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. 1990 Aug;87(15):5878–5882. doi: 10.1073/pnas.87.15.5878

DNA octamer element can confer E1A trans-activation, and adenovirus infection results in a stimulation of the DNA-binding activity of OTF-1/NFIII factor.

S P Chellappan 1, J R Nevins 1
PMCID: PMC54432  PMID: 2143023

Abstract

Adenovirus E1A-dependent trans-activation of viral transcription involves the utilization and alteration of multiple sequence-specific transcription factors. Cellular genes are also activated by E1A, one example being the immunoglobulin heavy-chain locus when assayed by transfection into fibroblast cells. We have explored the basis for the E1A-dependent activation of this cellular transcription unit. We demonstrate that the ATTTGCAT ("octamer") element found in the heavy-chain enhancer and promoter is a target for E1A trans-activation since this sequence can confer inducibility to the normally unresponsive simian virus 40 early promoter. In addition, adenovirus infection stimulates the DNA-binding activity of the ubiquitous octamer-specific factor, OTF-1, and we presume that this is the basis for the stimulation of transcription. Although there are no octamer elements in the adenovirus genome that are known to be important for transcription, there are octamer elements in the viral terminal repeat sequences. These elements bind the NFIII factor and are important for the initiation of DNA replication. Since the NFIII factor has been shown to be identical to OTF-1, we suggest that the stimulation of OTF-1/NFIII activity during an adenovirus infection may be important for efficient initiation of adenovirus DNA synthesis.

