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PNAS 98 (20): 11024-11031

Copyright © 2001 by the National Academy of Sciences.

Colloquium Paper


COLLOQUIUM PAPER

Calcium regulation of neuronal gene expression

Anne E. West, Wen G. Chen, Matthew B. Dalva, Ricardo E. Dolmetsch, Jon M. Kornhauser, Adam J. Shaywitz, Mari A. Takasu, Xu Tao, and Michael E. Greenberg*

Division of Neuroscience, Children's Hospital, 300 Longwood Avenue, Boston, MA 02115

Abstract: Plasticity is a remarkable feature of the brain, allowing neuronal structure and function to accommodate to patterns of electrical activity. One component of these long-term changes is the activity-driven induction of new gene expression, which is required for both the long-lasting long-term potentiation of synaptic transmission associated with learning and memory, and the activitydependent survival events that help to shape and wire the brain during development. We have characterized molecular mechanisms by which neuronal membrane depolarization and subsequent calcium influx into the cytoplasm lead to the induction of new gene transcription. We have identified three points within this cascade of events where the specificity of genes induced by different types of stimuli can be regulated. By using the induction of the gene that encodes brain-derived neurotrophic factor (BDNF) as a model, we have found that the ability of a calcium influx to induce transcription of this gene is regulated by the route of calcium entry into the cell, by the pattern of phosphorylation induced on the transcription factor cAMP-response element (CRE) binding protein (CREB), and by the complement of active transcription factors recruited to the BDNF promoter. These results refine and expand the working model of activity-induced gene induction in the brain, and help to explain how different types of neuronal stimuli can activate distinct transcriptional responses.


* To whom reprint requests should be addressed. E-mail: michael.greenberg{at}tch.harvard.edu.

This paper was presented at the Inaugural Arthur M. Sackler Colloquium of the National Academy of Sciences, "Neural Signaling," held February 15–17, 2001, at the National Academy of Sciences in Washington, DC.

