Advances in Ca_V1.1 gating: New insights into permeation and voltage-sensing mechanisms

References

• Bannister RA, Beam KG. Ca(V)1.1: the atypical prototypical voltage-gated Ca2+ channel. Biochim Biophys Acta. 2013;1828:1587–16.
   PubMed Web of Science ®Google Scholar
• Block BA, Imagawa T, Campbell KP, et al. Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J Cell Biol. 1988;107:2587–2600.
   PubMed Web of Science ®Google Scholar
• Franzini-Armstrong C, Nunzi G. Junctional feet and particles in the triads of a fast-twitch muscle fibre. J Muscle Res Cell Motil. 1983;4:233–252.
   PubMed Web of Science ®Google Scholar
• Franzini-Armstrong C, Protasi F, Ramesh V. Comparative ultrastructure of Ca2+ release units in skeletal and cardiac muscle. Ann N Y Acad Sci. 1998;853:20–30.
   PubMed Web of Science ®Google Scholar
• Stanfield PR. A calcium dependent inward current in frog skeletal muscle fibres. Pflugers Arch. 1977;368:267–270.
   PubMed Web of Science ®Google Scholar
• Sanchez JA, Stefani E. Inward calcium current in twitch muscle fibres of the frog. J Physiol. 1978;283:197–209.
   PubMed Web of Science ®Google Scholar
• Robin G, Allard B. Voltage-gated Ca(2+) influx through L-type channels contributes to sarcoplasmic reticulum Ca(2+) loading in skeletal muscle. J Physiol. 2015;593:4781–4797.
   PubMed Web of Science ®Google Scholar
• Dayal A, Schrötter K, Pan Y, et al. The Ca(2+) influx through the mammalian skeletal muscle dihydropyridine receptor is irrelevant for muscle performance. Nat Commun. 2017;8:475.
   PubMed Web of Science ®Google Scholar
• Georgiou DK, Dagnino-Acosta A, Lee CS, et al. Ca2+ binding/permeation via calcium channel, CaV1.1, regulates the intracellular distribution of the fatty acid transport protein, CD36, and fatty acid metabolism. J Biol Chem. 2015;290:23751–23765.
   PubMed Web of Science ®Google Scholar
• Lee CS, Dagnino-Acosta A, Yarotskyy V, et al. Ca(2+) permeation and/or binding to CaV1.1 fine-tunes skeletal muscle Ca(2+) signaling to sustain muscle function. Skelet Muscle. 2015;5:4.
   PubMed Web of Science ®Google Scholar
• Tanabe T, Takeshima H, Mikami A, et al. Primary structure of the receptor for calcium channel blockers from skeletal muscle. Nature. 1987;328:313–318.
   PubMed Web of Science ®Google Scholar
• Ruth P, Röhrkasten A, Biel M, et al. Primary structure of the beta subunit of the DHP-sensitive calcium channel from skeletal muscle. Science. 1989;245:1115–1118.
   PubMed Web of Science ®Google Scholar
• Jay SD, Ellis SB, McCue AF, et al. Primary structure of the gamma subunit of the DHP-sensitive calcium channel from skeletal muscle. Science. 1990;248:490–492.
   PubMed Web of Science ®Google Scholar
• Campiglio M, Flucher BE. The role of auxiliary subunits for the functional diversity of voltage-gated calcium channels. J Cell Physiol. 2015;230:2019–2031.
   PubMed Web of Science ®Google Scholar
• Horstick EJ, Linsley JW, Dowling JJ, et al. Stac3 is a component of the excitation-contraction coupling machinery and mutated in Native American myopathy. Nat Commun. 2013;4:1952.
   PubMed Web of Science ®Google Scholar
• Nelson BR, Wu F, Liu Y, et al. Skeletal muscle-specific T-tubule protein STAC3 mediates voltage-induced Ca2+ release and contractility. Proc Natl Acad Sci U S A. 2013;110:11881–11886.
   PubMed Web of Science ®Google Scholar
• Polster A, Perni S, Bichraoui H, et al. Stac adaptor proteins regulate trafficking and function of muscle and neuronal L-type Ca2+ channels. Proc Natl Acad Sci U S A. 2015;112:602–606.