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Selected References

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

  1. Bagchi S., Raychaudhuri P., Nevins J. R. Phosphorylation-dependent activation of the adenovirus-inducible E2F transcription factor in a cell-free system. Proc Natl Acad Sci U S A. 1989 Jun;86(12):4352–4356. doi: 10.1073/pnas.86.12.4352. [DOI] [PMC free article] [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. Borrelli E., Hen R., Wasylyk C., Wasylyk B., Chambon P. The immunoglobulin heavy chain enhancer is stimulated by the adenovirus type 2 E1A products in mouse fibroblasts. Proc Natl Acad Sci U S A. 1986 May;83(9):2846–2849. doi: 10.1073/pnas.83.9.2846. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cullen B. R. Use of eukaryotic expression technology in the functional analysis of cloned genes. Methods Enzymol. 1987;152:684–704. doi: 10.1016/0076-6879(87)52074-2. [DOI] [PubMed] [Google Scholar]
  6. Feldman L. T., Imperiale M. J., Nevins J. R. Activation of early adenovirus transcription by the herpesvirus immediate early gene: evidence for a common cellular control factor. Proc Natl Acad Sci U S A. 1982 Aug;79(16):4952–4956. doi: 10.1073/pnas.79.16.4952. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ferguson B., Krippl B., Andrisani O., Jones N., Westphal H., Rosenberg M. E1A 13S and 12S mRNA products made in Escherichia coli both function as nucleus-localized transcription activators but do not directly bind DNA. Mol Cell Biol. 1985 Oct;5(10):2653–2661. doi: 10.1128/mcb.5.10.2653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gerster T., Roeder R. G. A herpesvirus trans-activating protein interacts with transcription factor OTF-1 and other cellular proteins. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6347–6351. doi: 10.1073/pnas.85.17.6347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. Hen R., Borrelli E., Chambon P. Repression of the immunoglobulin heavy chain enhancer by the adenovirus-2 E1A products. Science. 1985 Dec 20;230(4732):1391–1394. doi: 10.1126/science.2999984. [DOI] [PubMed] [Google Scholar]
  12. Hoeffler W. K., Kovelman R., Roeder R. G. Activation of transcription factor IIIC by the adenovirus E1A protein. Cell. 1988 Jun 17;53(6):907–920. doi: 10.1016/s0092-8674(88)90409-6. [DOI] [PubMed] [Google Scholar]
  13. Imperiale M. J., Hart R. P., Nevins J. R. An enhancer-like element in the adenovirus E2 promoter contains sequences essential for uninduced and E1A-induced transcription. Proc Natl Acad Sci U S A. 1985 Jan;82(2):381–385. doi: 10.1073/pnas.82.2.381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Imperiale M. J., Kao H. T., Feldman L. T., Nevins J. R., Strickland S. Common control of the heat shock gene and early adenovirus genes: evidence for a cellular E1A-like activity. Mol Cell Biol. 1984 May;4(5):867–874. doi: 10.1128/mcb.4.5.867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ito M., Sharma A., Lee A. S., Maxson R. Cell cycle regulation of H2b histone octamer DNA-binding activity in Chinese hamster lung fibroblasts. Mol Cell Biol. 1989 Feb;9(2):869–873. doi: 10.1128/mcb.9.2.869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Kovesdi I., Reichel R., Nevins J. R. Identification of a cellular transcription factor involved in E1A trans-activation. Cell. 1986 Apr 25;45(2):219–228. doi: 10.1016/0092-8674(86)90386-7. [DOI] [PubMed] [Google Scholar]
  18. LaBella F., Sive H. L., Roeder R. G., Heintz N. Cell-cycle regulation of a human histone H2b gene is mediated by the H2b subtype-specific consensus element. Genes Dev. 1988 Jan;2(1):32–39. doi: 10.1101/gad.2.1.32. [DOI] [PubMed] [Google Scholar]
  19. Lenardo M. J., Staudt L., Robbins P., Kuang A., Mulligan R. C., Baltimore D. Repression of the IgH enhancer in teratocarcinoma cells associated with a novel octamer factor. Science. 1989 Jan 27;243(4890):544–546. doi: 10.1126/science.2536195. [DOI] [PubMed] [Google Scholar]
  20. McKnight J. L., Kristie T. M., Roizman B. Binding of the virion protein mediating alpha gene induction in herpes simplex virus 1-infected cells to its cis site requires cellular proteins. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7061–7065. doi: 10.1073/pnas.84.20.7061. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Müller U., Roberts M. P., Engel D. A., Doerfler W., Shenk T. Induction of transcription factor AP-1 by adenovirus E1A protein and cAMP. Genes Dev. 1989 Dec;3(12A):1991–2002. doi: 10.1101/gad.3.12a.1991. [DOI] [PubMed] [Google Scholar]
  22. Nevins J. R. Definition and mapping of adenovirus 2 nuclear transcription. Methods Enzymol. 1980;65(1):768–785. doi: 10.1016/s0076-6879(80)65072-1. [DOI] [PubMed] [Google Scholar]
