ERK2: a logical AND gate critical for drug-induced plasticity?

Drug addiction results in part from the distortion of dopamine-controlled plasticity, and extracellular signal-regulated kinase (ERK) plays an important role in the underlying molecular mechanisms of this process. ERK is activated by drugs of abuse in a subset of neurons in reward-related brain regions. This activation, necessary for the expression of immediate early genes, depends upon dopamine D1 and glutamate receptors. Blockade of ERK activation prevents long-lasting behavioral changes, including psychomotor sensitization and conditioned place preference. It also interferes with drug craving and drug-associated memory reconsolidation. By contrast, ERK1 mutation enhances the effects of morphine and cocaine. We suggest that the ERK2 pathway acts as a logical AND gate, permissive for plasticity, in neurons on which dopamine-mediated reward signals and glutamate-mediated contextual information converge.

[1]  Angus C Nairn,et al.  DARPP-32: an integrator of neurotransmission. , 2004, Annual review of pharmacology and toxicology.

[2]  R. Malinow,et al.  Ras and Rap Control AMPA Receptor Trafficking during Synaptic Plasticity , 2002, Cell.

[3]  N. Hiroi,et al.  Regulation of ERK ( Extracellular Signal Regulated Kinase), Part of the Neurotrophin Signal Transduction Cascade, in the Rat Mesolimbic Dopamine System by Chronic Exposure to Morphine or Cocaine , 1996, The Journal of Neuroscience.

[4]  M. Besson,et al.  Δ9‐tetrahydrocannabinol‐induced MAPK/ERK and Elk‐1 activation in vivo depends on dopaminergic transmission , 2001, The European journal of neuroscience.

[5]  Todor V. Gerdjikov,et al.  Place preference induced by nucleus accumbens amphetamine is impaired by antagonists of ERK or p38 MAP kinases in rats. , 2004, Behavioral neuroscience.

[6]  L. Kaczmarek,et al.  Extracellular signal‐regulated kinases (ERKs) modulate cocaine‐induced gene expression in the mouse amygdala , 2005, The European journal of neuroscience.

[7]  Angus C. Nairn,et al.  Synaptic plasticity: one STEP at a time , 2006, Trends in Neurosciences.

[8]  M. Besson,et al.  Glutamate Induces Phosphorylation of Elk-1 and CREB, Along with c-fos Activation, via an Extracellular Signal-Regulated Kinase-Dependent Pathway in Brain Slices , 1999, Molecular and Cellular Biology.

[9]  M. Segal,et al.  Protein kinase C and ERK involvement in dendritic spine plasticity in cultured rodent hippocampal neurons , 2003, The European journal of neuroscience.

[10]  R. Palmiter,et al.  Reversal of supersensitive striatal dopamine D1 receptor signaling and extracellular signal-regulated kinase activity in dopamine-deficient mice , 2006, Neuroscience.

[11]  Scott J. Russo,et al.  Chromatin Remodeling Is a Key Mechanism Underlying Cocaine-Induced Plasticity in Striatum , 2005, Neuron.

[12]  J. Sweatt,et al.  Mitogen-activated protein kinases in synaptic plasticity and memory , 2004, Current Opinion in Neurobiology.

[13]  Karl Deisseroth,et al.  Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology , 2001, Nature Neuroscience.

[14]  L. Naldini,et al.  ERK1 and ERK2 mitogen-activated protein kinases affect Ras-dependent cell signaling differentially , 2006, Journal of biology.

[15]  Ying Xia,et al.  Cocaine-Induced Intracellular Signaling and Gene Expression Are Oppositely Regulated by the Dopamine D1 and D3 Receptors , 2004, The Journal of Neuroscience.

[16]  Hyejin Kang,et al.  Translational Control by MAPK Signaling in Long-Term Synaptic Plasticity and Memory , 2004, Cell.

[17]  J. Girault,et al.  Role of the ERK pathway in psychostimulant-induced locomotor sensitization , 2006, BMC Neuroscience.

[18]  B. Prasad,et al.  Neurotrophin-3 Contributes to the Initiation of Behavioral Sensitization to Cocaine by Activating the Ras/Mitogen-Activated Protein Kinase Signal Transduction Cascade , 1999, The Journal of Neuroscience.

[19]  Jesus Bertran-Gonzalez,et al.  Inhibition of ERK pathway or protein synthesis during reexposure to drugs of abuse erases previously learned place preference. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Andrew J. Crossthwaite,et al.  Inhibiting Src family tyrosine kinase activity blocks glutamate signalling to ERK1/2 and Akt/PKB but not JNK in cultured striatal neurones , 2004, Journal of neurochemistry.

[21]  T. Robbins,et al.  Neural systems of reinforcement for drug addiction: from actions to habits to compulsion , 2005, Nature Neuroscience.

[22]  Satoko Nishimoto,et al.  MAPK signalling: ERK5 versus ERK1/2 , 2006, EMBO reports.

[23]  Yehezkel Ben-Ari,et al.  The NMDA Receptor Is Coupled to the ERK Pathway by a Direct Interaction between NR2B and RasGRF1 , 2003, Neuron.

[24]  Joseph E LeDoux,et al.  Activation of extracellular signal‐regulated kinase– mitogen‐activated protein kinase cascade in the amygdala is required for memory reconsolidation of auditory fear conditioning , 2005, The European journal of neuroscience.

[25]  T. Robinson,et al.  Amphetamine‐evoked gene expression in striatopallidal neurons: regulation by corticostriatal afferents and the ERK/MAPK signaling cascade , 2004, Journal of neurochemistry.

[26]  T. Robinson,et al.  Knockout of ERK1 Enhances Cocaine-Evoked Immediate Early Gene Expression and Behavioral Plasticity , 2006, Neuropsychopharmacology.

