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. 1996 Dec 1;24(23):4751–4758. doi: 10.1093/nar/24.23.4751

Nucleosome assembly on the human c-fos promoter interferes with transcription factor binding.

C Schild-Poulter 1, P Sassone-Corsi 1, M Granger-Schnarr 1, M Schnarr 1
PMCID: PMC146296  PMID: 8972862

Abstract

cAMP-responsive-element (CRE)-binding factors interaction with nucleosomal DNA has been investigated in vitro on the human c-fos promoter. Analysis of nucleosome reconstitution of this promoter shows a preferential nucleosome positioning on the proximal promoter sequences, including the CRE centered at -60 relative to the start site of transcription. CRE-binding protein (CREB) and modulator protein (CREM) are unable to interact with their recognition site incorporated in a nucleosome. However, competition between transcription factor binding and nucleosome assembly allows CREM binding and induces important modifications in the nucleosomal structure suggesting the displacement of nucleosomes. These findings imply that binding of transcription factors to the CRE prior to cAMP induction might be required to prevent the incorporation of this element in a nucleosome.

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Selected References

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  1. Adams C. C., Workman J. L. Nucleosome displacement in transcription. Cell. 1993 Feb 12;72(3):305–308. doi: 10.1016/0092-8674(93)90109-4. [DOI] [PubMed] [Google Scholar]
  2. Almouzni G., Méchali M., Wolffe A. P. Competition between transcription complex assembly and chromatin assembly on replicating DNA. EMBO J. 1990 Feb;9(2):573–582. doi: 10.1002/j.1460-2075.1990.tb08145.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Archer T. K., Cordingley M. G., Wolford R. G., Hager G. L. Transcription factor access is mediated by accurately positioned nucleosomes on the mouse mammary tumor virus promoter. Mol Cell Biol. 1991 Feb;11(2):688–698. doi: 10.1128/mcb.11.2.688. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blomquist P., Li Q., Wrange O. The affinity of nuclear factor 1 for its DNA site is drastically reduced by nucleosome organization irrespective of its rotational or translational position. J Biol Chem. 1996 Jan 5;271(1):153–159. doi: 10.1074/jbc.271.1.153. [DOI] [PubMed] [Google Scholar]
  5. Buttinelli M., Di Mauro E., Negri R. Multiple nucleosome positioning with unique rotational setting for the Saccharomyces cerevisiae 5S rRNA gene in vitro and in vivo. Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9315–9319. doi: 10.1073/pnas.90.20.9315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Czarnota G. J., Ottensmeyer F. P. Structural states of the nucleosome. J Biol Chem. 1996 Feb 16;271(7):3677–3683. doi: 10.1074/jbc.271.7.3677. [DOI] [PubMed] [Google Scholar]
  7. Deschamps J., Meijlink F., Verma I. M. Identification of a transcriptional enhancer element upstream from the proto-oncogene fos. Science. 1985 Dec 6;230(4730):1174–1177. doi: 10.1126/science.3865371. [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. Dey A., Nebert D. W., Ozato K. The AP-1 site and the cAMP- and serum response elements of the c-fos gene are constitutively occupied in vivo. DNA Cell Biol. 1991 Sep;10(7):537–544. doi: 10.1089/dna.1991.10.537. [DOI] [PubMed] [Google Scholar]
  10. Dong F., Hansen J. C., van Holde K. E. DNA and protein determinants of nucleosome positioning on sea urchin 5S rRNA gene sequences in vitro. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5724–5728. doi: 10.1073/pnas.87.15.5724. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dong F., Nelson C., Ausio J. Analysis of the changes in the structure and hydration of the nucleosome core particle at moderate ionic strengths. Biochemistry. 1990 Nov 27;29(47):10710–10716. doi: 10.1021/bi00499a020. [DOI] [PubMed] [Google Scholar]
