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The Journal of Neuroscience, June 1, 1999, 19(11):4337-4348
The Mitogen-Activated Protein Kinase Cascade Couples PKA and PKC
to cAMP Response Element Binding Protein Phosphorylation in Area CA1 of
Hippocampus
Erik D.
Roberson ,
Joey D.
English ,
J. Paige
Adams ,
Joel
C.
Selcher ,
Christine
Kondratick, and
J. David
Sweatt
Division of Neuroscience, Baylor College of Medicine, Houston,
Texas 77030
Activation of the mitogen-activated protein kinase (MAPK) cascade
recently was discovered to play an important role in synaptic plasticity in area CA1 of rat hippocampus. However, the upstream mechanisms regulating MAPK activity and the downstream effectors of
MAPK in the hippocampus are uncharacterized. In the present studies we
observed that hippocampal MAPK activation is regulated by both the PKA
and PKC systems; moreover, we found that a wide variety of
neuromodulatory neurotransmitter receptors (metabotropic glutamate
receptors, muscarinic acetylcholine receptors, dopamine receptors, and
 -adrenergic receptors) couple to MAPK activation via these two
cascades. In additional studies we observed that PKC is a powerful
regulator of CREB phosphorylation in area CA1. MAPK plays a critical
role in transcriptional regulation by PKC, because MAPK activation is a
necessary component for increased CREB phosphorylation in response to
the activation of this kinase. Surprisingly, we also observed that MAPK
activation is necessary for PKA coupling to CREB phosphorylation in
area CA1. Overall, these studies indicate an unexpected richness of
diversity in the regulation of MAPK in the hippocampus and suggest the
possibility of a broad role for the MAPK cascade in regulating gene
expression in long-term forms of hippocampal synaptic plasticity.
Key words:
MAPK; PKA; PKC; CREB; hippocampus; LTP; learning and
memory
Copyright © 1999 Society for Neuroscience 0270-6474/99/19114337-12$05.00/0
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N. Takagi, K. Miyake-Takagi, K. Takagi, H. Tamura, and S. Takeo
Altered Extracellular Signal-regulated Kinase Signal Transduction by the Muscarinic Acetylcholine and Metabotropic Glutamate Receptors after Cerebral Ischemia
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R.-R. Ji, K. Befort, G. J. Brenner, and C. J. Woolf
ERK MAP Kinase Activation in Superficial Spinal Cord Neurons Induces Prodynorphin and NK-1 Upregulation and Contributes to Persistent Inflammatory Pain Hypersensitivity
J. Neurosci.,
January 15, 2002;
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[Abstract]
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M. G. Giovannini, R. D. Blitzer, T. Wong, K. Asoma, P. Tsokas, J. H. Morrison, R. Iyengar, and E. M. Landau
Mitogen-Activated Protein Kinase Regulates Early Phosphorylation and Delayed Expression of Ca2+/Calmodulin-Dependent Protein Kinase II in Long-Term Potentiation
J. Neurosci.,
September 15, 2001;
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[Abstract]
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[PDF]
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A. Garcia, C. V. Alvarez, R. G. Smith, and C. Dieguez
Regulation of PIT-1 Expression By Ghrelin and GHRP-6 Through the GH Secretagogue Receptor
Mol. Endocrinol.,
September 1, 2001;
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[Abstract]
[Full Text]
[PDF]
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P. Calabresi, P. Gubellini, B. Picconi, D. Centonze, A. Pisani, P. Bonsi, P. Greengard, R. A. Hipskind, E. Borrelli, and G. Bernardi
Inhibition of Mitochondrial Complex II Induces a Long-Term Potentiation of NMDA-Mediated Synaptic Excitation in the Striatum Requiring Endogenous Dopamine
J. Neurosci.,
July 15, 2001;
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[Abstract]
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[PDF]
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K. T. Dineley, M. Westerman, D. Bui, K. Bell, K. H. Ashe, and J. D. Sweatt
{beta}-Amyloid Activates the Mitogen-Activated Protein Kinase Cascade via Hippocampal {alpha}7 Nicotinic Acetylcholine Receptors: In Vitro and In Vivo Mechanisms Related to Alzheimer's Disease
J. Neurosci.,
June 15, 2001;
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[Abstract]
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[PDF]
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A. Tozzi, E. Guatteo, L. Caputi, G. Bernardi, and N. B. Mercuri
Group I mGluRs Coupled to G Proteins Are Regulated by Tyrosine Kinase in Dopamine Neurons of the Rat Midbrain
J Neurophysiol,
June 1, 2001;
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[Abstract]
[Full Text]
[PDF]
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M. W. Swank and J. D. Sweatt
Increased Histone Acetyltransferase and Lysine Acetyltransferase Activity and Biphasic Activation of the ERK/RSK Cascade in Insular Cortex During Novel Taste Learning
J. Neurosci.,
May 15, 2001;
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[Abstract]
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S. A. Josselyn, C. Shi, W. A. Carlezon Jr, R. L. Neve, E. J. Nestler, and M. Davis
Long-Term Memory Is Facilitated by cAMP Response Element-Binding Protein Overexpression in the Amygdala