   PubMed Web of Science ®Google Scholar
• Polster A, Nelson BR, Olson EN, et al. Stac3 has a direct role in skeletal muscle-type excitation-contraction coupling that is disrupted by a myopathy-causing mutation. Proc Natl Acad Sci U S A. 2016;113:10986–10991.
   PubMed Web of Science ®Google Scholar
• Lacerda AE, Kim HS, Ruth P, et al. Normalization of current kinetics by interaction between the alpha 1 and beta subunits of the skeletal muscle dihydropyridine-sensitive Ca2+ channel. Nature. 1991;352:527–530.
   PubMed Web of Science ®Google Scholar
• Singer D, Biel M, Lotan I, et al. The roles of the subunits in the function of the calcium channel. Science. 1991;253:1553–1557.
   PubMed Web of Science ®Google Scholar
• Perni S. The builders of the junction: roles of junctophilin1 and junctophilin2 in the assembly of the sarcoplasmic reticulum-plasma membrane junctions in striated muscle. Biomolecules. 2022;12:109.
   PubMed Web of Science ®Google Scholar
• Pettersen EF, Goddard TD, Huang CC, et al. UCSF Chimera–a visualization system for exploratory research and analysis. J Comput Chem. 2004;25:1605–1612.
   PubMed Web of Science ®Google Scholar
• Catterall WA, Wisedchaisri G, Zheng N. The chemical basis for electrical signaling. Nat Chem Biol. 2017;13:455–463.
   PubMed Web of Science ®Google Scholar
• Yang J, Ellinor PT, Sather WA, et al. Molecular determinants of Ca2+ selectivity and ion permeation in L-type Ca2+ channels. Nature. 1993;366:158–161.
   PubMed Web of Science ®Google Scholar
• DeLano WL. The PyMOL molecular graphics system. 2002.
   Google Scholar
• Tuluc P, Molenda N, Schlick B, et al. A CaV1.1 Ca2+ channel splice variant with high conductance and voltage-sensitivity alters EC coupling in developing skeletal muscle. Biophys J. 2009;96:35–44.
   PubMed Web of Science ®Google Scholar
• Perez-Reyes E, Wei XY, Castellano A, et al. Molecular diversity of L-type calcium channels. Evidence for alternative splicing of the transcripts of three non-allelic genes. J Biol Chem. 1990;265:20430–20436.
   PubMed Web of Science ®Google Scholar
• Armstrong CM, Bezanilla FM, Horowicz P. Twitches in the presence of ethylene glycol bis(-aminoethyl ether)-N,N’-tetracetic acid. Biochim Biophys Acta. 1972;267:605–608.
   PubMed Web of Science ®Google Scholar
• Dirksen RT, Beam KG. Role of calcium permeation in dihydropyridine receptor function. Insights into channel gating and excitation-contraction coupling. J Gen Physiol. 1999;114:393–403.
   PubMed Web of Science ®Google Scholar
• Schredelseker J, Shrivastav M, Dayal A, et al. Non-Ca2+-conducting Ca2+ channels in fish skeletal muscle excitation-contraction coupling. Proc Natl Acad Sci U S A. 2010;107:5658–5663.
   PubMed Web of Science ®Google Scholar
• Dayal A, Fernández-Quintero ML, Liedl KR, et al. Pore mutation N617D in the skeletal muscle DHPR blocks Ca(2+) influx due to atypical high-affinity Ca(2+) binding. Elife. 2021;10. DOI:10.7554/eLife.63435
   Web of Science ®Google Scholar
• Idoux R, Fuster C, Jacquemond V, et al. Divalent cations permeation in a Ca(2+) non-conducting skeletal muscle dihydropyridine receptor mouse model. Cell Calcium. 2020;91:102256.
   PubMed Web of Science ®Google Scholar
• Bannister RA, Beam KG. Properties of Na+ currents conducted by a skeletal muscle L-type Ca2+ channel pore mutant (SkEIIIK). Channels. 2011;5:262–268.
