Skip to main content
Log in

Organization of junctional sarcoplasmic reticulum proteins in skeletal muscle fibers

  • Review Article
  • Published:
Journal of Muscle Research and Cell Motility Aims and scope Submit manuscript

Abstract

The sarcoplasmic reticulum (SR) of striated muscles is specialized for releasing Ca2+ following sarcolemma depolarization in order to activate muscle contraction. To this end, the SR forms a network of longitudinal tubules and cisternae that surrounds the myofibrils and, at the same time, participates to the assembly of the triadic junctional membrane complexes formed by the close apposition of one t-tubule, originated from the sarcolemma, and two SR terminal cisternae. Advancements in understanding the molecular basis of the SR structural organization have identified an interaction between sAnk1, a transmembrane protein located on the longitudinal SR (l-SR) tubules, and obscurin, a myofibrillar protein. The direct interaction between these two proteins results in molecular contacts that have the overall effect to stabilize the l-SR tubules along myofibrils in skeletal muscle fibers. Less known is the structural organization of the sites in the SR that are specialized for Ca2+ release and are positioned at the junctional SR (j-SR), i.e. the region of the terminal cisternae that faces the t-tubule at triads. At the j-SR, several trans-membrane proteins like triadin, junctin, or intra-luminal SR proteins like calsequestrin, are assembled together with the ryanodine receptor, the SR Ca2+ release channel, into a macromolecular complex specialized in releasing Ca2+. At triads, the 12 nm-wide gap between the t-tubule and the j-SR allows the ryanodine receptor on the j-SR to be functionally coupled with the voltage-gated L-type calcium channel on the t-tubule in order to allow the transduction of the voltage-induced signal into Ca2+ release through the ryanodine receptor channels. The muscle-specific junctophilin isoforms (JPH1 and JPH2) are anchored to the j-SR with a trans-membrane segment present at the C-terminus and are capable to bind the sarcolemma with a series of phospholipid-binding motifs localized at the N-terminus. Accordingly, through this dual interaction, JPH1 and JPH2 are responsible for the assembly of the triadic junctional membrane complexes. Recent data indicate that junctophilins seem also to interact with other proteins of the excitation–contraction machinery, suggesting that they may contribute to hold excitation–contraction coupling proteins to the sites where the j-SR is being organized.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Ackermann MA, Ziman AP, Strong J, Zhang Y, Hartford AK, Ward CW, Randall WR, Kontrogianni-Konstantopoulos A, Bloch RJ (2011) Integrity of the network sarcoplasmic reticulum in skeletal muscle requires small ankyrin 1. J Cell Sci 124:3619–3630

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ainbinder A, Boncompagni S, Protasi F, Dirksen RT (2015) Role of mitofusin-2 in mitochondrial localization and calcium uptake in skeletal muscle. Cell Calcium 57:14–24

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Alleman RJ, Katunga LA, Nelson MAM, Brown DA, Anderson EJ (2014) The “Goldilocks Zone” from a redox perspective–adaptive versus deleterious responses to oxidative stress in striated muscle. Front Physiol 5:358–378

    Article  PubMed Central  PubMed  Google Scholar 

  • Amoasii L, Hnia K, Chicanne G, Brech A, Cowling BS, Müller MM, Schwab Y, Koebel P, Ferry A, Payrastre B, Laporte J (2013) Myotubularin and PtdIns3P remodel the sarcoplasmic reticulum in muscle in vivo. J Cell Sci 126:1806–1819

    Article  PubMed  CAS  Google Scholar 

  • Anderson AA, Treves S, Biral D, Betto R, Sandonà D, Ronjat M, Zorzato F (2003) The novel skeletal muscle sarcoplasmic reticulum JP45 Protein. J Biol Chem 278:39987–39992

    Article  PubMed  CAS  Google Scholar 

  • Armani A, Galli S, Giacomello E, Bagnato P, Barone V, Rossi D, Sorrentino V (2006) Molecular interactions with obscurin are involved in the localization of muscle-specific small ankyrin1 isoforms to subcompartments of the sarcoplasmic reticulum. Exp Cell Res 312:3546–3558

    Article  PubMed  CAS  Google Scholar 

  • Arvanitis DA, Vafiadaki E, Fan GC, Mitton BA, Gregory KN, Del Monte F, Kontrogianni-Konstantopoulos A, Sanoudou D, Kranias EG (2007) Histidine-rich Ca-binding protein interacts with sarcoplasmic reticulum Ca-ATPase. Am J Physiol Heart Circ Physiol 93:H1581–H1589

    Article  CAS  Google Scholar 

  • Asghari P, Scriven DR, Sanatani S, Gandhi SK, Campbell AI, Moore ED (2014) Non-uniform and variable arrangements of ryanodine receptors within mammalian ventricular couplons. Circ Res 115:252–262

    Article  PubMed  CAS  Google Scholar 

  • Bagnato P, Barone V, Giacomello E, Rossi D, Sorrentino V (2003) Binding of an ankyrin-1 isoform to obscurin suggests a molecular link between the sarcoplasmic reticulum and myofibrils in striated muscles. J Cell Biol 160:245–253

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Barone F, Genazzani AA, Conti A, Churchill GC, Palombi F, Ziparo E, Sorrentino V, Galione A, Filippini A (2002) A pivotal role for cADPR-mediated Ca2+ signaling: regulation of endothelin-induced contraction in peritubular smooth muscle cells. FASEB J 16:697–705

    Article  PubMed  CAS  Google Scholar 

  • Baumann O, Walz B (2001) Endoplasmic reticulum of animal cells and its organization into structural and functional domains. Int Rev Cytol 205:149–214

    Article  PubMed  CAS  Google Scholar 

  • Beard NA, Dulhunty AF (2015) C-terminal residues of skeletal muscle calsequestrin are essential for calcium binding and for skeletal ryanodine receptor inhibition. Skelet Muscle 5:6

