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. 1989 Jul;63(7):3057–3064. doi: 10.1128/jvi.63.7.3057-3064.1989

Independent cyclic AMP and E1A induction of adenovirus early region 4 expression.

M A Leza 1, P Hearing 1
PMCID: PMC250861  PMID: 2542614

Abstract

A cellular transcription factor, ATF, binds to a repeated element in the adenovirus early region 4 (E4) promoter. ATF also binds to other viral early promoter regions and to the cyclic AMP (cAMP) response elements of cellular genes. In this report, we demonstrate that a single ATF-binding site located immediately upstream of the E4 TATA box, between -62 and -46, mediates induction of E4 transcription by 8-bromoadenosine-3',5-cyclic monophosphate or cholera toxin in the human hepatoma cell line HepG2 and rat pheochromocytoma cell line PC12. Different ATF-binding sites in the E4 control region independently conferred cAMP inducibility on the simian virus 40 early promoter in PC12 cells. Induction of E4 expression by cAMP was also observed in virus-infected HepG2 cells. Other viral early promoter regions that contain ATF-binding sites (E1A and E2A) were also induced by cAMP in infected cells. E4 expression was activated by the E1A 13S mRNA products in HepG2 cells. E1A trans activation appears to be distinct from the cAMP response.

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Selected References

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

  1. 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]
  2. 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]
  3. 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]
  4. Büchler W., Walter U., Jastorff B., Lohmann S. M. Catalytic subunit of cAMP-dependent protein kinase is essential for cAMP-mediated mammalian gene expression. FEBS Lett. 1988 Feb 8;228(1):27–32. doi: 10.1016/0014-5793(88)80577-5. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Comb M., Birnberg N. C., Seasholtz A., Herbert E., Goodman H. M. A cyclic AMP- and phorbol ester-inducible DNA element. 1986 Sep 25-Oct 1Nature. 323(6086):353–356. doi: 10.1038/323353a0. [DOI] [PubMed] [Google Scholar]
  7. Cortes P., Buckbinder L., Leza M. A., Rak N., Hearing P., Merino A., Reinberg D. EivF, a factor required for transcription of the adenovirus EIV promoter, binds to an element involved in EIa-dependent activation and cAMP induction. Genes Dev. 1988 Aug;2(8):975–990. doi: 10.1101/gad.2.8.975. [DOI] [PubMed] [Google Scholar]
  8. Deutsch P. J., Hoeffler J. P., Jameson J. L., Habener J. F. Cyclic AMP and phorbol ester-stimulated transcription mediated by similar DNA elements that bind distinct proteins. Proc Natl Acad Sci U S A. 1988 Nov;85(21):7922–7926. doi: 10.1073/pnas.85.21.7922. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Engel D. A., Hardy S., Shenk T. cAMP acts in synergy with E1A protein to activate transcription of the adenovirus early genes E4 and E1A. Genes Dev. 1988 Dec;2(12A):1517–1528. doi: 10.1101/gad.2.12a.1517. [DOI] [PubMed] [Google Scholar]
  10. Evans R. M. The steroid and thyroid hormone receptor superfamily. Science. 1988 May 13;240(4854):889–895. doi: 10.1126/science.3283939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Fink J. S., Verhave M., Kasper S., Tsukada T., Mandel G., Goodman R. H. The CGTCA sequence motif is essential for biological activity of the vasoactive intestinal peptide gene cAMP-regulated enhancer. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6662–6666. doi: 10.1073/pnas.85.18.6662. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gilardi P., Perricaudet M. The E4 promoter of adenovirus type 2 contains an E1A dependent cis-acting element. Nucleic Acids Res. 1986 Nov 25;14(22):9035–9049. doi: 10.1093/nar/14.22.9035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Grove J. R., Price D. J., Goodman H. M., Avruch J. Recombinant fragment of protein kinase inhibitor blocks cyclic AMP-dependent gene transcription. Science. 1987 Oct 23;238(4826):530–533. doi: 10.1126/science.2821622. [DOI] [PubMed] [Google Scholar]
