2,024
Views
6
CrossRef citations to date
0
Altmetric
Review

Regulatory mechanisms of mitochondrial BKCa channels

ORCID Icon, ORCID Icon, ORCID Icon, & ORCID Icon
Pages 424-437 | Received 01 Feb 2021, Accepted 05 Apr 2021, Published online: 06 May 2021

References

  • Xu W, Liu Y, Wang S, et al. Cytoprotective role of Ca2+- activated K+ channels in the cardiac inner mitochondrial membrane. Science. 2002;298:1029–1033.
  • Singh H, Lu R, Bopassa JC, et al. mitoBKCa is encoded by the Kcnma1 gene, and a splicing sequence defines its mitochondrial location. Proc Natl Acad Sci U S A. 2013;110:10836–10841.
  • Zhang J, Li M, Zhang Z, et al. The mitochondrial BKCa channel cardiac interactome reveals BKCa association with the mitochondrial import receptor subunit Tom22, and the adenine nucleotide translocator. Mitochondrion. 2017;33:84–101.
  • Balderas E, Torres NS, Rosa-Garrido M, et al. MitoBKCa channel is functionally associated with its regulatory beta1 subunit in cardiac mitochondria. J Physiol. 2019;597:3817–3832.
  • Kravenska Y, Nieznanska H, Nieznanski K, et al. The monomers, oligomers, and fibrils of amyloid-beta inhibit the activity of mitoBKCa channels by a membrane-mediated mechanism. Biochim Biophys Acta Biomembr. 2020;1862:183337.
  • Schreiber M, Salkoff L. A novel calcium-sensing domain in the BK channel. Biophys J. 1997;73:1355–1363
  • Wojtovich AP, Sherman TA, Nadtochiy SM, et al. SLO-2 is cytoprotective and contributes to mitochondrial potassium transport. PLoS One. 2011;6:e28287.
  • Gururaja Rao S, Bednarczyk P, Towheed A, et al. BKCa (Slo) Channel Regulates Mitochondrial Function and Lifespan in Drosophila melanogaster. Cells. 2019;8. DOI:https://doi.org/10.3390/cells8090945
  • Koszela-Piotrowska I, Matkovic K, Szewczyk A, et al. A large-conductance calcium-activated potassium channel in potato (Solanum tuberosum) tuber mitochondria. Biochem J. 2009;424:307–316.
  • Laskowski M, Kicinska A, Szewczyk A, et al. Mitochondrial large-conductance potassium channel from Dictyostelium discoideum. Int J Biochem Cell Biol. 2015;60:167–175.
  • Díaz L, Meera P, Amigo J, et al. Role of the S4 segment in a voltage-dependent calcium-sensitive potassium (hSlo) channel. J Biol Chem. 1998;273:32430–32436.
  • Horrigan FT, Aldrich RW. Allosteric voltage gating of potassium channels II. Mslo channel gating charge movement in the absence of Ca(2+). J Gen Physiol. 1999;114:305–336.
  • Horrigan FT, Cui J, Aldrich RW. Allosteric voltage gating of potassium channels I. Mslo ionic currents in the absence of Ca(2+). J Gen Physiol. 1999;114:277–304.
  • Stefani E, Ottolia M, Noceti F, et al. Voltage-controlled gating in a large conductance Ca2+-sensitive K+channel (hslo). Proc Natl Acad Sci U S A. 1997;94:5427–5431.
  • Siemen D, Loupatatzis C, Borecky J, et al. Ca2+-Activated K Channel of the BK-Type in the Inner Mitochondrial Membrane of a Human Glioma Cell Line. Biochim Biophys Res Comm. 1999;257:549–554.
  • Barrett JN, Barrett EF, Dribin LB. Calcium-dependent slow potassium conductance in rat skeletal myotubes. In Press. 1981; 82.
  • Latorre R, Oberhauser A, Labarca P, et al. Varieties of calcium-activated potassium channels. Ann Rev Physiol. 1989;51:385–399.
  • Latorre R, Vergara C, Hidalgo C. Reconstitution in planar lipid bilayers of a Ca2+-dependent K+ channel from transverse tubule membranes isolated from rabbit skeletal muscle. Proc Natl Acad Sci USA. 1982;79:805–809.
  • Balderas E, Zhang J, Stefani E, et al. Mitochondrial BKCa channel. Front Physiol. 2015;6:104.
  • Singh H, Stefani E, Toro L. Intracellular BK(Ca) (iBK(Ca)) channels. J Physiol. 2012;590:5937–5947.
