Microdomains in the Cardiovascular System pp 293-319 | Cite as
Distribution and Regulation of L-Type Ca2+ Channels in Cardiomyocyte Microdomains
Abstract
Cardiac excitation involves action potential generation by individual cells and its conduction from cell to cell through intercellular gap junctions. Excitation of the cellular membrane results in opening of the voltage-gated L-type Ca2+ channels, which allow a small amount of Ca2+ to enter the cell. This triggers the release of a much greater amount of Ca2+ from the intracellular Ca2+ store, the sarcoplasmic reticulum, and gives rise to the systolic Ca2+ transient and contraction. These processes are highly regulated by the autonomic nervous system, which ensures the acute and reliable contractile function of the heart and the short-term modulation of this function upon changes in heart rate or workload. Recently, it became evident that discrete clusters of L-type Ca2+ channels exist in the sarcolemma, where they form an interacting network with regulatory proteins and receptors. It allows the specificity, reliability, and accuracy of autonomic modulation of the excitation-contraction processes by a variety of neurohormonal pathways. Disruption in subcellular targeting of calcium channels and associated signaling pathways may contribute to the pathophysiology of a variety of cardiac diseases including heart failure and certain arrhythmias. This chapter reviews the emerging understanding of microdomain-specific distribution, functioning, regulation, and remodeling of L-type Ca2+ channels in atrial and ventricular myocytes and their contributions to the cellular signaling and cardiac pathology.
Keywords
L-type calcium channel Cardiomyocyte Microdomain Caveolin Calcium signaling Remodeling Heart failure Atrial fibrillationNotes
Compliance with Ethical Standards
Conflict of Interest Statement
The authors declare that they have no conflict of interest.
References
- Andersen OS, Koeppe RE (2007) Bilayer thickness and membrane protein function: an energetic perspective. Annu Rev Biophys Biomol Struct 36:107–130PubMedCrossRefGoogle Scholar
- Balijepalli RC, Kamp TJ (2008) Caveolae, ion channels and cardiac arrhythmias. Prog Biophys Mol Biol 98:149–160PubMedCrossRefGoogle Scholar
- Balijepalli RC, Lokuta AJ, Maertz NA et al (2003) Depletion of T-tubules and specific subcellular changes in sarcolemmal proteins in tachycardia-induced heart failure. Cardiovasc Res 59:67–77PubMedCrossRefGoogle Scholar
- Balijepalli RC, Foell JD, Hall DD et al (2006) Localization of cardiac L-type Ca2+ channels to a caveolar macromolecular signaling complex is required for beta(2)-adrenergic regulation. Proc Natl Acad Sci U S A 103:7500–7505PubMedPubMedCentralCrossRefGoogle Scholar
- Balycheva M, Glukhov A, Schobesberger S et al (2014) Increased open probability of L-type calcium channels localized in T-tubules in patients with chronic atrial fibrillation: role of channel subunits. Circulation 130:A18709Google Scholar
- Banfi C, Brioschi M, Wait R et al (2006) Proteomic analysis of membrane microdomains derived from both failing and non-failing human hearts. Proteomics 6:1976–1988PubMedCrossRefGoogle Scholar
- Bers DM (2002) Cardiac excitation-contraction coupling. Nature 415:198–205PubMedCrossRefGoogle Scholar
- Best JM, Kamp TJ (2012) Different subcellular populations of L-type Ca2+ channels exhibit unique regulation and functional roles in cardiomyocytes. J Mol Cell Cardiol 52:376–387PubMedCrossRefGoogle Scholar
