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J. Biol. Chem., Vol. 276, Issue 32, 29891-29898, August 10, 2001

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Characteristics of a Store-operated Calcium-permeable Channel
SARCOENDOPLASMIC RETICULUM CALCIUM PUMP FUNCTION CONTROLS CHANNEL GATING^*

Xibao Liu and Indu S. Ambudkar

From the Secretory Physiology Section, GTTB, NIDCR, National Institutes of Health, Bethesda, Maryland 20892

We examined the single channel properties and regulation of store-operated calcium channels (SOCC). In human submandibular gland cells, carbachol (CCh) induced flickery channel activity while thapsigargin (Tg) induced burst-like activity, with relatively lower open probability (NP_o) and longer mean open time. Tg- and CCh-activated channels were permeable to Na⁺ and Ba²⁺, but not to NMDG, in the absence of Ca²⁺. The channels exhibited similar Ca²⁺, Na⁺, and Ba²⁺ conductances and were inhibited by 2-aminoethoxydiphenylborate, xestospongin C, Gd³⁺, and La³⁺. CCh stimulated flickery activity changed to burst-like activity by (i) addition of Tg, (ii) using Na⁺ instead of Ca²⁺, (iii) using Ca²⁺-free bath solution, or (iv) buffering [Ca²⁺]_i with BAPTA-AM. Buffering [Ca²⁺]_i induced a 2-fold increase in NP_o of Tg-stimulated SOCC. Reducing free [Ca²⁺] in the endoplasmic reticulum with the divalent cation chelator, N,N,N',N'-tetrakis(2-pyridylmethyl)ethylenediamine (TPEN), induced burst-like channel activity similar to that seen with CCh + Tg. Thus, SOCC is activated by stimulation of muscarinic receptors, inhibition of the sarcoendoplasmic Ca²⁺ pump, and lowering [Ca²⁺] in the internal store. Importantly, SOCC activity depends on [Ca²⁺]_i and the free [Ca²⁺] in the internal store. These novel findings reveal that SERCA plays a major role in the gating of SOCC by (i) refilling the internal Ca²⁺ store(s) and (ii) decreasing the [Ca²⁺]_i-dependent inhibition.

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