The formation of skeletal muscle myotubes requires functional membrane receptors activated by extracellular ATP

Brain Research Reviews

Volumn 47, Issue 1-3, 2004, Pages 174-188

  Araya, Roberto ^a   Riquelme, Manuel A ^a   Brandan, Enrique ^a   Sáez, Juan C ^a,b  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

C 2C12 cells; Cell differentiation and migration; Development and regeneration; MyoD; Myogenin; Myotubes; P2 receptors; Terminal differentiation

Indexed keywords

ADENOSINE TRIPHOSPHATE; APYRASE; CREATINE KINASE; ETHIDIUM BROMIDE; LUCIFER YELLOW; MEMBRANE RECEPTOR; MYOGENIN; PURINE P2X RECEPTOR; PURINE P2X7 RECEPTOR; PURINE P2Y RECEPTOR; PURINERGIC RECEPTOR BLOCKING AGENT; RECEPTOR BLOCKING AGENT; SURAMIN; XESTOSPONGIN C;

CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL CYCLE; CELL DIFFERENTIATION; CELL FUSION; CELL MIGRATION; CONFERENCE PAPER; ENZYME ACTIVITY; ENZYME ANALYSIS; FLUORESCENCE; GAP JUNCTION; IMMUNOFLUORESCENCE; MUSCLE DEVELOPMENT; MYOBLAST; MYOTUBE; NONHUMAN; NORTHERN BLOTTING; ONTOGENY; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SKELETAL MUSCLE; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL DIFFERENTIATION; CELL LINE; EXTRACELLULAR FLUID; FLUORESCENT DYES; GAP JUNCTIONS; INTRACELLULAR FLUID; MICE; MUSCLE FIBERS; MUSCLE, SKELETAL; MYOGENIN; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, PURINERGIC P2; SARCOLEMMA;

EID: 9644269169     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresrev.2004.06.003     Document Type: Conference Paper

References (112)

1. Adi S., Bin-Abbas B., Wu N.Y., Rosenthal S.M. Early stimulation and late inhibition of extracellular signal-regulated kinase 1/2 phosphorylation by IGF-I: a potential mechanism mediating the switch in IGF-I action on skeletal muscle differentiation. Endocrinology. 143:2002;511-516
2. Anastasi S., Giordano S., Sthandier O., Gambarotta G., Maione R., Comoglio P., Amati P. A natural hepatocyte growth factor/scatter factor autocrine loop in myoblast cells and the effect of the constitutive Met kinase activation on myogenic differentiation. J. Cell Biol. 137:1997;1057-1068
3. Andrés V., Walsh K. Myogenin expression, cell cycle withdrawal, and phenotypic differentiation are temporally separable events that precede cell fusion upon myogenesis. J. Cell Biol. 132:1996;657-666
4. Araya R., Brandan E., Sáez J.C. P2 receptor blockade reduces gap junctional communication and inhibits differentiation and fusion of skeletal muscle myoblast. Mol. Biol. Cell. 11:2000;S113a
5. 3R-mediated, slow calcium signal in skeletal muscle cells. J. Gen. Physiol. 121:2003;3-16
6. Araya R., Eckardt D., Riquelme M.A., Willecke K., Sáez J.C. Presence and importance of connexin43 during myogenesis. Cell Commun. Adhes. 10:2003;451-456
7. Augustine J.A., Secrist J.P., Daniels J.K., Leibson J., Abraham R.T. Signal transduction through the T cell antigen receptor. Activation of phospholipase C through a G protein-independent coupling mechanism. J. Immunol. 146:1991;2889-2897
8. Balogh S., Naus C.G., Merrifield P.A. Expression of gap junctions in culture rat L6 cells during myogenesis. Dev. Biol. 155:1993;351-360
9. Bernheim L., Liu J.H., Hamann M., Haenggeli C.A., Fischer-Lougheed J., Bader C.R. Contribution of a non-inactivating potassium current to the resting membrane potential of fusion-competent human myoblasts. J. Physiol. 493:1996;129-141
