Inositol 1,4,5 trisphosphate receptor 1 is a key player of human myoblast differentiation

Cell Calcium

Volumn 56, Issue 6, 2014, Pages 513-521

  Antigny, Fabrice ^a   Konig, Stéphane ^a   Bernheim, Laurent ^a   Frieden, Maud ^a  

^a Geneva Medical Center   (Switzerland)

Author keywords

Calcium channel; Calcium signaling; Inositol 1,4,5 trisphosphate receptor; Myogenesis; Skeletal muscle

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM ION; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; MYOCYTE ENHANCER FACTOR 2; MYOGENIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NFAT; CALCIUM; ITPR1 PROTEIN, HUMAN;

ARTICLE; CALCIUM TRANSPORT; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; MUSCLE DEVELOPMENT; MYOBLAST; MYOTUBE; PROTEIN EXPRESSION; PROTEIN FUNCTION; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; GENETICS; PHYSIOLOGY;

CALCIUM; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL DIFFERENTIATION; CELLS, CULTURED; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; MEF2 TRANSCRIPTION FACTORS; MYOBLASTS, SKELETAL; MYOGENIN; NFATC TRANSCRIPTION FACTORS; RNA, SMALL INTERFERING;

EID: 84922285784     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2014.10.014     Document Type: Article

References (52)