  • Ohya S, Kuwata Y, Sakamoto K, et al. Cardioprotective effects of estradiol include the activation of large-conductance Ca(2+)-activated K(+) channels in cardiac mitochondria. Am J Physiol Heart Circ Physiol. 2005;289:H1635–H1642.
  • Soltysinska E, Bentzen BH, Barthmes M, et al. KCNMA1 encoded cardiac BK channels afford protection against ischemia-reperfusion injury. PLoS One. 2014;9:e103402.
  • Frankenreiter S, Bednarczyk P, Kniess A, et al. cGMP-Elevating Compounds and Ischemic Conditioning Provide Cardioprotection Against Ischemia and Reperfusion Injury via Cardiomyocyte-Specific BK Channels. Circulation. 2017;136:2337–2355.
  • Barrett JN, Magleby KL, Pallotta BS. Properties of single calcium-activated potassium channels in cultured rat muscle. J Physiol. 1982;331:211–230.
  • Blatz AL, Magleby KL. Ion conductance and selectivity of single calcium-activated potassium channels in cultured rat muscle. J Gen Physiol. 1984;84:1–23.
  • Meech RW, Standen NB. Potassium activation in helix aspersa neurons under voltage clamp: a component mediated by calcium influx. J Physiol. 1975;249:211–239.
  • Cox DH, Cui J, Aldrich RW. Allosteric gating of a large conductance Ca-activated K+ channel. J Gen Physiol. 1997;110:257–281.
  • Horrigan FT, Aldrich RW. Coupling between voltage sensor activation, Ca2+ binding and channel opening in large conductance (BK) potassium channels. J Gen Physiol. 2002;120:267–305.
  • Lee US, Cui J. BK channel activation: structural and functional insights. Trends Neurosci. 2010;33:415–423.
  • Ma Z, Lou XJ, Horrigan FT. Role of charged residues in the S1-S4 voltage sensor of BK channels. J Gen Physiol. 2006;127:309–328.
  • Pantazis A, Gudzenko V, Savalli N, et al. Operation of the voltage sensor of a human voltage- and Ca2+-activated K+ channel. Proc Natl Acad Sci U S A. 2010;107:4459–4464.
  • Rothberg BS, Magleby KL. 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;111:751–780.
  • Rothberg BS, Magleby KL. Gating kinetics of single large-conductance Ca2+-activated K+ channels in high Ca2+ suggest a two-tiered allosteric gating mechanism. J Gen Physiol. 1999;114:93–124.
  • Hoshi T, Pantazis A, Olcese R. Transduction of voltage and Ca2+ signals by Slo1 BK channels. Physiology (Bethesda). 2013;28:172–189.
  • Yuan P, Leonetti MD, Pico AR, et al. Structure of the human BK channel Ca2+-activation apparatus at 3.0 A resolution. Science. 2010;329:182–186.
  • Yusifov T, Javaherian AD, Pantazis A, et al. The RCK1 domain of the human BKCa channel transduces Ca2+ binding into structural rearrangements. J Gen Physiol. 2010;136:189–202.
  • Yusifov T, Savalli N, Gandhi CS, et al. The RCK2 domain of the human BKCa channel is a calcium sensor. Proc Natl Acad Sci U S A. 2008;105:376–381.
  • Savalli N, Pantazis A, Yusifov T, et al. The contribution of RCK domains to human BK channel allosteric activation. J Biol Chem. 2012;287:21741–21750.
  • Hite RK, Tao X, MacKinnon R. Structural basis for gating the high-conductance Ca(2+)-activated K(+) channel. Nature. 2017;541:52–57.
  • Tao X, Hite RK, MacKinnon R. Cryo-EM structure of the open high-conductance Ca(2+)-activated K(+) channel. Nature. 2017;541:46–51.
  • Yuan P, Leonetti MD, Hsiung Y, et al. Open structure of the Ca2+ gating ring in the high-conductance Ca2+-activated K+ channel. Nature. 2012;481:94–97.
  • Geng Y, Deng Z, Zhang G, et al. Coupling of Ca(2+) and voltage activation in BK channels through the alphaB helix/voltage sensor interface. Proc Natl Acad Sci U S A. 2020;117:14512–14521.
  • Miranda P, Giraldez T, Holmgren M. Interactions of divalent cations with calcium binding sites of BK channels reveal independent motions within the gating ring. Proc Natl Acad Sci U S A. 2016;113:14055–14060.