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Beard NA, Sakowska MM, Dulhunty AF, Laver DR (2002) Calsequestrin is an inhibitor of skeletal muscle ryanodine receptor calcium release channels. Biophys J 82:310–320

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Beard NA, Casarotto MG, Wei L, Varsányi M, Laver DR, Dulhunty AF (2005) Regulation of ryanodine receptors by calsequestrin: effect of high luminal Ca2+ and phosphorylation. Biophys J 88:3444–3454

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Beavers DL, Wang W, Ather S, Voigt N, Garbino A, Dixit SS, Landstrom AP, Li N, Wang Q, Olivotto I, Dobrev D, Ackerman MJ, Wehrens XH (2013) Mutation E169 K in junctophilin-2 causes atrial fibrillation due to impaired RyR2 stabilization. J Am Coll Cardiol 62:2010–2019

    Article  PubMed  CAS  Google Scholar 

  • Bennett V, Baines AJ (2001) Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol Rev 81:1353–1392

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Birkenmeier CS, Sharp JJ, Gifford EJ, Deveau SA, Barker JE (1998) An alternative first exon in the distal end of the erythroid ankyrin gene leads to production of a small isoform containing an NH2-terminal membrane anchor. Genomics 50:79–88

    Article  PubMed  CAS  Google Scholar 

  • Boncompagni S, Rossi AE, Micaroni M, Beznoussenko GV, Polishchuk RS, Dirksen RT, Protasi F (2009) Mitochondria are linked to calcium stores in striated muscle by developmentally regulated tethering structures. Mol Biol Cell 20:1058–1067

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Boncompagni S, Thomas M, Lopez JR, Allen PD, Yuan Q, Kranias EG, Franzini-Armstrong C, Perez CF (2012) Triadin/Junctin double null mouse reveals a differential role for triadin and junctin in anchoring CASQ to the jSR and regulating Ca2+ homeostasis. PLoS One 7:e39962. doi:10.1371/journal.pone.0039962

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Brandt NR, Franklin G, Brunschwig J, Caswell AH (2001) The role of mitsugumin 29 in transverse tubules of rabbit skeletal muscle. Arch Biochem Biophys 385:406–409

    Article  PubMed  CAS  Google Scholar 

  • Brotto MA, Nagaraj RY, Brotto LS, Takeshima H, Ma J, Nosek TM (2004) Defective maintenance of intracellular Ca2+ homeostasis is linked to increased muscle fatigability in the MG29 null mice. Cell Res 14:373–378

    Article  PubMed  CAS  Google Scholar 

  • Bublitz M, Musgaard M, Poulsen H, Thøgersen L, Olesen C, Schiøtt B, Morth JP, Møller JV, Nissen P (2013) Ion pathways in the sarcoplasmic reticulum Ca2+-ATPase. J Biol Chem 288:10759–10765

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Buraei Z, Yang J (2010) The β subunit of voltage-gated Ca2+ channels. Physiol Rev 90:1461–1506

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Busby B, Oashi T, Willis CD, Ackermann MA, Kontrogianni-Konstantopoulos A, MacKerell AD Jr, Bloch RJ (2011) Electrostatic interactions mediate binding of obscurin to small ankyrin 1: biochemical and molecular modeling studies. J Mol Biol 408:321–334

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Catterall WA (2011) Voltage-gated calcium channels. Cold Spring Harb Perspect Biol 3:a003947. doi:10.1101/cshperspect.a003947

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Cusimano V, Pampinella F, Giacomello E, Sorrentino V (2009) Assembly and dynamics of proteins of the longitudinal and junctional sarcoplasmic reticulum in skeletal muscle cells. Proc Natl Acad Sci USA 106:4695–4700

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • De Brito OM, Scorrano L (2008) Mitofusin-2 tethers endoplasmic reticulum to mitochondria. Nature 456:605–610

    Article  PubMed  CAS  Google Scholar 

  • Delbono O, Xia JX, Treves S, Wang Z, Jimenez-Moreno R, Payne AM, Messi ML, Briguet A, Schaerer F, Nishi M, Takeshima H, Zorzato F (2007) Loss of skeletal muscle strength by ablation of the sarcoplasmic reticulum protein JP45. Proc Natl Acad Sci USA 104:20108–20113

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Delbono O, Messi ML, Wang Z, Treves S, Mosca B, Bergamelli L, Nishi M, Takeshima H, Shi H, Xue B, Zorzato F (2012) Endogenously determined restriction of food intake overcomes excitation-contraction uncoupling in JP45KO mice with aging. Exp Gerontol 47:304–316

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Divet A, Paesante S, Grasso C, Cavagna D, Tiveron C, Paolini C, Protasi F, Huchet-Cadiou C, Treves S, Zorzato F (2007) Increased Ca2+ storage capacity of the skeletal muscle sarcoplasmic reticulum of transgenic mice over-expressing membrane bound calcium binding protein junctate. J Cell Physiol 213:464–474

    Article  PubMed  CAS  Google Scholar 

  • Dorn GW II, Song M, Walsh K (2015) Functional implications of mitofusin 2-mediated mitochondrial-SR tethering. J Mol Cell Cardiol 78:123–128

    Article  PubMed  CAS  Google Scholar 

  • Eisner V, Csordas G, Hajnoczky G (2014) Interactions between sarco-endoplasmic reticulum and mitochondria in cardiac and skeletal muscle-pivotal roles in Ca2+ and reactive oxygen species signaling. J Cell Sci 126:2965–2978

    Article  CAS  Google Scholar 

  • Falcone S, Roman W, Hnia K, Gache V, Didier N, Laine J, Aurade F, Marty I, Nishino I, Charlet-Berguerand N, Romero NB, Marazzi G, Sassoon D, Laporte J, Gomes ER (2014) N–WASP is required for amphiphysin-2/BIN1-dependent nuclear positioning and triad organization in skeletal muscle and is involved in the pathophysiology of centronuclear myopathy. EMBO Mol Med 6:1455–1475

