Abstract
Cells that have intrinsic electrical excitability utilize changes in membrane potential to communicate with neighboring cells and initiate cellular cascades. Excitable cells like neurons and myocytes have evolved highly specialized subcellular architectures to translate these electrical signals into cellular events. One such structural specialization is sarco-/endoplasmic reticulum-plasma membrane contact sites. These membrane contact sites are positioned by specific membrane-membrane tethering proteins and contain an ever-expanding list of additional proteins that organize information transfer across the junctional space (~ 15–25 nm distance) to shape membrane identity and control cellular excitability. In this chapter we discuss how contacts between the sarco-/endoplasmic reticulum and plasma membrane are essential for regulated excitation-contraction coupling in striated muscle and control of lipid-dependent ion channels.
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References
Amarilio R, Ramachandran S, Sabanay H, Lev S (2005) Differential regulation of endoplasmic reticulum structure through VAP-Nir protein interaction. J Biol Chem 280:5934–5944
Armstrong CM, Bezanilla FM, Horowicz P (1972) Twitches in the presence of ethylene glycol bis( β-aminoethyl ether)-N,N′-tetracetic acid. Biochim Biophys Acta 267:605-608
Balla T (2013) Phosphoinositides: tiny lipids with giant impact on cell regulation. Physiol Rev 93:1019–1137
Bennett HJ, Davenport JB, Collins RF, Trafford AW, Pinali C, Kitmitto A (2013) Human junctophilin-2 undergoes a structural rearrangement upon binding PtdIns(3,4,5)P3 and the S101R mutation identified in hypertrophic cardiomyopathy obviates this response. Biochem J 456:205–217
Berridge MJ (2008) Smooth muscle cell calcium activation mechanisms. J Physiol 586:5047–5061
Bers DM (2002) Cardiac excitation-contraction coupling. Nature 415:198–205
Bers DM, Guo T (2005) Calcium signaling in cardiac ventricular myocytes. Ann N Y Acad Sci 1047:86–98
Beurg M, Ahern CA, Vallejo P, Conklin MW, Powers PA, Gregg RG, Coronado R (1999) Involvement of the carboxy-terminus region of the dihydropyridine receptor β1a subunit in excitation-contraction coupling of skeletal muscle. Biophys J 77:2953–2967
Block BA, Imagawa T, Campbell KP, Franzini-Armstrong C (1988) Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J Cell Biol 107:2587–2600
Brown DA, Adams PR (1980) Muscarinic suppression of a novel voltage-sensitive K+ current in a vertebrate neurone. Nature 283:673–676
Chang CL, Hsieh TS, Yang TT, Rothberg KG, Azizoglu DB, Volk E, Liao JC, Liou J (2013) Feedback regulation of receptor-induced Ca2+ signaling mediated by E-Syt1 and Nir2 at endoplasmic reticulum-plasma membrane junctions. Cell Rep 5:813–825
Cheng H, Lederer WJ (2008) Calcium sparks. Physiol Rev 88:1491–1545
Cheng H, Lederer WJ, Cannell MB (1993) Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science 262:740–744
Chung J, Nakatsu F, Baskin JM, De Camilli P (2015a) Plasticity of PI4KIIIα interactions at the plasma membrane. EMBO Rep 16:312–320
Chung J, Torta F, Masai K, Lucast L, Czapla H, Tanner LB, Narayanaswamy P, Wenk MR, Nakatsu F, De Camilli P (2015b) PI4P/phosphatidylserine countertransport at ORP5- and ORP8-mediated ER-plasma membrane contacts. Science 349:428–432
Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651–657
Dickson EJ, Jensen JB, Hille B (2014) Golgi and plasma membrane pools of PI(4)P contribute to plasma membrane PI(4,5)P2 and maintenance of KCNQ2/3 ion channel current. Proc Natl Acad Sci USA 111:E2281–E2290
Dickson EJ, Jensen JB, Vivas O, Kruse M, Traynor-Kaplan AE, Hille B (2016) Dynamic formation of ER-PM junctions presents a lipid phosphatase to regulate phosphoinositides. J Cell Biol 213:33–48
Dixon RE, Yuan C, Cheng EP, Navedo MF, Santana LF (2012) Ca2+ signaling amplification by oligomerization of L-type Cav1.2 channels. Proc Natl Acad Sci USA 109:1749–1754
