{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T19:34:02Z","timestamp":1790278442282,"version":"4.1.0"},"reference-count":72,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,2,26]],"date-time":"2021-02-26T00:00:00Z","timestamp":1614297600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell Dev. Biol."],"abstract":"<jats:p>Tubular Aggregate Myopathy (TAM) is a hereditary ultra-rare muscle disorder characterized by muscle weakness and cramps or myasthenic features. Biopsies from TAM patients show the presence of tubular aggregates originated from sarcoplasmic reticulum due to altered Ca<jats:sup>2+<\/jats:sup> homeostasis. TAM is caused by gain-of-function mutations in STIM1 or ORAI1, proteins responsible for Store-Operated-Calcium-Entry (SOCE), a pivotal mechanism in Ca<jats:sup>2+<\/jats:sup> signaling. So far there is no cure for TAM and the mechanisms through which <jats:italic>STIM1<\/jats:italic> or <jats:italic>ORAI1<\/jats:italic> gene mutation lead to muscle dysfunction remain to be clarified. It has been established that post-natal myogenesis critically relies on Ca<jats:sup>2+<\/jats:sup> influx through SOCE. To explore how Ca<jats:sup>2+<\/jats:sup> homeostasis dysregulation associated with TAM impacts on muscle differentiation cascade, we here performed a functional characterization of myoblasts and myotubes deriving from patients carrying STIM1 L96V mutation by using fura-2 cytofluorimetry, high content imaging and real-time PCR. We demonstrated a higher resting Ca<jats:sup>2+<\/jats:sup> concentration and an increased SOCE in STIM1 mutant compared with control, together with a compensatory down-regulation of genes involved in Ca<jats:sup>2+<\/jats:sup> handling (<jats:italic>RyR1, Atp2a1, Trpc1)<\/jats:italic>. Differentiating STIM1 L96V myoblasts persisted in a mononuclear state and the fewer multinucleated myotubes had distinct morphology and geometry of mitochondrial network compared to controls, indicating a defect in the late differentiation phase. The alteration in myogenic pathway was confirmed by gene expression analysis regarding early (<jats:italic>Myf5, Mef2D<\/jats:italic>) and late (<jats:italic>DMD, Tnnt3<\/jats:italic>) differentiation markers together with mitochondrial markers (<jats:italic>IDH3A, OGDH)<\/jats:italic>. We provided evidences of mechanisms responsible for a defective myogenesis associated to TAM mutant and validated a reliable cellular model usefull for TAM preclinical studies.<\/jats:p>","DOI":"10.3389\/fcell.2021.635063","type":"journal-article","created":{"date-parts":[[2021,2,26]],"date-time":"2021-02-26T05:26:42Z","timestamp":1614317202000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":17,"title":["Gain-of-Function STIM1 L96V Mutation Causes Myogenesis Alteration in Muscle Cells From a Patient Affected by Tubular Aggregate Myopathy"],"prefix":"10.3389","volume":"9","author":[{"given":"Elena","family":"Conte","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alessandra","family":"Pannunzio","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paola","family":"Imbrici","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giulia Maria","family":"Camerino","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lorenzo","family":"Maggi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marina","family":"Mora","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sara","family":"Gibertini","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ornella","family":"Cappellari","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Annamaria","family":"De Luca","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mauro","family":"Coluccia","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonella","family":"Liantonio","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2021,2,26]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"29004","DOI":"10.1074\/jbc.M801297200","article-title":"Cooperative synergy between NFAT and MyoD regulates myogenin expression and myogenesis","volume":"283","author":"Armand","year":"2008","journal-title":"J. Biol. Chem."