   PubMed Web of Science ®Google Scholar
• Beqollari D, Dockstader K, Bannister RA. A skeletal muscle L-type Ca(2+) channel with a mutation in the selectivity filter (Ca(V)1.1 E1014K) conducts K. J Biol Chem. 2018;293:3126–3133.
   PubMed Web of Science ®Google Scholar
• Hodgkin AL, Huxley AF. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952;117:500–544.
   PubMed Web of Science ®Google Scholar
• Schneider MF, Chandler WK. Voltage dependent charge movement of skeletal muscle: a possible step in excitation-contraction coupling. Nature. 1973;242:244–246.
   PubMed Web of Science ®Google Scholar
• Rios E, Pizarro G. Voltage sensor of excitation-contraction coupling in skeletal muscle. Physiol Rev. 1991;71:849–908.
   PubMed Web of Science ®Google Scholar
• Vergara JC. Charge movement in a cut skeletal muscle fiber (Abstract). Biophys J. 1978;21:167.
   Web of Science ®Google Scholar
• Caputo C, Bolanos P. Effects of D-600 on intramembrane charge movement of polarized and depolarized frog muscle fibers. J Gen Physiol. 1989;94:43–64.
   PubMed Web of Science ®Google Scholar
• Stühmer W, Conti F, Suzuki H, et al. Structural parts involved in activation and inactivation of the sodium channel. Nature. 1989;339:597–603.
   PubMed Web of Science ®Google Scholar
• Seoh SA, Sigg D, Papazian DM, et al. Voltage-sensing residues in the S2 and S4 segments of the Shaker K+ channel. Neuron. 1996;16:1159–1167.
   PubMed Web of Science ®Google Scholar
• Li-Smerin Y, Hackos DH, Swartz KJ. alpha-helical structural elements within the voltage-sensing domains of a K(+) channel. J Gen Physiol. 2000;115:33–50.
   PubMed Web of Science ®Google Scholar
• Tao X, Lee A, Limapichat W, et al. A gating charge transfer center in voltage sensors. Science. 2010;328:67–73.
   PubMed Web of Science ®Google Scholar
• Bannister RA, Moua O, Ohrtman JD, et al. Effects of Alanine Substitutions For Highly-Conserved Phenylalanines In The Skeletal Muscle L-type calcium channel. Biophys J. 2008;98:516a.
   Web of Science ®Google Scholar
• Tuluc P, Yarov-Yarovoy V, Benedetti B, et al. Molecular interactions in the voltage sensor controlling gating properties of CaV calcium channels. Structure. 2016;24:261–271.
   PubMed Web of Science ®Google Scholar
• Tuluc P, Benedetti B, Coste de Bagneaux P, et al. Two distinct voltage-sensing domains control voltage sensitivity and kinetics of current activation in CaV1.1 calcium channels. J Gen Physiol. 2016;147:437–449.
   PubMed Web of Science ®Google Scholar
• Fernández-Quintero ML, El Ghaleb Y, Tuluc P, et al. Structural determinants of voltage-gating properties in calcium channels. Elife. 2021;10. DOI:10.7554/eLife.64087
   Web of Science ®Google Scholar
• Kovacs L, Rios E, Schneider MF. Calcium transients and intramembrane charge movement in skeletal muscle fibres. Nature. 1979;279:391–396.
   PubMed Web of Science ®Google Scholar
• Beam KG, Knudson CM, Powell JA. A lethal mutation in mice eliminates the slow calcium current in skeletal muscle cells. Nature. 1986;320:168–170.
   PubMed Web of Science ®Google Scholar
• Rios E, Brum G. Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature. 1987;325:717–720.
   PubMed Web of Science ®Google Scholar
• Tanabe T, Beam KG, Powell JA, et al. Restoration of excitation-contraction coupling and slow calcium current in dysgenic muscle by dihydropyridine receptor complementary DNA. Nature. 1988;336:134–139.
   PubMed Web of Science ®Google Scholar
• Nakai J, Tanabe T, Konno T, et al. Localization in the II-III loop of the dihydropyridine receptor of a sequence critical for excitation-contraction coupling. J Biol Chem. 1998;273:24983–24986.