- Bhargava A, Lin X, Novak P et al (2013) Super-resolution scanning patch clamp reveals clustering of functional ion channels in adult ventricular myocyte. Circ Res 112:1112–1120PubMedPubMedCentralCrossRefGoogle Scholar
- Bootman MD, Higazi DR, Coombes S et al (2006) Calcium signalling during excitation-contraction coupling in mammalian atrial myocytes. J Cell Sci 119:3915–3925PubMedCrossRefGoogle Scholar
- Boulware MI, Kordasiewicz H, Mermelstein PG (2007) Caveolin proteins are essential for distinct effects of membrane estrogen receptors in neurons. J Neurosci 27:9941–9950PubMedCrossRefGoogle Scholar
- Brette F, Komukai K, Orchard CH (2002) Validation of formamide as a detubulation agent in isolated rat cardiac cells. Am J Physiol Heart Circ Physiol 283:H1720–H1728PubMedCrossRefGoogle Scholar
- Brette F, Despa S, Bers DM et al (2005) Spatiotemporal characteristics of SR Ca2+ uptake and release in detubulated rat ventricular myocytes. J Mol Cell Cardiol 39:804–812PubMedCrossRefGoogle Scholar
- Bristow MR, Ginsburg R, Minobe W et al (1982) Decreased catecholamine sensitivity and beta-adrenergic-receptor density in failing human hearts. N Engl J Med 307:205–211PubMedCrossRefGoogle Scholar
- Bristow MR, Ginsburg R, Umans V et al (1986) Beta 1- and beta 2-adrenergic-receptor subpopulations in nonfailing and failing human ventricular myocardium: coupling of both receptor subtypes to muscle contraction and selective beta 1-receptor down-regulation in heart failure. Circ Res 59:297–309PubMedCrossRefGoogle Scholar
- Brundel BJ, Van Gelder IC, Henning RH et al (2001) Ion channel remodeling is related to intraoperative atrial effective refractory periods in patients with paroxysmal and persistent atrial fibrillation. Circulation 103:684–690PubMedCrossRefGoogle Scholar
- Brundel BJ, Ausma J, van Gelder IC et al (2002) Activation of proteolysis by calpains and structural changes in human paroxysmal and persistent atrial fibrillation. Cardiovasc Res 54:380–389PubMedCrossRefGoogle Scholar
- Bryant S, Kimura TE, Kong CH et al (2014) Stimulation of ICa by basal PKA activity is facilitated by caveolin-3 in cardiac ventricular myocytes. J Mol Cell Cardiol 68:47–55PubMedPubMedCentralCrossRefGoogle Scholar
- Caldwell JL, Smith CE, Taylor RF et al (2014) Dependence of cardiac transverse tubules on the BAR domain protein amphiphysin II (BIN-1). Circ Res 115:986–996PubMedPubMedCentralCrossRefGoogle Scholar
- Carl SL, Felix K, Caswell AH et al (1995) Immunolocalization of sarcolemmal dihydropyridine receptor and sarcoplasmic reticular triadin and ryanodine receptor in rabbit ventricle and atrium. J Cell Biol 129:673–682PubMedCrossRefGoogle Scholar
- Carnegie GK, Means CK, Scott JD (2009) A-kinase anchoring proteins: from protein complexes to physiology and disease. IUBMB Life 61:394–406PubMedPubMedCentralCrossRefGoogle Scholar
- Cavalli A, Eghbali M, Minosyan TY et al (2007) Localization of sarcolemmal proteins to lipid rafts in the myocardium. Cell Calcium 42:313–322PubMedPubMedCentralCrossRefGoogle Scholar
- Cerrone M, Delmar M (2014) Desmosomes and the sodium channel complex: implications for arrhythmogenic cardiomyopathy and Brugada syndrome. Trends Cardiovasc Med 24:184–190PubMedPubMedCentralCrossRefGoogle Scholar
- Cheng EP, Yuan C, Navedo MF et al (2011) Restoration of normal L-type Ca2+ channel function during Timothy syndrome by ablation of an anchoring protein. Circ Res 109:255–261PubMedPubMedCentralCrossRefGoogle Scholar