},{"key":"B2","doi-asserted-by":"publisher","first-page":"780","DOI":"10.1016\/j.molcel.2017.05.028","article-title":"Intracellular Ca2+ sensing: its role in calcium homeostasis and signaling","volume":"66","author":"Bagur","year":"2017","journal-title":"Mol. Cell."},{"key":"B3","doi-asserted-by":"publisher","first-page":"1761","DOI":"10.1002\/humu.23338","article-title":"Identification and characterization of three novel mutations in the CASQ1 gene in four patients with tubular aggregate myopathy","volume":"38","author":"Barone","year":"2017","journal-title":"Hum. Mutat."},{"key":"B4","doi-asserted-by":"publisher","first-page":"426","DOI":"10.1002\/humu.23172","article-title":"ORAI1 Mutations with Distinct Channel Gating Defects in Tubular Aggregate Myopathy","volume":"38","author":"B\u00f6hm","year":"2017","journal-title":"Hum. Mutat."},{"key":"B5","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1016\/j.ajhg.2012.12.007","article-title":"Constitutive activation of the calcium sensor STIM1 causes tubular-aggregate myopathy","volume":"92","author":"B\u00f6hm","year":"2013","journal-title":"Am. J. Hum. Genet."},{"key":"B6","doi-asserted-by":"publisher","first-page":"824","DOI":"10.1136\/jmedgenet-2014-102623","article-title":"Clinical, histological and genetic characterisation of patients with tubular aggregate myopathy caused by mutations in STIM1","volume":"51","author":"B\u00f6hm","year":"2014","journal-title":"J. Med. Genet."},{"key":"B7","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.ceca.2018.07.008","article-title":"Gain-of-function mutations in STIM1 and ORAI1 causing tubular aggregate myopathy and Stormorken syndrome","volume":"76","author":"B\u00f6hm","year":"2018","journal-title":"Cell Calcium"},{"key":"B8","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1007\/s00401-017-1775-x","article-title":"CASQ1 mutations impair calsequestrin polymerization and cause tubular aggregate myopathy","volume":"135","author":"B\u00f6hm","year":"2018","journal-title":"Acta Neuropathol."},{"key":"B9","doi-asserted-by":"publisher","first-page":"611","DOI":"10.1373\/clinchem.2008.112797","article-title":"The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments","volume":"55","author":"Bustin","year":"2009","journal-title":"Clin. Chem."},{"key":"B10","doi-asserted-by":"publisher","first-page":"20849","DOI":"10.1074\/jbc.R116.735894","article-title":"Why calcium? How calcium became the best communicator","volume":"291","author":"Carafoli","year":"2016","journal-title":"J. Biol. Chem."},{"key":"B11","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1002\/path.1832","article-title":"The origin of tubular aggregates in human myopathies","volume":"207","author":"Chevessier","year":"2005","journal-title":"J. Pathol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"e378","DOI":"10.1038\/emm.2017.208","article-title":"A focus on extracellular Ca2+ entry into skeletal muscle","volume":"49","author":"Cho","year":"2017","journal-title":"Exp. Mol. Med."},{"key":"B13","doi-asserted-by":"publisher","first-page":"19140","DOI":"10.1038\/s41598-019-55745-z","article-title":"A muscular hypotonia-associated STIM1 mutant at R429 induces abnormalities in intracellular Ca2+ movement and extracellular Ca2+ entry in skeletal muscle","volume":"9","author":"Choi","year":"2019","journal-title":"Sci. Rep."},{"key":"B14","doi-asserted-by":"publisher","first-page":"386","DOI":"10.1002\/jcsm.12185","article-title":"Growth hormone secretagogues prevent dysregulation of skeletal muscle calcium homeostasis in a rat model of cisplatin-induced cachexia","volume":"8","author":"Conte","year":"2017","journal-title":"J. Cachexia Sarcopenia Muscle"},{"key":"B15","doi-asserted-by":"publisher","first-page":"dmm041111","DOI":"10.1242\/dmm.041111","article-title":"A luminal EF-hand mutation in STIM1 in mice causes the clinical hallmarks of tubular aggregate myopathy","volume":"13","author":"Cordero-Sanchez","year":"2019","journal-title":"Dis. Model. Mech."},{"key":"B16","doi-asserted-by":"publisher","first-page":"22437","DOI":"10.1074\/jbc.M110.118984","article-title":"Human muscle economy myoblast differentiation and excitation-contraction coupling use the same molecular partners, STIM1 and STIM2","volume":"285","author":"Darbellay","year":"2010","journal-title":"J. Biol. Chem."