10. + current, Ih-eag, contributes to the hyperpolarization of human fusion-competent myoblasts. J. Physiol. 512:1998;317-323
11. 2+ signaling during terminal differentiation (fusion) of human myoblasts. Proc. Natl. Acad. Sci. U. S. A. 97:2000;7627-7632
12. Bisaggio R.D., Nihei O.K., Persechini P.M., Savino W., Alves L.A. Characterization of P2 receptors in thymic epithelial cells. Cell. Mol. Biol. 47:2001;19-31
13. Bo X., Schoepfer R., Burnstock G. Molecular cloning and characterization of a novel ATP P2X receptor subtype from embryonic chick skeletal muscle. J. Biol. Chem. 275:2000;14401-14407
14. Borneman A., Kuschel R., Fujisawa-Sehara A. Analysis for transcript expression of meltrin alpha in normal, regenerating, and denervated rat muscle. J. Muscle Res. Cell Motil. 21:2000;475-480
15. Brunetti A., Goldfine I.D. Role of myogenin in myoblast differentiation and its regulation by fibroblast growth factor. J. Biol. Chem. 265:1990;5960-5963
16. Buck E.D., Nguyen H.T., Pessah I.N., Allen P.D. Dyspedic mouse skeletal muscle express major elements of the triadic junction but lacks detectable ryanodine receptor protein function. J. Biol. Chem. 272:1997;7360-7367
17. 3 metabolism during skeletal muscle development in vivo and in vitro. Comp. Biochem. Physiol. 116:1997;173-181
18. Chamberlain J.S., Jaynes J.B., Hauschka S.D. Regulation of creatine kinase induction in differentiating mouse myoblast. Mol. Cell. Biol. 5:1985;484-492
19. Changeux J.P. Compartmentalized transcription of acetylcholine receptor genes during motor endplate epigenesis. New Biol. 3:1991;413-429
20. Cheng Z.Q., Adi S., Wu N.Y., Hsiao D., Woo E.J., Filvaroff E.H., Gustafson T.A., Rosenthal S.M. Functional inactivation of the IGF-I receptor delays differentiation of skeletal muscle cells. J. Endocrinol. 167:2000;175-182
21. Collet C., Strube C., Csernoch L., Mallouk N., Ojeda C., Allard B., Jacquemond V. Effects of extracellular ATP on freshly isolated mouse skeletal muscle cells during pre-natal and postnatal development. Pflügers Arch. 443:2002;771-778
22. Colomar A., Amedee T. ATP stimulation of P2X(7) receptors activates three different ionic conductances on cultures mouse Schwann cells. Eur. J. Neurosci. 14:2001;927-936
23. Constantin B., Cronier L. Involvement of gap junctional communication in myogenesis. Int. Rev. Cytol. 196:2000;1-65
24. Copello J.A., Qi Y., Jeyakumar L.H., Ogunbunmi E., Fleischer S. Lack of effect of cADPribose and NAADP on the activity of skeletal muscle and heart ryanodine receptors. Cell Calcium. 30:2001;269-284
25. Cox P.G., Gunter M. The effect of calcium ion concentration on myotube formation in vitro. Exp. Cell Res. 79:1973;169-178
26. Cseri J., Szappanos H., Szigeti G.P., Csernatony Z., Kovacs L., Csernoch L. A purinergic signal transduction pathway in mammalian skeletal muscle cells in culture. Pflugers Arch. 443:2002;731-738
27. Dahl E., Winterhager E., Traub O., Willecke K. Expression of gap junction genes, connexin 40 and connexin 43, during fetal mouse development. Anat. Embryol. 191:1995;267-278
28. David J.D., See W.M., Higginbotham C.A. Fusion of chick embryo skeletal myoblast: role of calcium influx preceding membrane fusion. Dev. Biol. 82:1981;297-307
