Abstract
The Ca2+-dependent gating mechanism of cloned BK channels from Drosophila (dSlo) was studied. Both a natural variant (A1/C2/E1/G3/IO) and a mutant (S942A) were expressed in Xenopus oocytes, and single-channel currents were recorded from excised patches of membrane. Stability plots were used to define stable segments of data. Unlike native BK channels from rat skeletal muscle in which increasing internal Ca2+ concentration (Cai2+) in the range of 5 to 30 microM increases mean open time, increasing Cai2+ in this range for dSlo had little effect on mean open time. However, further increases in Cai2+ to 300 or 3000 microM then typically increased dSlo mean open time. Kinetic schemes for the observed Ca2+-dependent gating kinetics of dSlo were evaluated by fitting two-dimensional dwell-time distributions using maximum likelihood techniques and by comparing observed dependency plots with those predicted by the models. Previously described kinetic schemes that largely account for the Ca2+-dependent kinetics of native BK channels from rat skeletal muscle did not adequately describe the Ca2+ dependence of dSlo. An expanded version of these schemes which, in addition to the Ca2+-activation steps, permitted a Ca2+-facilitated transition from each open state to a closed state, could approximate the Ca2+-dependent kinetics of dSlo, suggesting that Ca2+ may exert dual effects on gating.
Full Text
The Full Text of this article is available as a PDF (458.1 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Adelman J. P., Shen K. Z., Kavanaugh M. P., Warren R. A., Wu Y. N., Lagrutta A., Bond C. T., North R. A. Calcium-activated potassium channels expressed from cloned complementary DNAs. Neuron. 1992 Aug;9(2):209–216. doi: 10.1016/0896-6273(92)90160-f. [DOI] [PubMed] [Google Scholar]
- Atkinson N. S., Robertson G. A., Ganetzky B. A component of calcium-activated potassium channels encoded by the Drosophila slo locus. Science. 1991 Aug 2;253(5019):551–555. doi: 10.1126/science.1857984. [DOI] [PubMed] [Google Scholar]
- Blatz A. L., Magleby K. L. Quantitative description of three modes of activity of fast chloride channels from rat skeletal muscle. J Physiol. 1986 Sep;378:141–174. doi: 10.1113/jphysiol.1986.sp016212. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bowlby M. R., Levitan I. B. Kinetic variability and modulation of dSlo, a cloned calcium-dependent potassium channel. Neuropharmacology. 1996;35(7):867–875. doi: 10.1016/0028-3908(96)00090-1. [DOI] [PubMed] [Google Scholar]
- Butler A., Tsunoda S., McCobb D. P., Wei A., Salkoff L. mSlo, a complex mouse gene encoding "maxi" calcium-activated potassium channels. Science. 1993 Jul 9;261(5118):221–224. doi: 10.1126/science.7687074. [DOI] [PubMed] [Google Scholar]
- Ciorba M. A., Heinemann S. H., Weissbach H., Brot N., Hoshi T. Modulation of potassium channel function by methionine oxidation and reduction. Proc Natl Acad Sci U S A. 1997 Sep 2;94(18):9932–9937. doi: 10.1073/pnas.94.18.9932. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Colquhoun D., Hawkes A. G. On the stochastic properties of single ion channels. Proc R Soc Lond B Biol Sci. 1981 Mar 6;211(1183):205–235. doi: 10.1098/rspb.1981.0003. [DOI] [PubMed] [Google Scholar]
- Cox D. H., Cui J., Aldrich R. W. Allosteric gating of a large conductance Ca-activated K+ channel. J Gen Physiol. 1997 Sep;110(3):257–281. doi: 10.1085/jgp.110.3.257. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Crouzy S. C., Sigworth F. J. Yet another approach to the dwell-time omission problem of single-channel analysis. Biophys J. 1990 Sep;58(3):731–743. doi: 10.1016/S0006-3495(90)82416-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DiChiara T. J., Reinhart P. H. Distinct effects of Ca2+ and voltage on the activation and deactivation of cloned Ca(2+)-activated K+ channels. J Physiol. 1995 Dec 1;489(Pt 2):403–418. doi: 10.1113/jphysiol.1995.sp021061. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DiChiara T. J., Reinhart P. H. Redox modulation of hslo Ca2+-activated K+ channels. J Neurosci. 1997 Jul 1;17(13):4942–4955. doi: 10.1523/JNEUROSCI.17-13-04942.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eigen M. New looks and outlooks on physical enzymology. Q Rev Biophys. 1968 May;1(1):3–33. doi: 10.1017/s0033583500000445. [DOI] [PubMed] [Google Scholar]