  12. Fascher K. D., Schmitz J., Hörz W. Role of trans-activating proteins in the generation of active chromatin at the PHO5 promoter in S. cerevisiae. EMBO J. 1990 Aug;9(8):2523–2528. doi: 10.1002/j.1460-2075.1990.tb07432.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fedor M. J., Lue N. F., Kornberg R. D. Statistical positioning of nucleosomes by specific protein-binding to an upstream activating sequence in yeast. J Mol Biol. 1988 Nov 5;204(1):109–127. doi: 10.1016/0022-2836(88)90603-1. [DOI] [PubMed] [Google Scholar]
  14. Felsenfeld G. Chromatin as an essential part of the transcriptional mechanism. Nature. 1992 Jan 16;355(6357):219–224. doi: 10.1038/355219a0. [DOI] [PubMed] [Google Scholar]
  15. Foulkes N. S., Laoide B. M., Schlotter F., Sassone-Corsi P. Transcriptional antagonist cAMP-responsive element modulator (CREM) down-regulates c-fos cAMP-induced expression. Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5448–5452. doi: 10.1073/pnas.88.12.5448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Foulkes N. S., Sassone-Corsi P. More is better: activators and repressors from the same gene. Cell. 1992 Feb 7;68(3):411–414. doi: 10.1016/0092-8674(92)90178-f. [DOI] [PubMed] [Google Scholar]
  17. Grunstein M. Histone function in transcription. Annu Rev Cell Biol. 1990;6:643–678. doi: 10.1146/annurev.cb.06.110190.003235. [DOI] [PubMed] [Google Scholar]
  18. Hayes J. J., Tullius T. D., Wolffe A. P. The structure of DNA in a nucleosome. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7405–7409. doi: 10.1073/pnas.87.19.7405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hayes J. J., Wolffe A. P. The interaction of transcription factors with nucleosomal DNA. Bioessays. 1992 Sep;14(9):597–603. doi: 10.1002/bies.950140905. [DOI] [PubMed] [Google Scholar]
  20. Herrera R. E., Shaw P. E., Nordheim A. Occupation of the c-fos serum response element in vivo by a multi-protein complex is unaltered by growth factor induction. Nature. 1989 Jul 6;340(6228):68–70. doi: 10.1038/340068a0. [DOI] [PubMed] [Google Scholar]
  21. Hurst H. C. Transcription factors. 1: bZIP proteins. Protein Profile. 1994;1(2):123–168. [PubMed] [Google Scholar]
  22. Janknecht R., Cahill M. A., Nordheim A. Signal integration at the c-fos promoter. Carcinogenesis. 1995 Mar;16(3):443–450. doi: 10.1093/carcin/16.3.443. [DOI] [PubMed] [Google Scholar]
  23. Kamakaka R. T., Bulger M., Kadonaga J. T. Potentiation of RNA polymerase II transcription by Gal4-VP16 during but not after DNA replication and chromatin assembly. Genes Dev. 1993 Sep;7(9):1779–1795. doi: 10.1101/gad.7.9.1779. [DOI] [PubMed] [Google Scholar]
  24. Kornberg R. D., Lorch Y. Interplay between chromatin structure and transcription. Curr Opin Cell Biol. 1995 Jun;7(3):371–375. doi: 10.1016/0955-0674(95)80092-1. [DOI] [PubMed] [Google Scholar]
  25. Kwon H., Imbalzano A. N., Khavari P. A., Kingston R. E., Green M. R. Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex. Nature. 1994 Aug 11;370(6489):477–481. doi: 10.1038/370477a0. [DOI] [PubMed] [Google Scholar]
  26. Lee D. Y., Hayes J. J., Pruss D., Wolffe A. P. A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell. 1993 Jan 15;72(1):73–84. doi: 10.1016/0092-8674(93)90051-q. [DOI] [PubMed] [Google Scholar]
  27. Lee K. A., Masson N. Transcriptional regulation by CREB and its relatives. Biochim Biophys Acta. 1993 Sep 23;1174(3):221–233. doi: 10.1016/0167-4781(93)90191-f. [DOI] [PubMed] [Google Scholar]
  28. Lewin B. Chromatin and gene expression: constant questions, but changing answers. Cell. 1994 Nov 4;79(3):397–406. doi: 10.1016/0092-8674(94)90249-6. [DOI] [PubMed] [Google Scholar]