- Chen-Izu Y, McCulle SL, Ward CW et al (2006) Three-dimensional distribution of ryanodine receptor clusters in cardiac myocytes. Biophys J 91:1–13PubMedPubMedCentralCrossRefGoogle Scholar
- Chesley A, Lundberg MS, Asai T et al (2000) The beta(2)-adrenergic receptor delivers an antiapoptotic signal to cardiac myocytes through Gi-dependent coupling to phosphatidylinositol 3'-kinase. Circ Res 87:1172–1179PubMedCrossRefGoogle Scholar
- Christ T, Boknik P, Wohrl S et al (2004) L-type Ca2+ current downregulation in chronic human atrial fibrillation is associated with increased activity of protein phosphatases. Circulation 110:2651–2657PubMedCrossRefGoogle Scholar
- Clarke JD, Caldwell JL, Horn MA et al (2015) Perturbed atrial calcium handling in an ovine model of heart failure: potential roles for reductions in the L-type calcium current. J Mol Cell Cardiol 79:169–179PubMedPubMedCentralCrossRefGoogle Scholar
- Cloues RK, Sather WA (2000) Permeant ion binding affinity in subconductance states of an L-type Ca2+ channel expressed in Xenopus laevis oocytes. J Physiol 524(Pt 1):19–36PubMedPubMedCentralCrossRefGoogle Scholar
- Cohen AW, Park DS, Woodman SE et al (2003) Caveolin-1 null mice develop cardiac hypertrophy with hyperactivation of p42/44 MAP kinase in cardiac fibroblasts. Am J Physiol Cell Physiol 284:C457–C474PubMedCrossRefGoogle Scholar
- Dart C (2010) Lipid microdomains and the regulation of ion channel function. J Physiol 588:3169–3178PubMedPubMedCentralCrossRefGoogle Scholar
- Dibb KM, Clarke JD, Horn MA et al (2009) Characterization of an extensive transverse tubular network in sheep atrial myocytes and its depletion in heart failure. Circ Heart Fail 2:482–489PubMedCrossRefGoogle Scholar
- Dibb KM, Clarke JD, Eisner DA et al (2013) A functional role for transverse (t-) tubules in the atria. J Mol Cell Cardiol 58:84–91PubMedCrossRefGoogle Scholar
- Dobrev D, Teos LY, Lederer WJ (2009) Unique atrial myocyte Ca2+ signaling. J Mol Cell Cardiol 46:448–451PubMedCrossRefGoogle Scholar
- Edidin M (2003) The state of lipid rafts: from model membranes to cells. Annu Rev Biophys Biomol Struct 32:257–283PubMedCrossRefGoogle Scholar
- Epshtein Y, Chopra AP, Rosenhouse-Dantsker A et al (2009) Identification of a C-terminus domain critical for the sensitivity of Kir2.1 to cholesterol. Proc Natl Acad Sci U S A 106:8055–8060PubMedPubMedCentralCrossRefGoogle Scholar
- Feiner EC, Chung P, Jasmin JF et al (2011) Left ventricular dysfunction in murine models of heart failure and in failing human heart is associated with a selective decrease in the expression of caveolin-3. J Card Fail 17:253–263PubMedCrossRefGoogle Scholar
- Feng J, Yue L, Wang Z et al (1998) Ionic mechanisms of regional action potential heterogeneity in the canine right atrium. Circ Res 83:541–551PubMedCrossRefGoogle Scholar
- Foell JD, Balijepalli RC, Delisle BP et al (2004) Molecular heterogeneity of calcium channel beta-subunits in canine and human heart: evidence for differential subcellular localization. Physiol Genomics 17:183–200PubMedCrossRefGoogle Scholar
- Forssmann WG, Girardier L (1970) A study of the T system in rat heart. J Cell Biol 44:1–19PubMedPubMedCentralCrossRefGoogle Scholar
- Frisk M, Koivumaki JT, Norseng PA et al (2014) Variable t-tubule organization and Ca2+ homeostasis across the atria. Am J Physiol Heart Circ Physiol 307:H609–H620PubMedCrossRefGoogle Scholar
