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ype Calcium Channels: Multiple Proteins Tune Function

Cardiac L-type calcium channel regulation by Leucine-Rich Repeat-Containing Protein 10

ORCID Icon & ORCID Icon
Article: 2355121 | Received 20 Mar 2024, Accepted 10 May 2024, Published online: 19 May 2024

References

  • Ertel EA, Campbell KP, Harpold MM, et al. Nomenclature of voltage-gated calcium channels. Neuron. 2000;25(3):533–10. doi: 10.1016/S0896-6273(00)81057-0
  • Reuter H. The dependence of slow inward current in Purkinje fibres on the extracellular calcium-concentration. J Physiol. 1967;192(2):479–492. doi: 10.1113/jphysiol.1967.sp008310
  • Beuckelmann DJ, Wier WG. Mechanism of release of calcium from sarcoplasmic reticulum of guinea-pig cardiac cells. J Physiol. 1988;405(1):233–255. doi: 10.1113/jphysiol.1988.sp017331
  • Anderson K, Lai FA, Liu QY, et al. Structural and functional characterization of the purified cardiac ryanodine receptor-Ca2+ release channel complex. J Biol Chem. 1989;264(2):1329–1335. doi: 10.1016/S0021-9258(19)85090-1
  • Ebashi S. Ca2+ and the contractile proteins. J Mol Cell Cardiol. 1984;16(2):129–136. doi: 10.1016/S0022-2828(84)80701-4
  • Bassani JW, Bassani RA, Bers DM. Relaxation in rabbit and rat cardiac cells: species-dependent differences in cellular mechanisms. J Physiol. 1994;476(2):279–293. doi: 10.1113/jphysiol.1994.sp020130
  • Reuter H. Localization of beta adrenergic receptors, and effects of noradrenaline and cyclic nucleotides on action potentials, ionic currents and tension in mammalian cardiac muscle. J Physiol. 1974;242(2):429–451. doi: 10.1113/jphysiol.1974.sp010716
  • Beuckelmann DJ, Näbauer M, Erdmann E. Intracellular calcium handling in isolated ventricular myocytes from patients with terminal heart failure. Circulation. 1992;85(3):1046–1055. doi: 10.1161/01.CIR.85.3.1046
  • Splawski I, Timothy KW, Sharpe LM, et al. Ca(V)1.2 calcium channel dysfunction causes a multisystem disorder including arrhythmia and autism. Cell. 2004;119(1):19–31. doi: 10.1016/j.cell.2004.09.011
  • Bartos DC, Grandi E, Ripplinger CM. Ion channels in the heart. Compr Physiol. 2015;5(3):1423–1464.
  • Catterall WA. Voltage gated sodium and calcium channels: discovery, structure, function, and pharmacology. Channels (Austin). 2023;17(1):2281714. doi: 10.1080/19336950.2023.2281714
  • Yao X, Gao S, Yan N. Structural biology of voltage-gated calcium channels. Channels (Austin). 2024;18(1):2290807. doi: 10.1080/19336950.2023.2290807
  • Angelotti T, Hofmann F. Tissue-specific expression of splice variants of the mouse voltage-gated calcium channel alpha2/delta subunit. FEBS Lett. 1996;397(2–3):331–337. doi: 10.1016/S0014-5793(96)01205-7
  • Foell JD, Balijepalli RC, Delisle BP, et al. Molecular heterogeneity of calcium channel β-subunits in canine and human heart: evidence for differential subcellular localization. Physiol Genomics. 2004;17(2):183–200. doi: 10.1152/physiolgenomics.00207.2003
  • Tang ZZ, Hong X, Wang J, et al. Signature combinatorial splicing profiles of rat cardiac- and smooth-muscle Cav1.2 channels with distinct biophysical properties. Cell Calcium. 2007;41(5):417–428. doi: 10.1016/j.ceca.2006.08.002
  • Tang ZZ, Liang MC, Lu S, et al. Transcript scanning reveals novel and extensive splice variations in human l-type voltage-gated calcium channel, cav1.2 α1 subunit. J Biol Chem. 2004;279(43):44335–44343. doi: 10.1074/jbc.M407023200
  • Liu G, Papa A, Katchman AN, et al. Mechanism of adrenergic Ca(V)1.2 stimulation revealed by proximity proteomics. Nature. 2020;577(7792):695–700. doi: 10.1038/s41586-020-1947-z
