Role of High Voltage-Gated Ca2+ Channel Subunits in Pancreatic β-Cell Insulin Release. From Structure to Function
Abstract
:1. Introduction
2. Glucose-Induced Insulin Secretion (GIIS)
3. High Voltage-Gated Ca2+ Channel Structure
4. α1 Subunit
5. CaV1.2 and CaV1.3 L-Type Ca2+ Channels
6. CaV2.3 R-Type Calcium Channels
7. CaV2.1 P/Q- Type Ca2+ Channels
8. β-Subunits
9. α2δ Subunits
10. γ Subunit
11. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Bonnevie-Nielsen, V.; Steffes, M.W.; Lernmark, A. A major loss in islet mass and b-cell function precedes hyperglycemia in mice given multiple low doses of streptozotocin. Diabetes 1981, 30, 424–429. [Google Scholar] [CrossRef] [PubMed]
- Hollander, P.M.; Asplin, C.M.; Palmer, J.P. Glucose modulation of insulin and glucagon secretion in nondiabetic and diabetic man. Diabetes 1982, 31, 489–495. [Google Scholar] [CrossRef]
- Vergari, E.; Denwood, G.; Salehi, A.; Zhang, Q.; Adam, J.; Alrifaiy, A.; Wernstedt Asterholm, I.; Benrick, A.; Chibalina, M.V.; Eliasson, L.; et al. Somatostatin secretion by Na+-dependent Ca2+-induced Ca2+ release in pancreatic delta-cells. Nat. Metab. 2020, 2, 32–40. [Google Scholar] [CrossRef]
- Rorsman, P.; Huising, M.O. The somatostatin-secreting pancreatic delta-cell in health and disease. Natnat. Rev. Endocrinol. 2018, 14, 404–414. [Google Scholar] [CrossRef] [PubMed]
- Rodriguez-Diaz, R.; Dando, R.; Jacques-Silva, M.C.; Fachado, A.; Molina, J.; Abdulreda, M.H.; Ricordi, C.; Roper, S.D.; Berggren, P.O.; Caicedo, A. Alpha cells secrete acetylcholine as a non-neuronal paracrine signal priming beta cell function in humans. Nat. Med. 2011, 17, 888–892. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rorsman, P.; Ashcroft, F.M. Pancreatic beta-cell electrical activity and insulin secretion: Of mice and men. Physiol. Rev. 2018, 98, 117–214. [Google Scholar] [CrossRef]
- Rorsman, P.; Braun, M. Regulation of insulin secretion in human pancreatic islets. Annu. Rev. Physiol. 2013, 75, 155–179. [Google Scholar] [CrossRef] [PubMed]
- Rorsman, P.; Eliasson, L.; Renstrom, E.; Gromada, J.; Barg, S.; Gopel, S. The cell physiology of biphasic insulin secretion. News Physiol. Sci. 2000, 15, 72–77. [Google Scholar] [CrossRef] [PubMed]
- Hattersley, A.T.; Ashcroft, F.M. Activating mutations in kir6.2 and neonatal diabetes: New clinical syndromes, new scientific insights, and new therapy. Diabetes 2005, 54, 2503–2513. [Google Scholar] [CrossRef] [Green Version]
- Ellard, S.; Flanagan, S.E.; Girard, C.A.; Patch, A.M.; Harries, L.W.; Parrish, A.; Edghill, E.L.; Mackay, D.J.; Proks, P.; Shimomura, K.; et al. Permanent neonatal diabetes caused by dominant, recessive, or compound heterozygous sur1 mutations with opposite functional effects. Am. J. Hum. Genet. 2007, 81, 375–382. [Google Scholar] [CrossRef] [Green Version]
- Girard, C.A.; Wunderlich, F.T.; Shimomura, K.; Collins, S.; Kaizik, S.; Proks, P.; Abdulkader, F.; Clark, A.; Ball, V.; Zubcevic, L.; et al. Expression of an activating mutation in the gene encoding the katp channel subunit kir6.2 in mouse pancreatic beta cells recapitulates neonatal diabetes. J. Clin. Investig. 2009, 119, 80–90. [Google Scholar] [PubMed] [Green Version]
- Ashcroft, F.M.; Rorsman, P. K(atp) channels and islet hormone secretion: New insights and controversies. Nat. Rev. Endocrinol. 2013, 9, 660–669. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ashcroft, F.M.; Harrison, D.E.; Ashcroft, S.J. Glucose induces closure of single potassium channels in isolated rat pancreatic beta-cells. Nature 1984, 312, 446–448. [Google Scholar] [CrossRef] [PubMed]
- Kang, C.; Xie, L.; Gunasekar, S.K.; Mishra, A.; Zhang, Y.; Pai, S.; Gao, Y.; Kumar, A.; Norris, A.W.; Stephens, S.B.; et al. Swell1 is a glucose sensor regulating beta-cell excitability and systemic glycaemia. Nat. Commun. 2018, 9, 367. [Google Scholar] [CrossRef] [Green Version]
- Gopel, S.; Kanno, T.; Barg, S.; Galvanovskis, J.; Rorsman, P. Voltage-gated and resting membrane currents recorded from b-cells in intact mouse pancreatic islets. J. Physiol. 1999, 521, 717–728. [Google Scholar] [CrossRef]
- Braun, M.; Ramracheya, R.; Bengtsson, M.; Zhang, Q.; Karanauskaite, J.; Partridge, C.; Johnson, P.R.; Rorsman, P. Voltage-gated ion channels in human pancreatic beta-cells: Electrophysiological characterization and role in insulin secretion. Diabetes 2008, 57, 1618–1628. [Google Scholar] [CrossRef] [Green Version]
- Rorsman, P.; Eliasson, L.; Kanno, T.; Zhang, Q.; Gopel, S. Electrophysiology of pancreatic beta-cells in intact mouse islets of langerhans. Prog. Biophys. Mol. Biol. 2011, 107, 224–235. [Google Scholar] [CrossRef]
- Tsien, R.W. Calcium channels in excitable cell membranes. Annu. Rev. Physiol 1983, 45, 341–358. [Google Scholar] [CrossRef] [PubMed]
- Bezanilla, F. The voltage sensor in voltage-dependent ion channels. Physiol. Rev. 2000, 80, 555–592. [Google Scholar] [CrossRef]
- Zhang, X.; Yan, N. The conformational shifts of the voltage sensing domains between na(v)rh and na(v)ab. Cell Res. 2013, 23, 444–447. [Google Scholar] [CrossRef] [Green Version]
- Papazian, D.M.; Shao, X.M.; Seoh, S.A.; Mock, A.F.; Huang, Y.; Wainstock, D.H. Electrostatic interactions of s4 voltage sensor in shaker k+ channel. Neuron 1995, 14, 1293–1301. [Google Scholar] [CrossRef] [Green Version]
- Zamponi, G.W.; Striessnig, J.; Koschak, A.; Dolphin, A.C. The physiology, pathology, and pharmacology of voltage-gated calcium channels and their future therapeutic potential. Pharm. Rev. 2015, 67, 821–870. [Google Scholar] [CrossRef] [Green Version]
- Flucher, B.E. Specific contributions of the four voltage-sensing domains in l-type calcium channels to gating and modulation. J. Gen. Physiol. 2016, 148, 91–95. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Andranovits, S.; Beyl, S.; Hohaus, A.; Zangerl-Plessl, E.M.; Timin, E.; Hering, S. Key role of segment is4 in cav1.2 inactivation: Link between activation and inactivation. Pflug. Arch. 2017, 469, 1485–1493. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vasseur, M.; Debuyser, A.; Joffre, M. Sensitivity of pancreatic beta cell to calcium channel blockers. An electrophysiologic study of verapamil and nifedipine. Fundam. Clin. Pharm. 1987, 1, 95–113. [Google Scholar] [CrossRef] [PubMed]
- Henquin, J.C.; Ishiyama, N.; Nenquin, M.; Ravier, M.A.; Jonas, J.C. Signals and pools underlying biphasic insulin secretion. Diabetes 2002, 51 (Suppl. S1), S60–S67. [Google Scholar] [CrossRef] [Green Version]
- Henquin, J.C.; Nenquin, M.; Ravier, M.A.; Szollosi, A. Shortcomings of current models of glucose-induced insulin secretion. Diabetesobes. Metab. 2009, 11, 168–179. [Google Scholar] [CrossRef] [PubMed]
- Henquin, J.C. Glucose-induced insulin secretion in isolated human islets: Does it truly reflect beta-cell function in vivo? Mol. Metab. 2021, 48, 101212. [Google Scholar] [CrossRef]
- Curry, D.L.; Bennett, L.L.; Grodsky, G.M. Dynamics of insulin secretion by the perfused rat pancreas. Endocrinology 1968, 83, 572–584. [Google Scholar] [CrossRef] [PubMed]
- Barg, S.; Ma, X.; Eliasson, L.; Galvanovskis, J.; Gopel, S.O.; Obermuller, S.; Platzer, J.; Renstrom, E.; Trus, M.; Atlas, D.; et al. Fast exocytosis with few Ca(2+) channels in insulin-secreting mouse pancreatic b cells. Biophys. J. 2001, 81, 3308–3323. [Google Scholar] [CrossRef] [Green Version]
- Barg, S.; Eliasson, L.; Renstrom, E.; Rorsman, P. A subset of 50 secretory granules in close contact with l-type Ca2+ channels accounts for first-phase insulin secretion in mouse beta-cells. Diabetes 2002, 51, S74–S82. [Google Scholar] [CrossRef] [Green Version]