- Gathercole DV, Colling DJ, Skepper JN et al (2000) Immunogold-labeled L-type calcium channels are clustered in the surface plasma membrane overlying junctional sarcoplasmic reticulum in Guinea-pig myocytes-implications for excitation-contraction coupling in cardiac muscle. J Mol Cell Cardiol 32:1981–1994PubMedCrossRefGoogle Scholar
- George MS, Pitt GS (2006) The real estate of cardiac signaling: location, location, location. Proc Natl Acad Sci U S A 103:7535–7536PubMedPubMedCentralCrossRefGoogle Scholar
- Glukhov AV, Balycheva M, Sanchez-Alonso JL et al (2015a) Direct evidence for microdomain-specific localization and remodeling of functional L-type calcium channels in rat and human atrial myocytes. Circulation 132:2372–2384PubMedPubMedCentralCrossRefGoogle Scholar
- Glukhov AV, Kalyanasundaram A, Lou Q et al (2015b) Calsequestrin 2 deletion causes sinoatrial node dysfunction and atrial arrhythmias associated with altered sarcoplasmic reticulum calcium cycling and degenerative fibrosis within the mouse atrial pacemaker complex. Eur Heart J 36:686–697PubMedCrossRefGoogle Scholar
- Gomez AM, Valdivia HH, Cheng H et al (1997) Defective excitation-contraction coupling in experimental cardiac hypertrophy and heart failure. Science 276:800–806PubMedCrossRefGoogle Scholar
- Gondo N, Ono K, Mannen K et al (1998) Four conductance levels of cloned cardiac L-type Ca2+ channel alpha1 and alpha1/beta subunits. FEBS Lett 423:86–92PubMedCrossRefGoogle Scholar
- Gray PC, Tibbs VC, Catterall WA et al (1997) Identification of a 15-kDa cAMP-dependent protein kinase-anchoring protein associated with skeletal muscle L-type calcium channels. J Biol Chem 272:6297–6302PubMedCrossRefGoogle Scholar
- Harvey RD, Calaghan SC (2012) Caveolae create local signalling domains through their distinct protein content, lipid profile and morphology. J Mol Cell Cardiol 52:366–375PubMedCrossRefGoogle Scholar
- Hatem SN, Benardeau A, Rucker-Martin C et al (1997) Different compartments of sarcoplasmic reticulum participate in the excitation-contraction coupling process in human atrial myocytes. Circ Res 80:345–353PubMedCrossRefGoogle Scholar
- Hayashi T, Arimura T, Ueda K et al (2004) Identification and functional analysis of a caveolin-3 mutation associated with familial hypertrophic cardiomyopathy. Biochem Biophys Res Commun 313:178–184PubMedCrossRefGoogle Scholar
- He J, Conklin MW, Foell JD et al (2001) Reduction in density of transverse tubules and L-type Ca2+ channels in canine tachycardia-induced heart failure. Cardiovasc Res 49:298–307PubMedCrossRefGoogle Scholar
- He JQ, Balijepalli RC, Haworth RA et al (2005) Crosstalk of beta-adrenergic receptor subtypes through Gi blunts beta-adrenergic stimulation of L-type Ca2+ channels in canine heart failure. Circ Res 97:566–573PubMedCrossRefGoogle Scholar
- Heinzel FR, Bito V, Biesmans L et al (2008) Remodeling of T-tubules and reduced synchrony of Ca2+ release in myocytes from chronically ischemic myocardium. Circ Res 102:338–346PubMedCrossRefGoogle Scholar
- Heinzel FR, MacQuaide N, Biesmans L et al (2011) Dyssynchrony of Ca2+ release from the sarcoplasmic reticulum as subcellular mechanism of cardiac contractile dysfunction. J Mol Cell Cardiol 50:390–400PubMedCrossRefGoogle Scholar
- Hong T, Yang H, Zhang SS et al (2014) Cardiac BIN1 folds T-tubule membrane, controlling ion flux and limiting arrhythmia. Nat Med 20:624–632PubMedPubMedCentralCrossRefGoogle Scholar
