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The Journal of Neuroscience, October 6, 2004, 24(40):8829-8837; doi:10.1523/JNEUROSCI.2167-04.2004

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Cellular/Molecular
Coregulation of Glutamate Uptake and Long-Term Sensitization in Aplysia

Omar Khabour,¹ Jonathan Levenson,¹ Lisa C. Lyons,¹ Lorna S. Kategaya,¹ Jeannie Chin,² John H. Byrne,² and Arnold Eskin¹

¹Department of Biology and Biochemistry, University of Houston, Houston, Texas 77204-5001, and ² Department of Neurobiology and Anatomy, University of Texas-Houston Medical School, Houston, Texas 77225

In Aplysia, long-term facilitation (LTF) at sensorimotor synapses of the pleural-pedal ganglia is mediated by an increase in the release of a neurotransmitter, which appears to be glutamate. Glutamate uptake also is increased in sensory neurons 24 hr after the induction of long-term sensitization (Levenson et al., 2000b). The present study investigated whether the same signaling pathways were involved in the long-term increase in glutamate uptake as in the induction of LTF. Thus, roles for cAMP, PKA (cAMP-dependent protein kinase), MAPK (mitogen-activated protein kinase), and tyrosine kinase in the regulation of glutamate uptake were tested. We found that 5-HT increased cAMP and activated PKA in sensory neurons. Exposure of pleural-pedal ganglia to analogs of cAMP or forskolin increased glutamate uptake 24 hr after treatments. Inhibitors of PKA (KT5720), MAPK (U0126 and PD98059), and tyrosine kinase (genistein) blocked the long-term increase in glutamate uptake produced by 5-HT. In addition, bpV, a tyrosine phosphatase inhibitor, facilitated the ability of subthreshold levels of 5-HT to increase glutamate uptake. Inhibition of PKC, which is not involved in LTF, had no effect on the long-term increase in glutamate uptake produced by 5-HT. Furthermore, activation of PKC by phorbol-12,13-dibutyrate did not produce long-term changes in glutamate uptake. The results demonstrate that the same constellation of second messengers and kinases is involved in the long-term regulation of both glutamate release and glutamate uptake. These similarities in signaling pathways suggest that regulation of glutamate release and uptake during formation of long-term memory are coordinated through coregulation of these two processes.

Key words: glutamate uptake; cAMP-PKA; MAPK; tyrosine kinase; Aplysia; sensitization

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Received June 3, 2004; revised August 6, 2004; accepted August 9, 2004.

This article has been cited by other articles:

				M. Michel, I. Kemenes, U. Muller, and G. Kemenes Different phases of long-term memory require distinct temporal patterns of PKA activity after single-trial classical conditioning Learn. Mem., August 26, 2008; 15(9): 694 - 702. [Abstract] [Full Text] [PDF]

				J.-A Lee, S.-H. Lee, C. Lee, D.-J. Chang, Y. Lee, H. Kim, Y.-H. Cheang, H.-G. Ko, Y.-S. Lee, H. Jun, et al. PKA-activated ApAF-ApC/EBP heterodimer is a key downstream effector of ApCREB and is necessary and sufficient for the consolidation of long-term facilitation J. Cell Biol., September 11, 2006; 174(6): 827 - 838. [Abstract] [Full Text] [PDF]

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