  29. Lu Q., Wallrath L. L., Granok H., Elgin S. C. (CT)n (GA)n repeats and heat shock elements have distinct roles in chromatin structure and transcriptional activation of the Drosophila hsp26 gene. Mol Cell Biol. 1993 May;13(5):2802–2814. doi: 10.1128/mcb.13.5.2802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. McPherson C. E., Shim E. Y., Friedman D. S., Zaret K. S. An active tissue-specific enhancer and bound transcription factors existing in a precisely positioned nucleosomal array. Cell. 1993 Oct 22;75(2):387–398. doi: 10.1016/0092-8674(93)80079-t. [DOI] [PubMed] [Google Scholar]
  31. Meersseman G., Pennings S., Bradbury E. M. Mobile nucleosomes--a general behavior. EMBO J. 1992 Aug;11(8):2951–2959. doi: 10.1002/j.1460-2075.1992.tb05365.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Molina C. A., Foulkes N. S., Lalli E., Sassone-Corsi P. Inducibility and negative autoregulation of CREM: an alternative promoter directs the expression of ICER, an early response repressor. Cell. 1993 Dec 3;75(5):875–886. doi: 10.1016/0092-8674(93)90532-u. [DOI] [PubMed] [Google Scholar]
  33. Nichols M., Weih F., Schmid W., DeVack C., Kowenz-Leutz E., Luckow B., Boshart M., Schütz G. Phosphorylation of CREB affects its binding to high and low affinity sites: implications for cAMP induced gene transcription. EMBO J. 1992 Sep;11(9):3337–3346. doi: 10.1002/j.1460-2075.1992.tb05412.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Perlmann T., Wrange O. Specific glucocorticoid receptor binding to DNA reconstituted in a nucleosome. EMBO J. 1988 Oct;7(10):3073–3079. doi: 10.1002/j.1460-2075.1988.tb03172.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Peterson C. L., Tamkun J. W. The SWI-SNF complex: a chromatin remodeling machine? Trends Biochem Sci. 1995 Apr;20(4):143–146. doi: 10.1016/s0968-0004(00)88990-2. [DOI] [PubMed] [Google Scholar]
  36. Piña B., Brüggemeier U., Beato M. Nucleosome positioning modulates accessibility of regulatory proteins to the mouse mammary tumor virus promoter. Cell. 1990 Mar 9;60(5):719–731. doi: 10.1016/0092-8674(90)90087-u. [DOI] [PubMed] [Google Scholar]
  37. Robertson L. M., Kerppola T. K., Vendrell M., Luk D., Smeyne R. J., Bocchiaro C., Morgan J. I., Curran T. Regulation of c-fos expression in transgenic mice requires multiple interdependent transcription control elements. Neuron. 1995 Feb;14(2):241–252. doi: 10.1016/0896-6273(95)90282-1. [DOI] [PubMed] [Google Scholar]
  38. Roth S. Y., Dean A., Simpson R. T. Yeast alpha 2 repressor positions nucleosomes in TRP1/ARS1 chromatin. Mol Cell Biol. 1990 May;10(5):2247–2260. doi: 10.1128/mcb.10.5.2247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sassone-Corsi P., Visvader J., Ferland L., Mellon P. L., Verma I. M. Induction of proto-oncogene fos transcription through the adenylate cyclase pathway: characterization of a cAMP-responsive element. Genes Dev. 1988 Dec;2(12A):1529–1538. doi: 10.1101/gad.2.12a.1529. [DOI] [PubMed] [Google Scholar]
  40. Schild C., Claret F. X., Wahli W., Wolffe A. P. A nucleosome-dependent static loop potentiates estrogen-regulated transcription from the Xenopus vitellogenin B1 promoter in vitro. EMBO J. 1993 Feb;12(2):423–433. doi: 10.1002/j.1460-2075.1993.tb05674.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Simon R. H., Felsenfeld G. A new procedure for purifying histone pairs H2A + H2B and H3 + H4 from chromatin using hydroxylapatite. Nucleic Acids Res. 1979 Feb;6(2):689–696. doi: 10.1093/nar/6.2.689. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Simpson R. T. Nucleosome positioning: occurrence, mechanisms, and functional consequences. Prog Nucleic Acid Res Mol Biol. 1991;40:143–184. doi: 10.1016/s0079-6603(08)60841-7. [DOI] [PubMed] [Google Scholar]
  43. Svaren J., Chalkley R. The structure and assembly of active chromatin. Trends Genet. 1990 Feb;6(2):52–56. doi: 10.1016/0168-9525(90)90074-g. [DOI] [PubMed] [Google Scholar]