},{"key":"B17","doi-asserted-by":"publisher","first-page":"5370","DOI":"10.1074\/jbc.M806726200","article-title":"STIM1- and Orai1-dependent store-operated calcium entry regulates human myoblast differentiation","volume":"284","author":"Darbellay","year":"2009","journal-title":"J. Biol. Chem."},{"key":"B18","doi-asserted-by":"publisher","first-page":"266","DOI":"10.1042\/bst0080266","article-title":"The role of calcium in the regulation of mitochondrial metabolism","volume":"8","author":"Denton","year":"1980","journal-title":"Biochem. Soc. Trans."},{"key":"B19","doi-asserted-by":"publisher","first-page":"637","DOI":"10.1093\/hmg\/ddu477","article-title":"Dominant mutations in ORAI1 cause tubular aggregate myopathy with hypocalcemia via constitutive activation of store-operated Ca2? channels","volume":"24","author":"Endo","year":"2015","journal-title":"Hum. Mol. Genet."},{"key":"B20","doi-asserted-by":"publisher","first-page":"2576","DOI":"10.1038\/s41467-019-10226-9","article-title":"DRP1-mediated mitochondrial shape controls calcium homeostasis and muscle mass","volume":"10","author":"Favaro","year":"2019","journal-title":"Nat. Commun."},{"key":"B21","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1016\/j.ceca.2018.10.001","article-title":"STIM1 R304W causes muscle degeneration and impaired platelet activation in mice","volume":"76","author":"Gamage","year":"2018","journal-title":"Cell Calcium"},{"key":"B22","doi-asserted-by":"publisher","first-page":"3706","DOI":"10.1093\/hmg\/ddu079","article-title":"Enhanced Ca2? influx from STIM1-Orai1 induces muscle pathology in mouse models of muscular dystrophy","volume":"23","author":"Goonasekera","year":"2014","journal-title":"Hum. Mol. Genet."},{"key":"B23","doi-asserted-by":"publisher","first-page":"3440","DOI":"10.1016\/S0021-9258(19)83641-4","article-title":"A new generation of Ca2+ indicators with greatly improved fluorescence properties","volume":"260","author":"Grynkiewicz","year":"1985","journal-title":"J. Biol. Chem."},{"key":"B24","doi-asserted-by":"publisher","first-page":"4536","DOI":"10.1038\/s41467-018-06816-8","article-title":"Calcium sensing by the STIM1 ER-luminal domain","volume":"9","author":"Gudlur","year":"2018","journal-title":"Nat. Commun."},{"key":"B25","doi-asserted-by":"publisher","first-page":"861","DOI":"10.1016\/j.nmd.2017.05.002","article-title":"Complex phenotypes associated with STIM1 mutations in both coiled coil and EF-hand domains","volume":"27","author":"Harris","year":"2017","journal-title":"Neuromuscul. Disord."},{"key":"B26","doi-asserted-by":"publisher","first-page":"870","DOI":"10.1007\/s00415-014-7287-x","article-title":"Childhood onset tubular aggregate myopathy associated with de novo STIM1 mutations","volume":"261","author":"Hedberg","year":"2014","journal-title":"J. Neurol."},{"key":"B27","doi-asserted-by":"publisher","first-page":"4481","DOI":"10.1242\/dev.155523","article-title":"The hallmarks of cell-cell fusion","volume":"144","author":"Hern\u00e1ndez","year":"2017","journal-title":"Development"},{"key":"B28","doi-asserted-by":"publisher","first-page":"re2","DOI":"10.1126\/scisignal.2003832","article-title":"Signaling mechanisms in mammalian myoblast fusion","volume":"6","author":"Hindi","year":"2013","journal-title":"Sci. Signal."},{"key":"B29","doi-asserted-by":"publisher","first-page":"737","DOI":"10.1038\/s41598-017-18658-3","article-title":"The effect of differentiation and TGF\u03b2 on mitochondrial respiration and mitochondrial enzyme abundance in cultured primary human skeletal muscle cells","volume":"8","author":"Hoffmann","year":"2018","journal-title":"Sci. Rep."},{"key":"B30","doi-asserted-by":"publisher","first-page":"870","DOI":"10.1038\/sj.cdd.4401260","article-title":"Dynamics of mitochondrial morphology in healthy cells and during apoptosis","volume":"10","author":"Karbowski","year":"2003","journal-title":"Cell. Death Differ"},{"key":"B31","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1006\/dbio.2001.0179","article-title":"Altered Primary Myogenesis in NFATC3\u2212\/\u2212 mice leads to decreased muscle size in the adult","volume":"232","author":"Kegley","year":"2001","journal-title":"Dev. Biol."