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N. R. Mahapatra, M. Mahata, P. P. Hazra, P. M. McDonough, D. T. O'Connor, and S. K. Mahata (2004)
J. Biol. Chem. 279, 51107-51121
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Nuclear Calcium/Calmodulin Regulates Memory Consolidation.
K. Limback-Stokin, E. Korzus, R. Nagaoka-Yasuda, and M. Mayford (2004)
J. Neurosci. 24, 10858-10867
   Abstract »    Full Text »    PDF »
The Kinetic Profile of Intracellular Calcium Predicts Long-Term Potentiation and Long-Term Depression.
I. Ismailov, D. Kalikulov, T. Inoue, and M. J. Friedlander (2004)
J. Neurosci. 24, 9847-9861
   Abstract »    Full Text »    PDF »
Long-term Potentiation of Wound-induced Exocytosis and Plasma Membrane Repair Is Dependant on cAMP-response Element-mediated Transcription via a Protein Kinase C- and p38 MAPK-dependent Pathway.
T. Togo (2004)
J. Biol. Chem. 279, 44996-45003
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Depolarization of Skeletal Muscle Cells induces Phosphorylation of cAMP Response Element Binding Protein via Calcium and Protein Kinase C{alpha}.
C. Cardenas, M. Muller, E. Jaimovich, F. Perez, D. Buchuk, A. F. G. Quest, and M. A. Carrasco (2004)
J. Biol. Chem. 279, 39122-39131
   Abstract »    Full Text »    PDF »
Distinct Intracellular Calcium Profiles Following Influx Through N- Versus L-Type Calcium Channels: Role of Ca2+-Induced Ca2+ Release.
K. Tully and S. N. Treistman (2004)
J Neurophysiol 92, 135-143
   Abstract »    Full Text »    PDF »
Choline Transporter 1 Maintains Cholinergic Function in Choline Acetyltransferase Haploinsufficiency.
E. P. Brandon, T. Mellott, D. P. Pizzo, N. Coufal, K. A. D'Amour, K. Gobeske, M. Lortie, I. Lopez-Coviella, B. Berse, L. J. Thal, et al. (2004)
J. Neurosci. 24, 5459-5466
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Seven in absentia homolog 1A mediates ubiquitination and degradation of group 1 metabotropic glutamate receptors.
K. Moriyoshi, K. Iijima, H. Fujii, H. Ito, Y. Cho, and S. Nakanishi (2004)
PNAS 101, 8614-8619
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Store-Operated Ca2+ Entry Activates the CREB Transcription Factor in Vascular Smooth Muscle.
R. A. Pulver, P. Rose-Curtis, M. W. Roe, G. C. Wellman, and K. M. Lounsbury (2004)
Circ. Res. 94, 1351-1358
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Developmentally regulated role for Ras-GRFs in coupling NMDA glutamate receptors to Ras, Erk and CREB.
X. Tian, T. Gotoh, K. Tsuji, E. H. Lo, S. Huang, and L. A. Feig (2004)
EMBO J. 23, 1567-1575
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Phosphorylation of Conserved Casein Kinase Sites Regulates cAMP-response Element-binding Protein DNA Binding in Drosophila.
J. Horiuchi, W. Jiang, H. Zhou, P. Wu, and J. C. P. Yin (2004)
J. Biol. Chem. 279, 12117-12125
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CRE-Mediated Transcription Is Increased in Huntington's Disease Transgenic Mice.
K. Obrietan and K. R. Hoyt (2004)
J. Neurosci. 24, 791-796
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Identification of calcium- and nitric oxide-regulated genes by differential analysis of library expression (DAzLE).
H. Li, X. Gu, V. L. Dawson, and T. M. Dawson (2004)
PNAS 101, 647-652
   Abstract »    Full Text »    PDF »
Dendrite Development Regulated by CREST, a Calcium-Regulated Transcriptional Activator.
H. Aizawa, S.-C. Hu, K. Bobb, K. Balakrishnan, G. Ince, I. Gurevich, M. Cowan, and A. Ghosh (2004)
Science 303, 197-202
   Abstract »    Full Text »    PDF »
Accelerated dendritic development of rat cortical pyramidal cells and interneurons after biolistic transfection with BDNF and NT4/5.
M. J. Wirth, A. Brun, J. Grabert, S. Patz, and P. Wahle (2003)
Development 130, 5827-5838
   Abstract »    Full Text »    PDF »
Targeted Protein Degradation and Synapse Remodeling by an Inducible Protein Kinase.
D. T. S. Pak and M. Sheng (2003)
Science 302, 1368-1373
   Abstract »    Full Text »    PDF »
MOLECULAR BIOLOGY: MeCP2 Repression Goes Nonglobal.
R. Klose and A. Bird (2003)
Science 302, 793-795
   Abstract »    Full Text »    PDF »
EPPENDORF 2003 PRIZE-WINNING ESSAY: Ubiquitin and the Deconstruction of Synapses.
M. D. Ehlers (2003)
Science 302, 800-801
   Abstract »    Full Text »    PDF »
Derepression of BDNF Transcription Involves Calcium-Dependent Phosphorylation of MeCP2.
W. G. Chen, Q. Chang, Y. Lin, A. Meissner, A. E. West, E. C. Griffith, R. Jaenisch, and M. E. Greenberg (2003)
Science 302, 885-889
   Abstract »    Full Text »    PDF »
DNA Methylation-Related Chromatin Remodeling in Activity-Dependent Bdnf Gene Regulation.
K. Martinowich, D. Hattori, H. Wu, S. Fouse, F. He, Y. Hu, G. Fan, and Y. E. Sun (2003)
Science 302, 890-893
   Abstract »    Full Text »    PDF »
An Evolutionarily Conserved N-terminal Acetyltransferase Complex Associated with Neuronal Development.
N. Sugiura, S. M. Adams, and R. A. Corriveau (2003)
J. Biol. Chem. 278, 40113-40120
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