  • Woon MT, Long PA, Reilly L, et al. Pediatric dilated cardiomyopathy-associated lrrc10 (leucine-rich repeat–containing 10) variant reveals lrrc10 as an auxiliary subunit of cardiac l-type ca 2+ channels. JAHA. 2018;7(3). doi: 10.1161/JAHA.117.006428
  • Adameyko II, Adameyko II, Mudry RE, et al. Expression and regulation of mouse SERDIN1, a highly conserved cardiac-specific leucine-rich repeat protein. Dev Dyn. 2005;233(2):540–552. doi: 10.1002/dvdy.20368
  • Kim KH, Antkiewicz DS, Yan L, et al. Lrrc10 is required for early heart development and function in zebrafish. Dev Biol. 2007;308(2):494–506. doi: 10.1016/j.ydbio.2007.06.005
  • Nakane T, Satoh T, Inada Y, et al. Molecular cloning and expression of HRLRRP, a novel heart-restricted leucine-rich repeat protein. Biochem Biophys Res Commun. 2004;314(4):1086–1092. doi: 10.1016/j.bbrc.2003.12.202
  • Bella J, Hindle KL, McEwan PA, et al. The leucine-rich repeat structure. Cell Mol Life Sci. 2008;65(15):2307–2333. doi: 10.1007/s00018-008-8019-0
  • Ng AC, Eisenberg JM, Heath RJW, et al. Human leucine-rich repeat proteins: a genome-wide bioinformatic categorization and functional analysis in innate immunity. Proc Natl Acad Sci U S A. 2011;108 Suppl 1(Suppl 1):4631–4638. doi: 10.1073/pnas.1000093107
  • Yan J, Aldrich RW. LRRC26 auxiliary protein allows BK channel activation at resting voltage without calcium. Nature. 2010;466(7305):513–516. doi: 10.1038/nature09162
  • Yan J, Aldrich RW. BK potassium channel modulation by leucine-rich repeat-containing proteins. Proc Natl Acad Sci U S A. 2012;109(20):7917–7922. doi: 10.1073/pnas.1205435109
  • Jumper J, Evans R, Pritzel A, et al. Highly accurate protein structure prediction with AlphaFold. Nature. 2021;596(7873):583–589. doi: 10.1038/s41586-021-03819-2
  • Brody MJ, Cho E, Mysliwiec MR, et al. Lrrc10 is a novel cardiac-specific target gene of Nkx2-5 and GATA4. J Mol Cell Cardiol. 2013;62:237–246. doi: 10.1016/j.yjmcc.2013.05.020
  • Fan X, Yang Q, Wang Y, et al. Cloning and characterization of the cardiac-specific Lrrc10 promoter. BMB Rep. 2011;44(2):123–128. doi: 10.5483/BMBRep.2011.44.2.123
  • Brody MJ, Feng L, Grimes AC, et al. LRRC10 is required to maintain cardiac function in response to pressure overload. Am J Physiol Heart Circ Physiol. 2016;310(2):H269–78. doi: 10.1152/ajpheart.00717.2014
  • Brody MJ, Hacker TA, Patel JR, et al. Ablation of the cardiac-specific gene leucine-rich repeat containing 10 (Lrrc10) results in dilated cardiomyopathy. PLoS One. 2012;7(12):e51621. doi: 10.1371/journal.pone.0051621
  • Stockdale WT, Lemieux ME, Killen AC, et al. Heart regeneration in the Mexican Cavefish. Cell Rep. 2018;25(8):1997–2007.e7. doi: 10.1016/j.celrep.2018.10.072
  • Nguyen PD, Gooijers I, Campostrini G, et al. Interplay between calcium and sarcomeres directs cardiomyocyte maturation during regeneration. Science. 2023;380(6646):758–764. doi: 10.1126/science.abo6718
  • Salamon RJ, McKeon MC, Bae J, et al. LRRC10 regulates mammalian cardiomyocyte cell cycle during heart regeneration. NPJ Regen Med. 2023;8(1):39. doi: 10.1038/s41536-023-00316-0
  • Qu XK, Yuan F, Li R-G, et al. Prevalence and spectrum of LRRC10 mutations associated with idiopathic dilated cardiomyopathy. Mol Med Rep. 2015;12(3):3718–3724. doi: 10.3892/mmr.2015.3843
  • Huang L, Tang S, Chen Y, et al. Molecular pathological study on LRRC10 in sudden unexplained nocturnal death syndrome in the Chinese Han population. Int J Legal Med. 2017;131(3):621–628. doi: 10.1007/s00414-016-1516-z