   PubMed Web of Science ®Google Scholar
• Beurg M, Ahern CA, Vallejo P, et al. Involvement of the carboxy-terminus region of the dihydropyridine receptor beta1a subunit in excitation-contraction coupling of skeletal muscle. Biophys J. 1999;77:2953–2967.
   PubMed Web of Science ®Google Scholar
• Flucher BE, Campiglio M. STAC proteins: the missing link in skeletal muscle EC coupling and new regulators of calcium channel function. Biochim Biophys Acta Mol Cell Res. 2019;1866:1101–1110.
   PubMed Web of Science ®Google Scholar
• Nakai J, Dirksen RT, Nguyen HT, et al. Enhanced dihydropyridine receptor channel activity in the presence of ryanodine receptor. Nature. 1996;380:72–75.
   PubMed Web of Science ®Google Scholar
• Avila G, Dirksen RT. Functional impact of the ryanodine receptor on the skeletal muscle L-type Ca(2+) channel. J Gen Physiol. 2000;115:467–480.
   PubMed Web of Science ®Google Scholar
• Bannister RA, Sheridan DC, Beam KG. Distinct components of retrograde Ca(V)1.1-RyR1 coupling revealed by a lethal mutation in RyR1. Biophys J. 2016;110:912–921.
   PubMed Web of Science ®Google Scholar
• Bannister RA, Beam KG. Ryanodine modification of RyR1 retrogradely affects L-type Ca(2+) channel gating in skeletal muscle. J Muscle Res Cell Motil. 2009;30:217–223.
   PubMed Web of Science ®Google Scholar
• Bannister RA, Esteve E, Eltit JM, et al. A malignant hyperthermia-inducing mutation in RYR1 (R163C): consequent alterations in the functional properties of DHPR channels. J Gen Physiol. 2010;135:629–640.
   PubMed Web of Science ®Google Scholar
• Renaud JP, Chari A, Ciferri C, et al. Cryo-EM in drug discovery: achievements, limitations and prospects. Nat Rev Drug Discov. 2018;17:471–492.
   PubMed Web of Science ®Google Scholar
• Wu J, Yan Z, Li Z, et al. Structure of the voltage-gated calcium channel Cav1.1 complex. Science. 2015;350:aad2395.
   PubMed Web of Science ®Google Scholar
• Wu J, Yan Z, Li Z, et al. Structure of the voltage-gated calcium channel Ca(v)1.1 at 3.6 Å resolution. Nature. 2016;537:191–196.
   PubMed Web of Science ®Google Scholar
• Dolphin AC. Calcium channel auxiliary alpha2delta and beta subunits: trafficking and one step beyond. Nat Rev Neurosci. 2012;13:542–555.
   PubMed Web of Science ®Google Scholar
• El Ghaleb Y, Ortner NJ, Posch W, et al. Calcium current modulation by the γ1 subunit depends on alternative splicing of CaV1.1. J Gen Physiol. 2022;154. DOI:10.1085/jgp.202113028.
   PubMed Web of Science ®Google Scholar
• Carbonneau L, Bhattacharya D, Sheridan DC, et al. Multiple loops of the dihydropyridine receptor pore subunit are required for full-scale excitation-contraction coupling in skeletal muscle. Biophys J. 2005;89:243–255.
   PubMed Web of Science ®Google Scholar
• Cui Y, Tae HS, Norris NC, et al. A dihydropyridine receptor alpha1s loop region critical for skeletal muscle contraction is intrinsically unstructured and binds to a SPRY domain of the type 1 ryanodine receptor. Int J Biochem Cell Biol. 2009;41:677–686.
   PubMed Web of Science ®Google Scholar
• Gao S, Yao X, Yan N. Structure of human Ca(v)2.2 channel blocked by the painkiller ziconotide. Nature. 2021;596:143–147.
   PubMed Web of Science ®Google Scholar
• Pouvreau S, Berthier C, Blaineau S, et al. Membrane cholesterol modulates dihydropyridine receptor function in mice fetal skeletal muscle cells. J Physiol. 2004;555:365–381.