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Flucher BE (1992) Structural analysis of muscle development: transverse tubules, sarcoplasmic reticulum, and the triad. Dev Biol 154:245–260

    Article  PubMed  CAS  Google Scholar 

  • Flucher BE, Kasielke N, Grabner M (2000) The triad targeting signal of the skeletal muscle calcium channel is localized in the COOH terminus of the alpha (1S) subunit. J Cell Biol 151:467–478

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Franzini-Armstrong C (1991) Simultaneous maturation of transverse tubules and sarcoplasmic reticulum during muscle differentiation in the mouse. Dev Biol 146:353–363

    Article  PubMed  CAS  Google Scholar 

  • Galbiati F, Engelman JA, Volonte D, Zhang XL, Minetti C, Li M, Hou H Jr, Kneitz B, Edelman W, Lisanti MP (2001) Caveolin-3 null mice show a loss of caveolae, changes in the microdomain distribution of the dystrophin-glycoprotein complex, and t-tubule abnormalities. J Biol Chem 276:21425–21433

    Article  PubMed  CAS  Google Scholar 

  • Gallagher PG, Forget BG (1998) An alternate promoter directs expression of a truncated, muscle-specific isoform of the human ankyrin 1 gene. J Biol Chem 273:1339–1348

    Article  PubMed  CAS  Google Scholar 

  • Gallagher PG, Tse WT, Scarpa AL, Lux SE, Forget BG (1997) Structure and organization of the human ankyrin-1 gene. Basis for complexity of pre-mRNA processing. J Biol Chem 272:19220–19228

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Perez C, Schneider TG, Hajnoczky G, Csordas G (2011) Alignment of sarcoplasmic reticulum-mitochondrial junctions with mitochondrial contact points. Am J Physiol Heart Circ Physiol 301:H1907–H1915

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gautel M (2010) The sarcomeric cytoskeleton:who picks up the strain? Curr Opin Cell Biol 23:39–46

    Article  PubMed  CAS  Google Scholar 

  • Giacomello E, Sorrentino V (2009) Localization of ank1.5 in the sarcoplasmic reticulum precedes that of SERCA and RyR: relationship with the organization of obscurin in developing sarcomeres. Histochem Cell Biol 131:371–382

    Article  PubMed  CAS  Google Scholar 

  • Giacomello E, Quarta M, Paolini C, Squecco R, Fusco P, Toniolo L, Blaauw B, Formoso L, Rossi D, Birkenmeier C, Peters LL, Francini F, Protasi F, Reggiani C, Sorrentino V (2015) Deletion of small ankyrin 1 (sAnk1) isoforms results in structural and functional alterations in aging skeletal muscle fibers. Am J Physiol Cell Physiol 308:C123–C138

    Article  PubMed  CAS  Google Scholar 

  • Gokhin DS, Fowler VM (2011) Cytoplasmic gamma-actin and tropomodulin isoforms link to the sarcoplasmic reticulum in skeletal muscle fibers. J Cell Biol 194:105–120

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Golini L, Chouabe C, Berthier C, Cusimano V, Fornaro M, Bonvallet R, Formoso L, Giacomello E, Jacquemond V, Sorrentino V (2011) Junctophilin 1 and 2 proteins interact with the L-type Ca2+ channel dihydropyridine receptors (DHPRs) in skeletal muscle. J Biol Chem 286:43717–43725

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Goonasekera SA, Beard NA, Groom L, Kimura T, Lyfenko AD, Rosenfeld A, Marty I, Dulhunty AF, Dirksen RT (2007) Triadin binding to the C-terminal luminal loop of the ryanodine receptor is important for skeletal muscle excitation-contraction coupling. J Gen Physiol 130:365–378

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gouadon E, Schuhmeier RP, Ursu D, Anderson AA, Treves S, Zorzato F, Lehmann-Horn F, Melzer W (2006) A possible role of the junctional face protein JP-45 in modulating Ca2+ release in skeletal muscle. J Physiol 572:269–280

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gregory KN, Ginsburg KS, Bodi I, Hahn H, Marreez YM, Song Q, Padmanabhan PA, Mitton BA, Waggoner JR, Del Monte F, Park WJ, Dorn GW 2nd, Bers DM, Kranias EG (2006) Histidine-rich Ca binding protein: a regulator of sarcoplasmic reticulum calcium sequestration and cardiac function. J Mol Cell Cardiol 40:653–665

    Article  PubMed  CAS  Google Scholar 

  • Groh S, Marty I, Ottolia M, Prestipino G, Chapel A, Villaz M, Ronjat M (1999) Functional interaction of the cytoplasmic domain of triadin with the skeletal ryanodine receptor. J Biol Chem 274:12278–12283

    Article  PubMed  CAS  Google Scholar 

  • Guo W, Campbell KP (1995) Association of triadin with the ryanodine receptor and calsequestrin in the lumen of the sarcoplasmic reticulum. J Biol Chem 270:9027–9030

    Article  PubMed  CAS  Google Scholar 

  • Gyorke I, Hester N, Jones LR, Gyorke S (2004) The role of calsequestrin, triadin, and junctin in conferring cardiac ryanodine receptor responsiveness to luminal calcium. Biophys J 86:2121–2128

    Article  PubMed Central  PubMed  Google Scholar 

  • Han P, Cai W, Wang Y, Lam CK, Arvanitis DA, Singh VP, Chen S, Zhang H, Zhang R, Chen H, Kranias EG (2011) Catecholaminergic-induced arrhythmias in failing cardiomyocytes associated with human HRCS96A variant overexpression. Am J Physiol Heart Circ Physiol 301:H1588–H1595

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hirata Y, Brotto M, Weisleder N, Chu Y, Lin P, Zhao X, Thornton A, Komazaki S, Takeshima H, Ma J, Pan Z (2006) Uncoupling store-operated Ca2+ entry and altered Ca2+ release from sarcoplasmic reticulum through silencing of Junctophilin genes. Biophys J 90:4418–4427