- Olofsson, C.S.; Gopel, S.O.; Barg, S.; Galvanovskis, J.; Ma, X.; Salehi, A.; Rorsman, P.; Eliasson, L. Fast insulin secretion reflects exocytosis of docked granules in mouse pancreatic b-cells. Pflug. Arch. 2002, 444, 43–51. [Google Scholar] [CrossRef]
- Gaisano, H.Y. Recent new insights into the role of snare and associated proteins in insulin granule exocytosis. Diabetesobes. Metab. 2017, 19, 115–123. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Porte, D., Jr.; Pupo, A.A. Insulin responses to glucose: Evidence for a two pool system in man. J. Clin. Investig. 1969, 48, 2309–2319. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Doliba, N.M.; Qin, W.; Najafi, H.; Liu, C.; Buettger, C.W.; Sotiris, J.; Collins, H.W.; Li, C.; Stanley, C.A.; Wilson, D.F.; et al. Glucokinase activation repairs defective bioenergetics of islets of langerhans isolated from type 2 diabetics. Am. J. Physiol. Endocrinol. Metab. 2012, 302, E87–E102. [Google Scholar] [CrossRef] [Green Version]
- Wu, J.; Yan, Z.; Li, Z.; Qian, X.; Lu, S.; Dong, M.; Zhou, Q.; Yan, N. Structure of the voltage-gated calcium channel cav1.1 at 3.6 a resolution. Nature 2016, 537, 191–196. [Google Scholar] [CrossRef] [PubMed]
- Catterall, W.A. Voltage-gated calcium channels. Cold Spring Harb. Perspect. Biol. 2011, 3, a003947. [Google Scholar] [CrossRef] [PubMed]
- Flucher, B.E.; Obermair, G.J.; Tuluc, P.; Schredelseker, J.; Kern, G.; Grabner, M. The role of auxiliary dihydropyridine receptor subunits in muscle. J. Muscle Res. Cell Motil. 2005, 26, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Obermair, G.J.; Tuluc, P.; Flucher, B.E. Auxiliary Ca(2+) channel subunits: Lessons learned from muscle. Curr. Opin. Pharm. 2008, 8, 311–318. [Google Scholar] [CrossRef]
- Dolphin, A.C.; Lee, A. Presynaptic calcium channels: Specialized control of synaptic neurotransmitter release. Nat. Rev. Neurosci 2020, 21, 213–229. [Google Scholar] [CrossRef]
- Wu, J.; Yan, Z.; Li, Z.; Yan, C.; Lu, S.; Dong, M.; Yan, N. Structure of the voltage-gated calcium channel cav1.1 complex. Science 2015, 350, aad2395. [Google Scholar] [CrossRef]
- Catterall, W.A. Ion channel voltage sensors: Structure, function, and pathophysiology. Neuron 2010, 67, 915–928. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Findeisen, F.; Campiglio, M.; Jo, H.; Abderemane-Ali, F.; Rumpf, C.H.; Pope, L.; Rossen, N.D.; Flucher, B.E.; De Grado, W.F.; Minor, D.L., Jr. Stapled voltage-gated calcium channel (cav) alpha-interaction domain (aid) peptides act as selective protein-protein interaction inhibitors of cav function. ACS Chem. Neurosci. 2017, 8, 1313–1326. [Google Scholar] [CrossRef] [Green Version]
- Tuluc, P.; Yarov-Yarovoy, V.; Benedetti, B.; Flucher, B.E. Molecular interactions in the voltage sensor controlling gating properties of cav calcium channels. Structure 2016, 24, 261–271. [Google Scholar] [CrossRef] [Green Version]
- Coste de Bagneaux, P.; Campiglio, M.; Benedetti, B.; Tuluc, P.; Flucher, B.E. Role of putative voltage-sensor countercharge d4 in regulating gating properties of cav1.2 and cav1.3 calcium channels. Channels 2018, 12, 249–261. [Google Scholar] [CrossRef] [PubMed]
- Fernandez-Quintero, M.L.; El Ghaleb, Y.; Tuluc, P.; Campiglio, M.; Liedl, K.R.; Flucher, B.E. Structural determinants of voltage-gating properties in calcium channels. eLife 2021, 10, e64087. [Google Scholar] [CrossRef] [PubMed]
- Pantazis, A.; Savalli, N.; Sigg, D.; Neely, A.; Olcese, R. Functional heterogeneity of the four voltage sensors of a human l-type calcium channel. Proc. Natl. Acad. Sci. USA 2014, 111, 18381–18386. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Beyl, S.; Hohaus, A.; Andranovits, S.; Timin, E.; Hering, S. Upward movement of is4 and iiis4 is a rate-limiting stage in cav1.2 activation. Pflug. Arch. 2016, 468, 1895–1907. [Google Scholar] [CrossRef] [Green Version]
- Savalli, N.; Pantazis, A.; Sigg, D.; Weiss, J.N.; Neely, A.; Olcese, R. The alpha2delta-1 subunit remodels cav1.2 voltage sensors and allows Ca2+ influx at physiological membrane potentials. J. Gen. Physiol. 2016, 148, 147–159. [Google Scholar] [CrossRef] [Green Version]
- Tuluc, P.; Molenda, N.; Schlick, B.; Obermair, G.J.; Flucher, B.E.; Jurkat-Rott, K. 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. [Google Scholar] [CrossRef] [Green Version]
- Tuluc, P.; Flucher, B.E. Divergent biophysical properties, gating mechanisms, and possible functions of the two skeletal muscle ca(v)1.1 calcium channel splice variants. J. Muscle Res. Cell Motil. 2011, 32, 249–256. [Google Scholar] [CrossRef] [Green Version]
- Tuluc, P.; Benedetti, B.; Coste de Bagneaux, P.; Grabner, M.; Flucher, B.E. 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. [Google Scholar] [CrossRef] [Green Version]
- Flucher, B.E.; Tuluc, P. How and why are calcium currents curtailed in the skeletal muscle voltage-gated calcium channels? J. Physiol. 2017, 595, 1451–1463. [Google Scholar] [CrossRef] [PubMed]
- Pangrsic, T.; Singer, J.H.; Koschak, A. Voltage-gated calcium channels: Key players in sensory coding in the retina and the inner ear. Physiol Rev. 2018, 98, 2063–2096. [Google Scholar] [CrossRef] [PubMed]
- Jing, X.; Li, D.Q.; Olofsson, C.S.; Salehi, A.; Surve, V.V.; Caballero, J.; Ivarsson, R.; Lundquist, I.; Pereverzev, A.; Schneider, T.; et al. Cav2.3 calcium channels control second-phase insulin release. J. Clin. Investig. 2005, 115, 146–154. [Google Scholar] [CrossRef] [Green Version]
- Mastrolia, V.; Flucher, S.M.; Obermair, G.J.; Drach, M.; Hofer, H.; Renstrom, E.; Schwartz, A.; Striessnig, J.; Flucher, B.E.; Tuluc, P. Loss of alpha2delta-1 calcium channel subunit function increases the susceptibility for diabetes. Diabetes 2017, 66, 897–907. [Google Scholar] [CrossRef] [Green Version]
- Schulla, V.; Renstrom, E.; Feil, R.; Feil, S.; Franklin, I.; Gjinovci, A.; Jing, X.J.; Laux, D.; Lundquist, I.; Magnuson, M.A.; et al. Impaired insulin secretion and glucose tolerance in beta cell-selective ca(v)1.2 Ca2+ channel null mice. Embo. J. 2003, 22, 3844–3854. [Google Scholar] [CrossRef] [Green Version]
- Vignali, S.; Leiss, V.; Karl, R.; Hofmann, F.; Welling, A. Characterization of voltage-dependent sodium and calcium channels in mouse pancreatic a- and b-cells. J. Physiol. 2006, 572, 691–706. [Google Scholar] [CrossRef] [PubMed]
- Yang, S.N.; Berggren, P.O. The role of voltage-gated calcium channels in pancreatic beta-cell physiology and pathophysiology. Endocr. Rev. 2006, 27, 621–676. [Google Scholar] [CrossRef] [Green Version]
- Rios, E.; Brum, G. Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature 1987, 325, 717–720. [Google Scholar] [CrossRef]
- Bers, D.M.; Perez-Reyes, E. Ca channels in cardiac myocytes: Structure and function in ca influx and intracellular ca release. Cardiovasc. Res. 1999, 42, 339–360. [Google Scholar] [CrossRef] [Green Version]
- Cohen, S.M.; Ma, H.; Kuchibhotla, K.V.; Watson, B.O.; Buzsaki, G.; Froemke, R.C.; Tsien, R.W. Excitation-transcription coupling in parvalbumin-positive interneurons employs a novel cam kinase-dependent pathway distinct from excitatory neurons. Neuron 2016, 90, 292–307. [Google Scholar] [CrossRef] [Green Version]
- Hockerman, G.H.; Peterson, B.Z.; Johnson, B.D.; Catterall, W.A. Molecular determinants of drug binding and action on l-type calcium channels. Annu. Rev. Pharm. Toxicol. 1997, 37, 361–396. [Google Scholar] [CrossRef] [Green Version]
- Tikhonov, D.B.; Zhorov, B.S. Structural model for dihydropyridine binding to l-type calcium channels. J. Biol. Chem. 2009, 284, 19006–19017. [Google Scholar] [CrossRef] [Green Version]
