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Pathophysiological Significance of Store-Operated Calcium Entry in Cardiovascular and Skeletal Muscle Disorders and Angiogenesis

  • Javier Avila-Medina
  • Isabel Mayoral-González
  • Isabel Galeano-Otero
  • Pedro C. Redondo
  • Juan A. Rosado
  • Tarik SmaniEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1131)

Abstract

Store-Operated Ca2+ Entry (SOCE) is an important Ca2+ influx pathway expressed by several excitable and non-excitable cell types. SOCE is recognized as relevant signaling pathway not only for physiological process, but also for its involvement in different pathologies. In fact, independent studies demonstrated the implication of essential protein regulating SOCE, such as STIM, Orai and TRPCs, in different pathogenesis and cell disorders, including cardiovascular disease, muscular dystrophies and angiogenesis. Compelling evidence showed that dysregulation in the function and/or expression of isoforms of STIM, Orai or TRPC play pivotal roles in cardiac hypertrophy and heart failure, vascular remodeling and hypertension, skeletal myopathies, and angiogenesis. In this chapter, we summarized the current knowledge concerning the mechanisms underlying abnormal SOCE and its involvement in some diseases, as well as, we discussed the significance of STIM, Orai and TRPC isoforms as possible therapeutic targets for the treatment of angiogenesis, cardiovascular and skeletal muscle diseases.

Keywords

Cardiac disease Vascular disorders Skeletal muscle Angiogenesis 

Abbreviations

CRAC

Ca2+-Release Activated Ca2+ Channels

CREB

cAMP Response Element-Binding

DMD

Duchenne Muscular Dystrophy

EC

Endothelial Cell

EPC

Endothelial Progenitor Cell

ER/SR

Endoplasmic/Sarcoplasmic Reticulum

HF

Heart Failure

MD

Muscular Dystrophy

NFAT

Nuclear Factor of Activated T-cell

PAH

Pulmonary Arterial Hypertension

PASMC

Pulmonary Artery Smooth Muscle Cell

PDGF

Platelet-Derived Growth Factor

SERCA

Sarco/Endoplasmic Reticulum Ca2+ ATPase

siRNA

small interfering RNA

SOCC

Store-Operated Ca2+ Channel

SOCE

Store-Operated Ca2+ Entry

STIM1/2/1L

Stromal Interaction Molecule 1/2/1Large

TAC

Transverse Aortic Constriction

TRPC

Transient Receptor Potential-Canonical

VEGF

Vascular Endothelial Growth Factor

VSMC

Vascular Smooth Muscle Cell

Notes

Acknowledgements

This work was supported by FEDER funds and by Spanish Ministry of Economy and Competitiveness [BFU2016-74932-C2]; Institute of Carlos III [PI15/00203; CB16/11/00431]; and by the Andalusia Government [P12-CTS-1965; PI-0313-2016].