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Horstick EJ, Linsley JW, Dowling JJ, Hauser MA, McDonald KK, Ashley-Koch A, Saint-Amant L, Satish A, Cui WW, Zhoou W, Sprague SM, Stamm DS, Powell CM, Speer MC, Franzini-Armstrong C, Hirata H, Kuwada JY (2013) Stac3 is a component of the excitation–contraction coupling machinery and mutated in Native American myopathy. Nat Commun 4:1952

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hu H, Wang Z, Wei R, Fan G, Wang Q, Zhang K, Yina C (2015) The molecular architecture of dihydropyrindine receptor/L-type Ca2+ channel complex. Sci Rep 5:8370

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jayasinghe ID, Munro M, Baddeley D, Launikonis BS, Soeller C (2014) Observation of the molecular organization of calcium release sites in fast- and slow-twitch skeletal muscle with nanoscale imaging. J R Soc Interface. doi:10.1098/rsif.2014.0570

    PubMed Central  PubMed  Google Scholar 

  • Ji G, Feldman ME, Greene KS, Sorrentino V, Xin HB, Kotlikoff MI (2004) RYR2 proteins contribute to the formation of Ca(2+) sparks in smooth muscle. J Gen Physiol 123:377–386

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jiao Q, Takeshima H, Ishikawa Y, Minamisawa S (2012) Sarcalumenin plays a critical role in age-related cardiac dysfunction due to decreases in SERCA2a expression and activity. Cell Calcium 1:31–39

    Article  CAS  Google Scholar 

  • Kaisto T, Metsikkö K (2003) Distribution of the endoplasmic reticulum and its relationship with the sarcoplasmic reticulum in skeletal myofibers. Exp Cell Res 289:47–57

    Article  PubMed  CAS  Google Scholar 

  • Kee AJ, Schevzov G, Nair-Shalliker V, Robinson CS, Vrhovski B, Ghoddusi M, Qiu MR, Lin JJ, Weinberger R, Gunning PW, Hardeman EC (2004) Sorting of a nonmuscle tropomyosin to a novel cytoskeletal compartment in skeletal muscle results in muscular dystrophy. J Cell Biol 166:685–696

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kiselyov KI, Shin DM, Wang Y, Pessah IN, Allen PD, Muallem S (2000) Gating of store-operated channels by conformational coupling to ryanodine receptors. Mol Cell 6:421–431

    Article  PubMed  CAS  Google Scholar 

  • Knudson CM, Stang KK, Moomaw CR, Slaughter CA, Campbell KP (1993) Primary structure and topological analysis of a skeletal muscle-specific junctional sarcoplasmic reticulum glycoprotein (triadin). J Biol Chem 268:12646–12654

    PubMed  CAS  Google Scholar 

  • Kobayashi YM, Alseikhan BA, Jones LR (2000) Localization and characterization of the calsequestrin-binding domain of triadin 1. J Biol Chem 275:17639–17646

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kontrogianni-Konstantopoulos A, Bloch RJ (2003) The hydrophilic domain of small ankyrin-1 interacts with the two N-terminal immunoglobulin domains of titin. J Biol Chem 278:3985–3991

    Article  PubMed  CAS  Google Scholar 

  • Kontrogianni-Konstantopoulos A, Catino DH, Strong JC, Sutter S, Borisov AB, Pumplin DW, Russell MW, Bloch RJ (2006) Obscurin modulates the assembly and organization of sarcomeres and the sarcoplasmic reticulum. FASEB J 20:2102–2111

    Article  PubMed  CAS  Google Scholar 

  • Landstrom AP, Weisleder N, Batalden KB, Bos JM, Tester DJ, Ommen SR, Wehrens XHT, Claycomb WC, Ko JK, Hwang M, Pan Z, Ma J, Ackerman MJ (2007) Mutations in JPH2-encoded junctophilin-2 associated with hypertrophic cardiomyopathy in humans. J Molec Cell Cardiol 42:1026–1035

    Article  CAS  Google Scholar 

  • Landstrom AP, Kellen CA, Dixit SS, van Oort RJ, Garbino A, Weisleder N, Ma J, Wehrens XHT, Ackerman MJ (2011) Junctophilin-2 expression silencing causes cardiocyte hypertrophy and abnormal intracellular calcium-handling. Circ Heart Fail 4:214–223

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lange S, Ouyang K, Meyer G, Cui L, Cheng H, Lieber RL, Chen J (2009) Obscurin determines the architecture of the longitudinal sarcoplasmic reticulum. J Cell Sci 122:2640–2650

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lange S, Perera S, Teh P, Chen J (2012) Obscurin and KCTD6 regulate cullin-dependent small ankyrin-1 (sAnk1.5) protein turnover. Mol Biol Cell 23:2490–2504

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Leberer E, Timms BG, Campbell KP, MacLennan DH (1990) Purification, calcium binding properties, and ultrastructural localization of the 53,000- and 160,000 (sarcalumenin)-dalton glycoproteins of the sarcoplasmic reticulum. J Biol Chem 265:10118–10124

    PubMed  CAS  Google Scholar 

  • Lee HG, Kang H, Kim DH, Park WJ (2001) Interaction of HRC (Histidine-rich Ca2+ binding protein) and triadin in the lumen of sarcoplasmic reticulum. J Biol Chem 276:39533–39538

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Lee JM, Rho SH, Shin DW, Cho C, Park WJ, Eom SH (2004) Negatively charged amino acids within the intraluminal loop of ryanodine receptor are involved in the interaction with triadin. J Biol Chem 279:6994–7000

    Article  PubMed  CAS  Google Scholar 

  • Lee EH, Cherednichenko G, Pessah IN, Allen PD (2006) Functional coupling between TRPC3 and RyR1 regulates the expression of key triadic proteins. J Biol Chem 281:10042–10048