- Catterall, W.A.; Swanson, T.M. Structural basis for pharmacology of voltage-gated sodium and calcium channels. Mol. Pharm. 2015, 88, 141–150. [Google Scholar] [CrossRef]
- Hess, P.; Lansman, J.B.; Tsien, R.W. Different modes of ca channel gating behaviour favoured by dihydropyridine ca agonists and antagonists. Nature 1984, 311, 538–544. [Google Scholar] [CrossRef] [PubMed]
- Lee, K.S.; Tsien, R.W. Mechanism of calcium channel blockade by verapamil, d600, diltiazem and nitrendipine in single dialysed heart cells. Nature 1983, 302, 790–794. [Google Scholar] [CrossRef] [PubMed]
- Bean, B.P.; Sturek, M.; Puga, A.; Hermsmeyer, K. Calcium channels in muscle cells isolated from rat mesenteric arteries: Modulation by dihydropyridine drugs. Circ. Res. 1986, 59, 229–235. [Google Scholar] [CrossRef] [Green Version]
- Hamilton, S.L.; Yatani, A.; Brush, K.; Schwartz, A.; Brown, A.M. A comparison between the binding and electrophysiological effects of dihydropyridines on cardiac membranes. Mol. Pharm. 1987, 31, 221–231. [Google Scholar]
- Berjukow, S.; Hering, S. Voltage-dependent acceleration of ca(v)1.2 channel current decay by (+)- and (-)-isradipine. Br. J. Pharm. 2001, 133, 959–966. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shabbir, W.; Beyl, S.; Timin, E.N.; Schellmann, D.; Erker, T.; Hohaus, A.; Hockerman, G.H.; Hering, S. Interaction of diltiazem with an intracellularly accessible binding site on ca(v)1.2. Br. J. Pharm. 2011, 162, 1074–1082. [Google Scholar] [CrossRef] [Green Version]
- Devis, G.; Somers, G.; Van Obberghen, E.; Malaisse, W.J. Calcium antagonists and islet function. I. Inhibition of insulin release by verapamil. Diabetes 1975, 24, 247–251. [Google Scholar] [CrossRef]
- Levine, M.; Boyer, E.W.; Pozner, C.N.; Geib, A.J.; Thomsen, T.; Mick, N.; Thomas, S.H. Assessment of hyperglycemia after calcium channel blocker overdoses involving diltiazem or verapamil. Crit. Care Med. 2007, 35, 2071–2075. [Google Scholar] [CrossRef]
- Ovalle, F.; Grimes, T.; Xu, G.; Patel, A.J.; Grayson, T.B.; Thielen, L.A.; Li, P.; Shalev, A. Verapamil and beta cell function in adults with recent-onset type 1 diabetes. Nat. Med. 2018, 24, 1108–1112. [Google Scholar] [CrossRef]
- Sinnegger-Brauns, M.J.; Hetzenauer, A.; Huber, I.G.; Renstrom, E.; Wietzorrek, G.; Berjukov, S.; Cavalli, M.; Walter, D.; Koschak, A.; Waldschutz, R.; et al. Isoform-specific regulation of mood behavior and pancreatic beta cell and cardiovascular function by l-type Ca2+ channels. J. Clin. Investig. 2004, 113, 1430–1439. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Namkung, Y.; Skrypnyk, N.; Jeong, M.J.; Lee, T.; Lee, M.S.; Kim, H.L.; Chin, H.; Suh, P.G.; Kim, S.S.; Shin, H.S. Requirement for the l-type Ca(2+) channel alpha(1d) subunit in postnatal pancreatic beta cell generation. J. Clin. Investig. 2001, 108, 1015–1022. [Google Scholar] [CrossRef]
- Platzer, J.; Engel, J.; Schrott-Fischer, A.; Stephan, K.; Bova, S.; Chen, H.; Zheng, H.; Striessnig, J. Congenital deafness and sinoatrial node dysfunction in mice lacking class d l-type Ca2+ channels. Cell 2000, 102, 89–97. [Google Scholar] [CrossRef] [Green Version]
- Lipscombe, D.; Andrade, A.; Allen, S.E. Alternative splicing: Functional diversity among voltage-gated calcium channels and behavioral consequences. Biochim. Biophys. Acta 2013, 1828, 1522–1529. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bourinet, E.; Zamponi, G.W.; Stea, A.; Soong, T.W.; Lewis, B.A.; Jones, L.P.; Yue, D.T.; Snutch, T.P. The alpha 1e calcium channel exhibits permeation properties similar to low-voltage-activated calcium channels. J. Neurosci. 1996, 16, 4983–4993. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jones, L.P.; Wei, S.K.; Yue, D.T. Mechanism of auxiliary subunit modulation of neuronal alpha1e calcium channels. J. Gen. Physiol. 1998, 112, 125–143. [Google Scholar] [CrossRef] [Green Version]
- Matthes, J.; Yildirim, L.; Wietzorrek, G.; Reimer, D.; Striessnig, J.; Herzig, S. Disturbed atrio-ventricular conduction and normal contractile function in isolated hearts from cav1.3-knockout mice. Naunyn-Schmiedeberg’s Arch. Pharm. 2004, 369, 554–562. [Google Scholar] [CrossRef] [PubMed]
- Singh, A.; Gebhart, M.; Fritsch, R.; Sinnegger-Brauns, M.J.; Poggiani, C.; Hoda, J.C.; Engel, J.; Romanin, C.; Striessnig, J.; Koschak, A. Modulation of voltage- and Ca2+-dependent gating of cav1.3 l-type calcium channels by alternative splicing of a c-terminal regulatory domain. J. Biol. Chem. 2008, 283, 20733–20744. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Koschak, A.; Reimer, D.; Huber, I.; Grabner, M.; Glossmann, H.; Engel, J.; Striessnig, J. Alpha 1d (cav1.3) subunits can form l-type Ca2+ channels activating at negative voltages. J. Biol. Chem. 2001, 276, 22100–22106. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mangoni, M.E.; Couette, B.; Bourinet, E.; Platzer, J.; Reimer, D.; Striessnig, J.; Nargeot, J. Functional role of l-type cav1.3 ca2+ channels in cardiac pacemaker activity. Proc. Natl. Acad. Sci. USA 2003, 100, 5543–5548. [Google Scholar] [CrossRef] [Green Version]
- Marcantoni, A.; Vandael, D.H.; Mahapatra, S.; Carabelli, V.; Sinnegger-Brauns, M.J.; Striessnig, J.; Carbone, E. Loss of cav1.3 channels reveals the critical role of l-type and bk channel coupling in pacemaking mouse adrenal chromaffin cells. J. Neurosci. 2010, 30, 491–504. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vandael, D.H.; Zuccotti, A.; Striessnig, J.; Carbone, E. Ca(v)1.3-driven sk channel activation regulates pacemaking and spike frequency adaptation in mouse chromaffin cells. J. Neurosci. 2012, 32, 16345–16359. [Google Scholar] [CrossRef] [Green Version]
- Yang, G.; Shi, Y.; Yu, J.; Li, Y.; Yu, L.; Welling, A.; Hofmann, F.; Striessnig, J.; Juntti-Berggren, L.; Berggren, P.O.; et al. Cav1.2 and cav1.3 channel hyperactivation in mouse islet beta cells exposed to type 1 diabetic serum. Cell. Mol. Life Sci. 2015, 72, 1197–1207. [Google Scholar] [CrossRef]
- Engel, J.; Michna, M.; Platzer, J.; Striessnig, J. Calcium channels in mouse hair cells: Function, properties and pharmacology. Adv. Oto-Rhino-Laryngol. 2002, 59, 35–41. [Google Scholar]
- Zampini, V.; Johnson, S.L.; Franz, C.; Lawrence, N.D.; Munkner, S.; Engel, J.; Knipper, M.; Magistretti, J.; Masetto, S.; Marcotti, W. Elementary properties of cav1.3 Ca(2+) channels expressed in mouse cochlear inner hair cells. J. Physiol. 2010, 588, 187–199. [Google Scholar] [CrossRef] [Green Version]
- Lee, A.; Wang, S.; Williams, B.; Hagen, J.; Scheetz, T.E.; Haeseleer, F. Characterization of cav1.4 complexes (alpha11.4, beta2, and alpha2delta4) in hek293t cells and in the retina. J. Biol. Chem. 2015, 290, 1505–1521. [Google Scholar] [CrossRef] [Green Version]
- Sudhof, T.C. The presynaptic active zone. Neuron 2012, 75, 11–25. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gandasi, N.R.; Yin, P.; Riz, M.; Chibalina, M.V.; Cortese, G.; Lund, P.E.; Matveev, V.; Rorsman, P.; Sherman, A.; Pedersen, M.G.; et al. Ca2+ channel clustering with insulin-containing granules is disturbed in type 2 diabetes. J. Clin. Investig. 2017, 127, 2353–2364. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bokvist, K.; Eliasson, L.; Ammala, C.; Renstrom, E.; Rorsman, P. Co-localization of l-type Ca2+ channels and insulin-containing secretory granules and its significance for the initiation of exocytosis in mouse pancreatic b-cells. EMBO J. 1995, 14, 50–57. [Google Scholar] [CrossRef]