- Esguerra M., Wang J., Foster C. D., Adelman J. P., North R. A., Levitan I. B. Cloned Ca(2+)-dependent K+ channel modulated by a functionally associated protein kinase. Nature. 1994 Jun 16;369(6481):563–565. doi: 10.1038/369563a0. [DOI] [PubMed] [Google Scholar]
- Ferguson W. B. Competitive Mg2+ block of a large-conductance, Ca(2+)-activated K+ channel in rat skeletal muscle. Ca2+, Sr2+, and Ni2+ also block. J Gen Physiol. 1991 Jul;98(1):163–181. doi: 10.1085/jgp.98.1.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Giangiacomo K. M., Garcia-Calvo M., Knaus H. G., Mullmann T. J., Garcia M. L., McManus O. Functional reconstitution of the large-conductance, calcium-activated potassium channel purified from bovine aortic smooth muscle. Biochemistry. 1995 Dec 5;34(48):15849–15862. doi: 10.1021/bi00048a031. [DOI] [PubMed] [Google Scholar]
- Gibb A. J., Kojima H., Carr J. A., Colquhoun D. Expression of cloned receptor subunits produces multiple receptors. Proc Biol Sci. 1990 Nov 22;242(1304):108–112. doi: 10.1098/rspb.1990.0112. [DOI] [PubMed] [Google Scholar]
- Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
- Hicks G. A., Marrion N. V. Ca2+-dependent inactivation of large conductance Ca2+-activated K+ (BK) channels in rat hippocampal neurones produced by pore block from an associated particle. J Physiol. 1998 May 1;508(Pt 3):721–734. doi: 10.1111/j.1469-7793.1998.721bp.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hirschberg B., Maylie J., Adelman J. P., Marrion N. V. Gating of recombinant small-conductance Ca-activated K+ channels by calcium. J Gen Physiol. 1998 Apr;111(4):565–581. doi: 10.1085/jgp.111.4.565. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hoshi T., Zagotta W. N., Aldrich R. W. Shaker potassium channel gating. I: Transitions near the open state. J Gen Physiol. 1994 Feb;103(2):249–278. doi: 10.1085/jgp.103.2.249. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hudspeth A. J., Lewis R. S. Kinetic analysis of voltage- and ion-dependent conductances in saccular hair cells of the bull-frog, Rana catesbeiana. J Physiol. 1988 Jun;400:237–274. doi: 10.1113/jphysiol.1988.sp017119. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Keller B. U., Montal M. S., Hartshorne R. P., Montal M. Two-dimensional probability density analysis of single channel currents from reconstituted acetylcholine receptors and sodium channels. Arch Biochem Biophys. 1990 Jan;276(1):47–54. doi: 10.1016/0003-9861(90)90008-m. [DOI] [PubMed] [Google Scholar]
- Krause J. D., Foster C. D., Reinhart P. H. Xenopus laevis oocytes contain endogenous large conductance Ca2(+)-activated K+ channels. Neuropharmacology. 1996;35(7):1017–1022. doi: 10.1016/0028-3908(96)00134-7. [DOI] [PubMed] [Google Scholar]
- Lagrutta A., Shen K. Z., North R. A., Adelman J. P. Functional differences among alternatively spliced variants of Slowpoke, a Drosophila calcium-activated potassium channel. J Biol Chem. 1994 Aug 12;269(32):20347–20351. [PubMed] [Google Scholar]
- Laver D. R. Divalent cation block and competition between divalent and monovalent cations in the large-conductance K+ channel from Chara australis. J Gen Physiol. 1992 Aug;100(2):269–300. doi: 10.1085/jgp.100.2.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Magleby K. L., Song L. Dependency plots suggest the kinetic structure of ion channels. Proc Biol Sci. 1992 Aug 22;249(1325):133–142. doi: 10.1098/rspb.1992.0095. [DOI] [PubMed] [Google Scholar]
- Magleby K. L., Weiss D. S. Identifying kinetic gating mechanisms for ion channels by using two-dimensional distributions of simulated dwell times. Proc Biol Sci. 1990 Sep 22;241(1302):220–228. doi: 10.1098/rspb.1990.0089. [DOI] [PubMed] [Google Scholar]
- McManus O. B. Calcium-activated potassium channels: regulation by calcium. J Bioenerg Biomembr. 1991 Aug;23(4):537–560. doi: 10.1007/BF00785810. [DOI] [PubMed] [Google Scholar]
- McManus O. B., Helms L. M., Pallanck L., Ganetzky B., Swanson R., Leonard R. J. Functional role of the beta subunit of high conductance calcium-activated potassium channels. Neuron. 1995 Mar;14(3):645–650. doi: 10.1016/0896-6273(95)90321-6. [DOI] [PubMed] [Google Scholar]