  16. Gunning P., Ponte P., Okayama H., Engel J., Blau H., Kedes L. Isolation and characterization of full-length cDNA clones for human alpha-, beta-, and gamma-actin mRNAs: skeletal but not cytoplasmic actins have an amino-terminal cysteine that is subsequently removed. Mol Cell Biol. 1983 May;3(5):787–795. doi: 10.1128/mcb.3.5.787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hanaka S., Nishigaki T., Sharp P. A., Handa H. Regulation of in vitro and in vivo transcription of early-region IV of adenovirus type 5 by multiple cis-acting elements. Mol Cell Biol. 1987 Jul;7(7):2578–2587. doi: 10.1128/mcb.7.7.2578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hardy S., Shenk T. Adenoviral control regions activated by E1A and the cAMP response element bind to the same factor. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4171–4175. doi: 10.1073/pnas.85.12.4171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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]
  20. Hurst H. C., Jones N. C. Identification of factors that interact with the E1A-inducible adenovirus E3 promoter. Genes Dev. 1987 Dec;1(10):1132–1146. doi: 10.1101/gad.1.10.1132. [DOI] [PubMed] [Google Scholar]
  21. Imagawa M., Chiu R., Karin M. Transcription factor AP-2 mediates induction by two different signal-transduction pathways: protein kinase C and cAMP. Cell. 1987 Oct 23;51(2):251–260. doi: 10.1016/0092-8674(87)90152-8. [DOI] [PubMed] [Google Scholar]
  22. Jones N. C., Rigby P. W., Ziff E. B. Trans-acting protein factors and the regulation of eukaryotic transcription: lessons from studies on DNA tumor viruses. Genes Dev. 1988 Mar;2(3):267–281. doi: 10.1101/gad.2.3.267. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. Jungmann R. A., Russell D. H. Cyclic AMP, cyclic AMP-dependent protein kinase, and the regulation of gene expression. Life Sci. 1977 Jun 1;20(11):1787–1797. doi: 10.1016/0024-3205(77)90213-2. [DOI] [PubMed] [Google Scholar]
  25. Lee K. A., Green M. R. A cellular transcription factor E4F1 interacts with an E1a-inducible enhancer and mediates constitutive enhancer function in vitro. EMBO J. 1987 May;6(5):1345–1353. doi: 10.1002/j.1460-2075.1987.tb02374.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lee K. A., Hai T. Y., SivaRaman L., Thimmappaya B., Hurst H. C., Jones N. C., Green M. R. A cellular protein, activating transcription factor, activates transcription of multiple E1A-inducible adenovirus early promoters. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8355–8359. doi: 10.1073/pnas.84.23.8355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Leff T., Corden J., Elkaim R., Sassone-Corsi P. Transcriptional analysis of the adenovirus-5 EIII promoter: absence of sequence specificity for stimulation by EIa gene products. Nucleic Acids Res. 1985 Feb 25;13(4):1209–1221. doi: 10.1093/nar/13.4.1209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Lewis E. J., Harrington C. A., Chikaraishi D. M. Transcriptional regulation of the tyrosine hydroxylase gene by glucocorticoid and cyclic AMP. Proc Natl Acad Sci U S A. 1987 Jun;84(11):3550–3554. doi: 10.1073/pnas.84.11.3550. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Leza M. A., Hearing P. Cellular transcription factor binds to adenovirus early region promoters and to a cyclic AMP response element. J Virol. 1988 Aug;62(8):3003–3013. doi: 10.1128/jvi.62.8.3003-3013.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lin Y. S., Green M. R. Interaction of a common cellular transcription factor, ATF, with regulatory elements in both E1a- and cyclic AMP-inducible promoters. Proc Natl Acad Sci U S A. 1988 May;85(10):3396–3400. doi: 10.1073/pnas.85.10.3396. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Montminy M. R., Bilezikjian L. M. Binding of a nuclear protein to the cyclic-AMP response element of the somatostatin gene. Nature. 1987 Jul 9;328(6126):175–178. doi: 10.1038/328175a0. [DOI] [PubMed] [Google Scholar]
