Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1994 Dec;68(12):8288–8295. doi: 10.1128/jvi.68.12.8288-8295.1994

Stimulation of the adenovirus major late promoter in vitro by transcription factor USF is enhanced by the adenovirus DNA binding protein.

D C Zijderveld 1, F d'Adda di Fagagna 1, M Giacca 1, H T Timmers 1, P C van der Vliet 1
PMCID: PMC237297  PMID: 7966622

Abstract

Previous studies have shown that the sequence-independent adenovirus DNA binding protein (DBP) increases transcription from several promoters, notably from the adenovirus major late promoter (MLP) and the adeno-associated virus P5 promoter, both of which contain a USF/MLTF binding site. In order to study this mechanism, we have investigated the effects of DBP on the binding of USF/MLTF to MLP and on transcription from MLP by a reconstituted in vitro system. As shown by gel retardation and DNase I footprinting, upon saturation of DNA, DBP enhances the binding affinity of USF43 to the promoter three- to fourfold without changing the footprint pattern. In contrast, the binding of the TATA box binding protein to the promoter is not influenced by DBP. No protein-protein interactions between DBP and USF43 could be observed in the absence of DNA, suggesting that enhanced binding is caused by a change in DNA structure induced by the DBP-DNA complex. Employing a transcription system reconstituted with purified general transcription factors, we show that USF43 enhances basal transcription and that USF43-dependent transcription is further increased by DBP, while DBP alone does not have an effect on basal transcription. Our results suggest that transcription enhancement by DBP is based on a specific increase in the binding of a transcription factor to a promoter through subtle changes in DNA structure, similar to the mechanism by which DBP stimulates the initiation of DNA replication.