  23. Nevins J. R. Mechanism of activation of early viral transcription by the adenovirus E1A gene product. Cell. 1981 Oct;26(2 Pt 2):213–220. doi: 10.1016/0092-8674(81)90304-4. [DOI] [PubMed] [Google Scholar]
  24. Nevins J. R. Mechanisms of viral-mediated trans-activation of transcription. Adv Virus Res. 1989;37:35–83. doi: 10.1016/s0065-3527(08)60832-5. [DOI] [PubMed] [Google Scholar]
  25. O'Hare P., Goding C. R., Haigh A. Direct combinatorial interaction between a herpes simplex virus regulatory protein and a cellular octamer-binding factor mediates specific induction of virus immediate-early gene expression. EMBO J. 1988 Dec 20;7(13):4231–4238. doi: 10.1002/j.1460-2075.1988.tb03320.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. O'Neill E. A., Fletcher C., Burrow C. R., Heintz N., Roeder R. G., Kelly T. J. Transcription factor OTF-1 is functionally identical to the DNA replication factor NF-III. Science. 1988 Sep 2;241(4870):1210–1213. doi: 10.1126/science.3413485. [DOI] [PubMed] [Google Scholar]
  27. O'Neill E. A., Kelly T. J. Purification and characterization of nuclear factor III (origin recognition protein C), a sequence-specific DNA binding protein required for efficient initiation of adenovirus DNA replication. J Biol Chem. 1988 Jan 15;263(2):931–937. [PubMed] [Google Scholar]
  28. Preston C. M., Frame M. C., Campbell M. E. A complex formed between cell components and an HSV structural polypeptide binds to a viral immediate early gene regulatory DNA sequence. Cell. 1988 Feb 12;52(3):425–434. doi: 10.1016/s0092-8674(88)80035-7. [DOI] [PubMed] [Google Scholar]
  29. Pruijn G. J., van Driel W., van der Vliet P. C. Nuclear factor III, a novel sequence-specific DNA-binding protein from HeLa cells stimulating adenovirus DNA replication. Nature. 1986 Aug 14;322(6080):656–659. doi: 10.1038/322656a0. [DOI] [PubMed] [Google Scholar]
  30. Raychaudhuri P., Bagchi S., Nevins J. R. DNA-binding activity of the adenovirus-induced E4F transcription factor is regulated by phosphorylation. Genes Dev. 1989 May;3(5):620–627. doi: 10.1101/gad.3.5.620. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Reichel R., Kovesdi I., Nevins J. R. Developmental control of a promoter-specific factor that is also regulated by the E1A gene product. Cell. 1987 Feb 13;48(3):501–506. doi: 10.1016/0092-8674(87)90200-5. [DOI] [PubMed] [Google Scholar]
  33. Rosenfeld P. J., O'Neill E. A., Wides R. J., Kelly T. J. Sequence-specific interactions between cellular DNA-binding proteins and the adenovirus origin of DNA replication. Mol Cell Biol. 1987 Feb;7(2):875–886. doi: 10.1128/mcb.7.2.875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Schöler H. R., Hatzopoulos A. K., Balling R., Suzuki N., Gruss P. A family of octamer-specific proteins present during mouse embryogenesis: evidence for germline-specific expression of an Oct factor. EMBO J. 1989 Sep;8(9):2543–2550. doi: 10.1002/j.1460-2075.1989.tb08392.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Simon M. C., Fisch T. M., Benecke B. J., Nevins J. R., Heintz N. Definition of multiple, functionally distinct TATA elements, one of which is a target in the hsp70 promoter for E1A regulation. Cell. 1988 Mar 11;52(5):723–729. doi: 10.1016/0092-8674(88)90410-2. [DOI] [PubMed] [Google Scholar]
  36. Weeks D. L., Jones N. C. Adenovirus E3-early promoter: sequences required for activation by E1A. Nucleic Acids Res. 1985 Jul 25;13(14):5389–5402. doi: 10.1093/nar/13.14.5389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. Yee A. S., Raychaudhuri P., Jakoi L., Nevins J. R. The adenovirus-inducible factor E2F stimulates transcription after specific DNA binding. Mol Cell Biol. 1989 Feb;9(2):578–585. doi: 10.1128/mcb.9.2.578. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Yee A. S., Reichel R., Kovesdi I., Nevins J. R. Promoter interaction of the E1A-inducible factor E2F and its potential role in the formation of a multi-component complex. EMBO J. 1987 Jul;6(7):2061–2068. doi: 10.1002/j.1460-2075.1987.tb02471.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Yoshinaga S., Dean N., Han M., Berk A. J. Adenovirus stimulation of transcription by RNA polymerase III: evidence for an E1A-dependent increase in transcription factor IIIC concentration. EMBO J. 1986 Feb;5(2):343–354. doi: 10.1002/j.1460-2075.1986.tb04218.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Young K. S., Weigel R., Hiebert S., Nevins J. R. Adenovirus E1A-mediated negative control of genes activated during F9 differentiation. Mol Cell Biol. 1989 Jul;9(7):3109–3113. doi: 10.1128/mcb.9.7.3109. [DOI] [PMC free article] [PubMed] [Google Scholar]

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