References

  1. 1.
    Putney JW (1986) A model for receptor-regulated calcium entry. Cell Calcium 7:1–12CrossRefGoogle Scholar
  2. 2.
    Roos J, DiGregorio PJ, Yeromin AV et al (2005) STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol 169:435–445CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Hogan PG, Rao A (2015) Store-operated calcium entry: mechanisms and modulation. Biochem Biophys Res Commun 460:40–49CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Brandman O, Liou J, Park WS, Meyer T (2007) STIM2 is a feedback regulator that stabilizes basal cytosolic and endoplasmic reticulum Ca2+ levels. Cell 131:1327–1339CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Rosado JA, Diez R, Smani T, Jardín I (2015) STIM and Orai1 variants in store-operated calcium entry. Front Pharmacol 6:325PubMedPubMedCentralGoogle Scholar
  6. 6.
    Antigny F, Sabourin J, Saüc S, Bernheim L, Koenig S, Frieden M (2017) TRPC1 and TRPC4 channels functionally interact with STIM1L to promote myogenesis and maintain fast repetitive Ca2+ release in human myotubes. Biochim Biophys Acta 1864:806–813CrossRefGoogle Scholar
  7. 7.
    Horinouchi T, Higashi T, Higa T et al (2012) Different binding property of STIM1 and its novel splice variant STIM1L to Orai1, TRPC3, and TRPC6 channels. Biochem Biophys Res Commun 428:252–258CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Saüc S, Frieden M (2017) Neurological and motor disorders: TRPC in the skeletal muscle. Adv Exp Med Biol 993:557–575CrossRefGoogle Scholar
  9. 9.
    Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel SH, Tanasa B, Hogan PG, Lewis RS, Daly M, Rao A (2006) A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441:179–185CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Vig M, Beck A, Billingsley JM et al (2006) CRACM1 multimers form the ion-selective pore of the CRAC channel. Curr Biol 16:2073–2079CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Desai PN, Zhang X, Wu S, Janoshazi A, Bolimuntha S, Putney JW, Trebak M (2015) Multiple types of calcium channels arising from alternative translation initiation of the Orai1 message. Sci Signal 8:ra74CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Vaeth M, Yang J, Yamashita M et al (2017) ORAI2 modulates store-operated calcium entry and T cell-mediated immunity. Nat Commun 8:14714CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Lis A, Peinelt C, Beck A, Parvez S, Monteilh-Zoller M, Fleig A, Penner R (2007) CRACM1, CRACM2, and CRACM3 are store-operated Ca2+ channels with distinct functional properties. Curr Biol CB 17:794–800CrossRefGoogle Scholar
  14. 14.
    Mignen O, Thompson JL, Shuttleworth TJ (2008) Both Orai1 and Orai3 are essential components of the arachidonate-regulated Ca2+−selective (ARC) channels. J Physiol 586:185–195CrossRefGoogle Scholar
  15. 15.
    Gonzalez-Cobos JC, Zhang X, Zhang W et al (2013) Store-independent Orai1/3 channels activated by intracrine leukotriene C4: role in neointimal hyperplasia. Circ Res 112:1013–1025CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Ambudkar IS, de Souza LB, Ong HL (2017) TRPC1, Orai1, and STIM1 in SOCE: friends in tight spaces. Cell Calcium 63:33–39CrossRefGoogle Scholar
  17. 17.
    Avila-Medina J, Mayoral-Gonzalez I, Dominguez-Rodriguez A, Gallardo-Castillo I, Ribas J, Ordoñez A, Rosado JA, Smani T (2018) The complex role of store operated calcium entry pathways and related proteins in the function of cardiac, skeletal and vascular smooth muscle cells. Front Physiol 9:257CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Domínguez-Rodríguez A, Ruiz-Hurtado G, Sabourin J, Gómez AM, Alvarez JL, Benitah J-P (2015) Proarrhythmic effect of sustained EPAC activation on TRPC3/4 in rat ventricular cardiomyocytes. J Mol Cell Cardiol 87:74–78CrossRefGoogle Scholar
  19. 19.
    Avila-Medina J, Calderon-Sanchez E, Gonzalez-Rodriguez P, Monje-Quiroga F, Rosado JA, Castellano A, Ordonez A, Smani T (2016) Orai1 and TRPC1 proteins co-localize with CaV1.2 channels to form a signal complex in vascular smooth muscle cells. J Biol Chem 291:21148–21159CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    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
  21. 21.
    Stiber J, Hawkins A, Zhang Z-S et al (2008) STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nat Cell Biol 10:688–697CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Smani T, Shapovalov G, Skryma R, Prevarskaya N, Rosado JA (2015) Functional and physiopathological implications of TRP channels. Biochim Biophys Acta 1853:1772–1782CrossRefGoogle Scholar
  23. 23.
    Dominguez-Rodriguez A, Diaz I, Rodriguez-Moyano M, Calderon-Sanchez E, Rosado JA, Ordonez A, Smani T (2012) Urotensin-II signaling mechanism in rat coronary artery: role of STIM1 and Orai1-dependent store operated calcium influx in vasoconstriction. Arter Thromb Vasc Biol 32:1325–1332CrossRefGoogle Scholar
  24. 24.
    Rodriguez-Moyano M, Diaz I, Dionisio N, Zhang X, Avila-Medina J, Calderon-Sanchez E, Trebak M, Rosado JA, Ordonez A, Smani T (2013) Urotensin-II promotes vascular smooth muscle cell proliferation through store-operated calcium entry and EGFR transactivation. Cardiovasc Res 100:297–306CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    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
  26. 26.
    Bootman MD, Rietdorf K (2017) Tissue specificity: store-operated Ca2+ entry in cardiac myocytes. Adv Exp Med Biol 993:363–387CrossRefGoogle Scholar
  27. 27.
    Chang H-Y, Chen S-L, Shen M-R, Kung M-L, Chuang L-M, Chen Y-W (2017) Selective serotonin reuptake inhibitor, fluoxetine, impairs E-cadherin-mediated cell adhesion and alters calcium homeostasis in pancreatic beta cells. Sci Rep 7:3515CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Sabourin J, Le Gal L, Saurwein L, Haefliger J-A, Raddatz E, Allagnat F (2015) Store-operated Ca2+ entry mediated by Orai1 and TRPC1 participates to insulin secretion in rat β-cells. J Biol Chem 290:30530–30539CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Lacruz RS, Feske S (2015) Diseases caused by mutations in ORAI1 and STIM1. Ann N Y Acad Sci 1356:45–79CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Eder P (2017) Cardiac remodeling and disease: SOCE and TRPC signaling in cardiac pathology. Adv Exp Med Biol 993:505–521CrossRefGoogle Scholar
  31. 31.
    Pan Z, Brotto M, Ma J (2014) Store-operated Ca2+ entry in muscle physiology and diseases. BMB Rep 47:69–79CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Tanwar J, Trebak M, Motiani RK (2017) Cardiovascular and hemostatic disorders: role of STIM and Orai proteins in vascular disorders. Adv Exp Med Biol 993:425–452CrossRefGoogle Scholar
  33. 33.
    Hunton DL, Zou L, Pang Y, Marchase RB (2004) Adult rat cardiomyocytes exhibit capacitative calcium entry. Am J Physiol Heart Circ Physiol 286:H1124–H1132CrossRefGoogle Scholar
  34. 34.
    Kojima A, Kitagawa H, Omatsu-Kanbe M, Matsuura H, Nosaka S (2012) Presence of store-operated Ca2+ entry in C57BL/6J mouse ventricular myocytes and its suppression by sevoflurane. Br J Anaesth 109:352–360CrossRefGoogle Scholar
  35. 35.
    Uehara A, Yasukochi M, Imanaga I, Nishi M, Takeshima H (2002) Store-operated Ca2+ entry uncoupled with ryanodine receptor and junctional membrane complex in heart muscle cells. Cell Calcium 31:89–96CrossRefGoogle Scholar
  36. 36.
    Eder P, Molkentin JD (2011) TRPC channels as effectors of cardiac hypertrophy. Circ Res 108:265–272CrossRefGoogle Scholar
  37. 37.
    Bartoli F, Sabourin J (2017) Cardiac remodeling and disease: current understanding of STIM1/Orai1-mediated store-operated Ca2+ entry in cardiac function and pathology. Adv Exp Med Biol 993:523–534CrossRefGoogle Scholar
  38. 38.
    Yue Z, Xie J, Yu AS, Stock J, Du J, Yue L (2015) Role of TRP channels in the cardiovascular system. Am J Physiol Heart Circ Physiol 308:H157–H182CrossRefGoogle Scholar
  39. 39.
    Ljubojevic S, Radulovic S, Leitinger G et al (2014) Early remodeling of perinuclear Ca2+ stores and nucleoplasmic Ca2+ signaling during the development of hypertrophy and heart failure. Circulation 130:244–255CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Samak M, Fatullayev J, Sabashnikov A et al (2016) Cardiac hypertrophy: an introduction to molecular and cellular basis. Med Sci Monit Basic Res 22:75–79CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    McMullen JR, Jennings GL (2007) Differences between pathological and physiological cardiac hypertrophy: novel therapeutic strategies to treat heart failure. Clin Exp Pharmacol Physiol 34:255–262CrossRefGoogle Scholar
  42. 42.
    Collins HE, Zhu-Mauldin X, Marchase RB, Chatham JC (2013) STIM1/Orai1-mediated SOCE: current perspectives and potential roles in cardiac function and pathology. Am J Physiol Heart Circ Physiol 305:H446–H458CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Hulot J-S, Fauconnier J, Ramanujam D et al (2011) Critical role for stromal interaction molecule 1 in cardiac hypertrophy. Circulation 124:796–805CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Voelkers M, Salz M, Herzog N et al (2010) Orai1 and Stim1 regulate normal and hypertrophic growth in cardiomyocytes. J Mol Cell Cardiol 48:1329–1334CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Parks C, Alam MA, Sullivan R, Mancarella S (2016) STIM1-dependent Ca2+ microdomains are required for myofilament remodeling and signaling in the heart. Sci Rep 6:25372CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Luo X, Hojayev B, Jiang N, Wang ZV, Tandan S, Rakalin A, Rothermel BA, Gillette TG, Hill JA (2012) STIM1-dependent store-operated Ca2+ entry is required for pathological cardiac hypertrophy. J Mol Cell Cardiol 52:136–147CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Camacho Londoño JE, Tian Q, Hammer K et al (2015) A background Ca2+ entry pathway mediated by TRPC1/TRPC4 is critical for development of pathological cardiac remodelling. Eur Heart J 36:2257–2266CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Seth M, Zhang Z-S, Mao L et al (2009) TRPC1 channels are critical for hypertrophic signaling in the heart. Circ Res 105:1023–1030CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Bush EW, Hood DB, Papst PJ, Chapo JA, Minobe W, Bristow MR, Olson EN, McKinsey TA (2006) Canonical transient receptor potential channels promote cardiomyocyte hypertrophy through activation of calcineurin signaling. J Biol Chem 281:33487–33496CrossRefGoogle Scholar
  50. 50.
    Kuwahara K, Wang Y, McAnally J, Richardson JA, Bassel-Duby R, Hill JA, Olson EN (2006) TRPC6 fulfills a calcineurin signaling circuit during pathologic cardiac remodeling. J Clin Invest 116:3114–3126CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Horton JS, Buckley CL, Alvarez EM, Schorlemmer A, Stokes AJ (2014) The calcium release-activated calcium channel Orai1 represents a crucial component in hypertrophic compensation and the development of dilated cardiomyopathy. Channels Austin Tex 8:35–48CrossRefGoogle Scholar
  52. 52.
    Correll RN, Goonasekera SA, van Berlo JH et al (2015) STIM1 elevation in the heart results in aberrant Ca2+ handling and cardiomyopathy. J Mol Cell Cardiol 87:38–47CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Bénard L, Oh JG, Cacheux M et al (2016) Cardiac Stim1 silencing impairs adaptive hypertrophy and promotes heart failure through inactivation of mTORC2/Akt signaling. Circulation 133:1458–1471; discussion 1471CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    House SJ, Potier M, Bisaillon J, Singer HA, Trebak M (2008) The non-excitable smooth muscle: calcium signaling and phenotypic switching during vascular disease. Pflugers Arch 456:769–785CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Bisaillon JM, Motiani RK, Gonzalez-Cobos JC, Potier M, Halligan KE, Alzawahra WF, Barroso M, Singer HA, Jourd’heuil D, Trebak M (2010) Essential role for STIM1/Orai1-mediated calcium influx in PDGF-induced smooth muscle migration. Am J Physiol Cell Physiol 298:C993–C1005CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Giachini FR, Chiao CW, Carneiro FS, Lima VV, Carneiro ZN, Dorrance AM, Tostes RC, Webb RC (2009) Increased activation of stromal interaction molecule-1/Orai-1 in aorta from hypertensive rats: a novel insight into vascular dysfunction. Hypertension 53:409–416CrossRefGoogle Scholar
  57. 57.
    Kassan M, Ait-Aissa K, Radwan E et al (2016) Essential role of smooth muscle STIM1 in hypertension and cardiovascular dysfunction. Arter Thromb Vasc Biol 36:1900–1909CrossRefGoogle Scholar
  58. 58.
    Simo-Cheyou ER, Tan JJ, Grygorczyk R, Srivastava AK (2017) STIM-1 and ORAI-1 channel mediate angiotensin-II-induced expression of Egr-1 in vascular smooth muscle cells. J Cell Physiol 232:3496–3509CrossRefGoogle Scholar
  59. 59.
    Guo RW, Yang LX, Li MQ, Pan XH, Liu B, Deng YL (2012) Stim1- and Orai1-mediated store-operated calcium entry is critical for angiotensin II-induced vascular smooth muscle cell proliferation. Cardiovasc Res 93:360–370CrossRefGoogle Scholar
  60. 60.
    Mancarella S, Potireddy S, Wang Y et al (2013) Targeted STIM deletion impairs calcium homeostasis, NFAT activation, and growth of smooth muscle. FASEB J 27:893–906CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Zhang W, Trebak M (2014) Vascular balloon injury and intraluminal administration in rat carotid artery. J Vis Exp.  https://doi.org/10.3791/52045
  62. 62.
    Zhang W, Halligan KE, Zhang X et al (2011) Orai1-mediated I (CRAC) is essential for neointima formation after vascular injury. Circ Res 109:534–542CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Guo RW, Wang H, Gao P, Li MQ, Zeng CY, Yu Y, Chen JF, Song MB, Shi YK, Huang L (2009) An essential role for stromal interaction molecule 1 in neointima formation following arterial injury. Cardiovasc Res 81:660–668CrossRefGoogle Scholar
  64. 64.
    Jardin I, Albarrán L, Bermejo N, Salido GM, Rosado JA (2012) Homers regulate calcium entry and aggregation in human platelets: a role for Homers in the association between STIM1 and Orai1. Biochem J 445:29–38CrossRefGoogle Scholar
  65. 65.
    Jia S, Rodriguez M, Williams AG, Yuan JP (2017) Homer binds to Orai1 and TRPC channels in the neointima and regulates vascular smooth muscle cell migration and proliferation. Sci Rep 7:5075CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Pulina MV, Zulian A, Berra-Romani R, Beskina O, Mazzocco-Spezzia A, Baryshnikov SG, Papparella I, Hamlyn JM, Blaustein MP, Golovina VA (2010) Upregulation of Na+ and Ca2+ transporters in arterial smooth muscle from ouabain-induced hypertensive rats. Am J Physiol Heart Circ Physiol 298:H263–H274CrossRefGoogle Scholar
  67. 67.
    Souza Bomfim GH, Mendez-Lopez I, Arranz-Tagarro JA, Ferraz Carbonel AA, Roman-Campos D, Padin JF, Garcia AG, Jurkiewicz A, Jurkiewicz NH (2017) Functional upregulation of STIM-1/Orai-1-mediated store-operated Ca2+ contributing to the hypertension development elicited by chronic EtOH consumption. Curr Vasc Pharmacol 15:265–281CrossRefGoogle Scholar
  68. 68.
    Lin MJ, Leung GP, Zhang WM, Yang XR, Yip KP, Tse CM, Sham JS (2004) Chronic hypoxia-induced upregulation of store-operated and receptor-operated Ca2+ channels in pulmonary arterial smooth muscle cells: a novel mechanism of hypoxic pulmonary hypertension. Circ Res 95:496–505CrossRefGoogle Scholar
  69. 69.
    Zhang S, Patel HH, Murray F, Remillard CV, Schach C, Thistlethwaite PA, Insel PA, Yuan JX (2007) Pulmonary artery smooth muscle cells from normal subjects and IPAH patients show divergent cAMP-mediated effects on TRPC expression and capacitative Ca2+ entry. Am J Physiol Lung Cell Mol Physiol 292:L1202–L1210CrossRefGoogle Scholar
  70. 70.
    Ogawa A, Firth AL, Smith KA, Maliakal MV, Yuan JX (2012) PDGF enhances store-operated Ca2+ entry by upregulating STIM1/Orai1 via activation of Akt/mTOR in human pulmonary arterial smooth muscle cells. Am J Physiol Cell Physiol 302:C405–C411CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Hou X, Chen J, Luo Y, Liu F, Xu G, Gao Y (2013) Silencing of STIM1 attenuates hypoxia-induced PASMCs proliferation via inhibition of the SOC/Ca2+/NFAT pathway. Respir Res 14:2CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Fernandez RA, Wan J, Song S, Smith KA, Gu Y, Tauseef M, Tang H, Makino A, Mehta D, Yuan JX (2015) Upregulated expression of STIM2, TRPC6, and Orai2 contributes to the transition of pulmonary arterial smooth muscle cells from a contractile to proliferative phenotype. Am J Physiol Cell Physiol 308:C581–C593CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Wang J, Xu C, Zheng Q, Yang K, Lai N, Wang T, Tang H, Lu W (2017) Orai1, 2, 3 and STIM1 promote store-operated calcium entry in pulmonary arterial smooth muscle cells. Cell Death Discov 3:17074CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    He X, Song S, Ayon RJ, Balisterieri A, Black SM, Makino A, Wier WG, Zang WJ, Yuan JX (2018) Hypoxia selectively upregulates cation channels and increases cytosolic [Ca2+] in pulmonary, but not coronary, arterial smooth muscle cells. Am J Physiol Cell Physiol.  https://doi.org/10.1152/ajpcell.00272.2017
  75. 75.
    Dirksen RT (2009) Checking your SOCCs and feet: the molecular mechanisms of Ca2+ entry in skeletal muscle. J Physiol 587:3139–3147CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Stiber JA, Rosenberg PB (2011) The role of store-operated calcium influx in skeletal muscle signaling. Cell Calcium 49:341–349CrossRefGoogle Scholar
  77. 77.
    Sztretye M, Geyer N, Vincze J et al (2017) SOCE is important for maintaining sarcoplasmic calcium content and release in skeletal muscle fibers. Biophys J 113:2496–2507CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Edwards JN, Friedrich O, Cully TR, von Wegner F, Murphy RM, Launikonis BS (2010) Upregulation of store-operated Ca2+ entry in dystrophic mdx mouse muscle. Am J Physiol Cell Physiol 299:C42–C50CrossRefGoogle Scholar
  79. 79.
    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
  80. 80.
    Allen DG, Lamb GD, Westerblad H (2008) Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88:287–332CrossRefGoogle Scholar
  81. 81.
    Li T, Finch EA, Graham V, Zhang Z-S, Ding J-D, Burch J, Oh-hora M, Rosenberg P (2012) STIM1-Ca2+ signaling is required for the hypertrophic growth of skeletal muscle in mice. Mol Cell Biol 32:3009–3017CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Darbellay B, Arnaudeau S, König 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 284:5370–5380CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Oláh 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 49:415–425CrossRefGoogle Scholar