Dixon RE, Moreno CM, Yuan C, Opitz-Araya X, Binder MD, Navedo MF, Santana LF (2015) Graded Ca2+/calmodulin-dependent coupling of voltage-gated CaV1.2 channels. Elife 4
Fabiato A (1983) Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am J Physiol 245:C1–14
Feske S, Giltnane J, Dolmetsch R, Staudt LM, Rao A (2001) Gene regulation mediated by calcium signals in T lymphocytes. Nat Immunol 2:316–324
Franzini-Armstrong C, Protasi F (1997) Ryanodine receptors of striated muscles: a complex channel capable of multiple interactions. Physiol Rev 77:699–729
Giordano F, Saheki Y, Idevall-Hagren O, Colombo SF, Pirruccello M, Milosevic I, Gracheva EO, Bagriantsev SN, Borgese N, De Camilli P (2013) PI(4,5)P2-dependent and Ca2+-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 153:1494–1509
Gomez AM, Guatimosim S, Dilly KW, Vassort G, Lederer WJ (2001) Heart failure after myocardial infarction: altered excitation-contraction coupling. Circulation 104:688–693
Hansen SB, Tao X, MacKinnon R (2011) Structural basis of PIP2 activation of the classical inward rectifier K+ channel Kir2.2. Nature 477:495–498
Hilgemann DW, Ball R (1996) Regulation of cardiac Na+,Ca2+ exchange and KATP potassium channels by PIP2. Science 273:956–959
Hilgemann DW, Feng S, Nasuhoglu C (2001) The complex and intriguing lives of PIP2 with ion channels and transporters. Sci STKE 2001:re19
Hille B, Dickson E, Kruse M, Falkenburger B (2014) Dynamic metabolic control of an ion channel. Prog iMol Biol Transl Sci 123:219–247
Hille B, Dickson EJ, Kruse M, Vivas O, Suh BC (2015) Phosphoinositides regulate ion channels. Biochim Biophys Acta 1851:844–856
Hong TT, Smyth JW, Gao D, Chu KY, Vogan JM, Fong TS, Jensen BC, Colecraft HM, Shaw RM (2010) BIN1 localizes the L-type calcium channel to cardiac T-tubules. PLoS Biol 8:e1000312
Hou XW, Pedi L, Diver MM, Long SB (2012) Crystal structure of the calcium release-activated calcium channel Orai. Science 338:1308–1313
Idevall-Hagren O, Lu A, Xie B, De Camilli P (2015) Triggered Ca2+ influx is required for extended synaptotagmin 1-induced ER-plasma membrane tethering. EMBO J 34:2291–2305
Inoue M, Bridge JH (2003) Ca2+ sparks in rabbit ventricular myocytes evoked by action potentials: involvement of clusters of L-type Ca2+ channels. Circ Res 92:532–538
Ito K, Komazaki S, Sasamoto K, Yoshida M, Nishi M, Kitamura K, Takeshima H (2001) Deficiency of triad junction and contraction in mutant skeletal muscle lacking junctophilin type 1. J Cell Biol 154:1059–1067
Kim S, Kedan A, Marom M, Gavert N, Keinan O, Selitrennik M, Laufman O, Lev S (2013) The phosphatidylinositol-transfer protein Nir2 binds phosphatidic acid and positively regulates phosphoinositide signalling. EMBO Rep 14:891–899
Kim YJ, Guzman-Hernandez ML, Wisniewski E, Balla T (2015) Phosphatidylinositol-phosphatidic acid exchange by Nir2 at ER-PM contact sites maintains phosphoinositide signaling competence. Dev Cell 33:549–561
Komazaki S, Ito K, Takeshima H, Nakamura H (2002) Deficiency of triad formation in developing skeletal muscle cells lacking junctophilin type 1. FEBS Lett 524:225–229
Kotlikoff MI (2003) Calcium-induced calcium release in smooth muscle: the case for loose coupling. Prog iBiophys Mol Biol 83:171–191
Kruse M, Hille B (2013) The phosphoinositide sensitivity of the KV channel family. Channels (Austin, Tex) 7:530–536
Kruse M, Hammond GR, Hille B (2012) Regulation of voltage-gated potassium channels by PI(4,5)P2. J Gen Physiol 140:189–205
Kugler G, Weiss RG, Flucher BE, Grabner M (2004) Structural requirements of the dihydropyridine receptor α1S II–III loop for skeletal-type excitation-contraction coupling. J Biol Chem 279:4721–4728
Lanner JT, Georgiou DK, Joshi AD, Hamilton SL (2010) Ryanodine receptors: structure, expression, molecular details, and function in calcium release. Cold Spring Harb Perspect Biol 2:a003996