  • Giraldez T, Rothberg BS. Understanding the conformational motions of RCK gating rings. J Gen Physiol. 2017;149:431–441.
  • Meera P, Wallner M, Jiang Z, et al. A calcium switch for the functional coupling between a (hslo) and b subunits (KV,Cab) of maxi K channels. FEBS Lett. 1996;382:84–88.
  • Schiller J, Schiller Y, Stuart G, et al. Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J Physiol. 1997;505(Pt 3):605–616.
  • Marrion NV, Tavalin SJ. Selective activation of Ca2+-activated K+ channels by co-localized Ca2+ channels in hippocampal neurons. Nature. 1998;395:900–905.
  • Jaggar JH, Porter VA, Lederer WJ, et al. Calcium sparks in smooth muscle. Am J Physiol Cell Physiol. 2000;278:C235–C256.
  • Jeevaratnam K, Chadda KR, Huang CL, et al. Cardiac Potassium Channels: physiological Insights for Targeted Therapy. J Cardiovasc Pharmacol Ther. 2018;23:119–129.
  • Bauer TM, Murphy E. Role of Mitochondrial Calcium and the Permeability Transition Pore in Regulating Cell Death. Circ Res. 2020;126:280–293.
  • Kirichok Y, Krapivinsky G, Clapham DE. The mitochondrial calcium uniporter is a highly selective ion channel. Nature. 2004;427:360–364.
  • Bernardi P. Mitochondria in muscle cell death. Ital J Neurol Sci. 1999;20:395–400.
  • Testai L, Martelli A, Marino A, et al. The activation of mitochondrial BK potassium channels contributes to the protective effects of naringenin against myocardial ischemia/reperfusion injury. Biochem Pharmacol. 2013;85:1634–1643.
  • Aon MA, Cortassa S, Wei AC, et al. Energetic performance is improved by specific activation of K+ fluxes through K(Ca) channels in heart mitochondria. Biochim Biophys Acta. 2010;1797:71–80.
  • Halestrap AP, Richardson AP. The mitochondrial permeability transition: a current perspective on its identity and role in ischaemia/reperfusion injury. J Mol Cell Cardiol. 2015;78:129–141.
  • Wang X, Yin C, Xi L, et al. Opening of Ca2+-activated K+ channels triggers early and delayed preconditioning against I/R injury independent of NOS in mice. Am J Physiol Heart Circ Physiol. 2004;287:H2070–H2077.
  • Gonzalez-Perez V, Lingle CJ. Regulation of BK Channels by Beta and Gamma Subunits. Annu Rev Physiol. 2019;81:113–137.
  • Zeng XH, Xia XM, Lingle CJ. Redox-sensitive extracellular gates formed by auxiliary beta subunits of calcium-activated potassium channels. Nat Struct Biol. 2003;10:448–454.
  • Uebele VN, Lagrutta A, Wade T, et al. Cloning and functional expression of 2 families of {beta}-subunits of the large conductance calcium-activated K+ channel. J Biol Chem. 2000;275:23211–23218.
  • Xia XM, Ding JP, Zeng XH, et al. Rectification and rapid activation at low Ca2+ of Ca2+-activated, voltage-dependent BK currents: consequences of rapid inactivation by a novel beta subunit. J Neurosci. 2000;20:4890–4903.
  • Savalli N, Kondratiev A, De Quintana SB, et al. Modes of operation of the BKCa channel beta2 subunit. J Gen Physiol. 2007;130:117–131.
  • Orio P, Latorre R. Differential effects of beta 1 and beta 2 subunits on BK channel activity. J Gen Physiol. 2005;125:395–411.
  • Xia XM, Ding JP, Lingle CJ. Molecular basis for the inactivation of Ca2+- and voltage-dependent BK channels in adrenal chromaffin cells and rat insulinoma tumor cells. J Neurosci. 1999;19:5255–5264.
  • Dolan J, Walshe K, Alsbury S, et al. The extracellular leucine-rich repeat superfamily; a comparative survey and analysis of evolutionary relationships and expression patterns. BMC Genomics. 2007;8:320.
  • Yan J, Aldrich RW. BK potassium channel modulation by leucine-rich repeat-containing proteins. Proc Natl Acad Sci U S A. 2012;109:7917–7922.
  • Yan J, Aldrich RW. LRRC26 auxiliary protein allows BK channel activation at resting voltage without calcium. Nature. 2010;466:513–516.
