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The Journal of Neuroscience, October 15, 1999, 19(20):8830-8838

Domains Responsible for Constitutive and Ca2+-Dependent Interactions between Calmodulin and Small Conductance Ca2+-Activated Potassium Channels

John E. Keen1, Radwan Khawaled1, David L. Farrens2, Torben Neelands1, Andre Rivard1, Chris T. Bond1, Aaron Janowsky4, Bernd Fakler5, John P. Adelman1, and James Maylie3

1 Vollum Institute, 2 Departments of Biochemistry and Molecular Biology, 3 Obstetrics and Gynecology, and 4 Research Service, Veteran's Administration Medical Center, and Department of Psychiatry, Behavioral Neuroscience, and Physiology and Pharmacology, Oregon Health Sciences University, Portland Oregon, 97201, and 5 Department of Physiology, University of Tüebingen, Tüebingen, Germany

Small conductance Ca2+-activated potassium channels (SK channels) are coassembled complexes of pore-forming SK alpha  subunits and calmodulin. We proposed a model for channel activation in which Ca2+ binding to calmodulin induces conformational rearrangements in calmodulin and the alpha  subunits that result in channel gating. We now report fluorescence measurements that indicate conformational changes in the alpha  subunit after calmodulin binding and Ca2+ binding to the alpha  subunit-calmodulin complex. Two-hybrid experiments showed that the Ca2+-independent interaction of calmodulin with the alpha  subunits requires only the C-terminal domain of calmodulin and is mediated by two noncontiguous subregions; the ability of the E-F hands to bind Ca2+ is not required. Although SK alpha  subunits lack a consensus calmodulin-binding motif, mutagenesis experiments identified two positively charged residues required for Ca2+-independent interactions with calmodulin. Electrophysiological recordings of SK2 channels in membrane patches from oocytes coexpressing mutant calmodulins revealed that channel gating is mediated by Ca2+ binding to the first and second E-F hand motifs in the N-terminal domain of calmodulin. Taken together, the results support a calmodulin- and Ca2+-calmodulin-dependent conformational change in the channel alpha  subunits, in which different domains of calmodulin are responsible for Ca2+-dependent and Ca2+-independent interactions. In addition, calmodulin is associated with each alpha  subunit and must bind at least one Ca2+ ion for channel gating. Based on these results, a state model for Ca2+ gating was developed that simulates alterations in SK channel Ca2+ sensitivity and cooperativity associated with mutations in CaM.

Key words: SK channels; afterhyperpolarization; calmodulin; Ca2+-gating; Ca2+-independent interactions; state model

Copyright © 1999 Society for Neuroscience  0270-6474/99/19208830-09$05.00/0


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