Lee E, Marcucci M, Daniell L, Pypaert M, Weisz OA, Ochoa GC, Farsad K, Wenk MR, De Camilli P (2002) Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science 297:1193–1196
Logothetis DE, Petrou VI, Adney SK, Mahajan R (2010) Channelopathies linked to plasma membrane phosphoinositides. Pflugers Arch 460:321–341
Maeda K, Anand K, Chiapparino A, Kumar A, Poletto M, Kaksonen M, Gavin AC (2013) Interactome map uncovers phosphatidylserine transport by oxysterol-binding proteins. Nature 501:257–261
McCarl CA, Picard C, Khalil S, Kawasaki T, Rother J, Papolos A, Kutok J, Hivroz C, Ledeist F, Plogmann K et al (2009) ORAI1 deficiency and lack of store-operated Ca2+ entry cause immunodeficiency, myopathy, and ectodermal dysplasia. J Allergy Clin immunol 124:1311–1318.e1317
Minamisawa S, Oshikawa J, Takeshima H, Hoshijima M, Wang Y, Chien KR, Ishikawa Y, Matsuoka R (2004) Junctophilin type 2 is associated with caveolin-3 and is down-regulated in the hypertrophic and dilated cardiomyopathies. Biochem Biophys Res Commun 325:852–856
Moore DH, Ruska H (1957) Electron microscope study of mammalian cardiac muscle cells. J Biophys Biochem Cytol 3:261–268
Nakai J, Dirksen RT, Nguyen HT, Pessah IN, Beam KG, Allen PD (1996) Enhanced dihydropyridine receptor channel activity in the presence of ryanodine receptor. Nature 380:72–75
Nakai J, Sekiguchi N, Rando TA, Allen PD, Beam KG (1998a) Two regions of the ryanodine receptor involved in coupling with L-type Ca2+ channels. J Biol Chem 273:13403–13406
Nakai J, Tanabe T, Konno T, Adams B, Beam KG (1998b) Localization in the II-III loop of the dihydropyridine receptor of a sequence critical for excitation-contraction coupling. J Biol Chem 273:24983–24986
Nakatsu F, Baskin JM, Chung J, Tanner LB, Shui G, Lee SY, Pirruccello M, Hao M, Ingolia NT, Wenk MR et al (2012) PtdIns4P synthesis by PI4KIIIα at the plasma membrane and its impact on plasma membrane identity. J Cell Biol 199:1003–1016
Navedo MF, Santana LF (2013) CaV1.2 sparklets in heart and vascular smooth muscle. J Mol Cell Cardiol 58:67–76
Navedo MF, Cheng EP, Yuan C, Votaw S, Molkentin JD, Scott JD, Santana LF (2010) Increased coupled gating of L-type Ca2+ channels during hypertension and Timothy syndrome. Circ Res 106:748–756
Nishi M, Mizushima A, Nakagawara K, Takeshima H (2000) Characterization of human junctophilin subtype genes. Biochem Biophys Res Commun 273:920–927
Prakriya M, Lewis RS (2015) Store-operated calcium channels. Physiol Rev 95:1383–1436
Protasi F, Takekura H, Wang Y, Chen SR, Meissner G, Allen PD, Franzini-Armstrong C (2000) RYR1 and RYR3 have different roles in the assembly of calcium release units of skeletal muscle. Biophys J 79:2494–2508
Protasi F, Paolini C, Nakai J, Beam KG, Franzini-Armstrong C, Allen PD (2002) Multiple regions of RyR1 mediate functional and structural interactions with α1S-dihydropyridine receptors in skeletal muscle. Biophys J 83:3230–3244
Rohács T, Lopes CM, Jin T, Ramdya PP, Molnar Z, Logothetis DE (2003) Specificity of activation by phosphoinositides determines lipid regulation of Kir channels. Proc Natl Acad Sci USA 100:745–750
Sanders KM, Koh SD, Ro S, Ward SM (2012) Regulation of gastrointestinal motility – insights from smooth muscle biology. Nat Rev Gastroenterol Hepatol 9:633–645
Sheridan DC, Cheng W, Ahern CA, Mortenson L, Alsammarae D, Vallejo P, Coronado R (2003) Truncation of the carboxyl terminus of the dihydropyridine receptor β1a subunit promotes Ca2+ dependent excitation-contraction coupling in skeletal myotubes. Biophys J 84:220–237
Sheridan DC, Takekura H, Franzini-Armstrong C, Beam KG, Allen PD, Perez CF (2006) Bidirectional signaling between calcium channels of skeletal muscle requires multiple direct and indirect interactions. Proc Natl Acad Sci USA 103:19760–19765