- Horikawa YT, Panneerselvam M, Kawaraguchi Y et al (2011) Cardiac-specific overexpression of caveolin-3 attenuates cardiac hypertrophy and increases natriuretic peptide expression and signaling. J Am Coll Cardiol 57:2273–2283PubMedPubMedCentralCrossRefGoogle Scholar
- Hullin R, Khan IF, Wirtz S et al (2003) Cardiac L-type calcium channel beta-subunits expressed in human heart have differential effects on single channel characteristics. J Biol Chem 278:21623–21630PubMedCrossRefGoogle Scholar
- Insel PA, Head BP, Ostrom RS et al (2005) Caveolae and lipid rafts: G protein-coupled receptor signaling microdomains in cardiac myocytes. Ann N Y Acad Sci 1047:166–172PubMedCrossRefGoogle Scholar
- Johnson KR, Nicodemus-Johnson J, Carnegie GK et al (2012) Molecular evolution of A-kinase anchoring protein (AKAP)-7: implications in comparative PKA compartmentalization. BMC Evol Biol 12:125PubMedPubMedCentralCrossRefGoogle Scholar
- Kamp TJ, He JQ (2002) L-type Ca2+ channels gaining respect in heart failure. Circ Res 91:451–453PubMedCrossRefGoogle Scholar
- Kamp TJ, Hell JW (2000) Regulation of cardiac L-type calcium channels by protein kinase a and protein kinase C. Circ Res 87:1095–1102PubMedCrossRefGoogle Scholar
- Kawabe JI, Grant BS, Yamamoto M et al (2001) Changes in caveolin subtype protein expression in aging rat organs. Mol Cell Endocrinol 176:91–95PubMedCrossRefGoogle Scholar
- Kawai M, Hussain M, Orchard CH (1999) Excitation-contraction coupling in rat ventricular myocytes after formamide-induced detubulation. Am J Phys 277:H603–H609CrossRefGoogle Scholar
- Kirk MM, Izu LT, Chen-Izu Y et al (2003) Role of the transverse-axial tubule system in generating calcium sparks and calcium transients in rat atrial myocytes. J Physiol 547:441–451PubMedPubMedCentralCrossRefGoogle Scholar
- Klein G, Schroder F, Vogler D et al (2003) Increased open probability of single cardiac L-type calcium channels in patients with chronic atrial fibrillation. Role of phosphatase 2A. Cardiovasc Res 59:37–45PubMedCrossRefGoogle Scholar
- Le Scouarnec S, Bhasin N, Vieyres C et al (2008) Dysfunction in ankyrin-B-dependent ion channel and transporter targeting causes human sinus node disease. Proc Natl Acad Sci U S A 105:15617–15622PubMedPubMedCentralCrossRefGoogle Scholar
- Lenaerts I, Bito V, Heinzel FR et al (2009) Ultrastructural and functional remodeling of the coupling between Ca2+ influx and sarcoplasmic reticulum Ca2+ release in right atrial myocytes from experimental persistent atrial fibrillation. Circ Res 105:876–885PubMedCrossRefGoogle Scholar
- Lohse MJ, Engelhardt S, Eschenhagen T (2003) What is the role of beta-adrenergic signaling in heart failure? Circ Res 93:896–906PubMedCrossRefGoogle Scholar
- Louch WE, Bito V, Heinzel FR et al (2004) Reduced synchrony of Ca2+ release with loss of T-tubules-a comparison to Ca2+ release in human failing cardiomyocytes. Cardiovasc Res 62:63–73PubMedCrossRefGoogle Scholar
- Lyon AR, MacLeod KT, Zhang Y et al (2009) Loss of T-tubules and other changes to surface topography in ventricular myocytes from failing human and rat heart. Proc Natl Acad Sci U S A 106:6854–6859PubMedPubMedCentralCrossRefGoogle Scholar
- Mackenzie L, Bootman MD, Berridge MJ et al (2001) Predetermined recruitment of calcium release sites underlies excitation-contraction coupling in rat atrial myocytes. J Physiol 530:417–429PubMedPubMedCentralCrossRefGoogle Scholar