29. 7 receptor-mediated release of excitatory amino acids from astrocytes. J. Neurosci. 23:2003;1320-1328
30. Eftimie R., Brenner H.R., Buonanno A. Myogenin and MyoD join a family of skeletal muscle genes regulated by electrical activity. Proc. Natl. Acad. Sci. U. S. A. 15:1991;1349-1353
31. Entwistle A., Zalin R.J., Bevan S., Warner A.E. The control of chick myoblast fusion by ion channels operated by prostaglandins and acetylcholine. J. Cell Biol. 106:1988;1693-1702
32. Eugenín E.A., Brañes M.C., Berman J.W., Sáez J.C. TNF-alpha plus IFN-gamma induce connexin43 expression and formation of gap junctions between human monocytes/macrophages that enhance physiological responses. J. Immunol. 170:2003;1320-1328
33. Evans R.J., Lewis C., Buell G., North R.A., Surprenant A. Pharmacological characterization of heterologously expressed ATP-gated cation channels (P2X-purinoceptors). Mol. Pharmacol. 48:1995;178-183
34. Ewton D.Z., Falen S.L., Florini J.R. The type II insulin-like growth factor (IGF) receptor has low affinity for IGF-I analogs: pleiotypic actions of IGFs on myoblasts are apparently mediated by the type I receptor. Endocrinology. 120:1987;115-123
35. Ewton D.Z., Spizz G., Olson E.N., Florini J.R. Decrease in transforming growth factor-beta binding and action during differentiation in muscle cells. J. Biol. Chem. 263:1988;4029-4032
36. Ferrari D., Villalba M., Chiozzi P., Falzoni S., Ricciardi-Castagnoli P., Di Virgilio F. Mouse microglia cells express a plasma membrane pore gated by extracellular ATP. J. Immunol. 156:1996;1531-1539
37. Ferrari D., La Sala A., Chiozzi A., Falzoni S., Girolamoni G., Idzko M., Dichmann S., Norgauer J., Di Wirgilio F. The P2 purinergic receptor of human dendritic cells: identification and coupling to cytokine release. FASEB J. 14:2000;2466-2476
38. Florini J.R., Roberts A.B., Ewton D.Z., Falen S.L., Flanders K.C., Sporn M.B. Transforming growth factor-beta. A very potent inhibitor of myoblast differentiation, identical to the differentiation inhibitor secreted by Buffalo rat liver cells. J. Biol. Chem. 261:1986;16509-16513
39. Florini J.R., Ewton D.Z., Falen S.L., Van Wyk J.J. Biphasic concentration dependency of stimulation of myoblast differentiation by somatomedins. Am. J. Physiol. 250:1986;C771-C778
40. Fredette B.J., Landmesser L.T. A reevaluation of the role of innervation in primary and secondary myogenesis in developing chick muscle. Dev. Biol. 143:1991;19-35
41. Friday B.B., Horsley V., Pavlath G.K. Calcineurin activity is required for the initiation of skeletal muscle differentiation. J. Cell Biol. 149:2000;657-665
42. Gafni J., Munsch J.A., Lam T.H., Catlin M.C., Costa L.G., Molinski T.F., Pessah I.N. Xestospongins: potent membrane permeable blockers of the inositol 1,4,5-trisphosphate receptor. Neuron. 19:1997;723-733
43. Gilpin B.J., Loechel F., Mattei M.G., Engvall E., Albrechtsen R., Wewer U.M. A novel secreted form of human ADAM 12 (Meltrin α) provokes myogenesis in vivo. J. Biol. Chem. 273:1998;157-166
44. Goichberg P., Geiger B. Direct involvement of N-cadherin-mediated signaling in muscle differentiation. Mol. Biol. Cell. 9:1998;3119-3131
45. 2+-signaling and cell function. Curr. Mol. Med. 2:2002;273-282
46. Haggblad J., Eriksson H., Heilbronn E. ATP-induced cation influx in myotubes is additive to cholinergic agonist action. Acta Physiol. Scand. 125:1985;389-393