- Splawski, I.; Timothy, K.W.; Sharpe, L.M.; Decher, N.; Kumar, P.; Bloise, R.; Napolitano, C.; Schwartz, P.J.; Joseph, R.M.; Condouris, K.; et al. Ca(v)1.2 calcium channel dysfunction causes a multisystem disorder including arrhythmia and autism. Cell 2004, 119, 19–31. [Google Scholar] [CrossRef] [Green Version]
- Flanagan, S.E.; Vairo, F.; Johnson, M.B.; Caswell, R.; Laver, T.W.; Lango Allen, H.; Hussain, K.; Ellard, S. A cacna1d mutation in a patient with persistent hyperinsulinaemic hypoglycaemia, heart defects, and severe hypotonia. Pediatric Diabetes 2017, 18, 320–323. [Google Scholar] [CrossRef] [Green Version]
- De Mingo Alemany, M.C.; Mifsud Grau, L.; Moreno Macian, F.; Ferrer Lorente, B.; Leon Carinena, S. A de novo cacna1d missense mutation in a patient with congenital hyperinsulinism, primary hyperaldosteronism and hypotonia. Channels (Austin) 2020, 14, 175–180. [Google Scholar] [CrossRef]
- Reinbothe, T.M.; Alkayyali, S.; Ahlqvist, E.; Tuomi, T.; Isomaa, B.; Lyssenko, V.; Renstrom, E. The human l-type calcium channel ca(v)1.3 regulates insulin release and polymorphisms in cacna1d associate with type 2 diabetes. Diabetologia 2013, 56, 340–349. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Calorio, C.; Gavello, D.; Guarina, L.; Salio, C.; Sassoe-Pognetto, M.; Riganti, C.; Bianchi, F.T.; Hofer, N.T.; Tuluc, P.; Obermair, G.J.; et al. Impaired chromaffin cell excitability and exocytosis in autistic timothy syndrome ts2-neo mouse rescued by l-type calcium channel blockers. J. Physiol. 2019, 597, 1705–1733. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barbara, J.G.; Takeda, K. Voltage-dependent currents and modulation of calcium channel expression in zona fasciculata cells from rat adrenal gland. J. Physiol. 1995, 488, 609–622. [Google Scholar] [CrossRef]
- Enyeart, J.J.; Enyeart, J.A. Ca2+ and k+ channels of normal human adrenal zona fasciculata cells: Properties and modulation by acth and angii. J. Gen. Physiol. 2013, 142, 137–155. [Google Scholar] [CrossRef] [Green Version]
- Enyeart, J.J.; Enyeart, J.A. Adrenal fasciculata cells express t-type and rapidly and slowly activating l-type Ca2+ channels that regulate cortisol secretion. Am. J. Physiol. 2015, 308, C899–C918. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Soong, T.W.; Stea, A.; Hodson, C.D.; Dubel, S.J.; Vincent, S.R.; Snutch, T.P. Structure and functional expression of a member of the low voltage-activated calcium channel family. Science 1993, 260, 1133–1136. [Google Scholar] [CrossRef] [PubMed]
- Stephens, G.J.; Page, K.M.; Burley, J.R.; Berrow, N.S.; Dolphin, A.C. Functional expression of rat brain cloned alpha1e calcium channels in cos-7 cells. Pflug. Arch. 1997, 433, 523–532. [Google Scholar] [CrossRef]
- Qin, N.; Olcese, R.; Stefani, E.; Birnbaumer, L. Modulation of human neuronal alpha 1e-type calcium channel by alpha 2 delta-subunit. Am. J. Physiol 1998, 274, C1324–C1331. [Google Scholar] [CrossRef]
- Bourinet, E.; Stotz, S.C.; Spaetgens, R.L.; Dayanithi, G.; Lemos, J.; Nargeot, J.; Zamponi, G.W. Interaction of snx482 with domains iii and iv inhibits activation gating of alpha(1e) (ca(v)2.3) calcium channels. Biophys. J. 2001, 81, 79–88. [Google Scholar] [CrossRef] [Green Version]
- Holmkvist, J.; Tojjar, D.; Almgren, P.; Lyssenko, V.; Lindgren, C.M.; Isomaa, B.; Tuomi, T.; Berglund, G.; Renstrom, E.; Groop, L. Polymorphisms in the gene encoding the voltage-dependent Ca(2+) channel ca (v)2.3 (cacna1e) are associated with type 2 diabetes and impaired insulin secretion. Diabetologia 2007, 50, 2467–2475. [Google Scholar] [CrossRef] [Green Version]
- Trombetta, M.; Bonetti, S.; Boselli, M.; Turrini, F.; Malerba, G.; Trabetti, E.; Pignatti, P.; Bonora, E.; Bonadonna, R.C. Cacna1e variants affect beta cell function in patients with newly diagnosed type 2 diabetes. The verona newly diagnosed type 2 diabetes study (vnds) 3. PLoS ONE 2012, 7, e32755. [Google Scholar] [CrossRef] [Green Version]
- Saegusa, H.; Kurihara, T.; Zong, S.; Minowa, O.; Kazuno, A.; Han, W.; Matsuda, Y.; Yamanaka, H.; Osanai, M.; Noda, T.; et al. Altered pain responses in mice lacking alpha 1e subunit of the voltage-dependent Ca2+ channel. Proc. Natl. Acad. Sci. USA 2000, 97, 6132–6137. [Google Scholar] [CrossRef] [Green Version]
- Matsuda, Y.; Saegusa, H.; Zong, S.; Noda, T.; Tanabe, T. Mice lacking ca(v)2.3 (alpha1e) calcium channel exhibit hyperglycemia. Biochem. Biophys. Res. Commun. 2001, 289, 791–795. [Google Scholar] [CrossRef]
- Pereverzev, A.; Mikhna, M.; Vajna, R.; Gissel, C.; Henry, M.; Weiergraber, M.; Hescheler, J.; Smyth, N.; Schneider, T. Disturbances in glucose-tolerance, insulin-release, and stress-induced hyperglycemia upon disruption of the ca(v)2.3 (alpha 1e) subunit of voltage-gated Ca(2+) channels. Mol. Endocrinol. 2002, 16, 884–895. [Google Scholar] [PubMed] [Green Version]
- Pereverzev, A.; Salehi, A.; Mikhna, M.; Renstrom, E.; Hescheler, J.; Weiergraber, M.; Smyth, N.; Schneider, T. The ablation of the ca(v)2.3/e-type voltage-gated Ca2+ channel causes a mild phenotype despite an altered glucose induced glucagon response in isolated islets of langerhans. Eur. J. Pharm. 2005, 511, 65–72. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Q.; Bengtsson, M.; Partridge, C.; Salehi, A.; Braun, M.; Cox, R.; Eliasson, L.; Johnson, P.R.; Renstrom, E.; Schneider, T.; et al. R-type Ca(2+)-channel-evoked cicr regulates glucose-induced somatostatin secretion. Nat. Cell Biol. 2007, 9, 453–460. [Google Scholar] [CrossRef]
- Braun, M.; Ramracheya, R.; Amisten, S.; Bengtsson, M.; Moritoh, Y.; Zhang, Q.; Johnson, P.R.; Rorsman, P. Somatostatin release, electrical activity, membrane currents and exocytosis in human pancreatic delta cells. Diabetologia 2009, 52, 1566–1578. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Q.; Ramracheya, R.; Lahmann, C.; Tarasov, A.; Bengtsson, M.; Braha, O.; Braun, M.; Brereton, M.; Collins, S.; Galvanovskis, J.; et al. Role of katp channels in glucose-regulated glucagon secretion and impaired counterregulation in type 2 diabetes. Cell. Metab. 2013, 18, 871–882. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Briant, L.J.B.; Reinbothe, T.M.; Spiliotis, I.; Miranda, C.; Rodriguez, B.; Rorsman, P. Delta-cells and beta-cells are electrically coupled and regulate alpha-cell activity via somatostatin. J. Physiol. 2018, 596, 197–215. [Google Scholar] [CrossRef] [PubMed]
- Davalli, A.M.; Biancardi, E.; Pollo, A.; Socci, C.; Pontiroli, A.E.; Pozza, G.; Clementi, F.; Sher, E.; Carbone, E. Dihydropyridine-sensitive and -insensitive voltage-operated calcium channels participate in the control of glucose-induced insulin release from human pancreatic beta cells. J. Endocrinol. 1996, 150, 195–203. [Google Scholar] [CrossRef]
- Pietrobon, D.; Brennan, K.C. Genetic mouse models of migraine. J. Headache Pain 2019, 20, 79. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bichet, D.; Cornet, V.; Geib, S.; Carlier, E.; Volsen, S.; Hoshi, T.; Mori, Y.; De Waard, M. The i-ii loop of the Ca2+ channel alpha1 subunit contains an endoplasmic reticulum retention signal antagonized by the beta subunit. Neuron 2000, 25, 177–190. [Google Scholar] [CrossRef] [Green Version]
- Cornet, V.; Bichet, D.; Sandoz, G.; Marty, I.; Brocard, J.; Bourinet, E.; Mori, Y.; Villaz, M.; De Waard, M. Multiple determinants in voltage-dependent p/q calcium channels control their retention in the endoplasmic reticulum. Eur. J. Neurosci. 2002, 16, 883–895. [Google Scholar] [CrossRef]
- Altier, C.; Garcia-Caballero, A.; Simms, B.; You, H.; Chen, L.; Walcher, J.; Tedford, H.W.; Hermosilla, T.; Zamponi, G.W. The cavbeta subunit prevents rfp2-mediated ubiquitination and proteasomal degradation of l-type channels. Nat. Neurosci. 2011, 14, 173–180. [Google Scholar] [CrossRef]