- Makarewich CA, Correll RN, Gao H et al (2012) A caveolae-targeted L-type Ca2+ channel antagonist inhibits hypertrophic signaling without reducing cardiac contractility. Circ Res 110:669–674PubMedPubMedCentralCrossRefGoogle Scholar
- Mangoni ME, Couette B, Bourinet E et al (2003) Functional role of L-type Cav1.3 Ca2+ channels in cardiac pacemaker activity. Proc Natl Acad Sci U S A 100:5543–5548PubMedPubMedCentralCrossRefGoogle Scholar
- McDonald TF, Pelzer S, Trautwein W et al (1994) Regulation and modulation of calcium channels in cardiac, skeletal, and smooth muscle cells. Physiol Rev 74:365–507PubMedCrossRefGoogle Scholar
- Munro S (2003) Lipid rafts: elusive or illusive? Cell 115:377–388PubMedCrossRefGoogle Scholar
- Nattel S, Maguy A, Le Bouter S et al (2007) Arrhythmogenic ion-channel remodeling in the heart: heart failure, myocardial infarction, and atrial fibrillation. Physiol Rev 87:425–456PubMedCrossRefGoogle Scholar
- Nichols CB, Rossow CF, Navedo MF et al (2010) Sympathetic stimulation of adult cardiomyocytes requires association of AKAP5 with a subpopulation of L-type calcium channels. Circ Res 107:747–756PubMedCrossRefGoogle Scholar
- Nikolaev VO, Bunemann M, Schmitteckert E et al (2006a) Cyclic AMP imaging in adult cardiac myocytes reveals far-reaching beta1-adrenergic but locally confined beta2-adrenergic receptor-mediated signaling. Circ Res 99:1084–1091PubMedCrossRefGoogle Scholar
- Nikolaev VO, Gambaryan S, Lohse MJ (2006b) Fluorescent sensors for rapid monitoring of intracellular cGMP. Nat Methods 3:23–25PubMedCrossRefGoogle Scholar
- Nikolaev VO, Moshkov A, Lyon AR et al (2010) Beta2-adrenergic receptor redistribution in heart failure changes cAMP compartmentation. Science 327:1653–1657PubMedCrossRefGoogle Scholar
- Osterrieder W, Brum G, Hescheler J et al (1982) Injection of subunits of cyclic AMP-dependent protein kinase into cardiac myocytes modulates Ca2+ current. Nature 298:576–578PubMedCrossRefGoogle Scholar
- Ouadid H, Albat B, Nargeot J (1995) Calcium currents in diseased human cardiac cells. J Cardiovasc Pharmacol 25:282–291PubMedCrossRefGoogle Scholar
- Palade GE, Bruns RR (1968) Structural modulations of plasmalemmal vesicles. J Cell Biol 37:633–649PubMedPubMedCentralCrossRefGoogle Scholar
- Pani B, Singh BB (2009) Lipid rafts/caveolae as microdomains of calcium signaling. Cell Calcium 45:625–633PubMedPubMedCentralCrossRefGoogle Scholar
- Park DS, Cohen AW, Frank PG et al (2003) Caveolin-1 null (−/−) mice show dramatic reductions in life span. Biochemistry 42:15124–15131PubMedCrossRefGoogle Scholar
- Patel HH, Murray F, Insel PA (2008) Caveolae as organizers of pharmacologically relevant signal transduction molecules. Annu Rev Pharmacol Toxicol 48:359–391PubMedPubMedCentralCrossRefGoogle Scholar
- Perera RK, Nikolaev VO (2013) Compartmentation of cAMP signalling in cardiomyocytes in health and disease. Acta Physiol (Oxf) 207:650–662CrossRefGoogle Scholar
- Pike LJ (2004) Lipid rafts: heterogeneity on the high seas. Biochem J 378:281–292PubMedPubMedCentralCrossRefGoogle Scholar
- Ratajczak P, Damy T, Heymes C et al (2003) Caveolin-1 and -3 dissociations from caveolae to cytosol in the heart during aging and after myocardial infarction in rat. Cardiovasc Res 57:358–369PubMedCrossRefGoogle Scholar
- Razani B, Woodman SE, Lisanti MP (2002) Caveolae: from cell biology to animal physiology. Pharmacol Rev 54:431–467PubMedCrossRefGoogle Scholar
