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The Journal of Neuroscience, August 23, 2006, 26(34):8847-8856; doi:10.1523/JNEUROSCI.1919-06.2006

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Cellular/Molecular
Isoform Specificity of PKC Translocation in Living Aplysia Sensory Neurons and a Role for Ca²⁺-Dependent PKC APL I in the Induction of Intermediate-Term Facilitation

Yali Zhao,^1,3 Karina Leal,^2,3 * Carole Abi-Farah,^4 * Kelsey C. Martin,^1,3 Wayne S. Sossin,⁴ and Marc Klein^2,3

¹Department of Psychiatry and Biobehavioral Science, ²Department of Physiological Science, and ³Brain Research Institute, University of California at Los Angeles, Los Angeles, California 90095-1606, and ⁴Department of Neurology and Neurosurgery, McGill University, Montreal, Canada H3A 2B4

Correspondence should be addressed to Marc Klein, University of California at Los Angeles, Department of Physiological Science, 621 Charles Young Drive South, Los Angeles, CA 90095-1606. Email: kleinm{at}ucla.edu

Protein kinase Cs (PKCs) are important effectors of synaptic plasticity. In Aplysia, there are two major phorbol ester-activated PKCs, Ca²⁺-activated PKC Apl I and Ca²⁺-independent PKC Apl II. Functional Apl II, but not Apl I, in sensory neurons is required for a form of short-term facilitation induced at sensorimotor synapses by the facilitatory transmitter serotonin (5-HT). Because PKCs are activated by translocating from the cytoplasm to the membrane, we used fluorescently tagged PKCs to determine the isoform and cell-type specificity of translocation in living Aplysia neurons. In Sf9 cells, low levels of diacylglycerol translocate Apl II, but not Apl I, which requires calcium for translocation at low concentrations of diacylglycerol. Accordingly, application of 5-HT to Aplysia sensory neurons in the absence of neuronal firing translocates Apl II, but not Apl I, consistent with the role of Apl II in short-term facilitation. This translocation is observed in sensory neurons, but not in motor neurons. Apl I translocates only if 5-HT is coupled to firing in the sensory neuron; firing alone is ineffective. Because combined 5-HT and firing are required for the induction of one type of intermediate-term facilitation at these synapses, we asked whether this form of synaptic plasticity involves activation of Apl I. We report here that dominant-negative Apl I, but not Apl II, blocks intermediate-term facilitation. Thus, different isoforms of PKC translocate under different conditions to mediate distinct types of synaptic plasticity: Ca²⁺-independent Apl II is involved in short-term facilitation, and Ca²⁺-dependent Apl I contributes to intermediate-term facilitation.

Key words: synapses; synaptic transmission; synaptic plasticity; protein kinase C; Aplysia; learning

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Received May 4, 2005; revised July 18, 2006; accepted July 18, 2006.

Correspondence should be addressed to Marc Klein, University of California at Los Angeles, Department of Physiological Science, 621 Charles Young Drive South, Los Angeles, CA 90095-1606. Email: kleinm{at}ucla.edu

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