  44. Taylor I. C., Workman J. L., Schuetz T. J., Kingston R. E. Facilitated binding of GAL4 and heat shock factor to nucleosomal templates: differential function of DNA-binding domains. Genes Dev. 1991 Jul;5(7):1285–1298. doi: 10.1101/gad.5.7.1285. [DOI] [PubMed] [Google Scholar]
  45. Travers A. A. DNA conformation and protein binding. Annu Rev Biochem. 1989;58:427–452. doi: 10.1146/annurev.bi.58.070189.002235. [DOI] [PubMed] [Google Scholar]
  46. Treisman R. The serum response element. Trends Biochem Sci. 1992 Oct;17(10):423–426. doi: 10.1016/0968-0004(92)90013-y. [DOI] [PubMed] [Google Scholar]
  47. Tsukiyama T., Wu C. Purification and properties of an ATP-dependent nucleosome remodeling factor. Cell. 1995 Dec 15;83(6):1011–1020. doi: 10.1016/0092-8674(95)90216-3. [DOI] [PubMed] [Google Scholar]
  48. Ura K., Hayes J. J., Wolffe A. P. A positive role for nucleosome mobility in the transcriptional activity of chromatin templates: restriction by linker histones. EMBO J. 1995 Aug 1;14(15):3752–3765. doi: 10.1002/j.1460-2075.1995.tb00045.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Varga-Weisz P. D., Blank T. A., Becker P. B. Energy-dependent chromatin accessibility and nucleosome mobility in a cell-free system. EMBO J. 1995 May 15;14(10):2209–2216. doi: 10.1002/j.1460-2075.1995.tb07215.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Wallrath L. L., Lu Q., Granok H., Elgin S. C. Architectural variations of inducible eukaryotic promoters: preset and remodeling chromatin structures. Bioessays. 1994 Mar;16(3):165–170. doi: 10.1002/bies.950160306. [DOI] [PubMed] [Google Scholar]
  51. Wechsler D. S., Papoulas O., Dang C. V., Kingston R. E. Differential binding of c-Myc and Max to nucleosomal DNA. Mol Cell Biol. 1994 Jun;14(6):4097–4107. doi: 10.1128/mcb.14.6.4097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Winston F., Carlson M. Yeast SNF/SWI transcriptional activators and the SPT/SIN chromatin connection. Trends Genet. 1992 Nov;8(11):387–391. doi: 10.1016/0168-9525(92)90300-s. [DOI] [PubMed] [Google Scholar]
  53. Wolffe A. P. Implications of DNA replication for eukaryotic gene expression. J Cell Sci. 1991 Jun;99(Pt 2):201–206. doi: 10.1242/jcs.99.2.201. [DOI] [PubMed] [Google Scholar]
  54. Wolffe A. P. Implications of DNA replication for eukaryotic gene expression. J Cell Sci. 1991 Jun;99(Pt 2):201–206. doi: 10.1242/jcs.99.2.201. [DOI] [PubMed] [Google Scholar]
  55. Wolffe A. P. Nucleosome positioning and modification: chromatin structures that potentiate transcription. Trends Biochem Sci. 1994 Jun;19(6):240–244. doi: 10.1016/0968-0004(94)90148-1. [DOI] [PubMed] [Google Scholar]
  56. Wolffe A. P. The transcription of chromatin templates. Curr Opin Genet Dev. 1994 Apr;4(2):245–254. doi: 10.1016/s0959-437x(05)80051-6. [DOI] [PubMed] [Google Scholar]
  57. Wolffe A. P. Transcription: in tune with the histones. Cell. 1994 Apr 8;77(1):13–16. doi: 10.1016/0092-8674(94)90229-1. [DOI] [PubMed] [Google Scholar]
  58. Workman J. L., Kingston R. E. Nucleosome core displacement in vitro via a metastable transcription factor-nucleosome complex. Science. 1992 Dec 11;258(5089):1780–1784. doi: 10.1126/science.1465613. [DOI] [PubMed] [Google Scholar]
  59. de Groot R. P., Delmas V., Sassone-Corsi P. DNA bending by transcription factors CREM and CREB. Oncogene. 1994 Feb;9(2):463–468. [PubMed] [Google Scholar]
  60. van Dam H., Wilhelm D., Herr I., Steffen A., Herrlich P., Angel P. ATF-2 is preferentially activated by stress-activated protein kinases to mediate c-jun induction in response to genotoxic agents. EMBO J. 1995 Apr 18;14(8):1798–1811. doi: 10.1002/j.1460-2075.1995.tb07168.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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