Role of skeletal muscle proteoglycans during myogenesis

Matrix Biology

Volumn 32, Issue 6, 2013, Pages 289-297

  Brandan, Enrique ^a   Gutierrez, Jaime ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

Fibrosis; Growth factors; Muscular diseases; Proteoglycans; Skeletal muscle formation

Indexed keywords

BIGLYCAN; CHONDROITIN; CORE PROTEIN; DECORIN; DERMATAN SULFATE; GLYCOSAMINOGLYCAN; GLYPICAN 1; PERLECAN; PROTEOGLYCAN; PROTEOHEPARAN SULFATE; SYNDECAN 1; SYNDECAN 2; SYNDECAN 3; SYNDECAN 4;

CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; HUMAN; MUSCLE CELL; MUSCLE DEVELOPMENT; MUSCLE REGENERATION; MUSCULAR DYSTROPHY; MYOBLAST; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; SHORT SURVEY; SKELETAL MUSCLE;

MAMMALIA;

EID: 84882577289     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2013.03.007     Document Type: Short Survey

References (114)

1. 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.
2. Amenta A.R., Yilmaz A., Bogdanovich S., McKechnie B.A., Abedi M., Khurana T.S., Fallon J.R. Biglycan recruits utrophin to the sarcolemma and counters dystrophic pathology in mdx mice. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:762-767.
3. Amenta A.R., Creely H.E., Mercado M.L., Hagiwara H., McKechnie B.A., Lechner B.E., Rossi S.G., Wang Q., Owens R.T., Marrero E., Mei L., Hoch W., Young M.F., McQuillan D.J., Rotundo R.L., Fallon J.R. Biglycan is an extracellular MuSK binding protein important for synapse stability. J. Neurosci. 2012, 32:2324-2334.
4. 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. 1997, 137:1057-1068.
5. Anderson M.J., Fambrough D.M. Aggregates of acetylcholine receptors are associated with plaques of a basal lamina heparan sulfate proteoglycan on the surface of skeletal muscle fibers. J. Cell Biol. 1983, 97:1396-1411.
6. Andrade W., Brandan E. Isolation and characterization of rat skeletal muscle proteoglycan decorin and comparison with the human fibroblast decorin. Comp. Biochem. Physiol. B 1991, 100:565-570.
7. Arikawa-Hirasawa E., Rossi S.G., Rotundo R.L., Yamada Y. Absence of acetylcholinesterase at the neuromuscular junctions of perlecan-null mice. Nat. Neurosci. 2002, 5:119-123.
8. Bentzinger C.F., Wang Y.X., von Maltzahn J., Soleimani V.D., Yin H., Rudnicki M.A. Fibronectin regulates wnt7a signaling and satellite cell expansion. Cell Stem Cell 2013, 12:75-87.
9. Bernfield M., Gotte M., Park P.W., Reizes O., Fitzgerald M.L., Lincecum J., Zako M. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 1999, 68:729-777.
10. Bottaro D.P., Rubin J.S., Faletto D.L., Chan A.M., Kmiecik T.E., Vande Woude G.F., Aaronson S.A. Identification of the hepatocyte growth factor receptor as the c-met proto-oncogene product. Science 1991, 251:802-804.
11. Bowe M.A., Mendis D.B., Fallon J.R. The small leucine-rich repeat proteoglycan biglycan binds to alpha-dystroglycan and is upregulated in dystrophic muscle. J. Cell Biol. 2000, 148:801-810.
12. Brandan E., Inestrosa N.C. Binding of the asymmetric forms of acetylcholinesterase to heparin. Biochem. J. 1984, 221:415-422.
13. Brandan E., Inestrosa N.C. The synaptic form of acetylcholinesterase binds to cell-surface heparan sulfate proteoglycans. J. Neurosci. Res. 1986, 15:185-196.
14. Brandan E., Maldonado M., Garrido J., Inestrosa N.C. Anchorage of collagen-tailed acetylcholinesterase to the extracellular matrix is mediated by heparan sulfate proteoglycans. J. Cell Biol. 1985, 101:985-992.
15. 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.
16. Brandan E., Fuentes M.E., Andrade W. Decorin, a chondroitin/dermatan sulfate proteoglycan is under neural control in rat skeletal muscle. J. Neurosci. Res. 1992, 32:51-59.