[27]  P. Piazza,et al.  The MAPK pathway and Egr-1 mediate stress-related behavioral effects of glucocorticoids , 2005, Nature Neuroscience.

[28]  E. Nishida,et al.  ERK induces p35, a neuron-specific activator of Cdk5, through induction of Egr1 , 2001, Nature Cell Biology.

[29]  T. Sotnikova,et al.  Paradoxical Striatal Cellular Signaling Responses to Psychostimulants in Hyperactive Mice* , 2006, Journal of Biological Chemistry.

[30]  David P Wolfer,et al.  Knockout of ERK1 MAP Kinase Enhances Synaptic Plasticity in the Striatum and Facilitates Striatal-Mediated Learning and Memory , 2002, Neuron.

[31]  R. Huganir,et al.  MAPK cascade signalling and synaptic plasticity , 2004, Nature Reviews Neuroscience.

[32]  B. Everitt,et al.  Disrupting Reconsolidation of Drug Memories Reduces Cocaine-Seeking Behavior , 2005, Neuron.

[33]  Y. Shaham,et al.  Central amygdala ERK signaling pathway is critical to incubation of cocaine craving , 2005, Nature Neuroscience.

[34]  Daniele Lecca,et al.  Dopamine and drug addiction: the nucleus accumbens shell connection , 2004, Neuropharmacology.

[35]  J. Girault,et al.  Parsing Molecular and Behavioral Effects of Cocaine in Mitogen- and Stress-Activated Protein Kinase-1-Deficient Mice , 2005, The Journal of Neuroscience.

[36]  B. Roques,et al.  Importance of ERK activation in behavioral and biochemical effects induced by MDMA in mice , 2003, British journal of pharmacology.

[37]  M. Illario,et al.  Calcium/Calmodulin-dependent Protein Kinase II Binds to Raf-1 and Modulates Integrin-stimulated ERK Activation* , 2003, Journal of Biological Chemistry.

[38]  S. Hyman,et al.  Amphetamine and Dopamine-Induced Immediate Early Gene Expression in Striatal Neurons Depends on Postsynaptic NMDA Receptors and Calcium , 1996, The Journal of Neuroscience.

[39]  Cristina M. Alberini,et al.  Persistent Disruption of an Established Morphine Conditioned Place Preference , 2006, The Journal of Neuroscience.

[40]  W. Schultz.  Behavioral theories and the neurophysiology of reward. , 2006, Annual review of psychology.

[41]  J. Marshall,et al.  Molecular Substrates for Retrieval and Reconsolidation of Cocaine-Associated Contextual Memory , 2005, Neuron.

[42]  John Q. Wang,et al.  CaMKII regulates amphetamine-induced ERK1/2 phosphorylation in striatal neurons , 2002, Neuroreport.

[43]  C. Gerfen,et al.  D1 Dopamine Receptor Supersensitivity in the Dopamine-Depleted Striatum Results from a Switch in the Regulation of ERK1/2/MAP Kinase , 2002, The Journal of Neuroscience.

[44]  J. Girault,et al.  Plasticity-Associated Gene Krox24/Zif268 Is Required for Long-Lasting Behavioral Effects of Cocaine , 2006, The Journal of Neuroscience.

[45]  S. Davis,et al.  Activation of Mitogen-Activated Protein Kinase/Extracellular Signal-Regulated Kinase in Hippocampal Circuitry Is Required for Consolidation and Reconsolidation of Recognition Memory , 2003, The Journal of Neuroscience.

[46]  S. Hyman,et al.  Metabotropic Glutamate Receptors and Dopamine Receptors Cooperate to Enhance Extracellular Signal-Regulated Kinase Phosphorylation in Striatal Neurons , 2005, The Journal of Neuroscience.

[47]  J. Mandell,et al.  Differential localization of MAPK-activated protein kinases RSK1 and MSK1 in mouse brain. , 2005, Brain research. Molecular brain research.

[48]  J. Ferrell.  Self-perpetuating states in signal transduction: positive feedback, double-negative feedback and bistability. , 2002, Current opinion in cell biology.

[49]  M. Besson,et al.  Involvement of the Extracellular Signal-Regulated Kinase Cascade for Cocaine-Rewarding Properties , 2000, The Journal of Neuroscience.

[50]  W. Kolch.  Coordinating ERK/MAPK signalling through scaffolds and inhibitors , 2005, Nature Reviews Molecular Cell Biology.

[51]  T. Nabeshima,et al.  Regulations of methamphetamine reward by extracellular signal-regulated kinase 1/2/ets-like gene-1 signaling pathway via the activation of dopamine receptors. , 2004, Molecular pharmacology.

[52]  L. Mao,et al.  Amphetamine Increases Phosphorylation of Extracellular Signal-regulated Kinase and Transcription Factors in the Rat Striatum via Group I Metabotropic Glutamate Receptors , 2002, Neuropsychopharmacology.

[53]  S. Hyman,et al.  Neural mechanisms of addiction: the role of reward-related learning and memory. , 2006, Annual review of neuroscience.

[54]  Angus C Nairn,et al.  Regulation of a protein phosphatase cascade allows convergent dopamine and glutamate signals to activate ERK in the striatum. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Q. Tang,et al.  The Scaffold Protein Homer1b/c Links Metabotropic Glutamate Receptor 5 to Extracellular Signal-Regulated Protein Kinase Cascades in Neurons , 2005, The Journal of Neuroscience.

[56]  J. Girault,et al.  Addictive and non‐addictive drugs induce distinct and specific patterns of ERK activation in mouse brain , 2004, The European journal of neuroscience.