- Fang, K.; Colecraft, H.M. Mechanism of auxiliary beta-subunit-mediated membrane targeting of l-type (Ca(v)1.2) channels. J. Physiol. 2011, 589, 4437–4455. [Google Scholar] [CrossRef] [PubMed]
- Olcese, R.; Qin, N.; Schneider, T.; Neely, A.; Wei, X.; Stefani, E.; Birnbaumer, L. The amino terminus of a calcium channel beta subunit sets rates of channel inactivation independently of the subunit’s effect on activation. Neuron 1994, 13, 1433–1438. [Google Scholar] [CrossRef]
- Pragnell, M.; De Waard, M.; Mori, Y.; Tanabe, T.; Snutch, T.P.; Campbell, K.P. Calcium channel beta-subunit binds to a conserved motif in the i-ii cytoplasmic linker of the alpha 1-subunit. Nature 1994, 368, 67–70. [Google Scholar] [CrossRef]
- Gregg, R.G.; Messing, A.; Strube, C.; Beurg, M.; Moss, R.; Behan, M.; Sukhareva, M.; Haynes, S.; Powell, J.A.; Coronado, R.; et al. Absence of the beta subunit (cchb1) of the skeletal muscle dihydropyridine receptor alters expression of the alpha 1 subunit and eliminates excitation-contraction coupling. Proc. Natl. Acad. Sci. USA 1996, 93, 13961–13966. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Schredelseker, J.; Di Biase, V.; Obermair, G.J.; Felder, E.T.; Flucher, B.E.; Franzini-Armstrong, C.; Grabner, M. The beta 1a subunit is essential for the assembly of dihydropyridine-receptor arrays in skeletal muscle. Proc. Natl. Acad. Sci. USA 2005, 102, 17219–17224. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Weissgerber, P.; Held, B.; Bloch, W.; Kaestner, L.; Chien, K.R.; Fleischmann, B.K.; Lipp, P.; Flockerzi, V.; Freichel, M. Reduced cardiac l-type Ca2+ current in ca(v)beta2−/− embryos impairs cardiac development and contraction with secondary defects in vascular maturation. Circ. Res. 2006, 99, 749–757. [Google Scholar] [CrossRef] [Green Version]
- Berrow, N.S.; Campbell, V.; Fitzgerald, E.M.; Brickley, K.; Dolphin, A.C. Antisense depletion of beta-subunits modulates the biophysical and pharmacological properties of neuronal calcium channels. J. Physiol. 1995, 482, 481–491. [Google Scholar] [CrossRef]
- Ball, S.L.; Powers, P.A.; Shin, H.S.; Morgans, C.W.; Peachey, N.S.; Gregg, R.G. Role of the beta(2) subunit of voltage-dependent calcium channels in the retinal outer plexiform layer. Investig. Ophthalmol. Vis. Sci. 2002, 43, 1595–1603. [Google Scholar]
- Neef, J.; Gehrt, A.; Bulankina, A.V.; Meyer, A.C.; Riedel, D.; Gregg, R.G.; Strenzke, N.; Moser, T. The Ca2+ channel subunit beta2 regulates Ca2+ channel abundance and function in inner hair cells and is required for hearing. J. Neurosci. 2009, 29, 10730–10740. [Google Scholar] [CrossRef]
- Wei, S.K.; Colecraft, H.M.; DeMaria, C.D.; Peterson, B.Z.; Zhang, R.; Kohout, T.A.; Rogers, T.B.; Yue, D.T. Ca(2+) channel modulation by recombinant auxiliary beta subunits expressed in young adult heart cells. Circ. Res. 2000, 86, 175–184. [Google Scholar] [CrossRef] [Green Version]
- Meissner, M.; Weissgerber, P.; Londono, J.E.; Prenen, J.; Link, S.; Ruppenthal, S.; Molkentin, J.D.; Lipp, P.; Nilius, B.; Freichel, M.; et al. Moderate calcium channel dysfunction in adult mice with inducible cardiomyocyte-specific excision of the cacnb2 gene. J. Biol. Chem. 2011, 286, 15875–15882. [Google Scholar] [CrossRef] [Green Version]
- Buraei, Z.; Yang, J. Structure and function of the beta subunit of voltage-gated Ca2+ channels. Biochim. Biophys. Acta 2013, 1828, 1530–1540. [Google Scholar] [CrossRef] [Green Version]
- Hullin, R.; Khan, I.F.; Wirtz, S.; Mohacsi, P.; Varadi, G.; Schwartz, A.; Herzig, S. Cardiac l-type calcium channel beta-subunits expressed in human heart have differential effects on single channel characteristics. J. Biol. Chem. 2003, 278, 21623–21630. [Google Scholar] [CrossRef] [Green Version]
- Herzig, S.; Khan, I.F.; Grundemann, D.; Matthes, J.; Ludwig, A.; Michels, G.; Hoppe, U.C.; Chaudhuri, D.; Schwartz, A.; Yue, D.T.; et al. Mechanism of ca(v)1.2 channel modulation by the amino terminus of cardiac beta2-subunits. FASEB J. 2007, 21, 1527–1538. [Google Scholar] [CrossRef] [PubMed]
- Hullin, R.; Matthes, J.; von Vietinghoff, S.; Bodi, I.; Rubio, M.; D’Souza, K.; Friedrich Khan, I.; Rottlander, D.; Hoppe, U.C.; Mohacsi, P.; et al. Increased expression of the auxiliary beta(2)-subunit of ventricular l-type Ca(2)+ channels leads to single-channel activity characteristic of heart failure. PLoS ONE 2007, 2, e292. [Google Scholar] [CrossRef] [PubMed]
- Jangsangthong, W.; Kuzmenkina, E.; Bohnke, A.K.; Herzig, S. Single-channel monitoring of reversible l-type Ca(2+) channel ca(v)alpha(1)-ca(v)beta subunit interaction. Biophys. J. 2011, 101, 2661–2670. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Despang, P.; Salamon, S.; Breitenkamp, A.F.; Kuzmenkina, E.; Herzig, S.; Matthes, J. Autism-associated mutations in the cavbeta2 calcium-channel subunit increase Ba(2+)-currents and lead to differential modulation by the rgk-protein gem. Neurobiol. Dis. 2020, 136, 104721. [Google Scholar] [CrossRef] [PubMed]
- Buraei, Z.; Yang, J. The ss subunit of voltage-gated Ca2+ channels. Physiol. Rev. 2010, 90, 1461–1506. [Google Scholar] [CrossRef] [Green Version]
- Berggren, P.O.; Yang, S.N.; Murakami, M.; Efanov, A.M.; Uhles, S.; Kohler, M.; Moede, T.; Fernstrom, A.; Appelskog, I.B.; Aspinwall, C.A.; et al. Removal of Ca2+ channel beta3 subunit enhances Ca2+ oscillation frequency and insulin exocytosis. Cell 2004, 119, 273–284. [Google Scholar] [CrossRef] [Green Version]
- Murakami, M.; Fleischmann, B.; De Felipe, C.; Freichel, M.; Trost, C.; Ludwig, A.; Wissenbach, U.; Schwegler, H.; Hofmann, F.; Hescheler, J.; et al. Pain perception in mice lacking the beta3 subunit of voltage-activated calcium channels. J. Biol. Chem. 2002, 277, 40342–40351. [Google Scholar] [CrossRef] [Green Version]
- Namkung, Y.; Smith, S.M.; Lee, S.B.; Skrypnyk, N.V.; Kim, H.L.; Chin, H.; Scheller, R.H.; Tsien, R.W.; Shin, H.S. Targeted disruption of the Ca2+ channel beta3 subunit reduces n- and l-type Ca2+ channel activity and alters the voltage-dependent activation of p/q-type Ca2+ channels in neurons. Proc. Natl. Acad. Sci. USA 1998, 95, 12010–12015. [Google Scholar] [CrossRef] [Green Version]
- Lee, K.; Kim, J.; Kohler, M.; Yu, J.; Shi, Y.; Yang, S.N.; Ryu, S.H.; Berggren, P.O. Blocking Ca(2+) channel beta3 subunit reverses diabetes. Cell Rep. 2018, 24, 922–934. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Belkacemi, A.; Hui, X.; Wardas, B.; Laschke, M.W.; Wissenbach, U.; Menger, M.D.; Lipp, P.; Beck, A.; Flockerzi, V. Ip3 receptor-dependent cytoplasmic Ca(2+) signals are tightly controlled by cavbeta3. Cell Rep. 2018, 22, 1339–1349. [Google Scholar] [CrossRef] [Green Version]
- He, L.L.; Zhang, Y.; Chen, Y.H.; Yamada, Y.; Yang, J. Functional modularity of the beta-subunit of voltage-gated Ca2+ channels. Biophys. J. 2007, 93, 834–845. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Takahashi, S.X.; Mittman, S.; Colecraft, H.M. Distinctive modulatory effects of five human auxiliary beta2 subunit splice variants on l-type calcium channel gating. Biophys. J. 2003, 84, 3007–3021. [Google Scholar] [CrossRef] [Green Version]
- Miranda-Laferte, E.; Ewers, D.; Guzman, R.E.; Jordan, N.; Schmidt, S.; Hidalgo, P. The n-terminal domain tethers the voltage-gated calcium channel beta2e-subunit to the plasma membrane via electrostatic and hydrophobic interactions. J. Biol. Chem. 2014, 289, 10387–10398. [Google Scholar] [CrossRef] [Green Version]