    Article  PubMed  CAS  Google Scholar 

  • Lee KW, Maeng JS, Choi JY, Lee YR, Hwang CY, Park SS, Park HK, Chung BH, Lee SG, Kim YS, Jeon H, Eom SH, Kang C, do Kim H, Kwon KS (2012) Role of Junctin protein interactions in cellular dynamics of calsequestrin polymer upon calcium perturbation. J Biol Chem 287:1679–8167

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Leenhardt A, Denjoy I, Guicheney P (2012) Catecholaminergic polymorphic ventricular tachycardia. Circ Arrhythm Electrophysiol 5:1044–1052

    Article  PubMed  Google Scholar 

  • Li H, Ding X, Lopez JR, Takeshima H, Ma J, Allen PD, Eltit JM (2010) Impaired orai1-mediated resting Ca2+ entry reduces the cytosolic [Ca2+] and sarcoplasmic reticulum Ca2+ loading in quiescent junctophilin 1 knock-out myotubes. J Biol Chem 285:39171–39179

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Li L, Mirza S, Richardson SJ, Gallant EM, Thekkedam C, Pace SM, Zorzato F, Liu D, Beard NA, Dulhunty AF (2015) A new cytoplasmic interaction between junctin and ryanodine receptor Ca2+ release channels. J Cell Sci 128:951–963

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Logan CV, Szabadkai G, Sharpe JA, Parry DA, Torelli S, Childs AM, Kriek M, Phadke R, Johnson CA, Roberts NY, Bonthron DT, Pysden KA, Whyte T, Munteanu I, Foley AR, Wheway G, Szymanska K, Natarajan S, Abdelhamed ZA, Morgan JE, Roper H, Santen GW, Niks EH, van der Pol WL, Lindhout D, Raffaello A, De Stefani D, den Dunnen JT, Sun Y, Ginjaar I, Sewry CA, Hurles M, Rizzuto R, UK10 K Consortium, Duchen MR, Muntoni F, Sheridan E (2014) Loss-of-function mutations in MICU1 cause a brain and muscle disorder linked to primary alterations in mitochondrial calcium signaling. Nat Genet. 46:188–193

    Article  PubMed  CAS  Google Scholar 

  • Löhn M, Jessner W, Fürstenau M, Wellner M, Sorrentino V, Haller H, Luft FC, Gollasch M (2001) Regulation of calcium sparks and spontaneous transient outward currents by RyR3 in arterial vascular smooth muscle cells. Circ Res 89:1051–1057

    Article  PubMed  Google Scholar 

  • Mammucari C, Gherardi G, Zamparo I, Raffaello A, Boncompagni S, Chemello F, Cagnin S, Braga A, Zanin S, Pallafacchina G, Zentilin L, Sandri M, De Stefani D, Protasi F, Lanfranchi G, Rizzuto R (2015) The mitochondrial calcium uniporter controls skeletal muscle trophism in vivo. Cell Rep. 10:1269–1279

    Article  PubMed  CAS  Google Scholar 

  • Marty I (2014) Triadin regulation of the ryanodine receptor complex. J Physiol 1:1–6

    Google Scholar 

  • Marty I, Fauré J, Fourest-Lieuvin A, Vassilopoulos S, Oddoux S, Brocard J (2009) Triadin: what possible function 20 years later? J Physiol 587:3117–3121

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Matsushita Y, Furukawa T, Kasanuki H, Nishibatake M, Kurihara Y, Ikeda A, Kamatani N, Takeshima H, Matsuoka R (2007) Mutation of junctophilin type 2 associated with hypertrophic cardiomyopathy. J Hum Genet 52:543–548

    Article  PubMed  CAS  Google Scholar 

  • Meur G, Parker AK, Gergely FV, Taylor CW (2007) Targeting and retention of type 1 ryanodine receptors to the endoplasmic reticulum. J Biol Chem 282:23096–23103

    Article  PubMed  CAS  Google Scholar 

  • Min CK, Yeom DR, Lee K, Kwon H, Kang N, Kim Y, Park Z, Jeon H, Kim DH (2012) Coupling of ryanodine receptor 2 and voltage-dependent anion channel 2 is essential for Ca2+ transfer from the sarcoplasmic reticulum to the mitochondria in the heart. Biochem J 447:371–379

    Article  PubMed  CAS  Google Scholar 

  • Minamisawa S, Oshikawaa J, Takeshima H, Hoshijima M, Wang Y, Chien KR, Ishikawaa 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

    Article  PubMed  CAS  Google Scholar 

  • Murphy RM, Larkins NT, Mollica JP, Beard NA, Lamb GD (2009) Calsequestrin content and SERCA determine normal and maximal Ca2+ storage levels in sarcoplasmic reticulum of fast- and slow-twitch fibres of rat. J Physiol 587:443–460

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Murphy RM, Dutka TL, Horvath D, Bell JR, Delbridge LM, Lamb GD (2013) Ca2+-dependent proteolysis of junctophilin-1 and junctophilin-2 in skeletal and cardiac muscle. J Physiol 591:719–729

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Naon S, Scorrano L (2014) At the right distance: ER-mitochondria juxtaposition in cell life and death. Biochem Biophys Acta 1843:2184–2194

    Article  PubMed  CAS  Google Scholar 

  • Nelson BR, Wu F, Liu Y, Anderson DM, McAnally J, Lin W, Cannon SC, Bassel-Duby R, Olson EN (2013) Skeletal muscle-specific T-tubule protein STAC3 mediates voltage-induced Ca2+ release and contractility. PNAS 29:11881–11886

    Article  Google Scholar 

  • Nishi M, Sakagami H, Komazaki S, Kondo H, Takeshima H (2003) Coexpression of junctophilin type 3 and type 4 in brain. Brain Res Mol Brain Res 118:102–110

    Article  PubMed  CAS  Google Scholar 

  • Obermair GJ, Kugler G, Baumgartner S, Tuluc P, Grabner M, Flucher BE (2005) The Ca2+ channel α2δ1 subunit determines Ca2+ current kinetics in skeletal muscle but not targeting of α1s or excitation-contraction coupling. J Biol Chem 280:2229–2237

