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The Journal of Neuroscience, July 29, 2009, 29(30):9553-9562; doi:10.1523/JNEUROSCI.1512-09.2009

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Cellular/Molecular
Poly-(ADP-Ribose) Polymerase-1 Is Necessary for Long-Term Facilitation in Aplysia

A. Iván Hernández,^1,2 Jason Wolk,¹ Jiang-Yuan Hu,¹ Jinming Liu,¹ Takeshi Kurosu,¹ James H. Schwartz,¹  and Samuel Schacher¹

¹Department of Neuroscience, College of Physicians and Surgeons, Columbia University, New York State Psychiatric Institute, New York, New York 10032, and ²Department of Pathology, State University of New York, Downstate Medical Center, Brooklyn, New York 11203

Correspondence should be addressed to Samuel Schacher, Department of Neuroscience, College of Physicians and Surgeons, Columbia University, New York State Psychiatric Institute, 1051 Riverside Drive, New York, NY 10032. Email: sms2{at}columbia.edu

Activity-dependent long-term synaptic plasticity requires gene expression and protein synthesis. Identifying essential genes and studying their transcriptional and translational regulation are key steps to understanding how synaptic changes become long lasting. Recently, the enzyme poly-(ADP-ribose) polymerase 1 (PARP-1) was shown to be necessary for long-term memory (LTM) in Aplysia. Since PARP-1 decondenses chromatin, we hypothesize that this enzyme regulates the expression of specific genes essential for long-term synaptic plasticity that underlies LTM. We cloned Aplysia PARP-1 (ApPARP-1) and determined that its expression in sensory neurons is necessary for serotonin (5-HT)-mediated long-term facilitation (LTF) of sensorimotor neuron synapses. PARP enzymatic activity is also required, since transient application of PARP inhibitors blocked LTF. Differential display and RNA analysis of ganglia dissected from intact animals exposed to 5-HT identified the ribosomal RNA genes as PARP-dependent effector genes. The increase in the expression of rRNAs is long lasting and dynamic. Pulse-labeling RNA studies showed a PARP-dependent increase in rRNAs but not in the total RNA 24 h after 5-HT treatment. Moreover, the expression of both the AprpL27a (Aplysia ribosomal protein L27a) and the ApE2N (Aplysia ubiquitin-conjugating enzyme E2N) mRNAs also increased after 5-HT. Thus, our results suggest that 5-HT, in part by regulating PARP-1 activity, alters the expression of transcripts required for the synthesis of new ribosomes necessary for LTF.

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Received March 30, 2009; revised May 18, 2009; accepted June 19, 2009.

Correspondence should be addressed to Samuel Schacher, Department of Neuroscience, College of Physicians and Surgeons, Columbia University, New York State Psychiatric Institute, 1051 Riverside Drive, New York, NY 10032. Email: sms2{at}columbia.edu

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