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J. Biol. Chem., Vol. 277, Issue 48, 45969-45976, November 29, 2002

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Differences in Apparent Pore Sizes of Low and High Voltage-activated Ca²⁺ Channels^*

Mauro Cataldi^§, Edward Perez-Reyes^¶, and Richard W. Tsien

From the  Department of Molecular and Cellular Physiology, Stanford University School of Medicine, Stanford, California 94305-5345 and the ^¶ Department of Pharmacology, University of Virginia, Charlottesville, Virginia 22908

Pore size is of considerable interest in voltage-gated Ca²⁺ channels because they exemplify a fundamental ability of certain ion channels: to display large pore diameter, but also great selectivity for their ion of choice. We determined the pore size of several voltage-dependent Ca²⁺ channels of known molecular composition with large organic cations as probes. T-type channels supported by the Ca_V3.1, Ca_V3.2, and Ca_V3.3 subunits; L-type channels encoded by the Ca_V1.2, ₁, and ₂₁ subunits; and R-type channels encoded by the Ca_V2.3 and ₃ subunits were each studied using a Xenopus oocyte expression system. The weak permeabilities to organic cations were resolved by looking at inward tails generated upon repolarization after a large depolarizing pulse. Large inward NH currents and sizable methylammonium and dimethylammonium currents were observed in all of the channels tested, whereas trimethylammonium permeated only through L- and R-type channels, and tetramethylammonium currents were observed only in L-type channels. Thus, our experiments revealed an unexpected heterogeneity in pore size among different Ca²⁺ channels, with L-type channels having the largest pore (effective diameter = 6.2 Å), T-type channels having the tiniest pore (effective diameter = 5.1 Å), and R-type channels having a pore size intermediate between these extremes. These findings ran counter to first-order expectations for these channels based simply on their degree of selectivity among inorganic cations or on the bulkiness of their acidic side chains at the locus of selectivity.

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