17. 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.
18. Brandan E., Cabello-Verrugio C., Retamal C., Marzolo M.P. The low density lipoprotein receptor-related protein/2 macroglobulin receptor, LRP, functions as an endocytic receptor for decorin. J. Biol. Chem. 2006, (Revised form).
19. Brandan E., Retamal C., Cabello-Verrugio C., Marzolo M.P. The low density lipoprotein receptor-related protein functions as an endocytic receptor for decorin. J. Biol. Chem. 2006, 281:31562-31571.
20. Brandan E., Cabello-Verrugio C., Vial C. Novel regulatory mechanisms for the proteoglycans decorin and biglycan during muscle formation and muscular dystrophy. Matrix Biol. 2008, 27:700-708.
21. Brunetti A., Goldfine I.D. Role of myogenin in myoblast differentiation and its regulation by fibroblast growth factor. J. Biol. Chem. 1990, 265:5960-5963.
22. Cabello-Verrugio C., Brandan E. A novel modulatory mechanism of transforming growth factor-beta signaling through decorin and LRP-1. J. Biol. Chem. 2007, 282:18842-18850.
23. Cabello-Verrugio C., Santander C., Cofre C., Acuna M.J., Melo F., Brandan E. The internal region leucine-rich repeat 6 of decorin interacts with low density lipoprotein receptor-related protein-1, modulates transforming growth factor (TGF)-beta-dependent signaling, and inhibits TGF-beta-dependent fibrotic response in skeletal muscles. J. Biol. Chem. 2012, 287:6773-6787.
24. Caceres S., Cuellar C., Casar J.C., Garrido J., Schaefer L., Kresse H., Brandan E. Synthesis of proteoglycans is augmented in dystrophic mdx mouse skeletal muscle. Eur. J. Cell Biol. 2000, 79:173-181.
25. Campos A., Nunez R., Koenig C.S., Carey D.J., Brandan E. A lipid-anchored heparan sulfate proteoglycan is present in the surface of differentiated skeletal muscle cells. Isolation and biochemical characterization. Eur. J. Biochem. 1993, 216:587-595.
26. Carey D.J. Syndecans: multifunctional cell-surface co-receptors. Biochem. J. 1997, 327:1-16.
27. Carrino D.A., Caplan A.I. Isolation and preliminary characterization of proteoglycans synthesized by skeletal muscle. J. Biol. Chem. 1982, 257:14145-14154.
28. Carrino D.A., Caplan A.I. Structural characterization of chick embryonic skeletal muscle chondroitin sulfate proteoglycan. Connect Tissue Res. 1989, 19:35-50.
29. Carrino D.A., Sorrell J.M., Caplan A.I. Dynamic expression of proteoglycans during chicken skeletal muscle development and maturation. Poult. Sci. 1999, 78:769-777.
30. 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.
31. Casar J.C., McKechnie B.A., Fallon J.R., Young M.F., Brandan E. Transient up-regulation of biglycan during skeletal muscle regeneration: delayed fiber growth along with decorin increase in biglycan-deficient mice. Dev. Biol. 2004, 268:358-371.
32. Chen C.C., Lau L.F. Functions and mechanisms of action of CCN matricellular proteins. Int. J. Biochem. Cell Biol. 2009, 41:771-783.
33. Cornelison D., Filla M., Stanley H., Rapraeger A., Olwin 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.
34. Cornelison D.D., Wilcox-Adelman S.A., Goetinck P.F., Rauvala H., Rapraeger A.C., Olwin B.B. Essential and separable roles for Syndecan-3 and Syndecan-4 in skeletal muscle development and regeneration. Genes Dev. 2004, 18:2231-2236.
35. Cossu G., Biressi S. Satellite cells, myoblasts and other occasional myogenic progenitors: possible origin, phenotypic features and role in muscle regeneration. Semin. Cell Dev. Biol. 2005, 16:623-631.
36. Couchman J.R. Syndecans: proteoglycan regulators of cell-surface microdomains?. Nat. Rev. Mol. Cell Biol. 2003, 4:926-937.