1. Bernheim L., Bader C.R. Human myoblast differentiation: Ca(2+) channels are activated by K(+) channels. News Physiol. Sci. 2002, 17:22-26.
2. Arnaudeau S., Holzer N., Konig S., Bader C.R., Bernheim L. Calcium sources used by post-natal human myoblasts during initial differentiation. J. Cell. Physiol. 2006, 208:435-445.
3. Molkentin J.D., Olson E.N. Defining the regulatory networks for muscle development. Curr. Opin. Genet. Dev. 1996, 6:445-453.
4. Black B.L., Olson E.N. Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. Annu. Rev. Cell Dev. Biol. 1998, 14:167-196.
5. Konig S., Beguet A., Bader C.R., Bernheim L. The calcineurin pathway links hyperpolarization (Kir2.1)-induced Ca2+ signals to human myoblast differentiation and fusion. Development 2006, 133:3107-3114.
6. Stiber J.A., Tabatabaei N., Hawkins A.F., et al. Homer modulates NFAT-dependent signaling during muscle differentiation. Dev. Biol. 2005, 287:213-224.
7. Tamir Y., Bengal E. Phosphoinositide 3-kinase induces the transcriptional activity of MEF2 proteins during muscle differentiation. J. Biol. Chem. 2000, 275:34424-34432.
8. Chin E.R. The role of calcium and calcium/calmodulin-dependent kinases in skeletal muscle plasticity and mitochondrial biogenesis. Proc. Nutr. Soc. 2004, 63:279-286.
9. Stiber J.A., Rosenberg P.B. The role of store-operated calcium influx in skeletal muscle signaling. Cell Calcium 2011, 49:341-349.
10. Darbellay B., Arnaudeau S., Konig S., et al. STIM1- and Orai1-dependent store-operated calcium entry regulates human myoblast differentiation. J. Biol. Chem. 2009, 284:5370-5380.
11. Stiber J., Hawkins A., Zhang Z.S., et al. STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nat. Cell Biol. 2008, 10:688-697.
12. Darbellay B., Arnaudeau S., Ceroni D., Bader C.R., Konig S., Bernheim L. Human muscle economy myoblast differentiation and excitation-contraction coupling use the same molecular partners, STIM1 and STIM2. J. Biol. Chem. 2010, 285:22437-22447.
13. Antigny F., Koenig S., Bernheim L., Frieden M. During post-natal human myogenesis, normal myotube size requires TRPC1- and TRPC4-mediated Ca(2)(+) entry. J. Cell Sci. 2013, 126:2525-2533.
14. Taylor C.W., Genazzani A.A., Morris S.A. Expression of inositol trisphosphate receptors. Cell Calcium 1999, 26:237-251.
15. Antigny F., Norez C., Cantereau A., Becq F., Vandebrouck C. Abnormal spatial diffusion of Ca2+ in F508del-CFTR airway epithelial cells. Respir. Res. 2008, 9:70.
16. Lock J.T., Sinkins W.G., Schilling W.P. Protein S-glutathionylation enhances Ca2+-induced Ca2+ release via the IP3 receptor in cultured aortic endothelial cells. J. Physiol. 2012.
17. Horn T., Ullrich N.D., Egger M. 'Eventless' InsP3-dependent SR-Ca2+ release affecting atrial Ca2+ sparks. J. Physiol. 2013, 591:2103-2111.
18. Murray B.E., Ohlendieck K. Cross-linking analysis of the ryanodine receptor and alpha1-dihydropyridine receptor in rabbit skeletal muscle triads. Biochem. J. 1997, 324(Pt 2):689-696.
19. Wingertzahn M.A., Ochs R.S. Changes in ryanodine receptor-mediated calcium release during skeletal muscle differentiation. Proc. Soc. Exp. Biol. Med. 1999, 221:234-241.
20. Araya R., Riquelme M.A., Brandan E., Saez J.C. The formation of skeletal muscle myotubes requires functional membrane receptors activated by extracellular ATP. Brain Res. Brain Res. Rev. 2004, 47:174-188.
21. Moschella M.C., Watras J., Jayaraman T., Marks A.R. Inositol 1,4,5-trisphosphate receptor in skeletal muscle: differential expression in myofibres. J. Muscle Res. Cell Motil. 1995, 16:390-400.
22. Jaimovich E., Reyes R., Liberona J.L., Powell J.A. IP(3) receptors, IP(3) transients, and nucleus-associated Ca(2+) signals in cultured skeletal muscle. Am. J. Physiol. Cell Physiol. 2000, 278:C998-C1010.
23. Araya R., Liberona J.L., Cardenas J.C., et al. Dihydropyridine receptors as voltage sensors for a depolarization-evoked, IP3R-mediated, slow calcium signal in skeletal muscle cells. J. Gen. Physiol. 2003, 121:3-16.
24. Valdes J.A., Gaggero E., Hidalgo J., Leal N., Jaimovich E., Carrasco M.A. NFAT activation by membrane potential follows a calcium pathway distinct from other activity-related transcription factors in skeletal muscle cells. Am. J. Physiol. Cell Physiol. 2008, 294:C715-C725.
25. Mondin L., Balghi H., Constantin B., Cognard C., Sebille S. Negative modulation of inositol 1,4,5-trisphosphate type 1 receptor expression prevents dystrophin-deficient muscle cells death. Am. J. Physiol. Cell Physiol. 2009, 297:C1133-C1145.
26. Tjondrokoesoemo A., Li N., Lin P.H., et al. Type 1 inositol (1,4,5)-trisphosphate receptor activates ryanodine receptor 1 to mediate calcium spark signaling in adult mammalian skeletal muscle. J. Biol. Chem. 2013, 288:2103-2109.