Full text

PDF
8289

Images in this article

8290Image
on p.8290
8291Image
on p.8291
8292Image
on p.8292
8293Image
on p.8293

Selected References

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

  1. Blanar M. A., Rutter W. J. Interaction cloning: identification of a helix-loop-helix zipper protein that interacts with c-Fos. Science. 1992 May 15;256(5059):1014–1018. doi: 10.1126/science.1589769. [DOI] [PubMed] [Google Scholar]
  2. Bosher J., Leith I. R., Temperley S. M., Wells M., Hay R. T. The DNA-binding domain of nuclear factor I is sufficient to cooperate with the adenovirus type 2 DNA-binding protein in viral DNA replication. J Gen Virol. 1991 Dec;72(Pt 12):2975–2980. doi: 10.1099/0022-1317-72-12-2975. [DOI] [PubMed] [Google Scholar]
  3. Carr C. S., Sharp P. A. A helix-loop-helix protein related to the immunoglobulin E box-binding proteins. Mol Cell Biol. 1990 Aug;10(8):4384–4388. doi: 10.1128/mcb.10.8.4384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Carthew R. W., Chodosh L. A., Sharp P. A. An RNA polymerase II transcription factor binds to an upstream element in the adenovirus major late promoter. Cell. 1985 Dec;43(2 Pt 1):439–448. doi: 10.1016/0092-8674(85)90174-6. [DOI] [PubMed] [Google Scholar]
  5. Carthew R. W., Chodosh L. A., Sharp P. A. The major late transcription factor binds to and activates the mouse metallothionein I promoter. Genes Dev. 1987 Nov;1(9):973–980. doi: 10.1101/gad.1.9.973. [DOI] [PubMed] [Google Scholar]
  6. Chang L. S., Shenk T. The adenovirus DNA-binding protein stimulates the rate of transcription directed by adenovirus and adeno-associated virus promoters. J Virol. 1990 May;64(5):2103–2109. doi: 10.1128/jvi.64.5.2103-2109.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chase J. W., Williams K. R. Single-stranded DNA binding proteins required for DNA replication. Annu Rev Biochem. 1986;55:103–136. doi: 10.1146/annurev.bi.55.070186.000535. [DOI] [PubMed] [Google Scholar]
  8. Chatterjee P. K., Vayda M. E., Flint S. J. Adenoviral protein VII packages intracellular viral DNA throughout the early phase of infection. EMBO J. 1986 Jul;5(7):1633–1644. doi: 10.1002/j.1460-2075.1986.tb04406.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Chodosh L. A., Carthew R. W., Morgan J. G., Crabtree G. R., Sharp P. A. The adenovirus major late transcription factor activates the rat gamma-fibrinogen promoter. Science. 1987 Oct 30;238(4827):684–688. doi: 10.1126/science.3672119. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Cleat P. H., Hay R. T. Co-operative interactions between NFI and the adenovirus DNA binding protein at the adenovirus origin of replication. EMBO J. 1989 Jun;8(6):1841–1848. doi: 10.1002/j.1460-2075.1989.tb03579.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cleghon V., Voelkerding K., Morin N., Delsert C., Klessig D. F. Isolation and characterization of a viable adenovirus mutant defective in nuclear transport of the DNA-binding protein. J Virol. 1989 May;63(5):2289–2299. doi: 10.1128/jvi.63.5.2289-2299.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Du H., Roy A. L., Roeder R. G. Human transcription factor USF stimulates transcription through the initiator elements of the HIV-1 and the Ad-ML promoters. EMBO J. 1993 Feb;12(2):501–511. doi: 10.1002/j.1460-2075.1993.tb05682.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Giacca M., Gutierrez M. I., Menzo S., d'Adda di Fagagna F., Falaschi A. A human binding site for transcription factor USF/MLTF mimics the negative regulatory element of human immunodeficiency virus type 1. Virology. 1992 Jan;186(1):133–147. doi: 10.1016/0042-6822(92)90067-y. [DOI] [PubMed] [Google Scholar]
  15. Gregor P. D., Sawadogo M., Roeder R. G. The adenovirus major late transcription factor USF is a member of the helix-loop-helix group of regulatory proteins and binds to DNA as a dimer. Genes Dev. 1990 Oct;4(10):1730–1740. doi: 10.1101/gad.4.10.1730. [DOI] [PubMed] [Google Scholar]
  16. Handa H., Kingston R. E., Sharp P. A. Inhibition of adenovirus early region IV transcription in vitro by a purified viral DNA binding protein. Nature. 1983 Apr 7;302(5908):545–547. doi: 10.1038/302545a0. [DOI] [PubMed] [Google Scholar]
