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Science 4 September 1998:
Vol. 281. no. 5382, pp. 1505 - 1509
DOI: 10.1126/science.281.5382.1505
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Reports

CBP: A Signal-Regulated Transcriptional Coactivator Controlled by Nuclear Calcium and CaM Kinase IV

Sangeeta Chawla, * Giles E. Hardingham, * David R. Quinn, dagger Hilmar Bading ddagger

Recruitment of the coactivator, CREB binding protein (CBP), by signal-regulated transcription factors, such as CREB [adenosine 3',5'-monophosphate (cAMP) response element binding protein], is critical for stimulation of gene expression. The mouse pituitary cell line AtT20 was used to show that the CBP recruitment step (CREB phosphorylation on serine-133) can be uncoupled from CREB/CBP-activated transcription. CBP was found to contain a signal-regulated transcriptional activation domain that is controlled by nuclear calcium and calcium/calmodulin-dependent (CaM) protein kinase IV and by cAMP. Cytoplasmic calcium signals that stimulate the Ras mitogen-activated protein kinase signaling cascade or expression of the activated form of Ras provided the CBP recruitment signal but did not increase CBP activity and failed to activate CREB- and CBP-mediated transcription. These results identify CBP as a signal-regulated transcriptional coactivator and define a regulatory role for nuclear calcium and cAMP in CBP-dependent gene expression.

Medical Research Council, Laboratory of Molecular Biology, Hills Road, Cambridge CB2 2QH, UK.
*   These authors contributed equally to this work.

dagger    Present address: Department of Clinical Biochemistry, University of Cambridge, Addenbrooke's Hospital, Hills Road, Cambridge CB2 2QR, UK.

ddagger    To whom correspondence should be addressed. E-mail: hb1{at}mrc-lmb.cam.ac.uk

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A Novel Transcriptional Repression Domain Mediates p21WAF1/CIP1 Induction of p300 Transactivation.
A. W. Snowden, L. A. Anderson, G. A. Webster, and N. D. Perkins (2000)
Mol. Cell. Biol. 20, 2676-2686
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Calmodulin-Binding Peptide PEP-19 Modulates Activation of Calmodulin Kinase II In Situ.
R. A. Johanson, H. M. Sarau, J. J. Foley, and J. R. Slemmon (2000)
J. Neurosci. 20, 2860-2866
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A stimulus-specific role for CREB-binding protein (CBP) in T cell receptor-activated tumor necrosis factor alpha gene expression.
J. V. Falvo, B. M. N. Brinkman, A. V. Tsytsykova, E. Y. Tsai, T.-P. Yao, A. L. Kung, and A. E. Goldfeld (2000)
PNAS 97, 3925-3929
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A Tissue-Specific Coactivator of Steroid Receptors, Identified in a Functional Genetic Screen.
D. Knutti, A. Kaul, and A. Kralli (2000)
Mol. Cell. Biol. 20, 2411-2422
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Recruitment of CREB Binding Protein Is Sufficient for CREB-Mediated Gene Activation.
J.-R. Cardinaux, J. C. Notis, Q. Zhang, N. Vo, J. C. Craig, D. M. Fass, R. G. Brennan, and R. H. Goodman (2000)
Mol. Cell. Biol. 20, 1546-1552
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Phosphorylation of Steroid Receptor Coactivator-1. IDENTIFICATION OF THE PHOSPHORYLATION SITES AND PHOSPHORYLATION THROUGH THE MITOGEN-ACTIVATED PROTEIN KINASE PATHWAY.
B. G. Rowan, N. L. Weigel, and B. W. O'Malley (2000)
J. Biol. Chem. 275, 4475-4483
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The Homeodomain Protein Arix Promotes Protein Kinase A-dependent Activation of the Dopamine beta -Hydroxylase Promoter through Multiple Elements and Interaction with the Coactivator cAMP-response Element-binding Protein-binding Protein.
D. J. Swanson, M. Adachi, and E. J. Lewis (2000)
J. Biol. Chem. 275, 2911-2923
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The coregulator exchange in transcriptional functions of nuclear receptors.
C. K. Glass and M. G. Rosenfeld (2000)
Genes & Dev. 14, 121-141
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Ca2+-dependent Gene Expression Mediated by MEF2 Transcription Factors.
F. Blaeser, N. Ho, R. Prywes, and T. A. Chatila (2000)
J. Biol. Chem. 275, 197-209
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Regulatory Cascades Involving Calmodulin-Dependent Protein Kinases.
A. R. Means (2000)
Mol. Endocrinol. 14, 4-13
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Independent Repressor Domains in ZEB Regulate Muscle and T-Cell Differentiation.
A. A. Postigo and D. C. Dean (1999)
Mol. Cell. Biol. 19, 7961-7971
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Activation of PPAR Coactivator-1 Through Transcription Factor Docking.
P. Puigserver, G. Adelmant, Z. Wu, M. Fan, J. Xu, B. O'Malley, and B. M. Spiegelman (1999)
Science 286, 1368-1371
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Mycobacterium tuberculosis Inhibits IFN-{gamma} Transcriptional Responses Without Inhibiting Activation of STAT1.
L.-M. Ting, A. C. Kim, A. Cattamanchi, and J. D. Ernst (1999)
J. Immunol. 163, 3898-3906
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Gene Expression in Hippocampal Long-Term Potentiation.
S. M. Dudek and R. D. Fields (1999)
Neuroscientist 5, 275-279
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Cardiac-specific Overexpression of the alpha 1 Subunit of the L-type Voltage-dependent Ca2+ Channel in Transgenic Mice. LOSS OF ISOPROTERENOL-INDUCED CONTRACTION.
J. N. Muth, H. Yamaguchi, G. Mikala, I. L. Grupp, W. Lewis, H. Cheng, L.-S. Song, E. G. Lakatta, G. Varadi, and A. Schwartz (1999)
J. Biol. Chem. 274, 21503-21506
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Induction of Interleukin-6 Expression by Angiotensin II in Rat Vascular Smooth Muscle Cells.
Y. Funakoshi, T. Ichiki, K. Ito, and A. Takeshita (1999)
Hypertension 34, 118-125
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Regulation of the Human Interleukin-5 Promoter by Ets Transcription Factors. ETS1 AND ETS2, BUT NOT ELF-1, COOPERATE WITH GATA3 AND HTLV-I TAX1.
S. G. Blumenthal, G. Aichele, T. Wirth, A. P. Czernilofsky, A. Nordheim, and J. Dittmer (1999)
J. Biol. Chem. 274, 12910-12916
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Inhibition of p53 Transcriptional Activity by Bcl-2 Requires Its Membrane-anchoring Domain.
B. A. Froesch, C. Aime-Sempe, B. Leber, D. Andrews, and J. C. Reed (1999)
J. Biol. Chem. 274, 6469-6475
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Mitogen-Activated Protein Kinase and Protein Kinase A Signaling Pathways Stimulate Cholecystokinin Transcription via Activation of Cyclic Adenosine 3',5'-Monophosphate Response Element-Binding Protein.
T. v. O. Hansen, J. F. Rehfeld, and F. C. Nielsen (1999)
Mol. Endocrinol. 13, 466-475
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Calcium and cAMP Signals Differentially Regulate cAMP-responsive Element-binding Protein Function via a Rap1-Extracellular Signal-regulated Kinase Pathway.
S. S. Grewal, D. M. Fass, H. Yao, C. L. Ellig, R. H. Goodman, and P. J. S. Stork (2000)
J. Biol. Chem. 275, 34433-34441
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