   PubMed Web of Science ®Google Scholar
• Barrientos G, Sanchez-Aguilera P, Jaimovich E, et al. Membrane cholesterol in skeletal muscle: a novel player in excitation-contraction coupling and insulin resistance. J Diabetes Res. 2017;2017:3941898.
   PubMed Web of Science ®Google Scholar
• Mackinnon R. Structural biology. Voltage sensor meets lipid membrane. Science. 2004;306:1304–1305.
   PubMedGoogle Scholar
• Hille B, Dickson EJ, Kruse M, et al. Phosphoinositides regulate ion channels. Biochim Biophys Acta. 2015;1851:844–856.
   PubMed Web of Science ®Google Scholar
• Gao S, Yan N. Structural basis of the modulation of the voltage-gated calcium ion channel cav 1.1 by dihydropyridine compounds*. Angew Chem Int Ed Engl. 2021;60:3131–3137.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Huang G, Wu J, et al. Molecular basis for ligand modulation of a mammalian voltage-gated Ca(2+) channel. Cell. 2019;177:1495–506 e12.
   PubMed Web of Science ®Google Scholar
• Zamponi GW, Striessnig J, Koschak A, et al. The physiology, pathology, and pharmacology of voltage-gated calcium channels and their future therapeutic potential. Pharmacol Rev. 2015;67:821–870.
   PubMed Web of Science ®Google Scholar
• Walsh KB, Bryant SH, Schwartz A. Suppression of charge movement by calcium antagonists is not related to calcium channel block. Pflugers Arch. 1987;409:217–219.
   PubMed Web of Science ®Google Scholar
• Walsh KB, Bryant SH, Schwartz A. Action of diltiazem on excitation-contraction coupling in bullfrog skeletal muscle fibers. J Pharmacol Exp Ther. 1988;245:531–536.
   PubMed Web of Science ®Google Scholar
• Arrigoni C, Lolicato M, Shaya D, et al. Quaternary structure independent folding of voltage-gated ion channel pore domain subunits. Nat Struct Mol Biol. 2022;29:537–548.
   PubMed Web of Science ®Google Scholar
• Guy HR, Seetharamulu P. Molecular model of the action potential sodium channel. Proc Natl Acad Sci U S A. 1986;83:508–512.
   PubMed Web of Science ®Google Scholar
• Keynes RD, Elinder F. The screw-helical voltage gating of ion channels. Proc Biol Sci. 1999;266:843–852.
   PubMed Web of Science ®Google Scholar
• Garcia J, Tanabe T, Beam KG. Relationship of calcium transients to calcium currents and charge movements in myotubes expressing skeletal and cardiac dihydropyridine receptors. J Gen Physiol. 1994;103:125–147.
   PubMed Web of Science ®Google Scholar
• Brum G, Fitts R, Pizarro G, et al. Voltage sensors of the frog skeletal muscle membrane require calcium to function in excitation-contraction coupling. J Physiol. 1988;398:475–505.
   PubMed Web of Science ®Google Scholar
• Banks Q, Bibollet H, Contreras M, et al. Voltage sensor movements of Ca(V)1.1 during an action potential in skeletal muscle fibers. Proc Natl Acad Sci U S A. 2021;118. DOI:10.1073/pnas.2026116118.
   Web of Science ®Google Scholar
• Savalli N, Angelini M, Steccanella F, et al. The distinct role of the four voltage sensors of the skeletal CaV1.1 channel in voltage-dependent activation. J Gen Physiol. 2021;153:e202112915.
   PubMed Web of Science ®Google Scholar
• Mannuzzu LM, Moronne MM, Isacoff EY. Direct physical measure of conformational rearrangement underlying potassium channel gating. Science. 1996;271:213–216.
   PubMed Web of Science ®Google Scholar
• Cha A, Bezanilla F. Characterizing voltage-dependent conformational changes in the Shaker K+ channel with fluorescence. Neuron. 1997;19:1127–1140.
   PubMed Web of Science ®Google Scholar
• Savalli N, Kondratiev A, Toro L, et al. Voltage-dependent conformational changes in human Ca(2+)- and voltage-activated K(+) channel, revealed by voltage-clamp fluorometry. Proc Natl Acad Sci U S A. 2006;103:12619–12624.
