., Berk A. A TATA box implicated in E1A transcriptional activation of a simple adenovirus 2 promoter. Nature. 1987 Apr 2;326(6112):512–515. doi: 10.1038/326512a0. [DOI] [PubMed] [Google Scholar]
  43. Zain S., Sambrook J., Roberts R. J., Keller W., Fried M., Dunn A. R. Nucleotide sequence analysis of the leader segments in a cloned copy of adenovirus 2 fiber mRNA. Cell. 1979 Apr;16(4):851–861. doi: 10.1016/0092-8674(79)90100-4. [DOI] [PubMed] [Google Scholar]
  44. Zajchowski D. A., Boeuf H., Kédinger C. E1a inducibility of the adenoviral early E2a promoter is determined by specific combinations of sequence elements. Gene. 1987;58(2-3):243–256. doi: 10.1016/0378-1119(87)90379-9. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES