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Neurological and Motor Disorders: TRPC in the Skeletal Muscle

  • Sophie Saüc
  • Maud FriedenEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 993)

Abstract

Transient receptor potential canonical (TRPC) channels belong to the large family of TRPs that are mostly nonselective cation channels with a great variety of gating mechanisms. TRPC are composed of seven members that can all be activated downstream of agonist-induced phospholipase C stimulation, but some members are also stretch-activated and/or are part of the store-operated Ca2+ entry (SOCE) pathway. Skeletal muscles generate contraction via an explosive increase of cytosolic Ca2+ concentration resulting almost exclusively from sarcoplasmic reticulum Ca2+ channel opening. Even if neglected for a long time, it is now commonly accepted that Ca2+ entry via SOCE and other routes is essential to sustain contractions of the skeletal muscle. In addition, Ca2+ influx is required during muscle regeneration, and alteration of the influx is associated with myopathies. In this chapter, we review the implication of TRPC channels at different stages of muscle regeneration, in adult muscle fibers, and discuss their implication in myopathies.

Keywords

TRPC Skeletal muscle Calcium entry Muscle regeneration Myopathies 

References

  1. Allen DG, Whitehead NP, Froehner SC (2016) Absence of dystrophin disrupts skeletal muscle signaling: roles of Ca2+, reactive oxygen species, and nitric oxide in the development of muscular dystrophy. Physiol Rev 96:253–305CrossRefPubMedGoogle Scholar
  2. Ambudkar IS (2014) Ca(2+) signaling and regulation of fluid secretion in salivary gland acinar cells. Cell Calcium 55:297–305CrossRefPubMedPubMedCentralGoogle Scholar
  3. Antigny F, Koenig S, Bernheim L, Frieden M (2013) During post-natal human myogenesis, normal myotube size requires TRPC1- and TRPC4-mediated Ca(2+) entry. J Cell Sci 126:2525–2533CrossRefPubMedGoogle Scholar
  4. Araya R, Eckardt D, Maxeiner S, Kruger O, Theis M, Willecke K, Saez JC (2005) Expression of connexins during differentiation and regeneration of skeletal muscle: functional relevance of connexin43. J Cell Sci 118:27–37CrossRefPubMedGoogle Scholar
  5. Bakker AJ, Head SI, Williams DA, Stephenson DG (1993) Ca2+ levels in myotubes grown from the skeletal muscle of dystrophic (mdx) and normal mice. J Physiol 460:1–13CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bannister RA, Pessah IN, Beam KG (2009) The skeletal L-type Ca(2+) current is a major contributor to excitation-coupled Ca(2+) entry. J Gen Physiol 133:79–91CrossRefPubMedPubMedCentralGoogle Scholar
  7. Benavides Damm T, Richard S, Tanner S, Wyss F, Egli M, Franco-Obregon A (2013) Calcium-dependent deceleration of the cell cycle in muscle cells by simulated microgravity. FASEB J 27:2045–2054CrossRefPubMedGoogle Scholar
  8. Bentzinger CF, Wang YX, Rudnicki MA (2012) Building muscle: molecular regulation of myogenesis. Cold Spring Harb Perspect Biol 4(2). doi: 10.1101/cshperspect.a008342
  9. Berbey C, Weiss N, Legrand C, Allard B (2009) Transient receptor potential canonical type 1 (TRPC1) operates as a sarcoplasmic reticulum calcium leak channel in skeletal muscle. J Biol Chem 284:36387–36394CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bohm J, Chevessier F, Koch C, Peche GA, Mora M, Morandi L, Pasanisi B, Moroni I, Tasca G, Fattori F, Ricci E, Penisson-Besnier I, Nadaj-Pakleza A, Fardeau M, Joshi PR, Deschauer M, Romero NB, Eymard B, Laporte J (2014) Clinical, histological and genetic characterisation of patients with tubular aggregate myopathy caused by mutations in STIM1. J Med Genet 51:824–833CrossRefPubMedGoogle Scholar
  11. Cherednichenko G, Hurne AM, Fessenden JD, Lee EH, Allen PD, Beam KG, Pessah IN (2004) Conformational activation of Ca2+ entry by depolarization of skeletal myotubes. Proc Natl Acad Sci U S A 101:15793–15798CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cheung KK, Yeung SS, Au SW, Lam LS, Dai ZQ, Li YH, Yeung EW (2011) Expression and association of TRPC1 with TRPC3 during skeletal myogenesis. Muscle Nerve 44:358–365PubMedGoogle Scholar
  13. Collet C, Allard B, Tourneur Y, Jacquemond V (1999) Intracellular calcium signals measured with indo-1 in isolated skeletal muscle fibres from control and mdx mice. J Physiol 520(Pt 2):417–429CrossRefPubMedPubMedCentralGoogle Scholar
  14. Darbellay B, Arnaudeau S, Konig S, Jousset H, Bader C, Demaurex N, Bernheim L (2009) STIM1- and Orai1-dependent store-operated calcium entry regulates human myoblast differentiation. J Biol Chem 284:5370–5380CrossRefPubMedGoogle Scholar
  15. Darbellay B, Arnaudeau S, Bader CR, Konig S, Bernheim L (2011) STIM1L is a new actin-binding splice variant involved in fast repetitive Ca2+ release. J Cell Biol 194:335–346CrossRefPubMedPubMedCentralGoogle Scholar
  16. Dietrich A, Kalwa H, Rost BR, Gudermann T (2005) The diacylgylcerol-sensitive TRPC3/6/7 subfamily of cation channels: functional characterization and physiological relevance. Pflugers Arch 451:72–80CrossRefPubMedGoogle Scholar
  17. Dirksen RT (2009) Checking your SOCCs and feet: the molecular mechanisms of Ca2+ entry in skeletal muscle. J Physiol 587:3139–3147CrossRefPubMedPubMedCentralGoogle Scholar
  18. Ducret T, Vandebrouck C, Cao ML, Lebacq J, Gailly P (2006) Functional role of store-operated and stretch-activated channels in murine adult skeletal muscle fibres. J Physiol 575:913–924CrossRefPubMedPubMedCentralGoogle Scholar
  19. Edwards JN, Murphy RM, Cully TR, von Wegner F, Friedrich O, Launikonis BS (2010) Ultra-rapid activation and deactivation of store-operated Ca(2+) entry in skeletal muscle. Cell Calcium 47:458–467CrossRefPubMedGoogle Scholar
  20. Flucher BE, Franzini-Armstrong C (1996) Formation of junctions involved in excitation-contraction coupling in skeletal and cardiac muscle. Proc Natl Acad Sci U S A 93:8101–8106CrossRefPubMedPubMedCentralGoogle Scholar
  21. Formigli L, Meacci E, Sassoli C, Chellini F, Giannini R, Quercioli F, Tiribilli B, Squecco R, Bruni P, Francini F, Zecchi-Orlandini S (2005) Sphingosine 1-phosphate induces cytoskeletal reorganization in C2C12 myoblasts: physiological relevance for stress fibres in the modulation of ion current through stretch-activated channels. J Cell Sci 118:1161–1171CrossRefPubMedGoogle Scholar
  22. Formigli L, Sassoli C, Squecco R, Bini F, Martinesi M, Chellini F, Luciani G, Sbrana F, Zecchi-Orlandi S, Francini F, Maecci E (2009) Regulation of transient receptor potential canonical channel 1 (TRPC1) by sphingosine 1-phosphate in C2C12 myoblasts and its relevance for a role of mechanotransduction in skeletal muscle differentiation. J Cell Sci 122:1322–1333CrossRefPubMedGoogle Scholar
  23. Franco A Jr, Lansman JB (1990) Calcium entry through stretch-inactivated ion channels in mdx myotubes. Nature 344:670–673CrossRefPubMedGoogle Scholar
  24. Franco-Obregon A Jr, Lansman JB (1994) Mechanosensitive ion channels in skeletal muscle from normal and dystrophic mice. J Physiol 481(Pt 2):299–309CrossRefPubMedPubMedCentralGoogle Scholar
  25. Gailly P, Boland B, Himpens B, Casteels R, Gillis JM (1993) Critical evaluation of cytosolic calcium determination in resting muscle fibres from normal and dystrophic (mdx) mice. Cell Calcium 14:473–483CrossRefPubMedGoogle Scholar
  26. Gailly P, De Backer F, Van Schoor M, Gillis JM (2007) In situ measurements of calpain activity in isolated muscle fibres from normal and dystrophin-lacking mdx mice. J Physiol 582:1261–1275CrossRefPubMedPubMedCentralGoogle Scholar
  27. Gervasio OL, Whitehead NP, Yeung EW, Phillips WD, Allen DG (2008) TRPC1 binds to caveolin-3 and is regulated by Src kinase—role in Duchenne muscular dystrophy. J Cell Sci 121:2246–2255CrossRefPubMedGoogle Scholar
  28. Hartmann J, Dragicevic E, Adelsberger H, Henning HA, Sumser M, Abramowitz J, Blum R, Dietrich A, Freichel V, Birnbaumer L, Konnerth A (2008) TRPC3 channels are required for synaptic transmission and motor coordination. Neuron 59:392–398CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hawke TJ, Garry DJ (2001) Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 91:534–551PubMedGoogle Scholar
  30. Head SI (1993) Membrane potential, resting calcium and calcium transients in isolated muscle fibres from normal and dystrophic mice. J Physiol 469:11–19CrossRefPubMedPubMedCentralGoogle Scholar
  31. Hofmann T, Obukhov AG, Schaefer M, Harteneck C, Gudermann T, Schultz G (1999) Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 397:259–263CrossRefPubMedGoogle Scholar
  32. Huang GN, Zeng W, Kim JY, Yuan JP, Han L, Muallem S, Worley PF (2006) STIM1 carboxyl-terminus activates native SOC, I(crac) and TRPC1 channels. Nat Cell Biol 8:1003–1010CrossRefPubMedGoogle Scholar
  33. Imbert N, Cognard C, Duport G, Guillou C, Raymond G (1995) Abnormal calcium homeostasis in Duchenne muscular dystrophy myotubes contracting in vitro. Cell Calcium 18:177–186CrossRefPubMedGoogle Scholar
  34. Kawasaki BT, Liao Y, Birnbaumer L (2006) Role of Src in C3 transient receptor potential channel function and evidence for a heterogeneous makeup of receptor- and store-operated Ca2+ entry channels. Proc Natl Acad Sci U S A 103:335–340CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kruger J, Kunert-Keil C, Bisping F, Brinkmeier H (2008) Transient receptor potential cation channels in normal and dystrophic mdx muscle. Neuromuscul Disord 18:501–513CrossRefPubMedGoogle Scholar
  36. Kunert-Keil C, Bisping F, Kruger J, Brinkmeier H (2006) Tissue-specific expression of TRP channel genes in the mouse and its variation in three different mouse strains. BMC Genomics 7:159CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kurebayashi N, Ogawa Y (2001) Depletion of Ca2+ in the sarcoplasmic reticulum stimulates Ca2+ entry into mouse skeletal muscle fibres. J Physiol 533:185–199CrossRefPubMedPubMedCentralGoogle Scholar
  38. Lacruz RS, Feske S (2015) Diseases caused by mutations in ORAI1 and STIM1. Ann N Y Acad Sci 1356:45–79CrossRefPubMedPubMedCentralGoogle Scholar
  39. Lanner JT, Bruton JD, Assefaw-Redda Y, Andronache Z, Zhang SJ, Severa D, Zhang ZB, Melzer W, Zhang SL, Katz A, Westerblad H (2009) Knockdown of TRPC3 with siRNA coupled to carbon nanotubes results in decreased insulin-mediated glucose uptake in adult skeletal muscle cells. FASEB J 23:1728–1738CrossRefPubMedGoogle Scholar
  40. Launikonis BS, Rios E (2007) Store-operated Ca2+ entry during intracellular Ca2+ release in mammalian skeletal muscle. J Physiol 583:81–97CrossRefPubMedPubMedCentralGoogle Scholar
  41. Launikonis BS, Stephenson DG, Friedrich O (2009) Rapid Ca2+ flux through the transverse tubular membrane, activated by individual action potentials in mammalian skeletal muscle. J Physiol 587:2299–2312CrossRefPubMedPubMedCentralGoogle Scholar
  42. Lauritzen HP, Ploug T, Prats C, Tavare JM, Galbo H (2006) Imaging of insulin signaling in skeletal muscle of living mice shows major role of T-tubules. Diabetes 55:1300–1306CrossRefPubMedGoogle Scholar
  43. Lee EH, Cherednichenko G, Pessah IN, Allen PD (2006) Functional coupling between TRPC3 and RyR1 regulates the expressions of key triadic proteins. J Biol Chem 281:10042–10048CrossRefPubMedGoogle Scholar
  44. Leloup L, Mazeres G, Daury L, Cottin P, Brustis JJ (2006) Involvement of calpains in growth factor-mediated migration. Int J Biochem Cell Biol 38:2049–2063CrossRefPubMedGoogle Scholar
  45. Li S, Couet J, Lisanti MP (1996) Src tyrosine kinases, Galpha subunits, and H-Ras share a common membrane-anchored scaffolding protein, caveolin. Caveolin binding negatively regulates the auto-activation of Src tyrosine kinases. J Biol Chem 271:29182–29190CrossRefPubMedGoogle Scholar
  46. Li T, Finch EA, Graham V, Zhang ZS, Ding JD, Burch J, Oh-hora M, Rosenberg P (2012) STIM1-Ca(2+) signaling is required for the hypertrophic growth of skeletal muscle in mice. Mol Cell Biol 32:3009–3017CrossRefPubMedPubMedCentralGoogle Scholar
  47. Lichtenegger M, Groschner K (2014) TRPC3: a multifunctional signaling molecule. Handb Exp Pharmacol 222:67–84CrossRefPubMedGoogle Scholar
  48. Liu Y, Schneider MF (2014) FGF2 activates TRPC and Ca(2+) signaling leading to satellite cell activation. Front Physiol 5:38PubMedPubMedCentralGoogle Scholar
  49. Louis M, Zanou N, Van Schoor M, Gailly P (2008) TRPC1 regulates skeletal myoblast migration and differentiation. J Cell Sci 121:3951–3959CrossRefPubMedGoogle Scholar
  50. Lyfenko AD, Dirksen RT (2008) Differential dependence of store-operated and excitation-coupled Ca2+ entry in skeletal muscle on STIM1 and Orai1. J Physiol 586:4815–4824CrossRefPubMedPubMedCentralGoogle Scholar
  51. Maroto R, Raso A, Wood TG, Kurosky A, Martinac B, Hamill OP (2005) TRPC1 forms the stretch-activated cation channel in vertebrate cells. Nat Cell Biol 7:179–185CrossRefPubMedGoogle Scholar
  52. Matsumura CY, Taniguti AP, Pertille A, Santo Neto H, Marques MJ (2011) Stretch-activated calcium channel protein TRPC1 is correlated with the different degrees of the dystrophic phenotype in mdx mice. Am J Physiol Cell Physiol 301:C1344–C1350CrossRefPubMedGoogle Scholar
  53. McCarl CA, Picard C, Khalil S, Kawasaki T, Rother J, Papolos A, Kutok J, Hivroz C, Ledeist F, Plogmann K, Ehl S, Notheis G, Albert MH, Belohradsky BH, Kirschner J, Rao A, Fischer A, Feske S (2009) ORAI1 deficiency and lack of store-operated Ca2+ entry cause immunodeficiency, myopathy, and ectodermal dysplasia. J Allergy Clin Immunol 124:1311–1318CrossRefPubMedPubMedCentralGoogle Scholar
  54. Meacci E, Bini F, Sassoli C, Martinesi M, Squecco R, Chellini F, Zecchi-Orlandini S, Francini F, Formigli L (2010) Functional interaction between TRPC1 channel and connexin-43 protein: a novel pathway underlying S1P action on skeletal myogenesis. Cell Mol Life Sci 67:4269–4285CrossRefPubMedGoogle Scholar
  55. Millay DP, Goonasekera SA, Sargent MA, Maillet M, Aronow BJ, Molkentin JD (2009) Calcium influx is sufficient to induce muscular dystrophy through a TRPC-dependent mechanism. Proc Natl Acad Sci U S A 106:19023–19028CrossRefPubMedPubMedCentralGoogle Scholar
  56. Nesin V, Tsiokas L (2014) Trpc1. Handb Exp Pharmacol 222:15–51CrossRefPubMedGoogle Scholar
  57. Nilius B, Owsianik G (2010) Transient receptor potential channelopathies. Pflugers Arch 460:437–450CrossRefPubMedGoogle Scholar
  58. Nilius B, Owsianik G (2011) The transient receptor potential family of ion channels. Genome Biol 12:218CrossRefPubMedPubMedCentralGoogle Scholar
  59. Olah T, Fodor J, Ruzsnavszky O, Vincze J, Berbey C, Allard B, Csernoch L (2011) Overexpression of transient receptor potential canonical type 1 (TRPC1) alters both store operated calcium entry and depolarization-evoked calcium signals in C2C12 cells. Cell Calcium 49:415–425CrossRefPubMedGoogle Scholar
  60. Ong HL, de Souza LB, Ambudkar IS (2016) Role of TRPC Channels in Store-Operated Calcium Entry. Adv Exp Med Biol 898:87–109CrossRefPubMedGoogle Scholar
  61. Pedersen SF, Nilius B (2007) Transient receptor potential channels in mechanosensing and cell volume regulation. Methods Enzymol 428:183–207CrossRefPubMedGoogle Scholar
  62. Prakriya M, Lewis RS (2015) Store-operated calcium channels. Physiol Rev 95:1383–1436CrossRefPubMedPubMedCentralGoogle Scholar
  63. Pressmar J, Brinkmeier H, Seewald MJ, Naumann T, Rudel R (1994) Intracellular Ca2+ concentrations are not elevated in resting cultured muscle from Duchenne (DMD) patients and in MDX mouse muscle fibres. Pflugers Arch 426:499–505CrossRefPubMedGoogle Scholar
  64. Riccio A, Medhurst AD, Mattei C, Kelsell RE, Calver AR, Randall AD, Benham CD, Pangalos MN (2002) mRNA distribution analysis of human TRPC family in CNS and peripheral tissues. Brain Res Mol Brain Res 109:95–104CrossRefPubMedGoogle Scholar
  65. Romi F, Aarli JA, Gilhus NE (2007) Myasthenia gravis patients with ryanodine receptor antibodies have distinctive clinical features. Eur J Neurol 14:617–620CrossRefPubMedGoogle Scholar
  66. Rosenberg P, Hawkins A, Stiber J, Shelton JM, Hutcheson K, Bassel-Duby R, Shin DM, Yan Z, Williams RS (2004) TRPC3 channels confer cellular memory of recent neuromuscular activity. Proc Natl Acad Sci U S A 101:9387–9392CrossRefPubMedPubMedCentralGoogle Scholar
  67. Sabourin J, Lamiche C, Vandebrouck A, Magaud C, Rivet J, Cognard C, Bourmeyster N, Constantin B (2009) Regulation of TRPC1 and TRPC4 cation channels requires an alpha1-syntrophin-dependent complex in skeletal mouse myotubes. J Biol Chem 284:36248–36261CrossRefPubMedPubMedCentralGoogle Scholar
  68. Sorrentino V (2011) Sarcoplasmic reticulum: structural determinants and protein dynamics. Int J Biochem Cell Biol 43:1075–1078CrossRefPubMedGoogle Scholar
  69. Spassova MA, Hewavitharana T, Xu W, Soboloff J, Gill DL (2006) A common mechanism underlies stretch activation and receptor activation of TRPC6 channels. Proc Natl Acad Sci U S A 103:16586–16591CrossRefPubMedPubMedCentralGoogle Scholar
  70. Spencer MJ, Croall DE, Tidball JG (1995) Calpains are activated in necrotic fibers from mdx dystrophic mice. J Biol Chem 270:10909–10914CrossRefPubMedGoogle Scholar
  71. Squecco R, Sassoli C, Nuti F, Martinesi M, Chellini F, Nosi D, Zecchi-Orlandini S, Francini F, Formigli L, Maecci E (2006) Sphingosine 1-phosphate induces myoblast differentiation through Cx43 protein expression: a role for a gap junction-dependent and -independent function. Mol Biol Cell 17:4896–4910CrossRefPubMedPubMedCentralGoogle Scholar
  72. Stiber J, Hawkins A, Zhang ZS, Wang S, Burch J, Graham V, Ward CC, Seth M, Finch E, Malouf N, Williams RD, JP E, Rosenberg P (2008a) STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nat Cell Biol 10:688–697CrossRefPubMedPubMedCentralGoogle Scholar
  73. Stiber JA, Zhang ZS, Burch J, JP E, Zhang S, Truskey GA, Seth M, Yamaguchi N, Meissner G, Shah R, Worley PF, Williams RS, Rosenberg PB (2008b) Mice lacking Homer 1 exhibit a skeletal myopathy characterized by abnormal transient receptor potential channel activity. Mol Cell Biol 28:2637–2647CrossRefPubMedPubMedCentralGoogle Scholar
  74. Suchyna TM, Johnson JH, Hamer K, Leykam JF, Gage DA, Clemo HF, Baumgarten CM, Sachs F (2000) Identification of a peptide toxin from Grammostola spatulata spider venom that blocks cation-selective stretch-activated channels. J Gen Physiol 115:583–598CrossRefPubMedPubMedCentralGoogle Scholar
  75. Tajeddine N, Zanou N, Van Schoor M, Lebacq J, Gailly P (2010) TRPC1: subcellular localization? J Biol Chem 285:le1. Author reply le2CrossRefPubMedPubMedCentralGoogle Scholar
  76. Takamori M (2008) Autoantibodies against TRPC3 and ryanodine receptor in myasthenia gravis. J Neuroimmunol 200:142–144CrossRefPubMedGoogle Scholar
  77. Turner PR, Westwood T, Regen CM, Steinhardt RA (1988) Increased protein degradation results from elevated free calcium levels found in muscle from mdx mice. Nature 335:735–738CrossRefPubMedGoogle Scholar
  78. Vallejo-Illarramendi A, Toral-Ojeda I, Aldanondo G, Lopez de Munain A (2014) Dysregulation of calcium homeostasis in muscular dystrophies. Expert Rev Mol Med 16:e16CrossRefPubMedGoogle Scholar
  79. Vandebrouck C, Martin D, Colson-Van Schoor M, Debaix H, Gailly P (2002) Involvement of TRPC in the abnormal calcium influx observed in dystrophic (mdx) mouse skeletal muscle fibers. J Cell Biol 158:1089–1096CrossRefPubMedPubMedCentralGoogle Scholar
  80. Vandebrouck A, Sabourin J, Rivet J, Balghi H, Sebille S, Kitzis A, Raymond G, Cognard C, Bourmeyster N, Constantin B (2007) Regulation of capacitative calcium entries by alpha1-syntrophin: association of TRPC1 with dystrophin complex and the PDZ domain of alpha1-syntrophin. FASEB J 21:608–617CrossRefPubMedGoogle Scholar
  81. Wei-Lapierre L, Carrell EM, Boncompagni S, Protasi F, Dirksen RT (2013) Orai1-dependent calcium entry promotes skeletal muscle growth and limits fatigue. Nat Commun 4:2805CrossRefPubMedPubMedCentralGoogle Scholar
  82. Woo JS, Kim DH, Allen PD, Lee EH (2008) TRPC3-interacting triadic proteins in skeletal muscle. Biochem J 411:399–405CrossRefPubMedGoogle Scholar
  83. Woo JS, Cho CH, Kim DH, Lee EH (2010) TRPC3 cation channel plays an important role in proliferation and differentiation of skeletal muscle myoblasts. Exp Mol Med 42:614–627CrossRefPubMedPubMedCentralGoogle Scholar
  84. Woo JS, Lee KJ, Huang M, Cho CH, Lee EH (2014) Heteromeric TRPC3 with TRPC1 formed via its ankyrin repeats regulates the resting cytosolic Ca2+ levels in skeletal muscle. Biochem Biophys Res Commun 446:454–459CrossRefPubMedGoogle Scholar
  85. Woo JS, Hwang JH, Huang M, Ahn MK, Cho CH, Ma J, Lee EH (2015) Interaction between mitsugumin 29 and TRPC3 participates in regulating Ca(2+) transients in skeletal muscle. Biochem Biophys Res Commun 464:133–139CrossRefPubMedPubMedCentralGoogle Scholar
  86. Xia L, Cheung KK, Yeung SS, Yeung EW (2016) The involvement of transient receptor potential canonical type 1 in skeletal muscle regrowth after unloading-induced atrophy. J Physiol 594:3111–3126CrossRefPubMedPubMedCentralGoogle Scholar
  87. Yeung EW, Whitehead NP, Suchyna TM, Gottlieb PA, Sachs F, Allen DG (2005) Effects of stretch-activated channel blockers on [Ca2+]i and muscle damage in the mdx mouse. J Physiol 562:367–380CrossRefPubMedGoogle Scholar
  88. Yuan JP, Zeng W, Huang GN, Worley PF, Muallem S (2007) STIM1 heteromultimerizes TRPC channels to determine their function as store-operated channels. Nat Cell Biol 9:636–645CrossRefPubMedPubMedCentralGoogle Scholar
  89. Zanou N, Shapovalov G, Louis M, Tajeddine N, Gallo C, Van Schoor M, Anguish I, Cao ML, Schakman O, Dietrich A, Lebacq J, Ruegg U, Roulet E, Birnbaumer L, Gailly P (2010) Role of TRPC1 channel in skeletal muscle function. Am J Physiol Cell Physiol 298:C149–C162CrossRefPubMedGoogle Scholar
  90. Zanou N, Schakman O, Louis P, Ruegg UT, Dietrich A, Birnbaumer L, Gailly P (2012) Trpc1 ion channel modulates phosphatidylinositol 3-kinase/Akt pathway during myoblast differentiation and muscle regeneration. J Biol Chem 287:14524–14534CrossRefPubMedPubMedCentralGoogle Scholar
  91. Zeng W, Yuan JP, Kim MS, Choi YJ, Huang GN, Worley PF, Muallem S (2008) STIM1 gates TRPC channels, but not Orai1, by electrostatic interaction. Mol Cell 32:439–448CrossRefPubMedPubMedCentralGoogle Scholar
  92. Zhang BT, Yeung SS, Cheung KK, Chai ZY, Yeung EW (2014) Adaptive responses of TRPC1 and TRPC3 during skeletal muscle atrophy and regrowth. Muscle Nerve 49:691–699CrossRefPubMedGoogle Scholar

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© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of Cell Physiology and MetabolismUniversity of GenevaGenevaSwitzerland

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