  33. Montminy M. R., Sevarino K. A., Wagner J. A., Mandel G., Goodman R. H. Identification of a cyclic-AMP-responsive element within the rat somatostatin gene. Proc Natl Acad Sci U S A. 1986 Sep;83(18):6682–6686. doi: 10.1073/pnas.83.18.6682. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Raychaudhuri P., Rooney R., Nevins J. R. Identification of an E1A-inducible cellular factor that interacts with regulatory sequences within the adenovirus E4 promoter. EMBO J. 1987 Dec 20;6(13):4073–4081. doi: 10.1002/j.1460-2075.1987.tb02753.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Roesler W. J., Vandenbark G. R., Hanson R. W. Cyclic AMP and the induction of eukaryotic gene transcription. J Biol Chem. 1988 Jul 5;263(19):9063–9066. [PubMed] [Google Scholar]
  36. Rosenfeld M. G., Barrieux A. Regulation of protein synthesis by polypeptide hormones and cyclic AMP. Adv Cyclic Nucleotide Res. 1979;11:205–264. [PubMed] [Google Scholar]
  37. Sassone-Corsi P. Cyclic AMP induction of early adenovirus promoters involves sequences required for E1A trans-activation. Proc Natl Acad Sci U S A. 1988 Oct;85(19):7192–7196. doi: 10.1073/pnas.85.19.7192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Silver B. J., Bokar J. A., Virgin J. B., Vallen E. A., Milsted A., Nilson J. H. Cyclic AMP regulation of the human glycoprotein hormone alpha-subunit gene is mediated by an 18-base-pair element. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2198–2202. doi: 10.1073/pnas.84.8.2198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Strickland S., Smith K. K., Marotti K. R. Hormonal induction of differentiation in teratocarcinoma stem cells: generation of parietal endoderm by retinoic acid and dibutyryl cAMP. Cell. 1980 Sep;21(2):347–355. doi: 10.1016/0092-8674(80)90471-7. [DOI] [PubMed] [Google Scholar]
  40. Tsukada T., Fink J. S., Mandel G., Goodman R. H. Identification of a region in the human vasoactive intestinal polypeptide gene responsible for regulation by cyclic AMP. J Biol Chem. 1987 Jun 25;262(18):8743–8747. [PubMed] [Google Scholar]
  41. Wigler M., Silverstein S., Lee L. S., Pellicer A., Cheng Y. c., Axel R. Transfer of purified herpes virus thymidine kinase gene to cultured mouse cells. Cell. 1977 May;11(1):223–232. doi: 10.1016/0092-8674(77)90333-6. [DOI] [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. Yamamoto K. K., Gonzalez G. A., Biggs W. H., 3rd, Montminy M. R. Phosphorylation-induced binding and transcriptional efficacy of nuclear factor CREB. Nature. 1988 Aug 11;334(6182):494–498. doi: 10.1038/334494a0. [DOI] [PubMed] [Google Scholar]
  44. Yamamoto K. R. Steroid receptor regulated transcription of specific genes and gene networks. Annu Rev Genet. 1985;19:209–252. doi: 10.1146/annurev.ge.19.120185.001233. [DOI] [PubMed] [Google Scholar]
  45. 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]
  46. Zajchowski D. A., Boeuf H., Kédinger C. The adenovirus-2 early EIIa transcription unit possesses two overlapping promoters with different sequence requirements for EIa-dependent stimulation. EMBO J. 1985 May;4(5):1293–1300. doi: 10.1002/j.1460-2075.1985.tb03775.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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