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The Journal of Neuroscience, June 16, 2004, 24(24):5585-5591; doi:10.1523/JNEUROSCI.1296-04.2004

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Cellular/Molecular
Ligand-Dependent Activation of Slo Family Channels Is Defined by Interchangeable Cytosolic Domains

Xiao-Ming Xia, Xue Zhang, and Christopher J. Lingle

Department of Anesthesiology, Washington University School of Medicine, St. Louis, Missouri 63110

Large-conductance Ca²⁺- and voltage-regulated K⁺ channels (Slo1 BK-type) are controlled by two physiological stimuli, membrane voltage and cytosolic Ca²⁺. Regulation by voltage is similar to that in voltage-dependent K⁺ channels, arising from positively charged amino acids primarily within the S4 transmembrane helices. The basis for regulation by Ca²⁺ remains controversial. One viewpoint suggests that the extensive cytosolic C terminus contains the Ca²⁺ regulatory machinery, whereas another suggests that the pore-forming module contains the Ca²⁺-sensing elements. To address this issue, we take advantage of another Slo family member, the pH-regulated homolog Slo3. We reason that if the ligand-sensing apparatus is uniquely associated with a particular domain (either the pore or the cytosolic domain), exchange of those domains between Slo1 and Slo3 should result in exchange of ligand dependence in association with the key domain. The results show that the Slo3 cytosolic module confers pH-dependent regulation on the Slo1 pore module, whereas the Slo1 cytosolic module confers Ca²⁺-dependent regulation on the Slo3 pore module. Thus, ligand-specific regulation is defined by interchangeable cytosolic regulatory modules.

Key words: BK channels; calcium [Ca]; potassium; channel; oocyte; patch-clamp; Ca²⁺ dependence; Slo1; Slo3

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Received April 6, 2004; revised May 7, 2004; accepted May 10, 2004.

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