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J. Biol. Chem., Vol. 281, Issue 40, 30195-30211, October 6, 2006

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Molecular Network and Chromosomal Clustering of Genes Involved in Synaptic Plasticity in the Hippocampus^*

Chang Sin Park, Ruomu Gong, Joshua Stuart, and Shao-Jun Tang¹

From the Department of Neurobiology and Behavior, Center for Neurobiology of Learning and Memory, University of California, Irvine, California 92697-3800 and the Department of Biomolecular Engineering, University of California, Santa Cruz, California 95064

Gene transcription is required for establishing and maintaining the enduring form of long term potentiation (LTP). However, the transcriptome and its associated molecular programs that support LTP are not well understood. The purpose of this study was to identify activity-regulated genes (ARGs) and their molecular pathways that are modulated by LTP induction and to investigate the genomic mechanism for coordinating the transcription of ARGs. We performed time course DNA microarray analyses on the mouse dentate gyrus to determine the temporal genomic expression profiles of ARGs in response to LTP-inducing tetanic stimulation. Our studies uncovered ARGs that regulate various cellular processes, including the structure and function of the synapse, and offered an overview of the dynamic molecular programs that are probably important for LTP. Surprisingly, we found that ARGs are clustered on chromosomes, and ARG clusters are conserved during evolution. Although ARGs in the same cluster have apparently different molecular properties, they are functionally correlated by regulating LTP. In addition, ARGs in specific clusters are co-regulated by the cAMP-response element-binding protein. We propose that chromosomal clustering provides a genomic mechanism for coordinating the transcription of ARGs involved in LTP.

Received for publication, June 19, 2006 , and in revised form, July 19, 2006.

^* The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Fig. 1 and supplemental Tables 1-4.

¹ Supported by Whitehall Foundation, American Heart Association, EJLB Foundation, and United States Army Medical Research and Materiel Command. To whom correspondence should be addressed: 303 Qureshey Research Laboratory, Center for Neurobiology of Learning and Memory, University of California, Irvine, CA 92697-3800. Tel.: 949-824-9580; Fax: 949-824-9762; E-mail: stang{at}uci.edu.

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