},{"key":"B32","doi-asserted-by":"publisher","first-page":"45","DOI":"10.2741\/3230","article-title":"The integrative function of TRPC channels","volume":"14","author":"Kiselyov","year":"2009","journal-title":"Front. Biosci."},{"key":"B33","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1186\/2044-5040-1-16","article-title":"STIM1 as a key regulator for Ca2+ homeostasis in skeletal-muscle development and function","volume":"1","author":"Kiviluoto","year":"2011","journal-title":"Skelet. Muscle"},{"key":"B34","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1111\/nyas.12938","article-title":"Diseases caused by mutations in ORAI1 and STIM1","volume":"1356","author":"Lacruz","year":"2015","journal-title":"Ann N Y Acad Sci"},{"key":"B35","doi-asserted-by":"publisher","first-page":"9777","DOI":"10.3390\/ijms21249777","article-title":"Synthesis and characterization of store-operated calcium entry inhibitors active in the submicromolar range","volume":"21","author":"Le Guilcher","year":"2020","journal-title":"Int. J. Mol. Sci."},{"key":"B36","doi-asserted-by":"publisher","first-page":"1952","DOI":"10.3390\/ijms17111952","article-title":"Calcium dyshomeostasis in tubular aggregate myopathy","volume":"17","author":"Lee","year":"2016","journal-title":"Int. J. Mol. Sci."},{"key":"B37","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1042\/BJ20130178","article-title":"STIM1 negatively regulates Ca2? release from the sarcoplasmic reticulum in skeletal myotubes","volume":"453","author":"Lee","year":"2013","journal-title":"Biochem. J."},{"key":"B38","doi-asserted-by":"publisher","first-page":"39171","DOI":"10.1074\/jbc.M110.149690","article-title":"Impaired Orai1-mediated resting Ca2+ entry reduces the cytosolic [Ca2+] and sarcoplasmic reticulum Ca2+ loading in quiescent junctophilin 1 knock-out myotubes","volume":"285","author":"Li","year":"2010","journal-title":"J. Biol. Chem"},{"key":"B39","doi-asserted-by":"publisher","first-page":"3009","DOI":"10.1128\/MCB.06599-11","article-title":"STIM1-Ca(2+) signaling is required for the hypertrophic growth of skeletal muscle in mice","volume":"32","author":"Li","year":"2012","journal-title":"Mol. Cell. Biol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"445","DOI":"10.1007\/978-3-030-12457-1_17","article-title":"Molecular basis and regulation of store-operated calcium entry","volume":"1131","author":"Lopez","year":"2020","journal-title":"Adv. Exp. Med. Biol."},{"key":"B41","doi-asserted-by":"publisher","first-page":"3951","DOI":"10.1242\/jcs.037218","article-title":"TRPC1 regulates skeletal myoblast migration and differentiation","volume":"121","author":"Louis","year":"2008","journal-title":"J. Cell. Sci."},{"key":"B42","doi-asserted-by":"publisher","first-page":"e202012747","DOI":"10.1085\/jgp.202012747","article-title":"The Orai1 inhibitor BTP2 has multiple effects on Ca2+ handling in skeletal muscle","volume":"153","author":"Meizoso-Huesca","year":"2021","journal-title":"J Gen Physiol."},{"key":"B43","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1016\/j.ceca.2018.10.004","article-title":"Role of STIM1\/ORAI1-mediated store-operated Ca2+ entry in skeletal muscle physiology and disease","volume":"76","author":"Michelucci","year":"2018","journal-title":"Cell Calcium."},{"key":"B44","doi-asserted-by":"publisher","first-page":"e28628","DOI":"10.1371\/journal.pone.0028628","article-title":"A method for the direct identification of differentiating muscle cells by a fluorescent mitochondrial dye","volume":"6","author":"Miyake","year":"2011","journal-title":"PLoS ONE"},{"key":"B45","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1002\/humu.23899","article-title":"Tubular aggregate myopathy and stormorken syndrome: mutation spectrum and genotype\/phenotype correlation","volume":"41","author":"Morin","year":"2020","journal-title":"Hum. Mutat."