  84. 84.
    Antigny F, Koenig S, Bernheim L, Frieden M (2013) During post-natal human myogenesis, normal myotube size requires TRPC1- and TRPC4-mediated Ca2+ entry. J Cell Sci 126:2525–2533CrossRefGoogle Scholar
  85. 85.
    Xia L, Cheung K-K, 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
  86. 86.
    Böhm J, Chevessier F, Koch C et al (2014) Clinical, histological and genetic characterisation of patients with tubular aggregate myopathy caused by mutations in STIM1. J Med Genet 51:824–833CrossRefGoogle Scholar
  87. 87.
    Goonasekera SA, Davis J, Kwong JQ, Accornero F, Wei-LaPierre L, Sargent MA, Dirksen RT, Molkentin JD (2014) Enhanced Ca2+ influx from STIM1-Orai1 induces muscle pathology in mouse models of muscular dystrophy. Hum Mol Genet 23:3706–3715CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Brandsema JF, Darras BT (2015) Dystrophinopathies. Semin Neurol 35:369–384CrossRefGoogle Scholar
  89. 89.
    Kiviluoto S, Decuypere J-P, De Smedt H, Missiaen L, Parys JB, Bultynck G (2011) STIM1 as a key regulator for Ca2+ homeostasis in skeletal-muscle development and function. Skelet Muscle 1:16CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Vandebrouck C, Martin D, Schoor MC-V, 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
  91. 91.
    Cully TR, Edwards JN, Friedrich O, Stephenson DG, Murphy RM, Launikonis BS (2012) Changes in plasma membrane Ca-ATPase and stromal interacting molecule 1 expression levels for Ca2+ signaling in dystrophic mdx mouse muscle. Am J Physiol Cell Physiol 303:C567–C576CrossRefGoogle Scholar
  92. 92.
    Cully TR, Launikonis BS (2013) Store-operated Ca2+ entry is not required for store refilling in skeletal muscle. Clin Exp Pharmacol Physiol 40:338–344CrossRefGoogle Scholar
  93. 93.
    Shirokova N, Niggli E (2013) Cardiac phenotype of duchenne muscular dystrophy: insights from cellular studies. J Mol Cell Cardiol 58:217–224CrossRefGoogle Scholar
  94. 94.
    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
  95. 95.
    Fraisl P, Mazzone M, Schmidt T, Carmeliet P (2009) Regulation of angiogenesis by oxygen and metabolism. Dev Cell 16:167–179CrossRefGoogle Scholar
  96. 96.
    Stapor P, Wang X, Goveia J, Moens S, Carmeliet P (2014) Angiogenesis revisited – role and therapeutic potential of targeting endothelial metabolism. J Cell Sci 127:4331–4341CrossRefGoogle Scholar
  97. 97.
    Egginton S (2009) Invited review: activity-induced angiogenesis. Pflugers Arch 457:963–977CrossRefGoogle Scholar
  98. 98.
    Logsdon EA, Finley SD, Popel AS, Mac Gabhann F (2014) A systems biology view of blood vessel growth and remodelling. J Cell Mol Med 18:1491–1508CrossRefGoogle Scholar
  99. 99.
    Ingason AB, Goldstone AB, Paulsen MJ, Thakore AD, Truong VN, Edwards BB, Eskandari A, Bollig T, Steele AN, Woo YJ (2018) Angiogenesis precedes cardiomyocyte migration in regenerating mammalian hearts. J Thorac Cardiovasc Surg 155:1118–1127.e1CrossRefGoogle Scholar
  100. 100.
    Reddy K, Khaliq A, Henning RJ (2015) Recent advances in the diagnosis and treatment of acute myocardial infarction. World J Cardiol 7:243–276CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Melly L, Cerino G, Frobert A et al (2018) Myocardial infarction stabilization by cell-based expression of controlled vascular endothelial growth factor levels. J Cell Mol Med.  https://doi.org/10.1111/jcmm.13511
  102. 102.
    Li J, Cubbon RM, Wilson LA et al (2011) Orai1 and CRAC channel dependence of VEGF-activated Ca2+ entry and endothelial tube formation. Circ Res 108:1190–1198CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    Folkman J (1971) Tumor angiogenesis: therapeutic implications. N Engl J Med 285:1182–1186CrossRefGoogle Scholar