    Article  PubMed  CAS  Google Scholar 

  • Ohkura M, Furukawa K, Fujimori H, Kuruma A, Kawano S, Hiraoka M, Kuniyasu A, Nakayama H, Ohizumi Y (1998) Dual regulation of the skeletal muscle ryanodine receptor by triadin and calsequestrin. Biochemistry 37:12987–12993

    Article  PubMed  CAS  Google Scholar 

  • Park CS, Chen S, Lee H, Cha H, Hong S, Han P, Ginsburg KS, Jin S, Park I, Singh VP, Wang H, Franzini-Armstrong C, Park WJ, Bers DM, Kranias EG, Cho C, Kim DH (2013) Targeted ablation of the histidine-rich Ca2+ binding protein (HRC) gene is associated with abnormal SR Ca2+ cycling and severe pathology under pressure-overload stress. Basic Res Cardiol 108:344–361

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Perni S, Close M, Franzini-Armstrong C (2013) Novel details of calsequestrin gel conformation in situ. J Biol Chem 288:31358–31362

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Phimister AJ, Lango J, Lee EH, Ernst-Russell MA, Takeshima H, Ma J, Allen PD, Pessah IN (2007) Conformation-dependent stability of junctophilin 1 (JP1) and ryanodine receptor type 1 (RyR1) Channel complex is mediated by their hyper-reactive thiols. J Biol Chem 282:8667–8677

    Article  PubMed  CAS  Google Scholar 

  • Picas L, Viaud J, Schauer K, Vanni S, Hnia K, Fraisier V, Roux A, Bassereau P, Gaits-Iacovoni F, Payrastre B, Laporte J, Manneville J, Goud B (2014) BIN1/M-amphiphysin2 induces clustering of phosphoinositides to recruit its downstream partner dynamin. Nat Commun 5:5647–5659

    Article  PubMed  CAS  Google Scholar 

  • Poister A, Perni S, Bichraoui H, Beam KG (2015) Stac adaptor proteins regulate trafficking and function of muscle and neuronal L-type Ca2+ channels. PNAS 13:602–606

    Article  CAS  Google Scholar 

  • Porter NC, Resneck WG, O’Neill A, Van Rossum DB, Stone MR, Bloch RJ (2005) Association of small ankyrin 1 with the sarcoplasmic reticulum. Mol Membr Biol 22:421–432

    Article  PubMed  CAS  Google Scholar 

  • Protasi F, Paolini C, Dainese M (2009) Calsequestrin-1: a new candidate gene for malignant hyperthermia and exertional/environmental heat stroke. J Physiol 587:3095–3100

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Randazzo D, Giacomello E, Lorenzini S, Rossi D, Pierantozzi E, Blaauw B, Reggiani C, Lange S, Peter AK, Chen J, Sorrentino V (2013) Obscurin is required for ankyrinB-dependent dystrophin localization and sarcolemma integrity. J Cell Biol 200:523–536

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rebbeck RT, Karunasekara Y, Board PG, Beard AN, Casarotto MG, Dulhunty AF (2014) Skeletal muscle excitation–contraction coupling: who are the dancing partners? Int J Biochem Cell Biol 48:28–38

    Article  PubMed  CAS  Google Scholar 

  • Rios E, Pizarro G (1991) Voltage sensor of excitation-contraction coupling in skeletal muscle. Physiol Rev 71:849–908

    PubMed  CAS  Google Scholar 

  • Rizzuto R, Marchi S, Bonora M, Aguiari P, Bononi A, De Stefani D, Giorgi C, Leo S, Rimessi A, Siviero R, Zecchini E, Pinton P (2009) Ca2+ transfer from the ER to mitochondria: when, how and why. Biochim Biophys Acta 1787:1342–1351

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rossi AE, Dirksen RT (2006) Sarcoplasmic reticulum: the dynamic calcium governor of muscle. Muscle Nerve 33:715–731

    Article  PubMed  CAS  Google Scholar 

  • Rossi D, Simeoni I, Micheli M, Bootman M, Lipp P, Allen PD, Sorrentino V (2002) RyR1 and RyR3 isoforms provide distinct intracellular Ca2+ signals in HEK 293 cells. J Cell Sci 115:2497–2504

    PubMed  CAS  Google Scholar 

  • Rossi D, Barone V, Giacomello E, Cusimano V, Sorrentino V (2008) The sarcoplasmic reticulum: an organized patchwork of specialized domains. Traffic 9:1044–1049

    Article  PubMed  CAS  Google Scholar 

  • Rossi D, Bencini C, Maritati M, Benini F, Lorenzini S, Pierantozzi E, Scarcella AM, Paolini C, Protasi F, Sorrentino V (2014a) Distinct regions of triadin are required for targeting and retention at the junctional domain of the sarcoplasmic reticulum. Biochem J 458:407–417

    Article  PubMed  CAS  Google Scholar 

  • Rossi D, Vezzani B, Galli L, Paolini C, Toniolo L, Pierantozzi E, Spinozzi S, Barone V, Pegoraro E, Bello L, Cenacchi G, Vattemi G, Tomelleri G, Ricci G, Siciliano G, Protasi F, Reggiani C, Sorrentino V (2014b) A mutation in the CASQ1 gene causes a vacuolar myopathy with accumulation of sarcoplasmic reticulum protein aggregates. Hum Mutat 35:1163–1170

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Roux-Buisson N, Cacheux M, Fourest-Lieuvin A, Fauconnier J, Brocard J, Denjoy I, Durand P et al (2012) Absence of triadin, a protein of the calcium release complex, is responsible for cardiac arrhythmia with sudden death in human. Hum Molec Genet 21:2759–2767

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Royer B, Hnia K, Gavriilidis C, Tronchère H, Tosch V, Laporte J (2013) The myotubularin-amphiphysin 2 complex in membrane tubulation and centronuclear myopathies. EMBO Rep 14:907–915