},{"key":"B46","doi-asserted-by":"publisher","first-page":"4197","DOI":"10.1073\/pnas.1312520111","article-title":"Activating mutations in STIM1 and ORAI1 cause overlapping syndromes of tubular myopathy and congenital miosis","volume":"111","author":"Nesin","year":"2014","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B47","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1016\/j.bbrc.2017.06.094","article-title":"Mitochondrial dynamics coordinate cell differentiation","volume":"500","author":"Noguchi","year":"2018","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"B48","doi-asserted-by":"publisher","first-page":"876","DOI":"10.1016\/j.cell.2009.02.014","article-title":"STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1","volume":"136","author":"Park","year":"2009","journal-title":"Cell"},{"key":"B49","doi-asserted-by":"publisher","first-page":"C640","DOI":"10.1152\/ajpcell.00407.2004","article-title":"Expression levels of RyR1 and RyR3 control resting free Ca2+ in skeletal muscle","volume":"288","author":"Perez","year":"2005","journal-title":"Am. J. Physiol. Cell. Physiol."},{"key":"B50","doi-asserted-by":"publisher","first-page":"722","DOI":"10.1016\/j.bbrc.2012.11.082","article-title":"Positive feedback control between STIM1 and NFATc3 is required for C2C12 myoblast differentiation","volume":"430","author":"Phuong","year":"2013","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"B51","doi-asserted-by":"publisher","first-page":"1363","DOI":"10.1177\/44.12.8985128","article-title":"Analysis of mitochondrial morphology and function with novel fixable fluorescent stains","volume":"44","author":"Poot","year":"1996","journal-title":"J. Histochem. Cytochem."},{"key":"B52","doi-asserted-by":"publisher","first-page":"88","DOI":"10.1111\/j.1600-065X.2009.00820.x","article-title":"The molecular physiology of CRAC channels","volume":"231","author":"Prakriya","year":"2009","journal-title":"Immunol. Rev."},{"key":"B53","doi-asserted-by":"publisher","first-page":"2494","DOI":"10.1016\/S0006-3495(00)76491-5","article-title":"RYR1 and RYR3 have different roles in the assembly of calcium release units of skeletal muscle","volume":"79","author":"Protasi","year":"2000","journal-title":"Biophys. J"},{"key":"B54","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1007\/s12576-009-0069-z","article-title":"The cell boundary theorem: a simple law of the control of cytosolic calcium concentration","volume":"60","author":"R\u00edos","year":"2010","journal-title":"J. Physiol. Sci"},{"key":"B55","doi-asserted-by":"publisher","first-page":"9756","DOI":"10.1021\/acs.jmedchem.8b01512","article-title":"Pyrtriazoles, a novel class of store-operated calcium entry modulators: discovery, biological profiling, and in vivo proof-of-concept efficacy in acute pancreatitis","volume":"61","author":"Riva","year":"2018","journal-title":"J. Med. Chem."},{"key":"B56","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1186\/s13395-017-0149-3","article-title":"Myoblast fusion confusion: the resolution begins","volume":"8","author":"Sampath","year":"2018","journal-title":"Skelet. Muscle"},{"key":"B57","doi-asserted-by":"publisher","first-page":"eaax3194","DOI":"10.1126\/scisignal.aax3194","article-title":"Sequential activation of STIM1 links Ca2+ with luminal domain unfolding","volume":"12","author":"Schober","year":"2019","journal-title":"Sci Signal."},{"key":"B58","doi-asserted-by":"publisher","first-page":"604941","DOI":"10.3389\/fphys.2020.604941","article-title":"STIM1\/ORAI1 loss-of-function and gain-of-function mutations inversely impact on SOCE and calcium homeostasis and cause multi-systemic mirror diseases","volume":"11","author":"Silva-Rojas","year":"2020","journal-title":"Front. Physiol."},{"key":"B59","doi-asserted-by":"publisher","first-page":"1579","DOI":"10.1093\/hmg\/ddy446","article-title":"STIM1 over-activation generates a multi-systemic phenotype affecting the skeletal muscle, spleen, eye, skin, bones and immune system in mice","volume":"28","author":"Silva-Rojas","year":"2019","journal-title":"Hum. Mol. Genet."