Glycosaminoglycan mimetics trigger IP3-dependent intracellular calcium release in myoblasts

Matrix Biology

Volumn 29, Issue 4, 2010, Pages 317-329

  Martelly, Isabelle ^a   Singabraya, Dominique ^a   Vandebrouck, Aurélie ^b   Papy Garcia, Dulce ^a   Cognard, Christian ^b   Raymond, Guy ^b   Guillet Deniau, Isabelle ^c   Courty, Jose ^a   Constantin, Bruno ^b  

^a CNRS   (France)

^b UNIVERSITÉ DE POITIERS   (France)

^c INSTITUT COCHIN   (France)

Author keywords

Calcium; Heparin; IP3 receptor; Myoblast; RGTA (OTR4120); Serotonin receptor

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; CHOLINERGIC RECEPTOR; D 120; GLYCOSAMINOGLYCAN; HEPARIN; INOSITOL TRISPHOSPHATE; OTR 4120; PHOSPHOLIPASE C; PROTEIN TYROSINE KINASE; RYANODINE RECEPTOR; SEROTONIN 2A RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM MOBILIZATION; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL CULTURE; CELL DIFFERENTIATION; CONTROLLED STUDY; DRUG TARGETING; ENZYME ACTIVATION; IN VITRO STUDY; MOUSE; MUSCLE DEVELOPMENT; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE SATELLITE CELL;

ANIMALS; CALCIUM; CALCIUM, DIETARY; CELL DIFFERENTIATION; CELL LINE; CLONE CELLS; CYTOPLASM; GLYCOSAMINOGLYCANS; HEPARIN; INOSITOL PHOSPHATES; MICE; MUSCLE DEVELOPMENT; MYOBLASTS; RATS; RATS, WISTAR; RECEPTOR, SEROTONIN, 5-HT2A; REGENERATION; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SATELLITE CELLS, SKELETAL MUSCLE; SIGNAL TRANSDUCTION;

RATTUS;

EID: 77952544052     PISSN: 0945053X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.matbio.2010.02.002     Document Type: Article

References (54)