J. Neurosci.,
April 1, 2001;
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[Abstract]
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G.-Y. Wu, K. Deisseroth, and R. W. Tsien
Activity-dependent CREB phosphorylation: Convergence of a fast, sensitive calmodulin kinase pathway and a slow, less sensitive mitogen-activated protein kinase pathway
PNAS,
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[Abstract]
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K. H. Harum, L. Alemi, and M. V. Johnston
Cognitive impairment in Coffin-Lowry syndrome correlates with reduced RSK2 activation
Neurology,
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[Abstract]
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J. C. Selcher, T. Nekrasova, R. Paylor, G. E. Landreth, and J. D. Sweatt
Mice Lacking the ERK1 Isoform of MAP Kinase Are Unimpaired in Emotional Learning
Learn. Mem.,
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[Abstract]
[Full Text]
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E. Valjent, J.-C. Corvol, C. Pages, M.-J. Besson, R. Maldonado, and J. Caboche
Involvement of the Extracellular Signal-Regulated Kinase Cascade for Cocaine-Rewarding Properties
J. Neurosci.,
December 1, 2000;
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[Abstract]
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G. E. Schafe, C. M. Atkins, M. W. Swank, E. P. Bauer, J. D. Sweatt, and J. E. LeDoux
Activation of ERK/MAP Kinase in the Amygdala Is Required for Memory Consolidation of Pavlovian Fear Conditioning
J. Neurosci.,
November 1, 2000;
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[Abstract]
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E. Thiels, B. I. Kanterewicz, L. T. Knapp, G. Barrionuevo, and E. Klann
Protein Phosphatase-Mediated Regulation of Protein Kinase C during Long-Term Depression in the Adult Hippocampus In Vivo
J. Neurosci.,
October 1, 2000;
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[Abstract]
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D. E. Berman, S. Hazvi, V. Neduva, and Y. Dudai
The Role of Identified Neurotransmitter Systems in the Response of Insular Cortex to Unfamiliar Taste: Activation of ERK1-2 and Formation of a Memory Trace
J. Neurosci.,
September 15, 2000;
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[Abstract]
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A. W. Varga, A. E. Anderson, J. P. Adams, H. Vogel, and J. D. Sweatt
Input-Specific Immunolocalization of Differentially Phosphorylated Kv4.2 in the Mouse Brain
Learn. Mem.,
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[Abstract]
[Full Text]
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Y.-Y. Huang, K. C. Martin, and E. R. Kandel
Both Protein Kinase A and Mitogen-Activated Protein Kinase Are Required in the Amygdala for the Macromolecular Synthesis-Dependent Late Phase of Long-Term Potentiation
J. Neurosci.,
September 1, 2000;
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E. J. Weeber, C. M. Atkins, J. C. Selcher, A. W. Varga, B. Mirnikjoo, R. Paylor, M. Leitges, and J. D. Sweatt
A Role for the beta Isoform of Protein Kinase C in Fear Conditioning
J. Neurosci.,
August 15, 2000;
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[Abstract]
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A. M. Watabe, P. A. Zaki, and T. J. O'Dell
Coactivation of beta -Adrenergic and Cholinergic Receptors Enhances the Induction of Long-Term Potentiation and Synergistically Activates Mitogen-Activated Protein Kinase in the Hippocampal CA1 Region
J. Neurosci.,
August 15, 2000;
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[Abstract]
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[PDF]
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L. Zirpel, M. A. Janowiak, C. A. Veltri, and T. N. Parks
AMPA Receptor-Mediated, Calcium-Dependent CREB Phosphorylation in a Subpopulation of Auditory Neurons Surviving Activity Deprivation
J. Neurosci.,
August 15, 2000;
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[Abstract]
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S. Davis, P. Vanhoutte, C. Pages, J. Caboche, and S. Laroche
The MAPK/ERK Cascade Targets Both Elk-1 and cAMP Response Element-Binding Protein to Control Long-Term Potentiation-Dependent Gene Expression in the Dentate Gyrus In Vivo
J. Neurosci.,
June 15, 2000;
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[Abstract]
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A. Francesconi and R. M. Duvoisin
Opposing effects of protein kinase C and protein kinase A on metabotropic glutamate receptor signaling: Selective desensitization of the inositol trisphosphate/Ca2+ pathway by phosphorylation of the receptor-G protein-coupling domain
PNAS,
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[Abstract]
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B. I. Kanterewicz, N. N. Urban, D. B. T. McMahon, E. D. Norman, L. J. Giffen, M. F. Favata, P. A. Scherle, G. Barrionuevo, and E. Klann
The Extracellular Signal-Regulated Kinase Cascade Is Required for NMDA Receptor-Independent LTP in Area CA1 But Not Area CA3 of the Hippocampus
J. Neurosci.,
May 1, 2000;