47. Hall Z.W., Sanes J.R. Synaptic structure and development: the neuromuscular junction. Cell. 72:1993;99-121. (Suppl.)
48. Harden T.K., Barnard E.A., Boeynaems H.-M., Burnstock G., Dubyak G., Hourani S.M., Insel P.A. P2Y receptors. Girdlestone D. The IUPHAR Compendium of Receptor Characterization and Classification. 1998;209-217 IUPHAR Media, London
49. Hardy S., Kong Y., Konieczny S.F. Fibroblast growth factor inhibits MRF4 activity independently of the phosphorylation status of a conserved threonine residue within the DNA-binding domain. Mol. Cell. Biol. 13:1993;5943-5956
50. Hubscher C.H., Petruska J.C., Rau K.K., Johnson R.D. Co-expression of P2X receptor subunits on rat nodose neurons that bind the isolectin GS-I-B4. NeuroReport. 17:2001;2995-2997
51. Humphrey P.P., Khakh B.S., Kennedy C., King B.F., Burnstock G. P2X receptors. Girdlestone D. The IUPHAR Compendium of Receptor Characterization and Classification. 1998;195-208 IUPHAR Media, London
52. Jarlebark L.E., Housley G.D., Thorne P.R. Immunohistochemical localization of adenosine 5′-triphosphate-gated ion channel P2X(2) receptor subunits in adult and developing rat cochlea. J. Comp. Neurol. 421:2000;289-301
53. Kalderon N., Epstein M.L., Gilula N.B. Cell-to-cell communication and myogenesis. J. Cell Biol. 75:1977;788-806
54. 12 skeletal muscle cells. Arch. Biochem. Biophys. 401:2002;205-214
55. Kolb H.A., Wakelam M.J. Transmitter-like action of ATP on patched membranes of cultured myoblast and myotubes. Nature. 303:1983;621-623
56. Landmesser L. The development of motor projection patterns in the chick hind limb. J. Physiol. 284:1978;391-414
57. Larraín J., Cizmeci-Smith G., Troncoso V., Stahl R.C., Carey D.J., Brandan E. Syndecan-1 expression is down-regulated during myoblast terminal differentiation. Modulation by growth factors and retinoic acid. J. Biol. Chem. 272:1997;18418-18424
58. Launay T., Armand A.S., Charbonnier F., Mira J.C., Donsez E., Gallien C.L., Chanoine C. Expression and neural control of myogenic regulatory factor genes during regeneration of mouse soleus. J. Histochem. Cytochem. 49:2001;887-899
59. Lazarowski E.R., Boucher R.C., Harden T.K. Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules. Mol. Pharmacol. 64:2003;785-795
60. Lee S.J., Lee Y.H., Kim Y.S., Ryu S.H., Suh P.G. Transcriptional regulation of phospholipase C-gamma gene during muscle differentiation. Biochem. Biophys. Res. Commun. 206:1995;194-200
61. Li L., Zhou J., James G., Heller-Harrison R., Czech M.P., Olson E.N. FGF inactivates myogenic helix-loop-helix proteins through phosphorylation of a conserved protein kinase C site in their DNA-binding domains. Cell. 71:1992;1181-1194
62. + current and of hyperpolarization in human myoblast fusion. J. Physiol. 510:1998;467-476
63. Ludolph D.C., Konieczny S.F. Transcription factor families: musculing in on the myogenic program. FASEB J. 9:1995;1595-1604
64. Marteau F., Le Poul E., Communi D., Communi D., Labouret C., Savi P., Boeynaems J.M., González N.S. Pharmacological characterization of the human P2Y13 receptor. Mol. Pharmacol. 64:2003;104-112
65. Martínez A.D., Sáez J.C. Arachidonic acid-induced dye uncoupling in rat cortical astrocytes is mediated by arachidonic acid byproducts. Brain Res. 816:1999;411-423
66. Mege R.M., Goudou D., Giaume C., Nicolet M., Rieger F. Is intercellular communication via gap junctions required for myoblast fusion? Cell Adhes. Commun. 2:1994;329-343
67. 6, in developing chick skeletal muscle. Dev. Dyn. 216:1999;442-449