1. Aamiri A., Mobarek A., Carpentier G., Barritault D., Gautron J. Effects of substituted dextran on reinnervation of a skeletal muscle in adult rats during regeneration. CR Acad. Sci. III 1995, 318:1037-1043.
2. Alexakis C., Mestries P., Garcia S., Petit E., Barbier V., Papy-Garcia D., Sagot M.A., Barritault D., Caruelle J.P., Kern P. Structurally different RGTAs modulate collagen-type expression by cultured aortic smooth muscle cells via different pathways involving fibroblast growth factor-2 or transforming growth factor-beta1. FASEB J. 2004, 18:1147-1149.
3. Alvarez K., Fadic R., Brandan E. Augmented synthesis and differential localization of heparan sulfate proteoglycans in Duchenne muscular dystrophy. J. Cell. Biochem. 2002, 85:703-713.
4. 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.
5. Armand A.S., Bourajjaj M., Martinez-Martinez S., el Azzouzi H., da Costa Martins P.A., Hatzis P., Seidler T., Redondo J.M., De Windt L.J. Cooperative synergy between NFAT and MyoD regulates myogenin expression and myogenesis. J. Biol. Chem. 2008, 283:29004-29010.
6. 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.
7. Barbosa I., Garcia S., Barbier-Chassefiere V., Caruelle J.P., Martelly I., Papy-Garcia D. Improved and simple micro assay for sulfated glycosaminoglycans quantification in biological extracts and its use in skin and muscle tissue studies. Glycobiology 13, 647-653 2003.
8. Barbosa I., Morin C., Garcia S., Duchesnay A., Oudghir M., Jenniskens G., Miao H.Q., Guimond S., Carpentier G., Cebrian J., Caruelle J.P., van Kuppevelt T., Turnbull J., Martelly I., Papy-Garcia D. A synthetic glycosaminoglycan mimetic (RGTA) modifies natural glycosaminoglycan species during myogenesis. J. Cell Sci. 2005, 118:253-264.
9. Barre L., Venkatesan N., Magdalou J., Netter P., Fournel-Gigleux S., Ouzzine M. Evidence of calcium-dependent pathway in the regulation of human beta1, 3-glucuronosyltransferase-1 (GlcAT-I) gene expression: a key enzyme in proteoglycan synthesis. FASEB J. 2006, 20:1692-1694.
10. Brandan E., Fuentes M.E., Andrade W. The proteoglycan decorin is synthesized and secreted by differentiated myotubes. Eur. J. Cell Biol. 1991, 55:209-216.
11. Brandan E., Carey D.J., Larrain J., Melo F., Campos A. Synthesis and processing of glypican during differentiation of skeletal muscle cells. Eur. J. Cell Biol. 1996, 71:170-176.
12. Casar J.C., Cabello-Verrugio C., Olguin H., Aldunate R., Inestrosa N.C., Brandan E. Heparan sulfate proteoglycans are increased during skeletal muscle regeneration: requirement of syndecan-3 for successful fiber formation. J. Cell Sci. 2004, 117:73-84.
13. Cognard C., Constantin B., Rivet-Bastide M., Raymond G. Intracellular calcium transients induced by different kinds of stimulus during myogenesis of rat skeletal muscle cells studied by laser cytofluorimetry with Indo-1. Cell Calcium 1993, 14:333-348.
14. Constantin B., Cognard C., Raymond G. Myoblast fusion requires cytosolic calcium elevation but not activation of voltage-dependent calcium channels. Cell Calcium 1996, 19:365-374.
15. Constantin B., Sebille S., Cognard C. New insights in the regulation of calcium transfers by muscle dystrophin-based cytoskeleton: implications in DMD. J. Muscle Res. Cell Motil. 2006, 27:375-386.
16. Cornelison D.D., Filla M.S., Stanley H.M., Rapraeger A.C., Olwin B.B. Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Dev. Biol. 2001, 239:79-94.
17. Cossu G., Sampaolesi M. New therapies for muscular dystrophy: cautious optimism. Trends Mol. Med. 2004, 10:516-520.
18. Dahlman J.M., Bakkar N., He W., Guttridge D.C. NF-{kappa}B functions in stromal fibroblasts to regulate early postnatal muscle development. J. Biol. Chem. 2010, 285:5479-5487.