   PubMed Web of Science ®Google Scholar
• Pantazis A, Savalli N, Sigg D, et al. Functional heterogeneity of the four voltage sensors of a human L-type calcium channel. Proc Natl Acad Sci U S A. 2014;111:18381–18386.
   PubMed Web of Science ®Google Scholar
• Zheng J, Zagotta WN. Gating rearrangements in cyclic nucleotide-gated channels revealed by patch-clamp fluorometry. Neuron. 2000;28:369–374.
   PubMed Web of Science ®Google Scholar
• Priest M, Bezanilla F. Functional site-directed fluorometry. Adv Exp Med Biol. 2015;869:55–76.
   PubMed Web of Science ®Google Scholar
• Akabas MH. Cysteine modification: probing channel structure, function and conformational change. Adv Exp Med Biol. 2015;869:25–54.
   PubMed Web of Science ®Google Scholar
• DiFranco M, Quinonez M, Capote J, et al. DNA transfection of mammalian skeletal muscles using in vivo electroporation. J Vis Exp. 2009;2009:e1520.
   Google Scholar
• Samso M. A guide to the 3D structure of the ryanodine receptor type 1 by cryoEM. Protein Sci. 2017;26:52–68.
   PubMed Web of Science ®Google Scholar
• Bezanilla F. The voltage sensor in voltage-dependent ion channels. Physiol Rev. 2000;80:555–592.
   PubMed Web of Science ®Google Scholar
• Obermair GJ, Kugler G, Baumgartner S, et al. The Ca2+ channel alpha2delta-1 subunit determines Ca2+ current kinetics in skeletal muscle but not targeting of alpha1S or excitation-contraction coupling. J Biol Chem. 2005;280:2229–2237.
   PubMed Web of Science ®Google Scholar
• Andronache Z, Ursu D, Lehnert S, et al. The auxiliary subunit gamma 1 of the skeletal muscle L-type Ca2+ channel is an endogenous Ca2+ antagonist. Proc Natl Acad Sci U S A. 2007;104:17885–17890.
   PubMed Web of Science ®Google Scholar
• Savalli N, Pantazis A, Sigg D, et al. The alpha2delta-1 subunit remodels CaV1.2 voltage sensors and allows Ca2+ influx at physiological membrane potentials. J Gen Physiol. 2016;148:147–159.
   PubMed Web of Science ®Google Scholar
• Eltit JM, Bannister RA, Moua O, et al. Malignant hyperthermia susceptibility arising from altered resting coupling between the skeletal muscle L-type Ca2+ channel and the type 1 ryanodine receptor. Proc Natl Acad Sci U S A. 2012;109:7923–7928.
   PubMed Web of Science ®Google Scholar
• Flucher BE. Specific contributions of the four voltage-sensing domains in L-type calcium channels to gating and modulation. J Gen Physiol. 2016;148:91–95.
   PubMed Web of Science ®Google Scholar
• Tanabe T, Beam KG, Adams BA, et al. Regions of the skeletal muscle dihydropyridine receptor critical for excitation-contraction coupling. Nature. 1990;346:567–569.
   PubMed Web of Science ®Google Scholar
• Hernandez-Ochoa EO, Olojo RO, Rebbeck RT, et al. beta1a490-508, a 19-residue peptide from C-terminal tail of Cav1.1 beta1a subunit, potentiates voltage-dependent calcium release in adult skeletal muscle fibers. Biophys J. 2014;106:535–547.
   PubMed Web of Science ®Google Scholar
• Beqollari D, Romberg CF, Filipova D, et al. Rem uncouples excitation-contraction coupling in adult skeletal muscle fibers. J Gen Physiol. 2015;146:97–108.
   PubMed Web of Science ®Google Scholar
• Flucher BE. Skeletal muscle Ca(V)1.1 channelopathies. Pflugers Arch. 2020;472:739–754.
   PubMed Web of Science ®Google Scholar
• Cannon SC. Channelopathies of skeletal muscle excitability. Compr Physiol. 2015;5:761–790.
   PubMed Web of Science ®Google Scholar