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The Journal of Neuroscience, April 27, 2005, 25(17):4279-4287; doi:10.1523/JNEUROSCI.5019-04.2005

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Cellular/Molecular
Nuclear Ca²+ and the cAMP Response Element-Binding Protein Family Mediate a Late Phase of Activity-Dependent Neuroprotection

Sofia Papadia,¹ Patrick Stevenson,¹ Neil R. Hardingham,² Hilmar Bading,³ and Giles E. Hardingham¹

¹Centre for Neuroscience Research, University of Edinburgh, Summerhall, Edinburgh EH9 1QH, United Kingdom, ²Department of Physiology, University of Oxford, Oxford OX1 3PT, United Kingdom, and ³Department of Neurobiology, Interdisciplinary Center for Neurosciences, D-69120 Heidelberg, Germany

The mechanism by which physiological synaptic NMDA receptor activity promotes neuronal survival is not well understood. Here, we show that that an episode of synaptic activity can promote neuroprotection for a long time after that activity has ceased. This long-lasting or "late phase" of neuroprotection is dependent on nuclear calcium signaling and cAMP response element (CRE)-mediated gene expression. In contrast, neuroprotection evoked acutely by ongoing synaptic activity relies solely on the activation of the phosphatidylinositol 3-kinase/Akt pathway. This "acute phase" does not require nuclear calcium signaling and is independent of activation of the CRE-binding protein (CREB) family of transcription factors. Thus, activity-dependent neuroprotection comprises two mechanistically distinct phases that differ in their spatial requirements for calcium and in their reliance on the CREB family.

Key words: apoptosis; calcium; [Ca]; neuroprotection; NMDA receptors; CREB; CaM kinase

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Received Dec 9, 2004; revised February 16, 2005; accepted March 16, 2005.

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