Sobie EA, Ramay HR (2009) Excitation-contraction coupling gain in ventricular myocytes: insights from a parsimonious model. J Physiol 587:1293–1299
Song LS, Guatimosim S, Gomez-Viquez L, Sobie EA, Ziman A, Hartmann H, Lederer WJ (2005) Calcium biology of the transverse tubules in heart. Ann N Y Acad Sci 1047:99–111
Stefan CJ, Manford AG, Baird D, Yamada-Hanff J, Mao Y, Emr SD (2011) Osh proteins regulate phosphoinositide metabolism at ER-plasma membrane contact sites. Cell 144:389–401
Stiber J, Hawkins A, Zhang ZS, Wang S, Burch J, Graham V, Ward CC, Seth M, Finch E, Malouf N et al (2008) STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nat Cell Biol 10:688–697
Suh BC, Horowitz LF, Hirdes W, Mackie K, Hille B (2004) Regulation of KCNQ2/KCNQ3 current by G protein cycling: the kinetics of receptor-mediated signaling by Gq. J Gen Physiol 123:663–683
Suh BC, Kim DI, Falkenburger BH, Hille B (2012) Membrane-localized β-subunits alter the PIP2 regulation of high-voltage activated Ca2+ channels. Proc Natl Acad Sci USA 109:3161–3166
Szentpetery Z, Varnai P, Balla T (2010) Acute manipulation of Golgi phosphoinositides to assess their importance in cellular trafficking and signaling. Proc Natl Acad Sci USA 107:8225–8230
Takeshima H, Komazaki S, Nishi M, Iino M, Kangawa K (2000) Junctophilins: a novel family of junctional membrane complex proteins. Mol Cell 6:11–22
Tanabe T, Beam KG, Adams BA, Niidome T, Numa S (1990) Regions of the skeletal muscle dihydropyridine receptor critical for excitation-contraction coupling. Nature 346:567–569
van Oort RJ, Garbino A, Wang W, Dixit SS, Landstrom AP, Gaur N, De Almeida AC, Skapura DG, Rudy Y, Burns AR et al (2011) Disrupted junctional membrane complexes and hyperactive ryanodine receptors after acute junctophilin knockdown in mice. Circulation 123:979–988
Vivas O, Kruse M, Hille B (2014) Nerve growth factor sensitizes adult sympathetic neurons to the proinflammatory peptide bradykinin. J Neurosci 34:11959–11971
Wang SQ, Song LS, Lakatta EG, Cheng H (2001) Ca2+ signalling between single L-type Ca2+ channels and ryanodine receptors in heart cells. Nature 410:592–596
Whorton MR, MacKinnon R (2011) Crystal structure of the mammalian GIRK2 K+ channel and gating regulation by G proteins, PIP2, and sodium. Cell 147:199–208
Wu L, Bauer CS, X-g Z, Xie C, Yang J (2002) Dual regulation of voltage-gated calcium channels by PtdIns(4,5)P2. Nature 419:947–952
Xu M, Zhou P, Xu SM, Liu Y, Feng X, Bai SH, Bai Y, Hao XM, Han Q, Zhang Y et al (2007) Intermolecular failure of L-type Ca2+ channel and ryanodine receptor signaling in hypertrophy. PLoS Biol 5:e21
Zaydman MA, Cui J (2014) PIP2 regulation of KCNQ channels: biophysical and molecular mechanisms for lipid modulation of voltage-dependent gating. Front Physiol 5:195
Zaydman MA, Silva JR, Delaloye K, Li Y, Liang H, Larsson HP, Shi J, Cui J (2013) Kv7.1 ion channels require a lipid to couple voltage sensing to pore opening. Proc Natl Acad Sci USA 110:13180–13185
Zhang H, He C, Yan X, Mirshahi T, Logothetis DE (1999) Activation of inwardly rectifying K+ channels by distinct PtdIns(4,5)P2 interactions. Nat Cell Biol 1:183–188
Zhang H, Craciun LC, Mirshahi T, Rohács T, Lopes CM, Jin T, Logothetis DE (2003) PIP2 activates KCNQ channels, and its hydrolysis underlies receptor-mediated inhibition of M currents. Neuron 37:963–975
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Special thanks to Dr. Rose Ellen Dixon for critical comments on the chapter.
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Dickson, E.J. (2017). Endoplasmic Reticulum-Plasma Membrane Contacts Regulate Cellular Excitability. In: Tagaya, M., Simmen, T. (eds) Organelle Contact Sites. Advances in Experimental Medicine and Biology, vol 997. Springer, Singapore. https://doi.org/10.1007/978-981-10-4567-7_7
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