- Kazim, A.S.; Storm, P.; Zhang, E.; Renstrom, E. Palmitoylation of Ca(2+) channel subunit cavbeta2a induces pancreatic beta-cell toxicity via Ca(2+) overload. Biochem. Biophys. Res. Commun. 2017, 491, 740–746. [Google Scholar] [CrossRef] [PubMed]
- Hida, Y.; Ohtsuka, T. Cast and elks proteins: Structural and functional determinants of the presynaptic active zone. J. Biochem. 2010, 148, 131–137. [Google Scholar] [CrossRef] [Green Version]
- Billings, S.E.; Clarke, G.L.; Nishimune, H. Elks1 and Ca(2+) channel subunit beta4 interact and colocalize at cerebellar synapses. Neuroreport 2012, 23, 49–54. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kiyonaka, S.; Nakajima, H.; Takada, Y.; Hida, Y.; Yoshioka, T.; Hagiwara, A.; Kitajima, I.; Mori, Y.; Ohtsuka, T. Physical and functional interaction of the active zone protein cast/erc2 and the beta-subunit of the voltage-dependent Ca(2+) channel. J. Biochem. 2012, 152, 149–159. [Google Scholar] [CrossRef]
- Bonner-Weir, S. Morphological evidence for pancreatic polarity of beta-cell within islets of langerhans. Diabetes 1988, 37, 616–621. [Google Scholar] [CrossRef]
- Ohara-Imaizumi, M.; Aoyagi, K.; Yamauchi, H.; Yoshida, M.; Mori, M.X.; Hida, Y.; Tran, H.N.; Ohkura, M.; Abe, M.; Akimoto, Y.; et al. Elks/voltage-dependent Ca(2+) channel-beta subunit module regulates polarized Ca(2+) influx in pancreatic beta cells. Cell Rep. 2019, 26, 1213–1226. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Colecraft, H.M. Designer genetically encoded voltage-dependent calcium channel inhibitors inspired by rgk gtpases. J. Physiol. 2020, 598, 1683–1693. [Google Scholar] [CrossRef] [Green Version]
- Finlin, B.S.; Crump, S.M.; Satin, J.; Andres, D.A. Regulation of voltage-gated calcium channel activity by the rem and rad gtpases. Proc. Natl. Acad. Sci. USA 2003, 100, 14469–14474. [Google Scholar] [CrossRef] [Green Version]
- Finlin, B.S.; Mosley, A.L.; Crump, S.M.; Correll, R.N.; Ozcan, S.; Satin, J.; Andres, D.A. Regulation of l-type Ca2+ channel activity and insulin secretion by the rem2 gtpase. J. Biol. Chem. 2005, 280, 41864–41871. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, H.; Puhl, H.L., 3rd; Niu, S.L.; Mitchell, D.C.; Ikeda, S.R. Expression of rem2, an rgk family small gtpase, reduces n-type calcium current without affecting channel surface density. J. Neurosci. 2005, 25, 9762–9772. [Google Scholar] [CrossRef] [PubMed]
- Beguin, P.; Nagashima, K.; Gonoi, T.; Shibasaki, T.; Takahashi, K.; Kashima, Y.; Ozaki, N.; Geering, K.; Iwanaga, T.; Seino, S. Regulation of Ca2+ channel expression at the cell surface by the small g-protein kir/gem. Nature 2001, 411, 701–706. [Google Scholar] [CrossRef]
- Gunton, J.E.; Sisavanh, M.; Stokes, R.A.; Satin, J.; Satin, L.S.; Zhang, M.; Liu, S.M.; Cai, W.; Cheng, K.; Cooney, G.J.; et al. Mice deficient in gem gtpase show abnormal glucose homeostasis due to defects in beta-cell calcium handling. PLoS ONE 2012, 7, e39462. [Google Scholar] [CrossRef] [Green Version]
- Bannister, R.A.; Colecraft, H.M.; Beam, K.G. Rem inhibits skeletal muscle ec coupling by reducing the number of functional l-type Ca2+ channels. Biophys. J. 2008, 94, 2631–2638. [Google Scholar] [CrossRef] [Green Version]
- Yang, T.; Puckerin, A.; Colecraft, H.M. Distinct rgk gtpases differentially use alpha1- and auxiliary beta-binding-dependent mechanisms to inhibit cav1.2/cav2.2 channels. PLoS ONE 2012, 7, e37079. [Google Scholar]
- Ghiretti, A.E.; Paradis, S. Molecular mechanisms of activity-dependent changes in dendritic morphology: Role of rgk proteins. Trends. Neurosci. 2014, 37, 399–407. [Google Scholar] [CrossRef] [Green Version]
- Arikkath, J.; Campbell, K.P. Auxiliary subunits: Essential components of the voltage-gated calcium channel complex. Curr. Opin. Neurobiol. 2003, 13, 298–307. [Google Scholar] [CrossRef]
- Dolphin, A.C. Calcium channel auxiliary alpha(2)delta and beta subunits: Trafficking and one step beyond. Nat. Rev. Neurosci. 2012, 13, 542–555. [Google Scholar] [CrossRef]
- Davies, A.; Kadurin, I.; Alvarez-Laviada, A.; Douglas, L.; Nieto-Rostro, M.; Bauer, C.S.; Pratt, W.S.; Dolphin, A.C. The alpha2delta subunits of voltage-gated calcium channels form gpi-anchored proteins, a posttranslational modification essential for function. Proc. Natl. Acad. Sci. USA 2010, 107, 1654–1659. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gurnett, C.A.; Felix, R.; Campbell, K.P. Extracellular interaction of the voltage-dependent Ca2+ channel alpha2delta and alpha1 subunits. J. Biol. Chem. 1997, 272, 18508–18512. [Google Scholar] [CrossRef] [Green Version]
- Felix, R.; Gurnett, C.A.; De Waard, M.; Campbell, K.P. Dissection of functional domains of the voltage-dependent ca2+ channel alpha2delta subunit. J. Neurosci. 1997, 17, 6884–6891. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Canti, C.; Dolphin, A.C. Cavbeta subunit-mediated up-regulation of cav2.2 currents triggered by d2 dopamine receptor activation. Neuropharmacology 2003, 45, 814–827. [Google Scholar] [CrossRef]
- Gurnett, C.A.; De Waard, M.; Campbell, K.P. Dual function of the voltage-dependent Ca2+ channel alpha 2 delta subunit in current stimulation and subunit interaction. Neuron 1996, 16, 431–440. [Google Scholar] [CrossRef] [Green Version]
- Bourdin, B.; Briot, J.; Tetreault, M.P.; Sauve, R.; Parent, L. Negatively charged residues in the first extracellular loop of the l-type cav1.2 channel anchor the interaction with the cavalpha2delta1 auxiliary subunit. J. Biol. Chem. 2017, 292, 17236–17249. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Briot, J.; Mailhot, O.; Bourdin, B.; Tetreault, M.P.; Najmanovich, R.; Parent, L. A three-way inter-molecular network accounts for the cavalpha2delta1-induced functional modulation of the pore-forming cav1.2 subunit. J. Biol. Chem. 2018, 293, 7176–7188. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luo, Z.D.; Calcutt, N.A.; Higuera, E.S.; Valder, C.R.; Song, Y.H.; Svensson, C.I.; Myers, R.R. Injury type-specific calcium channel alpha 2 delta-1 subunit up-regulation in rat neuropathic pain models correlates with antiallodynic effects of gabapentin. J. Pharm. Exp. 2002, 303, 1199–1205. [Google Scholar] [CrossRef]
- Dolphin, A.C. The alpha(2)delta subunits of voltage-gated calcium channels. Biochim. Biophys. Acta 2007, 28, 220–228. [Google Scholar]
- Obermair, G.J.; Kugler, G.; Baumgartner, S.; Tuluc, P.; Grabner, M.; Flucher, B.E. 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. [Google Scholar] [CrossRef] [Green Version]
- Tuluc, P.; Kern, G.; Obermair, G.J.; Flucher, B.E. Computer modeling of sirna knockdown effects indicates an essential role of the Ca2+ channel alpha2delta-1 subunit in cardiac excitation-contraction coupling. Proc. Natl. Acad. Sci. USA 2007, 104, 11091–11096. [Google Scholar] [CrossRef] [Green Version]
- Polster, A.; Perni, S.; Bichraoui, H.; Beam, K.G. Stac adaptor proteins regulate trafficking and function of muscle and neuronal l-type Ca2+ channels. Proc. Natl. Acad. Sci. USA 2015, 112, 602–606. [Google Scholar] [CrossRef] [Green Version]