  104. 104.
    Kohn EC, Alessandro R, Spoonster J, Wersto RP, Liotta LA (1995) Angiogenesis: role of calcium-mediated signal transduction. Proc Natl Acad Sci U S A 92:1307–1311CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Chen Y-F, Hsu K-F, Shen M-R (2016) The store-operated Ca2+ entry-mediated signaling is important for cancer spread. Biochim Biophys Acta 1863:1427–1435CrossRefGoogle Scholar
  106. 106.
    Chen Y-F, Chiu W-T, Chen Y-T, Lin P-Y, Huang H-J, Chou C-Y, Chang H-C, Tang M-J, Shen M-R (2011) Calcium store sensor stromal-interaction molecule 1-dependent signaling plays an important role in cervical cancer growth, migration, and angiogenesis. Proc Natl Acad Sci U S A 108:15225–15230CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Fiorio Pla A, Gkika D (2013) Emerging role of TRP channels in cell migration: from tumor vascularization to metastasis. Front Physiol 4:311CrossRefPubMedPubMedCentralGoogle Scholar
  108. 108.
    Martial S (2016) Involvement of ion channels and transporters in carcinoma angiogenesis and metastasis. Am J Physiol Cell Physiol 310:C710–C727CrossRefGoogle Scholar
  109. 109.
    Dragoni S, Laforenza U, Bonetti E et al (2011) Vascular endothelial growth factor stimulates endothelial colony forming cells proliferation and tubulogenesis by inducing oscillations in intracellular Ca2+ concentration. Stem Cells Dayt Ohio 29:1898–1907CrossRefGoogle Scholar
  110. 110.
    Li J, Bruns A-F, Hou B et al (2015) Orai3 surface accumulation and calcium entry evoked by vascular endothelial growth factor. Arterioscler Thromb Vasc Biol 35:1987–1994CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    Earley S, Brayden JE (2015) Transient receptor potential channels in the vasculature. Physiol Rev 95:645–690CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Antigny F, Girardin N, Frieden M (2012) Transient receptor potential canonical channels are required for in vitro endothelial tube formation. J Biol Chem 287:5917–5927CrossRefGoogle Scholar
  113. 113.
    Schmidt K, Dubrovska G, Nielsen G et al (2010) Amplification of EDHF-type vasodilatations in TRPC1-deficient mice. Br J Pharmacol 161:1722–1733CrossRefPubMedPubMedCentralGoogle Scholar
  114. 114.
    Sánchez-Hernández Y, Laforenza U, Bonetti E et al (2010) Store-operated Ca2+ entry is expressed in human endothelial progenitor cells. Stem Cells Dev 19:1967–1981CrossRefGoogle Scholar
  115. 115.
    Lodola F, Laforenza U, Bonetti E et al (2012) Store-operated Ca2+ entry is remodelled and controls in vitro angiogenesis in endothelial progenitor cells isolated from tumoral patients. PLoS One 7:e42541CrossRefPubMedPubMedCentralGoogle Scholar
  116. 116.
    Moccia F, Poletto V (2015) May the remodeling of the Ca2+ toolkit in endothelial progenitor cells derived from cancer patients suggest alternative targets for anti-angiogenic treatment? Biochim Biophys Acta 1853:1958–1973CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Javier Avila-Medina
    • 1
    • 2
  • Isabel Mayoral-González
    • 1
    • 2
    • 3
  • Isabel Galeano-Otero
    • 1
    • 2
  • Pedro C. Redondo
    • 4
  • Juan A. Rosado
    • 4
  • Tarik Smani
    • 1
    • 2
    • 5
    Email author
  1. 1.Department of Medical Physiology and BiophysicsUniversity of SevilleSevillaSpain
  2. 2.Institute of Biomedicine of Seville (IBiS)University Hospital of Virgen del Rocío/CSIC/University of SevilleSevillaSpain
  3. 3.Department of SurgeryUniversity of SevilleSevillaSpain
  4. 4.Department of Physiology, Cell Physiology Research Group and Institute of Molecular Pathology BiomarkersUniversity of ExtremaduraCáceresSpain
  5. 5.CIBERCVMadridSpain

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