Chromatin-Dependent Cooperativity between Constitutive and Inducible Activation Domains in CREB

doi:10.1128/MCB.21.23.7892-7900.2001

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Molecular and Cellular Biology, December 2001, p. 7892-7900, Vol. 21, No. 23
0270-7306/01/$04.00+0 DOI: 10.1128/MCB.21.23.7892-7900.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Chromatin-Dependent Cooperativity between Constitutive and Inducible Activation Domains in CREB

Hiroshi Asahara,¹ Buyung Santoso,² Ernesto Guzman,¹ Keyong Du,¹ Philip A. Cole,³ Irwin Davidson,⁴ and Marc Montminy¹^,^*

Peptide Biology Laboratories, Salk Institute for Biological Studies, La Jolla, California 92037-1002¹; Section of Molecular Biology and Center for Molecular Genetics, University of California San Diego, La Jolla, California 92093-0347²; Department of Pharmacology and Molecular Sciences, The Johns Hopkins University School of Medicine, Baltimore, Maryland 21205³; and Institut de Génétique et de Biologie Moléculaire et Cellulaire, CNRS/INSERM/ULP 67404 Illkirch Cedex France⁴

Received 19 March 2001/Returned for modification 14 June 2001/Accepted 28 August 2001

The cyclic AMP (cAMP)-responsive factor CREB induces target gene expression via constitutive (Q2) and inducible (KID, forkinase-inducible domain) activation domains that function synergisticallyin response to cellular signals. KID stimulates transcriptionvia a phospho (Ser133)-dependent interaction with the coactivatorparalogs CREB binding protein and p300, whereas Q2 recruits theTFIID complex via a direct association with hTAF_II130. Here weinvestigate the mechanism underlying cooperativity between theQ2 domain and KID in CREB by in vitro transcription assay withnaked DNA and chromatin templates containing the cAMP-responsivesomatostatin promoter. The Q2 domain was highly active on a nakedDNA template, and Ser133 phosphorylation had no additional effecton transcriptional initiation in crude extracts. Q2 activity wasrepressed on a chromatin template, however, and this repressionwas relieved by the phospho (Ser133) KID-dependent recruitmentof p300 histone acetyltransferase activity to the promoter. Inchromatin immunoprecipitation assays of NIH 3T3 cells, cAMP-dependentrecruitment of p300 to the somatostatin promoter stimulated acetylationof histone H4. Correspondingly, overexpression of hTAFII130 potentiatedCREB activity in cells exposed to cAMP, but had no effect on reportergene expression in unstimulated cells. We propose that cooperativitybetween the KID and Q2 domains proceeds via a chromatin-dependentmechanism in which recruitment of p300 facilitates subsequentinteraction of CREB withTFIID.

^* Corresponding author. Mailing address: Salk Institute, 10010 N. Torrey Pines Rd. La Jolla, CA 92037. Phone: (858) 453-4100,ext. 1394. Fax: (858) 625-9045. E-mail: montminy{at}salk.edu.

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