27. Blaauw B., Del Piccolo P., Rodriguez L., et al. No evidence for inositol 1,4,5-trisphosphate-dependent Ca2+ release in isolated fibers of adult mouse skeletal muscle. J. Gen. Physiol. 2012, 140:235-241.
28. Parker A.K., Gergely F.V., Taylor C.W. Targeting of inositol 1,4,5-trisphosphate receptors to the endoplasmic reticulum by multiple signals within their transmembrane domains. J. Biol. Chem. 2004, 279:23797-23805.
29. Baroffio A., Hamann M., Bernheim L., Bochaton-Piallat M.L., Gabbiani G., Bader C.R. Identification of self-renewing myoblasts in the progeny of single human muscle satellite cells. Differentiation 1996, 60:47-57.
30. Poburko D., Liao C.H., van Breemen C., Demaurex N. Mitochondrial regulation of sarcoplasmic reticulum Ca2+ content in vascular smooth muscle cells. Circ. Res. 2009, 104:104-112.
31. Antigny F., Jousset H., Konig S., Frieden M. Thapsigargin activates Ca(2)+ entry both by store-dependent, STIM1/Orai1-mediated, and store-independent, TRPC3/PLC/PKC-mediated pathways in human endothelial cells. Cell Calcium 2011, 49:115-127.
32. Vandesompele J., De Preter K., Pattyn F., et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3. research0034.1-research0034.11.
33. Konig S., Hinard V., Arnaudeau S., et al. Membrane hyperpolarization triggers myogenin and myocyte enhancer factor-2 expression during human myoblast differentiation. J. Biol. Chem. 2004, 279:28187-28196.
34. Bassel-Duby R., Olson E.N. Signaling pathways in skeletal muscle remodeling. Annu. Rev. Biochem. 2006, 75:19-37.
35. Ryten M., Yang S.Y., Dunn P.M., Goldspink G., Burnstock G. Purinoceptor expression in regenerating skeletal muscle in the mdx mouse model of muscular dystrophy and in satellite cell cultures. FASEB J. 2004, 18:1404-1406.
36. Adebiyi A., Zhao G., Narayanan D., Thomas-Gatewood C.M., Bannister J.P., Jaggar J.H. Isoform-selective physical coupling of TRPC3 channels to IP3 receptors in smooth muscle cells regulates arterial contractility. Circ. Res. 2010, 106:1603-1612.
37. Adebiyi A., Narayanan D., Jaggar J.H. Caveolin-1 assembles type 1 inositol 1,4,5-trisphosphate receptors and canonical transient receptor potential 3 channels into a functional signaling complex in arterial smooth muscle cells. J. Biol. Chem. 2011, 286:4341-4348.
38. Boulay G., Brown D.M., Qin N., et al. Modulation of Ca(2+) entry by polypeptides of the inositol 1,4,5-trisphosphate receptor (IP3R) that bind transient receptor potential (TRP): evidence for roles of TRP and IP3R in store depletion-activated Ca(2+) entry. Proc. Natl. Acad. Sci. 1999, 96:14955-14960.
39. Kiselyov K., Mignery G.A., Zhu M.X., Muallem S. The N-terminal domain of the IP3 receptor gates store-operated hTrp3 channels. Mol. Cell 1999, 4:423-429.
40. Dolmetsch R.E., Lewis R.S., Goodnow C.C., Healy J.I. Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature 1997, 386:855-858.
41. Lewis R.S. Calcium oscillations in T-cells: mechanisms and consequences for gene expression. Biochem. Soc. Trans. 2003, 31:925-929.
42. Quintana A., Griesemer D., Schwarz E.C., Hoth M. Calcium-dependent activation of T-lymphocytes. Pflugers Arch. 2005, 450:1-12.
43. Borodinsky L.N., Root C.M., Cronin J.A., Sann S.B., Gu X., Spitzer N.C. Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. Nature 2004, 429:523-530.
44. Ferreira-Martins J., Rondon-Clavo C., Tugal D., et al. Spontaneous calcium oscillations regulate human cardiac progenitor cell growth. Circ. Res. 2009, 105:764-774.
45. Tu M.K., Borodinsky L.N. Spontaneous calcium transients manifest in the regenerating muscle and are necessary for skeletal muscle replenishment. Cell Calcium 2014, 56:34-41.
46. Louis M., Zanou N., Van Schoor M., Gailly P. TRPC1 regulates skeletal myoblast migration and differentiation. J. Cell Sci. 2008, 121:3951-3959.
47. Sabourin J., Lamiche C., Vandebrouck A., et al. Regulation of TRPC1 and TRPC4 cation channels requires an alpha1-syntrophin-dependent complex in skeletal mouse myotubes. J. Biol. Chem. 2009, 284:36248-36261.
48. Vandebrouck A., Sabourin J., Rivet J., et al. Regulation of capacitative calcium entries by alpha1-syntrophin: association of TRPC1 with dystrophin complex and the PDZ domain of alpha1-syntrophin. FASEB J. 2007, 21:608-617.
49. Yuan J.P., Kim M.S., Zeng W., et al. TRPC channels as STIM1-regulated SOCs. Channels 2009, 3:221-225.
50. Zeng W., Yuan J.P., Kim M.S., et al. STIM1 gates TRPC channels, but not Orai1, by electrostatic interaction. Mol Cell. 2008, 32:439-448.
51. Cheng K.T., Ong H.L., Liu X., Ambudkar I.S. Contribution and regulation of TRPC channels in store-operated Ca(2+) entry. Curr. Top. Membr. 2013, 71:149-179.
52. Ambudkar I.S. TRPC1: a core component of store-operated calcium channels. Biochem. Soc. Trans. 2007, 35:96-100.