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J Biol Chem, Vol. 273, Issue 17, 10402-10410, April 24, 1998

Characterization of a Ca²⁺ Release-activated Nonselective Cation Current Regulating Membrane Potential and [Ca²⁺]_i Oscillations in Transgenically Derived -Cells

Michael W. Roe, Jennings F. Worley III^§, Feng Qian^¶, Natalia Tamarina, Anshu A. Mittal, Flora Dralyuk, Nathaniel T. Blair, Robert J. Mertz^§, Louis H. Philipson, and Iain D. Dukes^§

From the Departments of  Medicine and ^¶ Pharmacology and Physiology, University of Chicago, Chicago, Illinois 60637 and the ^§ Department of Cell Physiology, Glaxo Wellcome Research Institute, Research Triangle Park, North Carolina 27709

Although stimulation of insulin secretion by glucose is regulated by coupled oscillations of membrane potential and intracellular Ca²⁺ ([Ca²⁺]_i), the membrane events regulating these oscillations are incompletely understood. In the presence of glucose and tetraethylammonium, transgenically derived -cells (TC3-neo) exhibit coupled voltage and [Ca²⁺]_i oscillations strikingly similar to those observed in normal islets in response to glucose. Using these cells as a model system, we investigated the membrane conductance underlying these oscillations. Alterations in delayed rectifier or Ca²⁺-activated K⁺ channels were excluded as a source of the conductance oscillations, as they are completely blocked by tetraethylammonium. ATP-sensitive K⁺ channels were also excluded, since the ATP-sensitive K⁺ channel blocker tolbutamide substituted for glucose in inducing [Ca²⁺]_i oscillations. Thapsigargin, which depletes intracellular Ca²⁺ stores, and maitotoxin, an activator of nonselective cation channels, both converted the glucose-dependent [Ca²⁺]_i oscillations into a sustained elevation. On the other hand, both SKF 96365, a blocker of Ca²⁺ store-operated channels, and external Na⁺ removal suppressed the glucose-stimulated [Ca²⁺]_i oscillations. Maitotoxin activated a nonselective cation current in TC3 cells that was attenuated by removal of extracellular Na⁺ and by SKF 96365, in the same manner to a current activated in mouse -cells following depletion of intracellular Ca²⁺ stores. Currents similar to these are produced by the mammalian trp-related channels, a gene family that includes Ca²⁺ store-operated channels and inositol 1,4,5-trisphosphate-activated channels. We found several of the trp family genes were expressed in TC3 cells by reverse transcriptase polymerase chain reaction using specific primers, but by Northern blot analysis, mtrp-4 was the predominant message expressed. We conclude that a conductance underlying glucose-stimulated oscillations in -cells is provided by a Ca²⁺ store depletion-activated nonselective cation current, which is plausibly encoded by homologs of trp genes.

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