19. David J.D., See W.M., Higginbotham C.A. Fusion of chick embryo skeletal myoblasts: role of calcium influx preceding membrane union. Dev. Biol. 1981, 82:297-307.
20. Desgranges P., Barbaud C., Caruelle J.P., Barritault D., Gautron J. A substituted dextran enhances muscle fiber survival and regeneration in ischemic and denervated rat EDL muscle. FASEB J. 1999, 13:761-766.
21. Gautron J., Kedzia C., Husmann I., Barritault D. Acceleration of the regeneration of skeletal muscles in adult rats by dextran derivatives. CR Acad. Sci. III 1995, 318:671-676.
22. Grynkiewicz G., Poenie M., Tsien R.Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 1985, 260:3440-3450.
23. Guillet-Deniau I., Burnol A.F., Girard J. Identification and localization of a skeletal muscle serotonin 5-HT2A receptor coupled to the Jak/STAT pathway. J. Biol. Chem. 1997, 272:14825-14829.
24. Haggblad J., Eriksson H., Heilbronn E. Cell surface ATP (P2y) purinoceptors trigger and modulate multiple calcium fluxes in skeletal muscle cells. Prog. Brain Res. 1990, 84:111-116.
25. Jenniskens G.J., Ringvall M., Koopman W.J., Ledin J., Kjellen L., Willems P.H., Forsberg E., Veerkamp J.H., van Kuppevelt T.H. Disturbed Ca2+ kinetics in N-deacetylase/N-sulfotransferase-1 defective myotubes. J. Cell Sci. 2003, 116:2187-2193.
26. Kobayashi S., Kitazawa T., Somlyo A.V., Somlyo A.P. Cytosolic heparin inhibits muscarinic and alpha-adrenergic Ca2+ release in smooth muscle. Physiological role of inositol 1, 4, 5-trisphosphate in pharmacomechanical coupling. J. Biol. Chem. 1989, 264:17997-18004.
27. 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.
28. Kubis H.P., Hanke N., Scheibe R.J., Meissner J.D., Gros G. Ca2+ transients activate calcineurin/NFATc1 and initiate fast-to-slow transformation in a primary skeletal muscle culture. Am. J. Physiol. Cell Physiol. 2003, 285:C56-C63.
29. Lagord C., Carpentier G., Moraczewski J., Pons G., Climent F., Martelly I. Satellite cell myogenesis is highly stimulated by the kinase inhibitor iso-H7: comparison with HA1004 and staurosporine effects. Biochem. Biophys. Res. Commun. 1993, 191:928-936.
30. Lamb G.D., Posterino G.S., Stephenson D.G. Effects of heparin on excitation-contraction coupling in skeletal muscle toad and rat. J. Physiol. 1994, 474:319-329.
31. Larrain J., Alvarez J., Hassell J.R., Brandan E. Expression of perlecan, a proteoglycan that binds myogenic inhibitory basic fibroblast growth factor, is down regulated during skeletal muscle differentiation. Exp. Cell Res. 1997, 234:405-412.
32. Larrain J., Carey D.J., Brandan E. Syndecan-1 expression inhibits myoblast differentiation through a basic fibroblast growth factor-dependent mechanism. J. Biol. Chem. 1998, 273:32288-32296.
33. Lee K.H., Kim D.G., Shin N.Y., Song W.K., Kwon H., Chung C.H., Kang M.S. NF-kappaB-dependent expression of nitric oxide synthase is required for membrane fusion of chick embryonic myoblasts. Biochem. J. 1997, 324(Pt 1):237-242.
34. Lopez J.R., Terzic A. Inositol 1, 4, 5-trisphosphate-induced Ca2+ release is regulated by cytosolic Ca2+ in intact skeletal muscle. Pflugers Arch. 1996, 432:782-790.
35. Marchand E., Constantin B., Balghi H., Claudepierre M.C., Cantereau A., Magaud C., Mouzou A., Raymond G., Braun S., Cognard C. Improvement of calcium handling and changes in calcium-release properties after mini- or full-length dystrophin forced expression in cultured skeletal myotubes. Exp. Cell Res. 2004, 297:363-379.
36. Mullen G.P., Rogalski T.M., Bush J.A., Gorji P.R., Moerman D.G. Complex patterns of alternative splicing mediate the spatial and temporal distribution of perlecan/UNC-52 in Caenorhabditis elegans. Mol. Biol. Cell 1999, 10:3205-3221.
37. Ori A., Wilkinson M.C., Fernig D.G. The heparanome and regulation of cell function: structures, functions and challenges. Front. Biosci. 2008, 13:4309-4338.