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rudolf R, Mongillo M, Magalhaes PJ, Pozzan T (2004) In vivo monitoring of Ca2+ uptake into mitochondria of mouse skeletal muscle during contraction. J Cell Biol 166:527–536

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sacchetto R, Damiani E, Turcato F, Nori A, Marghret A (2001) Ca2+ -dependent interaction of triadin with histidine-rich Ca2+ binding protein carboxyl-terminal region. Biochem Biophys Res Commun 289:1125–1134

    Article  PubMed  CAS  Google Scholar 

  • Salanova M, Priori G, Barone V, Intravaia E, Flucher B, Ciruela F, McIlhinney RA, Parys JB, Mikoshiba K, Sorrentino V (2002) Homer proteins and InsP(3) receptors co-localise in the longitudinal sarcoplasmic reticulum of skeletal muscle fibres. Cell Calcium 32:193–200

    Article  PubMed  CAS  Google Scholar 

  • Shen X, Franzini-Armstrong C, Lopez JR, Jones LR, Kobayashi YM, Wang Y, Kerrick WGL, Caswell AH, Potter JD, Miller T, Allen PD, Perez CF (2007) Triadins modulate intracellular Ca2+ homeostasis but are not essential for excitation-contraction coupling in skeletal muscle. J Biol Chem 282:37864–37874

    Article  PubMed  CAS  Google Scholar 

  • Shimura M, Minamisawa S, Takeshima H, Jiao Q, Bai Y, Umemura S, Ishikawa Y (2008) Sarcalumenin alleviates stress-induced cardiac dysfunction by improving Ca2+ handling of the sarcoplasmic reticulum. Cardiovasc Res 77:362–370

    Article  PubMed  CAS  Google Scholar 

  • Shin DW, Ma J, Kim DH (2000) The asp-rich region at the carboxyl-terminus of calsequestrin binds to Ca(2+) and interacts with triadin. FEBS Lett 486:178–182

    Article  PubMed  CAS  Google Scholar 

  • Shin DW, Pan Z, Kim EK, Lee JM, Bhat MB, Parness J, Kim DH, Ma J (2003) A retrograde signal from calsequestrin for the regulation of store-operated Ca2+ entry in skeletal muscle. J Biol Chem 278:3286–3292

    Article  PubMed  CAS  Google Scholar 

  • Shirokova N, Shirokov R, Rossi D, González A, Kirsch WG, García J, Sorrentino V, Ríos E (1999) Spatially segregated control of Ca2+ release in developing skeletal muscle of mice. J Physiol 521:483–495

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sorrentino V, Barone V, Rossi D (2000) Intracellular Ca(2+) release channels in evolution. Curr Opin Genet Dev 10:662–667

    Article  PubMed  CAS  Google Scholar 

  • Takekura H, Sun X, Franzini-Armstrong C (1994) Development of the excitation-contraction coupling apparatus in skeletal muscle: peripheral and internal calcium release units are formed sequentially. J Muscle Res Cell Motil 15:102–118

    Article  PubMed  CAS  Google Scholar 

  • Takekura H, Flucher BE, Franzini-Armstrong C (2001) Sequential docking, molecular differentiation, and positioning of T-Tubule/SR junctions in developing mouse skeletal muscle. Dev Biol 239:204–214

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Takeshima H, Hoshijima M, Song LS (2015) Ca2+ microdomains organized by junctophilins. Cell Calcium. doi:10.1016/j.ceca.2015.01.007

    PubMed  Google Scholar 

  • Toussaint A, Cowling BS, Hnia K, Mohr M, Oldfors A, Schwab Y, Yis U, Maisonobe T, Stojkovic T, Wallgren-Pettersson C, Laugel V, Echaniz-Laguna A, Mandel JL, Nishino I, Laporte J (2011) Defects in amphiphysin 2 (BIN1) and triads in several forms of centronuclear myopathies. Acta Neuropathol 121:253–266

    Article  PubMed  Google Scholar 

  • Treves S, Feriotto G, Moccagatta L, Gambari R, Zorzato F (2000) Molecular cloning, expression, functional characterization, chromo- somal localization, and gene structure of junctate, a novel integral calcium binding protein of sarco(endo)plasmic reticulum membrane. J Biol Chem 275:39555–39568

    Article  PubMed  CAS  Google Scholar 

  • Treves S, Vukcevic M, Maj M, Thurnheer R, Mosca B, Zorzato F (2009) Minor sarcoplasmic reticulum membrane components that modulate excitation–contraction coupling in striated muscles. J Physiol 587:3071–3079

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ursu D, Schuhmeier RP, Freichel M, Flockerzi V, Melzer W (1994) Altered inactivation of Ca2+ current and Ca2+ release in mouse muscle fibers deficient in the DHP receptor gamma1 subunit. J Gen Physiol 124:605–618

    Article  CAS  Google Scholar 

  • van Oort RJ, Garbino A, Wang W, Dixit SS, Landstrom AP, Gaur N, De Almeida AC, Skapura DG, Rudy Y, Burns AR, Ackerman MJ, Wehrens XHT (2011) Receptors after acute Junctophilin knockdown in mice disrupted junctional membrane complexes and hyperactive ryanodine. Circulation 123:979–988

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Van B, Nishi M, Komazaki S, Ichimura A, Kakizawa S, Nakanaga K, Aoki J, Park K, Ma J, Ueyama T, Ogata T, Maruyama N, Takeshima H (2015) Mitsugumin 56 (hedgehog acyltransferase-like) is a sarcoplasmic reticulum-resident protein essential for postnatal muscle maturation. FEBS Lett 589:1095–1104

    Article  PubMed  CAS  Google Scholar 

  • Vance JE (2014) MAM (mitochondria-associated membranes) in mammalian cells: lipids and beyond. Biochim Biophys Acta 1841:595–609