  • Gonzalez-Perez V, Xia XM, Lingle CJ. Functional regulation of BK potassium channels by gamma1 auxiliary subunits. Proc Natl Acad Sci U S A. 2014;111:4868–4873.
  • Almassy J, Begenisich T. The LRRC26 protein selectively alters the efficacy of BK channel activators. Mol Pharmacol. 2012;81:21–30.
  • Carrasquel-Ursulaez W, Alvarez O, Bezanilla F, et al. Determination of the Stoichiometry between alpha- and gamma1 Subunits of the BK Channel Using LRET. Biophys J. 2018;114:2493–2497.
  • Gonzalez-Perez V, Ben Johny M, Xia XM, et al. Regulatory gamma1 subunits defy symmetry in functional modulation of BK channels. Proc Natl Acad Sci U S A. 2018;115:9923–9928.
  • Cui J, Yang H, Lee US. Molecular mechanisms of BK channel activation. Cell Mol Life Sci. 2009;66:852–875.
  • Kulawiak B, Bednarczyk P. Reconstitution of brain mitochondria inner membrane into planar lipid bilayer. Acta Neurobiol Exp. 2005;65:271–276
  • Gu XQ, Siemen D, Parvez S et al. Hypoxia increases BK channel activity in the inner mitochondrial membrane. Biochem Biophys Res Commun. 2007;358:311–316
  • Cheng Y, Gu XQ, Bednarczyk P et al. Hypoxia increases activity of the BK-channel in the inner mitochondrial membrane and reduces activity of the permeability transition pore. Cell Physiol Biochemistry. 2008;22:127–136
  • Skalska J, Piwonska M, Wyroba E et al. A novel potassium channel in skeletal muscle mitochondria. Biochimica et Biophysica Acta. 2008; 1777:651–659
  • Skalska J, Bednarczyk P, Piwonska M et al. Calcium ions regulate K+ uptake into brain mitochondria: The evidence for a novel potassium channel. Int J Mol Sci. 2009; 10:1104–1120
  • Lancaster B, Nicoll RA. Properties of two calcium-activated hyperpolarizations in rat hippocampal neurons. J Physiol. 1987;389:187–203.
  • Meredith AL, Wiler SW, Miller BH, et al. BK calcium-activated potassium channels regulate circadian behavioral rhythms and pacemaker output. Nat Neurosci. 2006;9:1041–1049.
  • Brayden JE, Nelson MT. Regulation of arterial tone by activation of calcium-dependent potassium channels. Science. 1992;256:532–535.
  • Ledoux J, Werner ME, Brayden JE, et al. Calcium-activated potassium channels and the regulation of vascular tone. Physiology (Bethesda). 2006;21:69–78.
  • Fahanik-Babaei J, Eliassi A, Saghiri R. How many types of large conductance Ca(+)(2)-activated potassium channels exist in brain mitochondrial inner membrane: evidence for a new mitochondrial large conductance Ca(2)(+)-activated potassium channel in brain mitochondria. Neuroscience. 2011;199:125–132.
  • Bednarczyk P, Koziel A, Jarmuszklewicz W, et al. Large-conductance Ca2+-activated potassium channel in mitochondria of endothelial EA.hy926 cells. Am J Physiol Heart Circ Physiol. 2013;304:H1415–H1427
  • Isaacson JS, Murphy GJ. Glutamate-mediated extrasynaptic inhibition: direct coupling of NMDA receptors to Ca(2+)-activated K+ channels. Neuron. 2001;31:1027–1034
  • Berkefeld H, Sailer CA, Bildl W, et al. BKCa-Cav channel complexes mediate rapid and localized Ca2+-activated K+ signaling. Science. 2006;314:615–620
  • Bao L, Cox DH. Gating and ionic currents reveal how the BKCa channel’s Ca2+ sensitivity is enhanced by its beta1 subunit. J Gen Physiol. 2005;126:393–412.
  • Brenner R, Perez GJ, Bonev AD, et al. Vasoregulation by the beta1 subunit of the calcium-activated potassium channel. Nature. 2000;407:870–876.
  • Nimigean CM, Magleby KL. The beta subunit increases the Ca2+ sensitivity of large conductance Ca2+-activated potassium channels by retaining the gating in the bursting states [In Process Citation]. J Gen Physiol. 1999;113:425–440.
  • Sweet TB, Cox DH. Measuring the influence of the BKCa {beta}1 subunit on Ca2+ binding to the BKCa channel. J Gen Physiol. 2009;133:139–150.