- Campiglio, M.; Coste de Bagneaux, P.; Ortner, N.J.; Tuluc, P.; Van Petegem, F.; Flucher, B.E. Stac proteins associate to the iq domain of cav1.2 and inhibit calcium-dependent inactivation. Proc. Natl. Acad. Sci. USA 2018, 115, 1376–1381. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Horstick, E.J.; Linsley, J.W.; Dowling, J.J.; Hauser, M.A.; McDonald, K.K.; Ashley-Koch, A.; Saint-Amant, L.; Satish, A.; Cui, W.W.; Zhou, W.; et al. Stac3 is a component of the excitation-contraction coupling machinery and mutated in native american myopathy. Nat. Commun. 2013, 4, 1952. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nelson, B.R.; Wu, F.; Liu, Y.; Anderson, D.M.; McAnally, J.; Lin, W.; Cannon, S.C.; Bassel-Duby, R.; Olson, E.N. Skeletal muscle-specific t-tubule protein stac3 mediates voltage-induced Ca2+ release and contractility. Proc. Natl. Acad. Sci. USA 2013, 110, 11881–11886. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Reinholt, B.M.; Ge, X.; Cong, X.; Gerrard, D.E.; Jiang, H. Stac3 is a novel regulator of skeletal muscle development in mice. PLoS ONE 2013, 8, e62760. [Google Scholar]
- Zhang, Y.; Cong, X.; Wang, A.; Jiang, H. Identification of the stac3 gene as a skeletal muscle-specifically expressed gene and a novel regulator of satellite cell differentiation in cattle. J. Anim. Sci. 2014, 92, 3284–3290. [Google Scholar] [CrossRef]
- Polster, A.; Nelson, B.R.; Olson, E.N.; Beam, K.G. Stac3 has a direct role in skeletal muscle-type excitation-contraction coupling that is disrupted by a myopathy-causing mutation. Proc. Natl. Acad. Sci. USA 2016, 113, 10986–10991. [Google Scholar] [CrossRef] [Green Version]
- Wong King Yuen, S.M.; Campiglio, M.; Tung, C.C.; Flucher, B.E.; Van Petegem, F. Structural insights into binding of stac proteins to voltage-gated calcium channels. Proc. Natl. Acad. Sci. USA 2017, 114, E9520–E9528. [Google Scholar] [CrossRef] [Green Version]
- Flucher, B.E.; 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. [Google Scholar] [CrossRef]
- Dai, S.; Klugbauer, N.; Zong, X.; Seisenberger, C.; Hofmann, F. The role of subunit composition on prepulse facilitation of the cardiac l-type calcium channel. FEBS Lett. 1999, 442, 70–74. [Google Scholar] [CrossRef] [Green Version]
- Platano, D.; Qin, N.; Noceti, F.; Birnbaumer, L.; Stefani, E.; Olcese, R. Expression of the alpha(2)delta subunit interferes with prepulse facilitation in cardiac l-type calcium channels. Biophys. J. 2000, 78, 2959–2972. [Google Scholar] [CrossRef] [Green Version]
- Fuller-Bicer, G.A.; Varadi, G.; Koch, S.E.; Ishii, M.; Bodi, I.; Kadeer, N.; Muth, J.N.; Mikala, G.; Petrashevskaya, N.N.; Jordan, M.A.; et al. Targeted disruption of the voltage-dependent calcium channel alpha2/delta-1-subunit. Am. J. Physiol. 2009, 297, H117–H124. [Google Scholar]
- Brodbeck, J.; Davies, A.; Courtney, J.M.; Meir, A.; Balaguero, N.; Canti, C.; Moss, F.J.; Page, K.M.; Pratt, W.S.; Hunt, S.P.; et al. The ducky mutation in cacna2d2 results in altered purkinje cell morphology and is associated with the expression of a truncated alpha 2 delta-2 protein with abnormal function. J. Biol. Chem. 2002, 277, 7684–7693. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wakamori, M.; Mikala, G.; Mori, Y. Auxiliary subunits operate as a molecular switch in determining gating behaviour of the unitary n-type Ca2+ channel current in xenopus oocytes. J. Physiol. 1999, 517, 659–672. [Google Scholar] [CrossRef]
- Dolphin, A.C. Voltage-gated calcium channels and their auxiliary subunits: Physiology and pathophysiology and pharmacology. J. Physiol. 2016, 594, 5369–5390. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Catterall, W.A. Structure and regulation of voltage-gated Ca2+ channels. Annu. Rev. Cell Dev. Biol. 2000, 16, 521–555. [Google Scholar] [CrossRef] [PubMed]
- Mauvais-Jarvis, F. Role of sex steroids in beta cell function, growth, and survival. Trends Endocrinol. Metab. Tem. 2016, 27, 844–855. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhou, Y.; Park, S.Y.; Su, J.; Bailey, K.; Ottosson-Laakso, E.; Shcherbina, L.; Oskolkov, N.; Zhang, E.; Thevenin, T.; Fadista, J.; et al. Tcf7l2 is a master regulator of insulin production and processing. Hum. Mol. Genet. 2014, 23, 6419–6431. [Google Scholar] [CrossRef] [Green Version]
- Ye, Y.; Barghouth, M.; Luan, C.; Kazim, A.; Zhou, Y.; Eliasson, L.; Zhang, E.; Hansson, O.; Thevenin, T.; Renstrom, E. The tcf7l2-dependent high-voltage activated calcium channel subunit alpha2delta-1 controls calcium signaling in rodent pancreatic beta-cells. Mol. Cell. Endocrinol. 2020, 502, 110673. [Google Scholar] [CrossRef] [PubMed]
- Vergult, S.; Dheedene, A.; Meurs, A.; Faes, F.; Isidor, B.; Janssens, S.; Gautier, A.; Le Caignec, C.; Menten, B. Genomic aberrations of the cacna2d1 gene in three patients with epilepsy and intellectual disability. Eur. J. Hum. Genet. Ejhg. 2015, 23, 628–632. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Templin, C.; Ghadri, J.R.; Rougier, J.S.; Baumer, A.; Kaplan, V.; Albesa, M.; Sticht, H.; Rauch, A.; Puleo, C.; Hu, D.; et al. Identification of a novel loss-of-function calcium channel gene mutation in short qt syndrome (sqts6). Eur. Heart J. 2011, 32, 1077–1088. [Google Scholar] [CrossRef]
- Burashnikov, E.; Pfeiffer, R.; Barajas-Martinez, H.; Delpon, E.; Hu, D.; Desai, M.; Borggrefe, M.; Haissaguerre, M.; Kanter, R.; Pollevick, G.D.; et al. Mutations in the cardiac l-type calcium channel associated with inherited j-wave syndromes and sudden cardiac death. Heart Rhythm 2010, 7, 1872–1882. [Google Scholar] [CrossRef] [Green Version]
- Bourdin, B.; Shakeri, B.; Tetreault, M.; Sauve, R.; Lesage, S.; Parent, L. Functional characterization of cav alpha2delta mutations associated with sudden cardiac death. J. Biol. Chem. 2015, 290, 2854–2869. [Google Scholar] [CrossRef] [Green Version]
- Gee, N.S.; Brown, J.P.; Dissanayake, V.U.; Offord, J.; Thurlow, R.; Woodruff, G.N. The novel anticonvulsant drug, gabapentin (neurontin), binds to the alpha2delta subunit of a calcium channel. J. Biol. Chem. 1996, 271, 5768–5776. [Google Scholar] [CrossRef] [Green Version]
- DeToledo, J.C.; Toledo, C.; DeCerce, J.; Ramsay, R.E. Changes in body weight with chronic, high-dose gabapentin therapy. Drug Monit. 1997, 19, 394–396. [Google Scholar] [CrossRef]
- Hoppe, C.; Rademacher, M.; Hoffmann, J.M.; Schmidt, D.; Elger, C.E. Bodyweight gain under pregabalin therapy in epilepsy: Mitigation by counseling patients? Seizure 2008, 17, 327–332. [Google Scholar] [CrossRef] [Green Version]
- Dolphin, A.C. Voltage-gated calcium channel alpha 2delta subunits: An assessment of proposed novel roles. F1000Res 2018, 7, 1830. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Geisler, S.; Schopf, C.L.; Obermair, G.J. Emerging evidence for specific neuronal functions of auxiliary calcium channel alpha(2)delta subunits. Gen. Physiol. Biophys. 2015, 34, 105–118. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tran-Van-Minh, A.; Dolphin, A.C. The alpha2delta ligand gabapentin inhibits the rab11-dependent recycling of the calcium channel subunit alpha2delta-2. J. Neurosci. 2010, 30, 12856–12867. [Google Scholar] [CrossRef] [Green Version]
- Bauer, C.S.; Nieto-Rostro, M.; Rahman, W.; Tran-Van-Minh, A.; Ferron, L.; Douglas, L.; Kadurin, I.; Sri Ranjan, Y.; Fernandez-Alacid, L.; Millar, N.S.; et al. The increased trafficking of the calcium channel subunit alpha2delta-1 to presynaptic terminals in neuropathic pain is inhibited by the alpha2delta ligand pregabalin. J. Neurosci. 2009, 29, 4076–4088. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hendrich, J.; Van Minh, A.T.; Heblich, F.; Nieto-Rostro, M.; Watschinger, K.; Striessnig, J.; Wratten, J.; Davies, A.; Dolphin, A.C. Pharmacological disruption of calcium channel trafficking by the α2β ligand gabapentin. Proc. Natl. Acad. Sci. USA 2008, 105, 3628–3633. [Google Scholar] [CrossRef] [Green Version]
- Todd, R.D.; McDavid, S.M.; Brindley, R.L.; Jewell, M.L.; Currie, K.P. Gabapentin inhibits catecholamine release from adrenal chromaffin cells. Anesthesiology 2012, 116, 1013–1024. [Google Scholar] [CrossRef] [Green Version]