- Richards MA, Clarke JD, Saravanan P et al (2011) Transverse tubules are a common feature in large mammalian atrial myocytes including human. Am J Physiol Heart Circ Physiol 301:H1996–H2005PubMedPubMedCentralCrossRefGoogle Scholar
- Romanenko VG, Rothblat GH, Levitan I (2002) Modulation of endothelial inward-rectifier K+ current by optical isomers of cholesterol. Biophys J 83:3211–3222PubMedPubMedCentralCrossRefGoogle Scholar
- Sanchez-Alonso JL, Bhargava A, O’Hara T et al (2016) Microdomain-specific modulation of L-type calcium channels leads to triggered ventricular arrhythmia in heart failure. Circ Res 119:944–955PubMedPubMedCentralCrossRefGoogle Scholar
- Schaper J, Kostin S, Hein S et al (2002) Structural remodelling in heart failure. Exp Clin Cardiol 7:64–68PubMedPubMedCentralGoogle Scholar
- Schotten U, Haase H, Frechen D et al (2003) The L-type Ca2+-channel subunits alpha1C and beta2 are not downregulated in atrial myocardium of patients with chronic atrial fibrillation. J Mol Cell Cardiol 35:437–443PubMedCrossRefGoogle Scholar
- Schroder E, Byse M, Satin J (2009) L-type calcium channel C terminus autoregulates transcription. Circ Res 104:1373–1381PubMedPubMedCentralCrossRefGoogle Scholar
- Schulson MN, Scriven DR, Fletcher P et al (2011) Couplons in rat atria form distinct subgroups defined by their molecular partners. J Cell Sci 124:1167–1174PubMedPubMedCentralCrossRefGoogle Scholar
- Scriven DR, Asghari P, Schulson MN et al (2010) Analysis of Cav1.2 and ryanodine receptor clusters in rat ventricular myocytes. Biophys J 99:3923–3929PubMedPubMedCentralCrossRefGoogle Scholar
- Sen L, Bialecki RA, Smith E et al (1992) Cholesterol increases the L-type voltage-sensitive calcium channel current in arterial smooth muscle cells. Circ Res 71:1008–1014PubMedCrossRefGoogle Scholar
- Shaw RM, Colecraft HM (2013) L-type calcium channel targeting and local signalling in cardiac myocytes. Cardiovasc Res 98:177–186PubMedPubMedCentralCrossRefGoogle Scholar
- Shibata EF, Brown TL, Washburn ZW et al (2006) Autonomic regulation of voltage-gated cardiac ion channels. J Cardiovasc Electrophysiol 17(Suppl 1):S34–S42PubMedCrossRefGoogle Scholar
- Simionescu M, Simionescu N, Palade GE (1975) Segmental differentiations of cell junctions in the vascular endothelium. The microvasculature. J Cell Biol 67:863–885PubMedCrossRefGoogle Scholar
- Simons K, Toomre D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1:31–39PubMedCrossRefGoogle Scholar
- Smyrnias I, Mair W, Harzheim D et al (2010) Comparison of the T-tubule system in adult rat ventricular and atrial myocytes, and its role in excitation-contraction coupling and inotropic stimulation. Cell Calcium 47:210–223PubMedCrossRefGoogle Scholar
- Song KS, Scherer PE, Tang Z et al (1996) Expression of caveolin-3 in skeletal, cardiac, and smooth muscle cells. Caveolin-3 is a component of the sarcolemma and co-fractionates with dystrophin and dystrophin-associated glycoproteins. J Biol Chem 271:15160–15165PubMedCrossRefGoogle Scholar
- Sprenger JU, Nikolaev VO (2013) Biophysical techniques for detection of cAMP and cGMP in living cells. Int J Mol Sci 14:8025–8046PubMedPubMedCentralCrossRefGoogle Scholar
- Stangherlin A, Zaccolo M (2012) Phosphodiesterases and subcellular compartmentalized cAMP signaling in the cardiovascular system. Am J Physiol Heart Circ Physiol 302:H379–H390PubMedCrossRefGoogle Scholar
- Takagishi Y, Rothery S, Issberner J et al (1997) Spatial distribution of dihydropyridine receptors in the plasma membrane of Guinea pig cardiac myocytes investigated by correlative confocal microscopy and label-fracture electron microscopy. J Electron Microsc 46:165–170CrossRefGoogle Scholar