  17. Hay R. T., Russell W. C. Recognition mechanisms in the synthesis of animal virus DNA. Biochem J. 1989 Feb 15;258(1):3–16. doi: 10.1042/bj2580003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kelly T. J., Wold M. S., Li J. Initiation of viral DNA replication. Adv Virus Res. 1988;34:1–42. doi: 10.1016/s0065-3527(08)60514-x. [DOI] [PubMed] [Google Scholar]
  19. Kirschbaum B. J., Pognonec P., Roeder R. G. Definition of the transcriptional activation domain of recombinant 43-kilodalton USF. Mol Cell Biol. 1992 Nov;12(11):5094–5101. doi: 10.1128/mcb.12.11.5094. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kitchingman G. R. Sequence of the DNA-binding protein of a human subgroup E adenovirus (type 4): comparisons with subgroup A (type 12), subgroup B (type 7), and subgroup C (type 5). Virology. 1985 Oct 15;146(1):90–101. doi: 10.1016/0042-6822(85)90055-8. [DOI] [PubMed] [Google Scholar]
  21. Kruijer W., van Schaik F. M., Sussenbach J. S. Structure and organization of the gene coding for the DNA binding protein of adenovirus type 5. Nucleic Acids Res. 1981 Sep 25;9(18):4439–4457. doi: 10.1093/nar/9.18.4439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kuil M. E., van Amerongen H., van der Vliet P. C., van Grondelle R. Complex formation between the adenovirus DNA-binding protein and single-stranded poly(rA). Cooperativity and salt dependence. Biochemistry. 1989 Dec 12;28(25):9795–9800. doi: 10.1021/bi00451a038. [DOI] [PubMed] [Google Scholar]
  23. Mansour S. L., Grodzicker T., Tjian R. Downstream sequences affect transcription initiation from the adenovirus major late promoter. Mol Cell Biol. 1986 Jul;6(7):2684–2694. doi: 10.1128/mcb.6.7.2684. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Miyamoto N. G., Moncollin V., Wintzerith M., Hen R., Egly J. M., Chambon P. Stimulation of in vitro transcription by the upstream element of the adenovirus-2 major late promoter involves a specific factor. Nucleic Acids Res. 1984 Dec 11;12(23):8779–8799. doi: 10.1093/nar/12.23.8779. [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. Morin N., Delsert C., Klessig D. F. Mutations that affect phosphorylation of the adenovirus DNA-binding protein alter its ability to enhance its own synthesis. J Virol. 1989 Dec;63(12):5228–5237. doi: 10.1128/jvi.63.12.5228-5237.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Morin N., Delsert C., Klessig D. F. Nuclear localization of the adenovirus DNA-binding protein: requirement for two signals and complementation during viral infection. Mol Cell Biol. 1989 Oct;9(10):4372–4380. doi: 10.1128/mcb.9.10.4372. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Paonessa G., Gounari F., Frank R., Cortese R. Purification of a NF1-like DNA-binding protein from rat liver and cloning of the corresponding cDNA. EMBO J. 1988 Oct;7(10):3115–3123. doi: 10.1002/j.1460-2075.1988.tb03178.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Peritz L. N., Fodor E. J., Silversides D. W., Cattini P. A., Baxter J. D., Eberhardt N. L. The human growth hormone gene contains both positive and negative control elements. J Biol Chem. 1988 Apr 15;263(11):5005–5007. [PubMed] [Google Scholar]
  31. Pognonec P., Roeder R. G. Recombinant 43-kDa USF binds to DNA and activates transcription in a manner indistinguishable from that of natural 43/44-kDa USF. Mol Cell Biol. 1991 Oct;11(10):5125–5136. doi: 10.1128/mcb.11.10.5125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Roy A. L., Meisterernst M., Pognonec P., Roeder R. G. Cooperative interaction of an initiator-binding transcription initiation factor and the helix-loop-helix activator USF. Nature. 1991 Nov 21;354(6350):245–248. doi: 10.1038/354245a0. [DOI] [PubMed] [Google Scholar]
  33. Sawadogo M. Multiple forms of the human gene-specific transcription factor USF. II. DNA binding properties and transcriptional activity of the purified HeLa USF. J Biol Chem. 1988 Aug 25;263(24):11994–12001. [PubMed] [Google Scholar]
  34. 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]
  35. Sawadogo M., Van Dyke M. W., Gregor P. D., Roeder R. G. Multiple forms of the human gene-specific transcription factor USF. I. Complete purification and identification of USF from HeLa cell nuclei. J Biol Chem. 1988 Aug 25;263(24):11985–11993. [PubMed] [Google Scholar]