68. Meyer M.P., Clarke J.D., Patel K., Townsend-Nicholson A., Burnstock G. Selective expression of purino receptor cP2Y1 suggests a role for nucleotide signaling in development of chick embryo. Dev. Dyn. 214:1999;152-158
69. Molkentin J.D., Black B.L., Martin J.F., Olson E.N. Cooperative activation of muscle gene expression by MEF2 and myogenic bHLH proteins. Cell. 83:1995;1125-1136
70. Murgia M., Hanau S., Pizzo P., Rippa M., Di Virgilio F. Oxidized ATP. An irreversible inhibitor of the macrophage purinergic P2Z receptor. J. Biol. Chem. 268:1993;8199-8203
71. 7 receptor characterized in murine dendritic cells: role on the induction of apoptosis. Blood. 96:2000;996-1005
72. Noble B.S., McMillan D.N., Maltin C.A. Calcitonin gene related peptide stimulates differentiation of neonatal rat myogenic cultures. Growth Regul. 3:1993;245-248
73. North R.A. Molecular physiology of P2X receptors. Physiol. Rev. 82:2002;1013-1067
74. Occhiodoro T., Bernheim L., Liu J.H., Bijlenga P., Sinnreich M., Bader C.R., Fischer-Lougheed J. Cloning of a human ether-a-go-go potassium channel expressed in myoblasts at the onset of fusion. FEBS Lett. 434:1998;177-182
75. Okazaki S., Kawai H., Arii Y., Yamaguchi H., Saito S. Effects of calcitonin gene-related peptide and interleukin 6 on myoblast differentiation. Cell Prolif. 29:1996;173-182
76. Olson E.N., Perry M., Schulz R.A. Regulation of muscle differentiation by the MEF2 family of MADS box transcription factors. Dev. Biol. 172:1995;2-14
77. Ontell M. Muscle satellite cells: a validated technique for light microscopic identification and a quantitative study of changes in their population following denervation. Anat. Rec. 178:1974;211-227
78. Proulx A., Merrifield P.A., Naus C.C. Blocking gap junctional intercellular communication in myoblasts inhibits myogenin and MRF4 expression. Dev. Genet. 20:1997;133-144
79. Przybylski R., Szigeti V., Davidheiser S., Kirby A.C. Calcium regulation of skeletal muscle myogenesis. II extracellular and cell surface effects. Cell Calcium. 15:1994;132-142
80. 3 signalling in muscle development and adult chemosensory functions. Dev. Biol. 171:1995;564-577
81. Ralevic V., Burnstock G. Receptors for purines and pyrimidines. Pharmacol. Rev. 50:1998;413-492
82. Rash J.E., Staehelin L.A. Freeze-cleave demonstration of gap junctions between skeletal myogenic cells in vivo. Dev. Biol. 36:1974;455-461
83. Rawls A., Olson E.N. MyoD meets its marker. Cell. 89:1997;5-8
84. Redman R.S., Silinsky E.M. ATP release together with acetylcholine as a mediator of neuromuscular depression at frog motor nerve endings. J. Physiol. 477:1994;117-127
85. Rudnicki M.A., Jaenisch R. The MyoD family of transcription factors and skeletal myogenesis. BioEssays. 17:1995;203-209
86. Rudnicki M.A., Schnegelsberg P.N., Stead R.H., Braun T., Arnold H.H., Jaenisch R. MyoD or Myf-5 is required for the formation of skeletal muscle. Cell. 75:1993;1351-1359
87. Ryten M., Hoebertz A., Burnstock G. Sequential expression of three receptor subtypes for extracellular ATP in developing rat skeletal muscle. Dev. Dyn. 221:2001;331-341
88. 5 receptor on satellite cells. J. Cell Biol. 158:2002;345-355
89. Schmalbruch H. Skeletal muscle fibers of newborn rats are coupled by gap junctions. Dev. Biol. 91:1982;485-490
90. Schnabel P., Gas H., Nohr T., Bohm M. G protein-independent stimulation of human myocardial phospholipase C by mastoparan. Br. J. Pharmacol. 122:1997;31-36
91. Schröder J.M. Phatologie der muskulatur. vol. 15:1982;Springer, Berlin
92. Shainberg A., Yagil G., Yaffe D. Control of myogenesis in vitro by calcium concentration in nutritional medium. Exp. Cell Res. 58:1969;163-167