- Tidball JG, Cederdahl JE, Bers DM (1991) Quantitative analysis of regional variability in the distribution of transverse tubules in rabbit myocardium. Cell Tissue Res 264:293–298PubMedCrossRefGoogle Scholar
- Timofeyev V, Myers RE, Kim HJ et al (2013) Adenylyl cyclase subtype-specific compartmentalization: differential regulation of L-type Ca2+ current in ventricular myocytes. Circ Res 112:1567–1576PubMedPubMedCentralCrossRefGoogle Scholar
- Trafford AW, Clarke JD, Richards MA et al (2013) Calcium signalling microdomains and the t-tubular system in atrial mycoytes: potential roles in cardiac disease and arrhythmias. Cardiovasc Res 98:192–203PubMedCrossRefGoogle Scholar
- Tsutsumi YM, Horikawa YT, Jennings MM et al (2008) Cardiac-specific overexpression of caveolin-3 induces endogenous cardiac protection by mimicking ischemic preconditioning. Circulation 118:1979–1988PubMedPubMedCentralCrossRefGoogle Scholar
- Wakili R, Yeh YH, Yan Qi X et al (2010) Multiple potential molecular contributors to atrial hypocontractility caused by atrial tachycardia remodeling in dogs. Circ Arrhythm Electrophysiol 3:530–541PubMedCrossRefGoogle Scholar
- Walden AP, Dibb KM, Trafford AW (2009) Differences in intracellular calcium homeostasis between atrial and ventricular myocytes. J Mol Cell Cardiol 46:463–473PubMedCrossRefGoogle Scholar
- Wei S, Guo A, Chen B et al (2010) T-tubule remodeling during transition from hypertrophy to heart failure. Circ Res 107:520–531PubMedPubMedCentralCrossRefGoogle Scholar
- Willoughby D, Cooper DM (2007) Organization and Ca2+ regulation of adenylyl cyclases in cAMP microdomains. Physiol Rev 87:965–1010PubMedCrossRefGoogle Scholar
- Woo AY, Xiao RP (2012) Beta-adrenergic receptor subtype signaling in heart: from bench to bedside. Acta Pharmacol Sin 33:335–341PubMedPubMedCentralCrossRefGoogle Scholar
- Woo SH, Cleemann L, Morad M (2003) Spatiotemporal characteristics of junctional and nonjunctional focal Ca2+ release in rat atrial myocytes. Circ Res 92:e1–11PubMedCrossRefGoogle Scholar
- Yamashita T, Nakajima T, Hazama H et al (1995) Regional differences in transient outward current density and inhomogeneities of repolarization in rabbit right atrium. Circulation 92:3061–3069PubMedCrossRefGoogle Scholar
- Yeh YH, Wakili R, Qi XY et al (2008) Calcium-handling abnormalities underlying atrial arrhythmogenesis and contractile dysfunction in dogs with congestive heart failure. Circ Arrhythm Electrophysiol 1:93–102PubMedCrossRefGoogle Scholar
- Zhang P, Mende U (2011) Regulators of G-protein signaling in the heart and their potential as therapeutic targets. Circ Res 109:320–333PubMedPubMedCentralCrossRefGoogle Scholar
- Zhang Q, Timofeyev V, Qiu H et al (2011) Expression and roles of Cav1.3 (alpha1D) L-type Ca2+ channel in atrioventricular node automaticity. J Mol Cell Cardiol 50:194–202PubMedCrossRefGoogle Scholar
- Zhao YY, Liu Y, Stan RV et al (2002) Defects in caveolin-1 cause dilated cardiomyopathy and pulmonary hypertension in knockout mice. Proc Natl Acad Sci U S A 99:11375–11380PubMedPubMedCentralCrossRefGoogle Scholar
- Zhu WZ, Wang SQ, Chakir K et al (2003) Linkage of beta1-adrenergic stimulation to apoptotic heart cell death through protein kinase A-independent activation of Ca2+/calmodulin kinase II. J Clin Invest 111:617–625PubMedPubMedCentralCrossRefGoogle Scholar