  36. Sirito M., Lin Q., Maity T., Sawadogo M. Ubiquitous expression of the 43- and 44-kDa forms of transcription factor USF in mammalian cells. Nucleic Acids Res. 1994 Feb 11;22(3):427–433. doi: 10.1093/nar/22.3.427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Stillman B. Initiation of eukaryotic DNA replication in vitro. Annu Rev Cell Biol. 1989;5:197–245. doi: 10.1146/annurev.cb.05.110189.001213. [DOI] [PubMed] [Google Scholar]
  38. Stuiver M. H., Bergsma W. G., Arnberg A. C., van Amerongen H., van Grondelle R., van der Vliet P. C. Structural alterations of double-stranded DNA in complex with the adenovirus DNA-binding protein. Implications for its function in DNA replication. J Mol Biol. 1992 Jun 20;225(4):999–1011. doi: 10.1016/0022-2836(92)90100-x. [DOI] [PubMed] [Google Scholar]
  39. Stuiver M. H., van der Vliet P. C. Adenovirus DNA-binding protein forms a multimeric protein complex with double-stranded DNA and enhances binding of nuclear factor I. J Virol. 1990 Jan;64(1):379–386. doi: 10.1128/jvi.64.1.379-386.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sugawara K., Gilead Z., Green M. Purification and molecular characterization of adenovirus type 2 DNA-binding protein. J Virol. 1977 Jan;21(1):338–346. doi: 10.1128/jvi.21.1.338-346.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Thanos D., Maniatis T. The high mobility group protein HMG I(Y) is required for NF-kappa B-dependent virus induction of the human IFN-beta gene. Cell. 1992 Nov 27;71(5):777–789. doi: 10.1016/0092-8674(92)90554-p. [DOI] [PubMed] [Google Scholar]
  42. Timmers H. T., Sharp P. A. The mammalian TFIID protein is present in two functionally distinct complexes. Genes Dev. 1991 Nov;5(11):1946–1956. doi: 10.1101/gad.5.11.1946. [DOI] [PubMed] [Google Scholar]
  43. Timmers H. T. Transcription initiation by RNA polymerase II does not require hydrolysis of the beta-gamma phosphoanhydride bond of ATP. EMBO J. 1994 Jan 15;13(2):391–399. doi: 10.1002/j.1460-2075.1994.tb06273.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Toth M., Doerfler W., Shenk T. Adenovirus DNA replication facilitates binding of the MLTF/USF transcription factor to the viral major late promoter within infected cells. Nucleic Acids Res. 1992 Oct 11;20(19):5143–5148. doi: 10.1093/nar/20.19.5143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Tucker P. A., Tsernoglou D., Tucker A. D., Coenjaerts F. E., Leenders H., van der Vliet P. C. Crystal structure of the adenovirus DNA binding protein reveals a hook-on model for cooperative DNA binding. EMBO J. 1994 Jul 1;13(13):2994–3002. doi: 10.1002/j.1460-2075.1994.tb06598.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Tóth E. C., Marusic L., Ochem A., Patthy A., Pongor S., Giacca M., Falaschi A. Interactions of USF and Ku antigen with a human DNA region containing a replication origin. Nucleic Acids Res. 1993 Jul 11;21(14):3257–3263. doi: 10.1093/nar/21.14.3257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Watt F., Molloy P. L. High mobility group proteins 1 and 2 stimulate binding of a specific transcription factor to the adenovirus major late promoter. Nucleic Acids Res. 1988 Feb 25;16(4):1471–1486. doi: 10.1093/nar/16.4.1471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Workman J. L., Roeder R. G., Kingston R. E. An upstream transcription factor, USF (MLTF), facilitates the formation of preinitiation complexes during in vitro chromatin assembly. EMBO J. 1990 Apr;9(4):1299–1308. doi: 10.1002/j.1460-2075.1990.tb08239.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Yu Y. T., Manley J. L. Generation and functional analyses for base-substitution mutants of the adenovirus 2 major late promoter. Nucleic Acids Res. 1984 Dec 21;12(24):9309–9321. doi: 10.1093/nar/12.24.9309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Zijderveld D. C., Stuiver M. H., van der Vliet P. C. The adenovirus DNA binding protein enhances intermolecular DNA renaturation but inhibits intramolecular DNA renaturation. Nucleic Acids Res. 1993 Jun 11;21(11):2591–2598. doi: 10.1093/nar/21.11.2591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Zijderveld D. C., van der Vliet P. C. Helix-destabilizing properties of the adenovirus DNA-binding protein. J Virol. 1994 Feb;68(2):1158–1164. doi: 10.1128/jvi.68.2.1158-1164.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. van der Vliet P. C., Levine A. J. DNA-binding proteins specific for cells infected by adenovirus. Nat New Biol. 1973 Dec 12;246(154):170–174. doi: 10.1038/newbio246170a0. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES