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J Neurophysiol 95: 2878-2888, 2006. First published January 25, 2006; doi:10.1152/jn.01352.2005
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beta2 and beta4 Subunits of BK Channels Confer Differential Sensitivity to Acute Modulation by Steroid Hormones

J. T. King1, P. V. Lovell1, M. Rishniw2, M. I. Kotlikoff2, M. L. Zeeman3 and D. P. McCobb1

1Department of Neurobiology and Behavior and 2Department of Biomedical Sciences, Cornell University, Ithaca, New York: and 3Department of Applied Mathematics, University of Texas, San Antonio, Texas

Submitted 22 December 2005; accepted in final form 24 January 2006

Membrane-associated receptors for rapid, steroidal neuromodulation remain elusive. Estradiol has been reported to facilitate activation of voltage- and Ca2+-dependent BK potassium channels encoded by Slo, if associated with beta1 subunits. We show here that 1) multiple members of the beta family confer sensitivity to multiple steroids on BK channels, 2) that beta subunits differentiate between steroids, and 3) that different betas have distinct relative preferences for particular steroids. Expressed in HEK 293 cells, inside-out patches with channels composed of Slo-{alpha} alone showed no steroid sensitivity. Cells expressing {alpha}beta4 exhibited potent, rapid, reversible, and dose-dependent potentiation by corticosterone (CORT; a glucocorticoid), and were potentiated to a lesser degree by other sex and stress steroids. In contrast, {alpha}beta2 channels were potentiated more strongly by dehydroepiandrosterone (DHEA; an enigmatic, stress-related adrenal androgen), and to a lesser extent by CORT, estradiol, testosterone, and DHEA-S. Cholesterol had no effect on any BK channel compositions tested. Conductance–voltage plots of channels composed of {alpha} plus beta2 or beta4 subunits were shifted in the negative direction by steroids, indicating greater activation at negative voltages. Thus our results argue that the variety of Slo-beta subunit coexpression patterns occurring in vivo expands the repertoire of Slo channel gating in yet another dimension not fully appreciated, rendering BK gating responsive to dynamic fluctuations in a multiple of steroid hormones.

Address for reprint requests and other correspondence: D. P. McCobb, Dept. of Neurobiology and Behavior, W153 Mudd Hall, Cornell Univ., Ithaca, NY 14853 (E-mail: dpm9{at}cornell.edu)




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