- Davies, A.; Hendrich, J.; Van Minh, A.T.; Wratten, J.; Douglas, L.; Dolphin, A.C. Functional biology of the alpha(2)delta subunits of voltage-gated calcium channels. Trends Pharmacol. Sci 2007, 28, 220–228. [Google Scholar] [CrossRef]
- Micheva, K.D.; Taylor, C.P.; Smith, S.J. Pregabalin reduces the release of synaptic vesicles from cultured hippocampal neurons. Mol. Pharm. 2006, 70, 467–476. [Google Scholar] [CrossRef] [Green Version]
- Cordeira, J.W.; Felsted, J.A.; Teillon, S.; Daftary, S.; Panessiti, M.; Wirth, J.; Sena-Esteves, M.; Rios, M. Hypothalamic dysfunction of the thrombospondin receptor alpha2delta-1 underlies the overeating and obesity triggered by brain-derived neurotrophic factor deficiency. J. Neurosci. 2014, 34, 554–565. [Google Scholar] [CrossRef] [Green Version]
- Felsted, J.A.; Meng, A.; Ameroso, D.; Rios, M. Sex-specific effects of alpha2delta-1 in the ventromedial hypothalamus of female mice controlling glucose and lipid balance. Endocrinology 2020, 161, bqaa06. [Google Scholar] [CrossRef]
- Felsted, J.A.; Chien, C.H.; Wang, D.; Panessiti, M.; Ameroso, D.; Greenberg, A.; Feng, G.; Kong, D.; Rios, M. Alpha2delta-1 in sf1(+) neurons of the ventromedial hypothalamus is an essential regulator of glucose and lipid homeostasis. Cell Rep. 2017, 21, 2737–2747. [Google Scholar] [CrossRef] [Green Version]
- Kurshan, P.T.; Oztan, A.; Schwarz, T.L. Presynaptic alpha2delta-3 is required for synaptic morphogenesis independent of its Ca2+-channel functions. Nat. Neurosci. 2009, 12, 1415–1423. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ablinger, C.; Geisler, S.M.; Stanika, R.I.; Klein, C.T.; Obermair, G.J. Neuronal alpha2delta proteins and brain disorders. Pflug. Arch. 2020, 472, 845–863. [Google Scholar] [CrossRef]
- Chen, J.; Li, L.; Chen, S.R.; Chen, H.; Xie, J.D.; Sirrieh, R.E.; MacLean, D.M.; Zhang, Y.; Zhou, M.H.; Jayaraman, V.; et al. The alpha2delta-1-nmda receptor complex is critically involved in neuropathic pain development and gabapentin therapeutic actions. Cell Rep. 2018, 22, 2307–2321. [Google Scholar] [CrossRef] [Green Version]
- Geisler, S.; Schopf, C.L.; Stanika, R.; Kalb, M.; Campiglio, M.; Repetto, D.; Traxler, L.; Missler, M.; Obermair, G.J. Presynaptic alpha2delta-2 calcium channel subunits regulate postsynaptic gabaa receptor abundance and axonal wiring. J. Neurosci. 2019, 39, 2581–2605. [Google Scholar] [CrossRef] [Green Version]
- Eroglu, C.; Allen, N.J.; Susman, M.W.; O’Rourke, N.A.; Park, C.Y.; Ozkan, E.; Chakraborty, C.; Mulinyawe, S.B.; Annis, D.S.; Huberman, A.D.; et al. Gabapentin receptor alpha2delta-1 is a neuronal thrombospondin receptor responsible for excitatory cns synaptogenesis. Cell 2009, 139, 380–392. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, F.X.; Gadotti, V.M.; Souza, I.A.; Chen, L.; Zamponi, G.W. Bk potassium channels suppress cavalpha2delta subunit function to reduce inflammatory and neuropathic pain. Cell Rep. 2018, 22, 1956–1964. [Google Scholar] [CrossRef] [Green Version]
- Xie, L.; Kang, Y.; Liang, T.; Dolai, S.; Xie, H.; Parsaud, L.; Lopez, J.A.; Lam, P.P.; James, D.E.; Sugita, S.; et al. Rala gtpase tethers insulin granules to l- and r-type calcium channels through binding alpha(2) delta-1 subunit. Traffic 2013, 14, 428–439. [Google Scholar] [CrossRef] [PubMed]
- Sharp, A.H.; Campbell, K.P. Characterization of the 1,4-dihydropyridine receptor using subunit-specific polyclonal antibodies. Evidence for a 32,000-da subunit. J. Biol. Chem. 1989, 264, 2816–2825. [Google Scholar] [CrossRef]
- Chen, R.S.; Deng, T.C.; Garcia, T.; Sellers, Z.M.; Best, P.M. Calcium channel gamma subunits: A functionally diverse protein family. Cell Biochem. Biophys. 2007, 47, 178–186. [Google Scholar] [CrossRef]
- Andronache, Z.; Ursu, D.; Lehnert, S.; Freichel, M.; Flockerzi, V.; Melzer, W. The auxiliary subunit gamma 1 of the skeletal muscle l-type Ca2+ channel is an endogenous Ca2+ antagonist. Proc. Natl. Acad. Sci. USA 2007, 104, 17885–17890. [Google Scholar] [CrossRef] [Green Version]
- Freise, D.; Held, B.; Wissenbach, U.; Pfeifer, A.; Trost, C.; Himmerkus, N.; Schweig, U.; Freichel, M.; Biel, M.; Hofmann, F.; et al. Absence of the gamma subunit of the skeletal muscle dihydropyridine receptor increases l-type Ca2+ currents and alters channel inactivation properties. J. Biol. Chem. 2000, 275, 14476–14481. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ursu, D.; Schuhmeier, R.P.; Freichel, M.; Flockerzi, V.; Melzer, W. Altered inactivation of Ca2+ current and Ca2+ release in mouse muscle fibers deficient in the dhp receptor gamma1 subunit. J. Gen. Physiol. 2004, 124, 605–618. [Google Scholar] [CrossRef] [Green Version]
- Singer, D.; Biel, M.; Lotan, I.; Flockerzi, V.; Hofmann, F.; Dascal, N. The roles of the subunits in the function of the calcium channel. Science 1991, 253, 1553–1557. [Google Scholar] [CrossRef] [Green Version]
- Wei, X.Y.; Perez-Reyes, E.; Lacerda, A.E.; Schuster, G.; Brown, A.M.; Birnbaumer, L. Heterologous regulation of the cardiac Ca2+ channel alpha 1 subunit by skeletal muscle beta and gamma subunits. Implications for the structure of cardiac l-type Ca2+ channels. J. Biol. Chem. 1991, 266, 21943–21947. [Google Scholar] [CrossRef]
- Klugbauer, N.; Dai, S.; Specht, V.; Lacinova, L.; Marais, E.; Bohn, G.; Hofmann, F. A family of gamma-like calcium channel subunits. FEBS Lett. 2000, 470, 189–197. [Google Scholar] [CrossRef] [Green Version]
- Sipos, I.; Pika-Hartlaub, U.; Hofmann, F.; Flucher, B.E.; Melzer, W. Effects of the dihydropyridine receptor subunits gamma and alpha2delta on the kinetics of heterologously expressed l-type Ca2+ channels. Pflug. Arch. 2000, 439, 691–699. [Google Scholar]
- Rousset, M.; Cens, T.; Restituito, S.; Barrere, C.; Black, J.L., 3rd; McEnery, M.W.; Charnet, P. Functional roles of gamma2, gamma3 and gamma4, three new Ca2+ channel subunits, in p/q-type Ca2+ channel expressed in xenopus oocytes. J. Physiol. 2001, 532, 583–593. [Google Scholar] [CrossRef] [PubMed]
- Yang, L.; Katchman, A.; Morrow, J.P.; Doshi, D.; Marx, S.O. Cardiac l-type calcium channel (cav1.2) associates with gamma subunits. FASEB J. 2011, 25, 928–936. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luan, C.; Ye, Y.; Singh, T.; Barghouth, M.; Eliasson, L.; Artner, I.; Zhang, E.; Renstrom, E. The calcium channel subunit gamma-4 is regulated by mafa and necessary for pancreatic beta-cell specification. Commun. Biol. 2019, 2, 106. [Google Scholar] [CrossRef] [Green Version]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Tuluc, P.; Theiner, T.; Jacobo-Piqueras, N.; Geisler, S.M. Role of High Voltage-Gated Ca2+ Channel Subunits in Pancreatic β-Cell Insulin Release. From Structure to Function. Cells 2021, 10, 2004. https://doi.org/10.3390/cells10082004
Tuluc P, Theiner T, Jacobo-Piqueras N, Geisler SM. Role of High Voltage-Gated Ca2+ Channel Subunits in Pancreatic β-Cell Insulin Release. From Structure to Function. Cells. 2021; 10(8):2004. https://doi.org/10.3390/cells10082004
Chicago/Turabian StyleTuluc, Petronel, Tamara Theiner, Noelia Jacobo-Piqueras, and Stefanie M. Geisler. 2021. "Role of High Voltage-Gated Ca2+ Channel Subunits in Pancreatic β-Cell Insulin Release. From Structure to Function" Cells 10, no. 8: 2004. https://doi.org/10.3390/cells10082004
APA StyleTuluc, P., Theiner, T., Jacobo-Piqueras, N., & Geisler, S. M. (2021). Role of High Voltage-Gated Ca2+ Channel Subunits in Pancreatic β-Cell Insulin Release. From Structure to Function. Cells, 10(8), 2004. https://doi.org/10.3390/cells10082004