},{"key":"B60","doi-asserted-by":"publisher","first-page":"369","DOI":"10.1080\/15548627.2015.1115172","article-title":"Mitophagy is required for mitochondrial biogenesis and myogenic differentiation of C2C12 myoblasts","volume":"12","author":"Sin","year":"2016","journal-title":"Autophagy"},{"key":"B61","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1016\/j.cell.2008.08.006","article-title":"Structural and mechanistic insights into STIM1-mediated initiation of store-operated calcium entry","volume":"135","author":"Stathopulos","year":"2008","journal-title":"Cell"},{"key":"B62","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1016\/j.ceca.2018.07.005","article-title":"CRAC channels as targets for drug discovery and development","volume":"74","author":"Stauderman","year":"2018","journal-title":"Cell Calcium"},{"key":"B63","doi-asserted-by":"publisher","first-page":"688","DOI":"10.1038\/ncb1731","article-title":"STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle","volume":"10","author":"Stiber","year":"2008","journal-title":"Nat. Cell. Biol."},{"key":"B64","doi-asserted-by":"publisher","first-page":"341","DOI":"10.1016\/j.ceca.2010.11.012","article-title":"The role of store-operated calcium influx in skeletal muscle signaling","volume":"49","author":"Stiber","year":"2011","journal-title":"Cell Calcium"},{"key":"B65","doi-asserted-by":"publisher","first-page":"91","DOI":"10.1016\/j.ceca.2016.02.005","article-title":"Calcium signaling in skeletal muscle development, maintenance and regeneration","volume":"59","author":"Tu","year":"2016","journal-title":"Cell Calcium"},{"key":"B66","doi-asserted-by":"publisher","first-page":"dmm044370","DOI":"10.1242\/dmm.044370","article-title":"Moving neuromuscular disorders research forward: from novel models to clinical studies","volume":"13","author":"van Putten","year":"2020","journal-title":"Dis. Model. Mech."},{"key":"B67","doi-asserted-by":"publisher","first-page":"e29353","DOI":"10.1371\/journal.pone.0029353","article-title":"Inhibition of Akt activity and calcium channel function coordinately drive cell-cell fusion in the BeWO choriocarcinoma placental cell line","volume":"7","author":"Vatish","year":"2012","journal-title":"PLoS ONE"},{"key":"B68","doi-asserted-by":"publisher","first-page":"577","DOI":"10.1016\/j.nmd.2015.04.005","article-title":"50 years to diagnosis: Autosomal dominant tubular aggregate myopathy caused by a novel STIM1 mutation","volume":"25","author":"Walter","year":"2015","journal-title":"Neuromuscul. Disord."},{"key":"B69","doi-asserted-by":"publisher","first-page":"2805","DOI":"10.1038\/ncomms3805","article-title":"Orai1-dependent calcium entry promotes skeletal muscle growth and limits fatigue","volume":"4","author":"Wei-Lapierre","year":"2013","journal-title":"Nat. Commun."},{"key":"B70","doi-asserted-by":"publisher","first-page":"5657","DOI":"10.1073\/pnas.1118947109","article-title":"Structural and mechanistic insights into the activation of stromal interaction molecule 1 (STIM1)","volume":"109","author":"Yang","year":"2012","journal-title":"Proc. Natl. Acad. Sci. U.S.A."},{"key":"B71","doi-asserted-by":"publisher","first-page":"615","DOI":"10.1016\/j.matbio.2007.06.004","article-title":"Altered extracellular matrix transcript expression and protein modulation in primary Duchenne muscular dystrophy myotubes","volume":"26","author":"Zanotti","year":"2007","journal-title":"Matrix Biol."},{"key":"B72","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1007\/978-3-319-57732-6_2","article-title":"The STIM-Orai pathway: STIM-Orai structures: isolated and in complex","volume":"993","author":"Zhu","year":"2017","journal-title":"Adv. Exp. Med. Biol"}],"container-title":["Frontiers in Cell and Developmental Biology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcell.2021.635063\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,2,26]],"date-time":"2021-02-26T05:26:45Z","timestamp":1614317205000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcell.2021.635063\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,2,26]]},"references-count":72,"alternative-id":["10.3389\/fcell.2021.635063"],"URL":"https:\/\/doi.org\/10.3389\/fcell.2021.635063","relation":{},"ISSN":["2296-634X"],"issn-type":[{"value":"2296-634X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,2,26]]},"article-number":"635063"}}