Journal of Neurophysiology, Vol 72, Issue 3 1240-1249, Copyright © 1994 by APS

ARTICLES

Activators of protein kinase C mimic serotonin-induced modulation of a voltage-dependent potassium current in pleural sensory neurons of Aplysia

S. Sugita, D. A. Baxter and J. H. Byrne
Department of Neurobiology and Anatomy, University of Texas Medical School at Houston 77225.

1. In the pleural mechanoafferent sensory neurons of Aplysia, serotonin (5-HT)-induced spike broadening consists of at least two components: a cAMP and protein kinase A (PKA)-dependent, rapidly developing component and a protein kinase C (PKC)-dependent, slowly developing component. Voltage-clamp experiments were conducted to identify currents that are modulated by PKC and thus may contribute to the slowly developing component of 5-HT-induced spike broadening. 2. We compared the effects of phorbol esters, activators of PKC, on membrane currents with those of 5-HT. Bath application of 5-HT had complex modulatory effects on currents elicited by voltage-clamp pulses to potentials > 0 mV. The kinetics of both activation and inactivation of the membrane currents were slowed by 5-HT. This led to a decrease in an outward current at the beginning of the voltage-clamp pulse and an increase at the end of the pulse. Previous work has shown that these effects represent, in part, the modulation of a large, voltage-dependent K+ current (IK,V) by 5-HT. 3. Active phorbol esters mimicked some of the actions of 5-HT on membrane currents in that they slowed activation and inactivation kinetics of current responses to voltage-clamp pulses more positive than 0 mV. This led to a decrease in an outward current at the beginning of the pulse and an increase at the end of the pulse. Because inactive phorbols did not mimic the actions of 5-HT, the effects of active phorbol esters appeared to be PKC specific. In addition, preexposure of the sensory neurons to active phorbol esters appeared to occlude the modulatory actions of 5-HT on IK,V. Thus it is likely that modulation of IK,V by 5-HT is mediated, at lease in part, by PKC. 4. To further characterize which currents were modulated by PKC, low concentrations of tetraethylammonium (TEA, 2 mM) were used to block Ca(2+)-activated K+ current (IK,Ca). Low TEA partially blocked the phorbol ester-induced increase of the outward current at the end of voltage-clamp pulses. These results agreed with previous reports that activation of PKC enhanced a fast component of IK,Ca in these sensory neurons. Such an enhancement would lead to an increase in outward current that should be blocked by low TEA. Low TEA, however, did not affect phorbol ester-induced decrease of the outward current at the beginning of pulse, where the predominant current is IK,V, which is less sensitive to TEA.(ABSTRACT TRUNCATED AT 400 WORDS)

This article has been cited by other articles:

				W. S. Sossin Isoform specificity of protein kinase Cs in synaptic plasticity Learn. Mem., April 2, 2007; 14(4): 236 - 246. [Abstract] [Full Text] [PDF]

				J. W. Jacklet and D. G. Tieman Nitric Oxide and Histamine Induce Neuronal Excitability by Blocking Background Currents in Neuron MCC of Aplysia J Neurophysiol, February 1, 2004; 91(2): 656 - 665. [Abstract] [Full Text] [PDF]

				D. Barbas, L. DesGroseillers, V. F. Castellucci, T. J. Carew, and S. Marinesco Multiple Serotonergic Mechanisms Contributing to Sensitization in Aplysia: Evidence of Diverse Serotonin Receptor Subtypes Learn. Mem., September 1, 2003; 10(5): 373 - 386. [Abstract] [Full Text] [PDF]

				J. E. Cohen, C. U. Onyike, V. L. McElroy, A. H. Lin, and T. W. Abrams Pharmacological Characterization of an Adenylyl Cyclase-Coupled 5-HT Receptor in Aplysia: Comparison With Mammalian 5-HT Receptors J Neurophysiol, March 1, 2003; 89(3): 1440 - 1455. [Abstract] [Full Text] [PDF]