38. Papy-Garcia D., Barbosa I., Duchesnay A., Saadi S., Caruelle J.P., Barritault D., Martelly I. Glycosaminoglycan mimetics (RGTA) modulate adult skeletal muscle satellite cell proliferation in vitro. J. Biomed. Mater. Res. 2002, 62:46-55.
39. Papy-Garcia D., Barbier-Chassefière V., Rouet V., Kerros M.-E., Klochendler C., Tournaire M.-C., Barritault D., Caruelle J.-P., Petit E. Nondegradative sulfation of polysaccharides. synthesis and structure characterization of biologically active heparan sulfate mimetics. Macromolecules 2005, 38:4647-4654.
40. Pinset C., Mulle C., Benoit P., Changeux J.P., Chelly J., Gros F., Montarras D. Functional adult acetylcholine receptor develops independently of motor innervation in Sol 8 mouse muscle cell line. EMBO J. 1991, 10:2411-2418.
41. Powell J.A., Molgo J., Adams D.S., Colasante C., Williams A., Bohlen M., Jaimovich E. IP3 receptors and associated Ca2+ signals localize to satellite cells and to components of the neuromuscular junction in skeletal muscle. J. Neurosci. 2003, 23:8185-8192.
42. Ralevic V., Burnstock G. Receptors for purines and pyrimidines. Pharmacol. Rev. 1998, 50:413-492.
43. 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.
44. Sanes J.R. The basement membrane/basal lamina of skeletal muscle. J. Biol. Chem. 278, 12601-12604. 2003.
45. Sanes J.R., Engvall E., Butkowski R., Hunter D.D. Molecular heterogeneity of basal laminae: isoforms of laminin and collagen IV at the neuromuscular junction and elsewhere. J. Cell. Biol. 1990, 111:1685-1699.
46. Sasisekharan R., Raman R., Prabhakar V. Glycomics approach to structure-function relationships of glycosaminoglycans. Annu. Rev. Biomed. Eng. 2006, 8:181-231.
47. Shinjo S.K., Tersariol I.L., Oliveira V., Nakaie C.R., Oshiro M.E., Ferreira A.T., Santos I.A., Dietrich C.P., Nader H.B. Heparin and heparan sulfate disaccharides bind to the exchanger inhibitor peptide region of Na+/Ca2+ exchanger and reduce the cytosolic calcium of smooth muscle cell lines. Requirement of C4-C5 unsaturation and 1-4 glycosidic linkage for activity. J.Biol. Chem. 2002, 277:48227-48233.
48. Talon S., Huchet-Cadiou C., Leoty C. Inositol 1, 4, 5-trisphosphate-sensitive Ca2+ release in rat fast- and slow-twitch skinned muscle fibres. Pflugers Arch. 1999, 438:804-816.
49. Valdes J.A., Hidalgo J., Galaz J.L., Puentes N., Silva M., Jaimovich E., Carrasco M.A. NF-kappaB activation by depolarization of skeletal muscle cells depends on ryanodine and IP3 receptor-mediated calcium signals. Am. J. Physiol. Cell Physiol. 2007, 292:C1960-C1970.
50. 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.
51. Yeung D., Zablocki K., Lien C.F., Jiang T., Arkle S., Brutkowski W., Brown J., Lochmuller H., Simon J., Barnard E.A., Gorecki D.C. Increased susceptibility to ATP via alteration of P2X receptor function in dystrophic mdx mouse muscle cells. FASEB J. 2006, 20:610-620.
52. Yue X.L., Lehri S., Li P., Barbier-Chassefiere V., Petit E., Huang Q.F., Albanese P., Barritault D., Caruelle J.P., Papy-Garcia D., Morin C. Insights on a new path of pre-mitochondrial apoptosis regulation by a glycosaminoglycan mimetic. Cell Death Differ. 2009, 16:770-781.
53. Zimowska M., Szczepankowska D., Streminska W., Papy D., Tournaire M.C., Gautron J., Barritault D., Moraczewski J., Martelly I. Heparan sulfate mimetics modulate calpain activity during rat Soleus muscle regeneration. J. Cell. Physiol. 2001, 188:178-187.
54. Zimowska M., Constantin B., Papy-Garcia D., Raymond G., Cognard C., Caruelle J.P., Moraczewski J., Martelly I. Novel glycosaminoglycan mimetic (RGTA, RGD120) contributes to enhance skeletal muscle satellite cell fusion by increasing intracellular Ca(2+) and calpain activity. J. Cell. Physiol. 2005, 205:237-245.