93. Shin K.S., Park J.Y., Ha D.B., Chung C.H., Kang M.S. Involvement of K(Ca) channels and stretch-activated channels in calcium influx, triggering membrane fusion of chick embryonic myoblasts. Dev. Biol. 175:1996;14-23
94. Silinsky E.M., Redman R.S. Synchronous release of ATP and neurotransmitter within milliseconds of a motor nerve impulse in the frog. J. Physiol. 492:1996;815-822
95. Snow M.H. A quantitative ultrastructural analysis of satellite cells in denervated fast and slow muscle of the mouse. Anat. Rec. 207:1983;593-604
96. Tarroni P., Rossi D., Conti A., Sorrentino V. Expression of the ryanodine receptor type 3 calcium release channel during development and differentiation of mammalian skeletal muscle cells. J. Biol. Chem. 272:1997;19808-19813
97. Ting A.T., Einspahr K.J., Abraham R.T., Leibson P.J. Fc gamma receptor signal transduction in natural killer cells. Coupling to phospholipase C via a G protein-independent, but tyrosine kinase-dependent pathway. J. Immunol. 147:1991;3122-3127
98. Tortorella L.L., Milasincic D.J., Pilch P.F. Critical proliferation-independent window for basic fibroblast growth factor repression of myogenesis via the p42/p44 MAPK signaling pathway. J. Biol. Chem. 276:2001;13709-13717
99. Tsim K.W., Barnard E.A. The signaling pathways mediated by P2Y nucleotide receptors in the formation and maintenance of the skeletal neuromuscular junction. NeuroSignals. 11:2002;58-64
100. Tureckova J., Wilson E.M., Cappalonga J.L., Rotwein P. Insulin-like growth factor-mediated muscle differentiation. Collaboration between phosphatidylinositol 3-kinase-aktsignaling pathways and myogenin. J. Biol. Chem. 276:2001;39264-39270
101. Virginio C., MacKenzie A., Rassendren F.A., North R.A., Surprenant A. Pore dilation of neuronal P2X receptor channels. Nat. Neurosci. 2:1999;315-321
102. Weintraub H. The MyoD family and myogenesis: redundancy, networks and thresholds. Cell. 75:1993;1241-1244
103. Weis J., Kaussen M., Calvo S., Buonanno A. Denervation induces a rapid nuclear accumulation of MRF4 in mature myofibers. Dev. Dyn. 218:2000;438-451
104. Wen L.T., Knowles A.F. Extracellular ATP and adenosine induce cell apoptosis of human hepatoma Li-7A cells via the A3 adenosine receptor. Br. J. Pharmacol. 140:2003;1009-1018
105. Wilson S.J., Harris A.J. Formation of myotubes in neural rat muscles. Dev. Biol. 156:1993;509-518
106. Wingertzahn M.A., Ochs R.S. Changes in ryanodine receptor-mediated calcium release during skeletal muscle differentiation. Proc. Soc. Exp. Biol. Med. 221:1999;234-241
107. Xu Q., Wu Z. The insulin-like growth factor-phosphatidylinositol 3-kinase-Akt signaling pathway regulates myogenin expression in normal myogenic cells but not in rhabdomyosarcoma-derived RD cells. J. Biol. Chem. 275:2000;36750-36757
108. Xu Q., Yu L., Liu L., Cheung C.F., Li X., Yee S., Yang X., Wu Z. p38 mitogen-activated protein kinase-, calcium-calmodulin-dependent protein kinase-, and calcineurin-mediated signaling pathways transcriptionally regulate myogenin expression. Mol. Biol. Cell. 13:2002;1940-1952
109. Yaffe D., Saxel O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature. 270:1977;725-727
110. Yagami-Hiromasa T., Sato T., Kurisaki T., Kamijo K., Nabeshima Y., Fujisawa-Sehara A. A metalloprotease-disintegrin participating in myoblast fusion. Nature. 377:1995;652-656
111. 12 myoblasts depends on the expression of endogenous IGFs and not serum depletion. Am. J. Physiol., Cell Physiol. 283:2002;C1278-C1286
112. Young S.H., Poo M.M. Spontaneous release of transmitter from growth cones of embryonic neurones. Nature. 305:1983;634-637