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The Journal of Neuroscience, July 15, 1999, 19(14):5861-5874
Ca2+-Permeable AMPA Receptors Induce Phosphorylation of cAMP Response Element-Binding Protein through a Phosphatidylinositol 3-Kinase-Dependent Stimulation of the Mitogen-Activated Protein Kinase Signaling Cascade in Neurons
Michael S. Perkinton1, Talvinder S. Sihra2, and Robert J. Williams1 1 Biochemical Neuropharmacology Group, Neuroscience Research Centre, Guy's, King's, and St. Thomas' Schools of Biomedical Sciences, Guy's Campus, London, SE1 9RT, United Kingdom, and 2 Department of Pharmacology, Medawar Building, University College London, London, WC1E 6BT, United Kingdom
Ca2+-permeable AMPA receptors may play a key role during developmental neuroplasticity, learning and memory, and neuronal loss in a number of neuropathologies. However, the intracellular signaling pathways used by AMPA receptors during such processes are not fully understood. The mitogen-activated protein kinase (MAPK) cascade is an attractive target because it has been shown to be involved in gene expression, synaptic plasticity, and neuronal stress. Using primary cultures of mouse striatal neurons and a phosphospecific MAPK antibody we addressed whether AMPA receptors can activate the MAPK cascade. We found that in the presence of cyclothiazide, AMPA caused a robust and direct (no involvement of NMDA receptors or L-type voltage-sensitive Ca2+ channels) Ca2+-dependent activation of MAPK through MAPK kinase (MEK). This activation was blocked by GYKI 53655, a noncompetitive selective antagonist of AMPA receptors. Probing the mechanism of this activation revealed an essential role for phosphatidylinositol 3-kinase (PI 3-kinase) and the involvement of a pertussis toxin (PTX)-sensitive G-protein, a Src family protein tyrosine kinase, and Ca2+/calmodulin-dependent kinase II. Similarly, kainate activated MAPK in a PI 3-kinase-dependent manner. AMPA receptor-evoked neuronal death and arachidonic acid mobilization did not appear to involve signaling through the MAPK pathway. However, AMPA receptor stimulation led to a Ca2+-dependent phosphorylation of the nuclear transcription factor CREB, which could be prevented by inhibitors of MEK or PI 3-kinase. Our results indicate that Ca2+-permeable AMPA receptors transduce signals from the cell surface to the nucleus of neurons through a PI 3-kinase-dependent activation of MAPK. This novel pathway may play a pivotal role in regulating synaptic plasticity in the striatum.
Key words: AMPA; mitogen-activated protein kinase; phosphatidylinositol 3-kinase; CREB; wortmannin; LY 294002; pertussis toxin; G-protein; PP2; cyclothiazide; glutamate; kainate; calcium/calmodulin-dependent kinase II; tyrosine kinase; AMPA toxicity; arachidonic acid; striatum; striatal neurons
Copyright © 1999 Society for Neuroscience 0270-6474/99/19145861-14$05.00/0
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