- McManus O. B., Magleby K. L. Accounting for the Ca(2+)-dependent kinetics of single large-conductance Ca(2+)-activated K+ channels in rat skeletal muscle. J Physiol. 1991 Nov;443:739–777. doi: 10.1113/jphysiol.1991.sp018861. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McManus O. B., Magleby K. L. Kinetic states and modes of single large-conductance calcium-activated potassium channels in cultured rat skeletal muscle. J Physiol. 1988 Aug;402:79–120. doi: 10.1113/jphysiol.1988.sp017195. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Methfessel C., Boheim G. The gating of single calcium-dependent potassium channels is described by an activation/blockade mechanism. Biophys Struct Mech. 1982;9(1):35–60. doi: 10.1007/BF00536014. [DOI] [PubMed] [Google Scholar]
- Mienville J., Barker J. L., Lange G. D. Mechanosensitive properties of BK channels from embryonic rat neuroepithelium. J Membr Biol. 1996 Oct;153(3):211–216. doi: 10.1007/s002329900124. [DOI] [PubMed] [Google Scholar]
- Nelson M. T., Cheng H., Rubart M., Santana L. F., Bonev A. D., Knot H. J., Lederer W. J. Relaxation of arterial smooth muscle by calcium sparks. Science. 1995 Oct 27;270(5236):633–637. doi: 10.1126/science.270.5236.633. [DOI] [PubMed] [Google Scholar]
- Petersen O. H., Maruyama Y. Calcium-activated potassium channels and their role in secretion. Nature. 1984 Feb 23;307(5953):693–696. doi: 10.1038/307693a0. [DOI] [PubMed] [Google Scholar]
- Reinhart P. H., Chung S., Martin B. L., Brautigan D. L., Levitan I. B. Modulation of calcium-activated potassium channels from rat brain by protein kinase A and phosphatase 2A. J Neurosci. 1991 Jun;11(6):1627–1635. doi: 10.1523/JNEUROSCI.11-06-01627.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Robitaille R., Garcia M. L., Kaczorowski G. J., Charlton M. P. Functional colocalization of calcium and calcium-gated potassium channels in control of transmitter release. Neuron. 1993 Oct;11(4):645–655. doi: 10.1016/0896-6273(93)90076-4. [DOI] [PubMed] [Google Scholar]
- Rothberg B. S., Bello R. A., Magleby K. L. Two-dimensional components and hidden dependencies provide insight into ion channel gating mechanisms. Biophys J. 1997 Jun;72(6):2524–2544. doi: 10.1016/S0006-3495(97)78897-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rothberg B. S., Bello R. A., Song L., Magleby K. L. High Ca2+ concentrations induce a low activity mode and reveal Ca2(+)-independent long shut intervals in BK channels from rat muscle. J Physiol. 1996 Jun 15;493(Pt 3):673–689. doi: 10.1113/jphysiol.1996.sp021414. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rothberg B. S., Magleby K. L. Kinetic structure of large-conductance Ca2+-activated K+ channels suggests that the gating includes transitions through intermediate or secondary states. A mechanism for flickers. J Gen Physiol. 1998 Jun;111(6):751–780. doi: 10.1085/jgp.111.6.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schreiber M., Salkoff L. A novel calcium-sensing domain in the BK channel. Biophys J. 1997 Sep;73(3):1355–1363. doi: 10.1016/S0006-3495(97)78168-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sigworth F. J., Sine S. M. Data transformations for improved display and fitting of single-channel dwell time histograms. Biophys J. 1987 Dec;52(6):1047–1054. doi: 10.1016/S0006-3495(87)83298-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Silberberg S. D., Lagrutta A., Adelman J. P., Magleby K. L. Wanderlust kinetics and variable Ca(2+)-sensitivity of dSlo [correction of Drosophila], a large conductance CA(2+)-activated K+ channel, expressed in oocytes. Biophys J. 1996 Jul;71(1):2640–2651. [PMC free article] [PubMed] [Google Scholar]
- Stefani E., Ottolia M., Noceti F., Olcese R., Wallner M., Latorre R., Toro L. Voltage-controlled gating in a large conductance Ca2+-sensitive K+channel (hslo). Proc Natl Acad Sci U S A. 1997 May 13;94(10):5427–5431. doi: 10.1073/pnas.94.10.5427. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thuringer D., Findlay I. Contrasting effects of intracellular redox couples on the regulation of maxi-K channels in isolated myocytes from rabbit pulmonary artery. J Physiol. 1997 May 1;500(Pt 3):583–592. doi: 10.1113/jphysiol.1997.sp022044. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wu Y. C., Art J. J., Goodman M. B., Fettiplace R. A kinetic description of the calcium-activated potassium channel and its application to electrical tuning of hair cells. Prog Biophys Mol Biol. 1995;63(2):131–158. doi: 10.1016/0079-6107(95)00002-5. [DOI] [PubMed] [Google Scholar]