  • Kim KH, Kim T-G, Micales BK, et al. Dynamic expression patterns of leucine-rich repeat containing protein 10 in the heart. Dev Dyn. 2007;236(8):2225–2234. doi: 10.1002/dvdy.21225
  • Lu F, Pu WT. The architecture and function of cardiac dyads. Biophys Rev. 2020;12(4):1007–1017. doi: 10.1007/s12551-020-00729-x
  • Del Rivero Morfin PJ, Chavez DS, Jayaraman S, et al. A genetically encoded actuator selectively boosts l-type calcium channels in diverse physiological settings. bioRxiv. 2023. doi: 10.1101/2023.09.22.558856
  • Kanevsky N, Dascal N. Regulation of maximal open probability is a separable function of Ca(v)beta subunit in L-type Ca2+ channel, dependent on NH2 terminus of alpha1C (Ca(v)1.2alpha). J Gen Physiol. 2006;128(1):15–36. doi: 10.1085/jgp.200609485
  • Simms BA, Souza IA, Rehak R, et al. The Cav1.2 N terminus contains a CaM kinase site that modulates channel trafficking and function. Pflugers Arch - Eur J Physiol. 2015;467(4):677–686. doi: 10.1007/s00424-014-1538-7
  • Hulme JT, Yarov‐Yarovoy V, Lin TW-C, et al. Autoinhibitory control of the CaV1.2 channel by its proteolytically processed distal C-terminal domain. J Physiol. 2006;576(1):87–102. doi: 10.1113/jphysiol.2006.111799
  • Shi C, Soldatov NM. Molecular determinants of voltage-dependent slow inactivation of the Ca2+ channel. J Biol Chem. 2002;277(9):6813–6821. doi: 10.1074/jbc.M110524200
  • Best JM, Kamp TJ. Different subcellular populations of L-type Ca2+ channels exhibit unique regulation and functional roles in cardiomyocytes. J Mol Cell Cardiol. 2012;52(2):376–387. doi: 10.1016/j.yjmcc.2011.08.014
  • Balijepalli RC, Foell JD, Hall DD, et al. Localization of cardiac L-type Ca 2+ channels to a caveolar macromolecular signaling complex is required for β 2 -adrenergic regulation. Proc Natl Acad Sci U S A. 2006;103(19):7500–7505. doi: 10.1073/pnas.0503465103
  • Makarewich CA, Correll RN, Gao H, et al. A caveolae-targeted l-type ca 2+ channel antagonist inhibits hypertrophic signaling without reducing cardiac contractility. Circ Res. 2012;110(5):669–674. doi: 10.1161/CIRCRESAHA.111.264028
  • Meguro T, Hong C, Asai K, et al. Cyclosporine attenuates pressure-overload hypertrophy in mice while enhancing susceptibility to decompensation and heart failure. Circ Res. 1999;84(6):735–740. doi: 10.1161/01.RES.84.6.735
  • Sanchez-Alonso JL, Fedele L, Copier JS, et al. Functional LTCC-β 2 AR complex needs caveolin-3 and is disrupted in heart failure. Circ Res. 2023;133(2):120–137. doi: 10.1161/CIRCRESAHA.123.322508
  • De Nittis P, Efthymiou S, Sarre A, et al. Inhibition of G-protein signalling in cardiac dysfunction of intellectual developmental disorder with cardiac arrhythmia (IDDCA) syndrome. J Med Genet. 2021;58(12):815–831. doi: 10.1136/jmedgenet-2020-107015
  • Lodder EM, De Nittis P, Koopman C, et al. GNB5 mutations cause an autosomal-recessive multisystem syndrome with sinus bradycardia and cognitive disability. Am J Hum Genet. 2016;99(3):704–710. doi: 10.1016/j.ajhg.2016.06.025
  • Mesirca P, Bidaud I, Mangoni ME. Rescuing cardiac automaticity in L-type Cav1.3 channelopathies and beyond. J Physiol. 2016;594(20):5869–5879. doi: 10.1113/JP270678
  • Baudot M, Torre E, Bidaud I, et al. Concomitant genetic ablation of L-type Cav1.3 (α1D) and T-type Cav3.1 (α1G) Ca2+ channels disrupts heart automaticity. Sci Rep. 2020;10(1):18906. doi: 10.1038/s41598-020-76049-7
  • Mangoni ME, Couette B, Bourinet E, et al. Functional role of L-type Cav1.3 Ca2+ channels in cardiac pacemaker activity. Proc Natl Acad Sci U S A. 2003;100(9):5543–5548. doi: 10.1073/pnas.0935295100