  • Tanaka Y, Meera P, Song M, et al. Molecular constituents of maxi KCa channels in human coronary smooth muscle. Predominant a + b subunit complexes. J Physiol. 1997;502:545–557.
  • Bautista L, Castro MJ, Lopez-Barneo J, et al. Hypoxia inducible factor-2alpha stabilization and maxi-K+ channel beta1-subunit gene repression by hypoxia in cardiac myocytes: role in preconditioning. Circ Res. 2009;104:1364–1372.
  • Xin F, Cheng Y, Ren J, et al. The extracellular loop of the auxiliary beta1-subunit is involved in the regulation of BKCa channel mechanosensitivity. Am J Physiol Cell Physiol. 2018;315:C485–C493.
  • Walewska A, Kulawiak B, Szewczyk A, et al. Mechanosensitivity of mitochondrial large-conductance calcium-activated potassium channels. Biochim Biophys Acta Bioenerg. 2018;1859:797–805.
  • Sukharev SI, Blount P, Martinac B, et al. A large-conductance mechanosensitive channel in E. coli encoded by mscL alone. Nature. 1994;368:265–268.
  • Levina N, Totemeyer S, Stokes NR, et al. Protection of Escherichia coli cells against extreme turgor by activation of MscS and MscL mechanosensitive channels: identification of genes required for MscS activity. Embo J. 1999;18:1730–1737.
  • Brohawn SG, Su Z, MacKinnon R. Mechanosensitivity is mediated directly by the lipid membrane in TRAAK and TREK1 K+ channels. Proc Natl Acad Sci U S A. 2014;111:3614–3619.
  • Murthy SE, Dubin AE, Whitwam T, et al. OSCA/TMEM63 are an Evolutionarily Conserved Family of Mechanically Activated Ion Channels. Elife. 2018;7.
  • Syeda R, Florendo MN, Cox CD, et al. Piezo1 Channels Are Inherently Mechanosensitive. Cell Rep. 2016;17:1739–1746.
  • Latorre R, Castillo K, Carrasquel-Ursulaez W, et al. Molecular Determinants of BK Channel Functional Diversity and Functioning. Physiol Rev. 2017;97:39–87.
  • Coste B, Mathur J, Schmidt M, et al. Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science. 2010;330:55–60.
  • Shin KC, Park HJ, Kim JG, et al. The Piezo2 ion channel is mechanically activated by low-threshold positive pressure. Sci Rep. 2019; 9: 6446
  • Zhao H, Sokabe M. Tuning the mechanosensitivity of a BK channel by changing the linker length. Cell Res. 2008;18:871–878.
  • Naruse K, Tang QY, Sokabe M. Stress-Axis Regulated Exon (STREX) in the C terminus of BK(Ca) channels is responsible for the stretch sensitivity. Biochem Biophys Res Commun. 2009;385:634–639.
  • Tian L, Jeffries O, McClafferty H, et al. Palmitoylation gates phosphorylation-dependent regulation of BK potassium channels. Proc Natl Acad Sci U S A. 2008;105:21006–21011.
  • Jeffries O, Geiger N, Rowe IC, et al. Palmitoylation of the S0-S1 linker regulates cell surface expression of voltage- and calcium-activated potassium (BK) channels. J Biol Chem. 2010;285:33307–33314.
  • Sanabria-Castro A, Alvarado-Echeverria I, Monge-Bonilla C. Molecular Pathogenesis of Alzheimer’s Disease: an Update. Ann Neurosci. 2017;24:46–54.
  • Wang W, Zhao F, Ma X, et al. Mitochondria dysfunction in the pathogenesis of Alzheimer’s disease: recent advances. Mol Neurodegeneration. 2020;15:30.
  • Reiss AB, Arain HA, Stecker MM, et al. Amyloid toxicity in Alzheimer’s disease. Rev Neurosci. 2018;29:613–627.
  • Ferreiro E, Oliveira CR, Pereira CMF. The release of calcium from the endoplasmic reticulum induced by amyloid-beta and prion peptides activates the mitochondrial apoptotic pathway. Neurobiol Dis. 2008;30:331–342.
  • Hanson-Petersen CA, Alikhani N, Behbahani H, et al. The amyloid b-peptide is imported into mitochondria via the TOM import machinery and localized to mitochondrial cristae. PNAS. 2008;105(35):13145–13150.
  • Gao Q, Fang Y, Zhang S, et al. Dynamic effect of beta-amyloid 42 on cell mechanics. J Biomech. 2019;86:79–88.