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J. Biol. Chem., Vol. 279, Issue 50, 52324-52330, December 10, 2004

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The Appearance of a Protein Kinase A-regulated Splice Isoform of slo Is Associated with the Maturation of Neurons That Control Reproductive Behavior^*

Yalan Zhang, William J. Joiner, Arin Bhattacharjee, Francois Rassendren¶, Neil S. Magoski||, and Leonard K. Kaczmarek**

From the Department of Pharmacology, Yale University School of Medicine, New Haven, Connecticut 06520, the Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania 94080, ^¶Institut de Genetique Humaine, CNRS UPR 1142, 141 Rue de la Cardonile, F-34396 Montpellier Cedex 5, France, and the ^||Department of Physiology, Queen's University, Kingston, Ontario K7L 3N6, Canada

In response to brief synaptic stimulation that activates protein kinase A (PKA), the bag cell neurons of Aplysia trigger the onset of reproductive behaviors by generating a prolonged afterdischarge. In juvenile animals, such afterdischarges are inhibited by a high density of Ca²⁺-activated K⁺ (BK) channels, encoded by the slo gene. An increase in this current also follows an afterdischarge in mature animals, contributing to a subsequent refractory state that limits reproductive behaviors. Using a bag cell cDNA library, we have isolated two alternative transcripts of the slo gene, differing in the presence (slo-a) or absence (slo-b) of a consensus phosphorylation site for PKA. Expression of either isoform in Chinese hamster ovary cells produced Ca²⁺- and voltage-dependent channels with macroscopic and unitary properties matching those in bag cell neurons. The isoforms differed, however, in their response to application of the catalytic subunit of PKA, which reduced the open probability of Slo-a, an effect that was reversed by a PKA inhibitor. In contrast, PKA had no effect on Slo-b. By immunocytochemistry, we determined that the PKA-regulated Slo-a subunit is present in adult, but not juvenile, bag cell neurons. Patch clamp recordings from adult and juvenile bag cell neurons confirmed that PKA decreases BK channel activity only in adults. Our findings suggest that a change in the identity of Slo isoforms expressed during development allows mature neurons to generate afterdischarges that are required for reproduction.

Received for publication, July 28, 2004 , and in revised form, September 13, 2004.

^* 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 nucleotide sequence(s) reported in this paper has been submitted to the DDBJ/GenBank^TM/EBI Data Bank with accession number(s) AY359443.

^** To whom correspondence should be addressed. Tel.: 203-785-4500; Fax: 203-785-5494; E-mail: leonard.kaczmarek{at}yale.edu.

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