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[Abstract]
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T. Pizzorusso, G. M. Ratto, E. Putignano, and L. Maffei
Brain-Derived Neurotrophic Factor Causes cAMP Response Element-Binding Protein Phosphorylation in Absence of Calcium Increases in Slices and Cultured Neurons from Rat Visual Cortex
J. Neurosci.,
April 15, 2000;
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[Abstract]
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K. Kolkova, V. Novitskaya, N. Pedersen, V. Berezin, and E. Bock
Neural Cell Adhesion Molecule-Stimulated Neurite Outgrowth Depends on Activation of Protein Kinase C and the Ras-Mitogen-Activated Protein Kinase Pathway
J. Neurosci.,
March 15, 2000;
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[Abstract]
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A. E. Anderson, J. P. Adams, Y. Qian, R. G. Cook, P. J. Pfaffinger, and J. D. Sweatt
Kv4.2 Phosphorylation by Cyclic AMP-dependent Protein Kinase
J. Biol. Chem.,
February 25, 2000;
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[Abstract]
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S. Otani, N. Auclair, J.-M. Desce, M.-P. Roisin, and F. Crepel
Dopamine Receptors and Groups I and II mGluRs Cooperate for Long-Term Depression Induction in Rat Prefrontal Cortex through Converging Postsynaptic Activation of MAP Kinases
J. Neurosci.,
November 15, 1999;
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[Abstract]
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T. D. Moody, H. J. Carlisle, and T. J. O'Dell
A Nitric Oxide-Independent and beta -Adrenergic Receptor-Sensitive Form of Metaplasticity Limits theta -Frequency Stimulation-Induced LTP in the Hippocampal CA1 Region
Learn. Mem.,
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[Abstract]
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Z. Yan, J. Feng, A. A. Fienberg, and P. Greengard
D2 dopamine receptors induce mitogen-activated protein kinase and cAMP response element-binding protein phosphorylation in neurons
PNAS,
September 28, 1999;
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[Abstract]
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J. D. Sweatt
Toward a Molecular Explanation for Long-Term Potentiation
Learn. Mem.,
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[Full Text]
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J. C. Selcher, C. M. Atkins, J. M. Trzaskos, R. Paylor, and J. D. Sweatt
A Necessity for MAP Kinase Activation in Mammalian Spatial Learning
Learn. Mem.,
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[Abstract]
[Full Text]
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L. J. Chandler, G. Sutton, N. R. Dorairaj, and D. Norwood
N-Methyl D-Aspartate Receptor-mediated Bidirectional Control of Extracellular Signal-regulated Kinase Activity in Cortical Neuronal Cultures
J. Biol. Chem.,
January 19, 2001;
276(4):
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[Abstract]
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S. S. Grewal, D. M. Fass, H. Yao, C. L. Ellig, R. H. Goodman, and P. J. S. Stork
Calcium and cAMP Signals Differentially Regulate cAMP-responsive Element-binding Protein Function via a Rap1-Extracellular Signal-regulated Kinase Pathway
J. Biol. Chem.,
October 27, 2000;
275(44):
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[Abstract]
[Full Text]
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P. Zanassi, M. Paolillo, A. Feliciello, E. V. Avvedimento, V. Gallo, and S. Schinelli
cAMP-dependent Protein Kinase Induces cAMP-response Element-binding Protein Phosphorylation via an Intracellular Calcium Release/ERK-dependent Pathway in Striatal Neurons
J. Biol. Chem.,
April 6, 2001;
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[Abstract]
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G.-Y. Wu, K. Deisseroth, and R. W. Tsien
Activity-dependent CREB phosphorylation: Convergence of a fast, sensitive calmodulin kinase pathway and a slow, less sensitive mitogen-activated protein kinase pathway
PNAS,
February 27, 2001;
98(5):
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[Abstract]
[Full Text]
[PDF]
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M. W. Jones, P. J. French, T. V. P. Bliss, and K. Rosenblum
Molecular Mechanisms of Long-Term Potentiation in the Insular Cortex In Vivo
J. Neurosci.,
November 1, 1999;
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[Abstract]
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[PDF]
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G. E. Schafe and J. E. LeDoux
Memory Consolidation of Auditory Pavlovian Fear Conditioning Requires Protein Synthesis and Protein Kinase A in the Amygdala
J. Neurosci.,
September 15, 2000;
20(18):
RC96 - RC96.
[Abstract]
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H. Viola, M. Furman, L. A. I. Izquierdo, M. Alonso, D. M. Barros, M. M. de Souza, I. Izquierdo, and J. H. Medina
Phosphorylated cAMP Response Element-Binding Protein as a Molecular Marker of Memory Processing in Rat Hippocampus: Effect of Novelty
J. Neurosci.,
December 1, 2000;
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[Abstract]
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