				P. F. Van Soest, J. C. Lodder, and K. S. Kits Activation of Protein Kinase C by Oxytocin-Related Conopressin Underlies Pacemaker Current in Lymnaea Central Neurons J Neurophysiol, November 1, 2000; 84(5): 2541 - 2551. [Abstract] [Full Text] [PDF]

				L. E. Fox and P. E. Lloyd Role of cAMP in the Short-Term Modulation of a Neuromuscular System in Aplysia J Neurophysiol, March 1, 2000; 83(3): 1567 - 1579. [Abstract] [Full Text] [PDF]

				C. C. Gandhi and L. D. Matzel Modulation of Presynaptic Action Potential Kinetics Underlies Synaptic Facilitation of Type B Photoreceptors after Associative Conditioning in Hermissenda J. Neurosci., March 1, 2000; 20(5): 2022 - 2035. [Abstract] [Full Text] [PDF]

				D. A. Baxter, C. C. Canavier, J. W. Clark Jr., and J. H. Byrne Computational Model of the Serotonergic Modulation of Sensory Neurons in Aplysia J Neurophysiol, December 1, 1999; 82(6): 2914 - 2935. [Abstract] [Full Text] [PDF]

				L. L. Stark and T. J. Carew Developmental Dissociation of Serotonin-Induced Spike Broadening and Synaptic Facilitation in Aplysia Sensory Neurons J. Neurosci., January 1, 1999; 19(1): 334 - 346. [Abstract] [Full Text] [PDF]

				P. F. van Soest and K. S. Kits Conopressin Affects Excitability, Firing, and Action Potential Shape Through Stimulation of Transient and Persistent Inward Currents in Mulluscan Neurons J Neurophysiol, April 1, 1998; 79(4): 1619 - 1632. [Abstract] [Full Text] [PDF]

				F. Manseau, W. S. Sossin, and V. F. Castellucci Long-Term Changes in Excitability Induced by Protein Kinase C Activation in Aplysia Sensory Neurons J Neurophysiol, March 1, 1998; 79(3): 1210 - 1218. [Abstract] [Full Text] [PDF]

				S. S. Bedi, A. Salim, S. Chen, and D. L. Glanzman Long-Term Effects of Axotomy on Excitability and Growth of Isolated Aplysia Sensory Neurons in Cell Culture: Potential Role of cAMP J Neurophysiol, March 1, 1998; 79(3): 1371 - 1383. [Abstract] [Full Text] [PDF]

				S. Sugita, D. A. Baxter, and J. H. Byrne Modulation of a cAMP/Protein Kinase A Cascade by Protein Kinase C in Sensory Neurons of Aplysia J. Neurosci., October 1, 1997; 17(19): 7237 - 7244. [Abstract] [Full Text] [PDF]

				K. Nakanishi, F. Zhang, D. A. Baxter, A. Eskin, and J. H. Byrne Role of Calcium-Calmodulin-Dependent Protein Kinase II in Modulation of Sensorimotor Synapses in Aplysia J Neurophysiol, July 1, 1997; 78(1): 409 - 416. [Abstract] [Full Text] [PDF]

				S. Barnes and J. W. Jacklet Ionic Currents of Isolated Retinal Pacemaker Neurons: Projected Daily Phase Differences and Selective Enhancement by a Phase-Shifting Neurotransmitter J Neurophysiol, June 1, 1997; 77(6): 3075 - 3084. [Abstract] [Full Text] [PDF]

				S. Sugita, D. A. Baxter, and J. H. Byrne Differential Effects of 4-Aminopyridine, Serotonin, and Phorbol Esters on Facilitation of Sensorimotor Connections in Aplysia J Neurophysiol, January 1, 1997; 77(1): 177 - 185. [Abstract] [Full Text] [PDF]

				W S Sossin An autonomous kinase generated during long-term facilitation in Aplysia is related to the Ca(2+)-independent protein kinase C Apl II. Learn. Mem., January 1, 1997; 3(5): 389 - 401. [Abstract] [PDF]

				L J Cleary, J H Byrne, and W N Frost Role of interneurons in defensive withdrawal reflexes in Aplysia. Learn. Mem., January 1, 1995; 2(3-4): 133 - 151. [PDF]