    Article  PubMed  CAS  Google Scholar 

  • Vlahovich N, Kee AJ, Van der Poel C, Kettle E, Hernandez-Deviez D, Lucas C, Lynch GS, Parton RG, Gunning PW, Hardeman EC (2009) Cytoskeletal Tropomyosin Tm5NM1 is required for normal excitation-contraction coupling in skeletal muscle. Mol Biol Cell 30:400–409

    Article  Google Scholar 

  • Wang S, Trumble WR, Liao H, Wesson CR, Dunker AK, Kang CH (1998) Crystal structure of calsequestrin from rabbit skeletal muscle sarcoplasmic reticulum. Nat Struct Biol 5:476–483

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Li X, Duan H, Fulton TR, Eu JP, Meissner G (2009) Altered stored calcium release in skeletal myotubes deficient of triadin and junctin. Cell Calcium 45:29–37

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wang L, Zhang L, Li S, Zheng Y, Yan X, Chen M, Wang H, Putney JW, Luo D (2015) Retrograde regulation of STIM1-Orai1 interaction and store-operated Ca2+ entry by calsequestrin. Sci Rep 5:11349

    Article  PubMed Central  PubMed  Google Scholar 

  • Wei L, Varsányi M, Dulhunty AF, Beard NA (2006) The conformation of calsequestrin determines its ability to regulate skeletal ryanodine receptors. Biophys J 91:1288–1301

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wei AL, Gallant EM, Dulhunty AF, Beard NA (2009) Junctin and triadin each activate skeletal ryanodine receptors but junctin alone mediates functional interactions with calsequestrin. Int J Biochem Cell Biol 41:2214–2224

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Weisleder N, Takeshima H, Ma J (2008) Immuno-proteomic approach to excitation–contraction coupling in skeletal and cardiac muscle: molecular insights revealed by the mitsugumins. Cell Calcium 43:1–8

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Whiteley G, Collins RF, Kitmitto A (2012) Characterization of the molecular architecture of human caveolin-3 and interaction with the skeletal muscle ryanodine receptor. J Biol Chem 287:40302–40316

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wium E, Dulhunty A, Beard NA (2012) A skeletal muscle ryanodine receptor interaction domain in triadin. PLoS One 7:e43817. doi:10.1371/journal.pone.0043817

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Woo JS, Hwang J, Ko J, Kim D, Ma J, Lee E (2009) Glutamate at position 227 of junctophilin-2 is involved in binding to TRPC3. Mol Cell Biochem 328:25–32

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Woo JS, Cho CH, Lee KJ, do Kim H, Ma J, Lee EH (2012) Hypertrophy in skeletal myotubes induced by junctophilin-2 mutant, Y141H, involves an increase in store-operated Ca2+ entry via orai1. J Biol Chem 287:14336–14348

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Woo JS, Hwang JH, Huang M, Ahn MK, Cho CH, Ma J, Lee EH (2015) Interaction between mitsugumin 29 and TRPC3 participates in regulating Ca2+ transients in skeletal muscle. Biochem Biophys Res Commun. doi:10.1016/j.bbrc.2015.06.096

    Google Scholar 

  • Yan Z, Bai XC, Yan C, Wu J, Li Z, Xie T, Peng W, Yin CC, Li X, Scheres SH, Shi Y, Yan N (2015) Structure of the rabbit ryanodine receptor RyR1 at near-atomic resolution. Nature 517:50–55

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yasuda T, Delbono O, Wang ZM, Messi ML, Girard T, Urwyler A, Treves S, Zorzato F (2013) JP-45/JSRP1 variants affect skeletal muscle excitation-contraction coupling by decreasing the sensitivity of the dihydropyridine receptor. Hum Mutat 34:184–190

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Young P, Ehler E, Gautel M (2001) Obscurin, a giant sarcomeric Rho guanine nucleotide exchange factor protein involved in sarcomere assembly. J Cell Biol 154:123–136

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zalk R, Lehnart SE, Marks AR (2007) Modulation of the ryanodine receptor and intracellular calcium. Annu Rev Biochem 76:367–385

    Article  PubMed  CAS  Google Scholar 

  • Zalk R, Clarke OB, des Georges A, Grassucci RA, Reiken S, Mancia F, Hendrickson WA, Hendrickson J, Marks AR (2015) Structure of a mammalian ryanodine receptor. Nature 517:44–49

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhang L, Kelley J, Schmeisser G, Kobayashi YM, Jones LR (1997) Complex formation between junctin, triadin, calsequestrin, and the ryanodine receptor. Proteins of the cardiac junctional sarcoplasmic reticulum membrane. J Biol Chem 272:23389–23397

    Article  PubMed  CAS  Google Scholar 

  • Zhang C, Chen B, Guo A, Zhu Y, Miller JD, Gao S, Yuan C, Kutschke W, Zimmerman K, Weiss RM, Wehrens XH, Hong J, Johnson FL, Santana LF, Anderson ME, Song LS (2014) Microtubule-mediated defects in junctophilin-2 trafficking contribute to myocyte transverse-tubule remodeling and Ca2+ handling dysfunction in heart failure. Circulation 129:1742–1750

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhou D, Birkenmeier CS, Williams MW, Sharp JJ, Barker JE, Bloch RJ (1997) Small, membrane-bound, alternatively spliced forms of ankyrin 1 associated with the sarcoplasmic reticulum of mammalian skeletal muscle. J Cell Biol 136:621–631

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ziman AP, Gómez-Viquez NL, Bloch RJ, Lederer WJ (2010) Excitation-contraction coupling changes during postnatal cardiac development. J Mol Cell Cardiol 48:379–386

    Article  PubMed Central  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vincenzo Sorrentino.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Barone, V., Randazzo, D., Del Re, V. et al. Organization of junctional sarcoplasmic reticulum proteins in skeletal muscle fibers. J Muscle Res Cell Motil 36, 501–515 (2015). https://doi.org/10.1007/s10974-015-9421-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10974-015-9421-5

Keywords

Navigation