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J Neurophysiol 88: 954-964, 2002;
0022-3077/02 $5.00
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The Journal of Neurophysiology Vol. 88 No. 2 August 2002, pp. 954-964
Copyright ©2002 by the American Physiological Society

Developmental Regulation of Neuronal KCa Channels by TGFbeta 1: An Essential Role for PI3 Kinase Signaling and Membrane Insertion

Loic Lhuillier and Stuart E. Dryer

Department of Biology and Biochemistry, University of Houston, Houston, Texas 77204-5513

Lhuillier, Loic and Stuart E. Dryer. Developmental Regulation of Neuronal KCa Channels by TGFbeta 1: An Essential Role for PI3 Kinase Signaling and Membrane Insertion. J. Neurophysiol. 88: 954-964, 2002. TGFbeta 1 is a target-derived factor responsible for the developmental expression of large-conductance Ca2+-activated K+ (KCa) channels in ciliary neurons of the chick ciliary ganglion. The acute effects of TGFbeta 1 on KCa channels are mediated by posttranslational events and require activation of the MAP kinase Erk. Here we show that TGFbeta 1 evokes robust phosphorylation of Akt/PKB, a protein kinase dependent on the products of phosphatidylinositol 3-OH kinase (PI3K). TGFbeta 1-evoked stimulation of KCa channels is blocked by the PI3K inhibitors wortmannin and LY294002. These drugs also inhibit TGFbeta 1 effects on Akt/PKB phosphorylation but have no effect on TGFbeta 1-evoked Erk activation. Application of the MEK1 inhibitor PD98059 blocked TGFbeta 1 effects on Erk but had no effect on Akt/PKB phosphorylation. These results indicate that PI3K and Erk represent parallel signaling cascades activated by TGFbeta 1 in ciliary neurons. The effects of TGFbeta 1 on functional expression of KCa are blocked by the microtubule inhibitors colchicine and nocodazole, by botulinum toxins A and E, and by brefeldin-A, an agent that disrupts the Golgi apparatus. These data indicate that translocation of a membrane protein, possibly Slowpoke (SLO), is required for the acute posttranslational effects of TGFbeta 1 on KCa channels. Confocal immunofluorescence studies with three different SLO antisera showed robust expression of SLO in multiple intracellular compartments of embryonic day 9-13 ciliary neurons, including the cell nucleus. These data suggest that TGFbeta 1 evokes insertion of SLO channels into the plasma membrane as a result of signaling cascades that entail activation of Erk and PI3K.




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