37. David G., Bai X.M., Van der Schueren B., Marynen P., Cassiman J.J., Van den Berghe H. Spatial and temporal changes in the expression of fibroglycan (syndecan-2) during mouse embryonic development. Development 1993, 119:841-854.
38. Deakin J.A., Lyon M. Differential regulation of hepatocyte growth factor/scatter factor by cell surface proteoglycans and free glycosaminoglycan chains. J. Cell Sci. 1999, 112:1999-2009.
39. Droguett R., Cabello-Verrugio C., Riquelme C., Brandan E. Extracellular proteoglycans modifies TGF-beta bio-availability attenuating its signaling during skeletal muscle differentiation. Matrix Biol. 2006, 25:332-341.
40. Fadic R., Mezzano V., Alvarez K., Cabrera D., Holmgren J., Brandan E. Increase in decorin and biglycan in Duchenne muscular dystrophy: role of fibroblasts as cell source of these proteoglycans in the disease. J. Cell. Mol. Med. 2006, 10:758-769.
41. Filmus J., Selleck S.B. Glypicans: proteoglycans with a surprise. J. Clin. Invest. 2001, 108:497-501.
42. Filmus J., Capurro M., Rast J. Glypicans. Genome Biol. 2008, 9:224.
43. Florini J.R., Ewton D.Z., Magri K.A. Hormones, growth factors, and myogenic differentiation. Annu. Rev. Physiol. 1991, 53:201-216.
44. Fuentealba L., Carey D.J., Brandan E. Antisense inhibition of syndecan-3 expression during skeletal muscle differentiation accelerates myogenesis through a basic fibroblast growth factor-dependent mechanism. J. Biol. Chem. 1999, 274:37876-37884.
45. Gao R., Brigstock D.R. Low density lipoprotein receptor-related protein (LRP) is a heparin-dependent adhesion receptor for connective tissue growth factor (CTGF) in rat activated hepatic stellate cells. Hepatol. Res. 2003, 27:214-220.
46. Gautam M., Noakes P.G., Moscoso L., Rupp F., Scheller R.H., Merlie J.P., Sanes J.R. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 1996, 85:525-535.
47. Gesemann M., Denzer A.J., Ruegg M.A. Acetylcholine receptor-aggregating activity of agrin isoforms and mapping of the active site. J. Cell Biol. 1995, 128:625-636.
48. Gillies A.R., Lieber R.L. Structure and function of the skeletal muscle extracellular matrix. Muscle Nerve 2011, 44:318-331.
49. Goetsch S.C., Hawke T.J., Gallardo T.D., Richardson J.A., Garry D.J. Transcriptional profiling and regulation of the extracellular matrix during muscle regeneration. Physiol. Genomics 2003, 14:261-271.
50. Gosselin L.E., Williams J.E., Deering M., Brazeau D., Koury S., Martinez D.A. Localization and early time course of TGF-beta 1 mRNA expression in dystrophic muscle. Muscle Nerve 2004, 30:645-653.
51. Gutierrez J., Brandan E. A novel mechanism of sequestering fibroblast growth factor 2 by glypican in lipid rafts, allowing skeletal muscle differentiation. Mol. Cell. Biol. 2010, 30:1634-1649.
52. Gutierrez J., Osses N., Brandan E. Changes in secreted and cell associated proteoglycan synthesis during conversion of myoblasts to osteoblasts in response to bone morphogenetic protein-2: role of decorin in cell response to BMP-2. J. Cell. Physiol. 2006, 206:58-67.
53. Hausser H., Schonherr E., Muller M., Liszio C., Bin Z., Fisher L.W., Kresse H. Receptor-mediated endocytosis of decorin: involvement of leucine-rich repeat structures. Arch. Biochem. Biophys. 1998, 349:363-370.
54. Henriquez J.P., Casar J.C., Fuentealba L., Carey D.J., Brandan E. Extracellular matrix histone H1 binds to perlecan, is present in regenerating skeletal muscle and stimulates myoblast proliferation. J. Cell Sci. 2002, 115:2041-2051.
55. Hildebrand A., Romaris M., Rasmussen L.M., Heinegard D., Twardzik D.R., Border W.A., Ruoslahti E. Interaction of the small interstitial proteoglycans biglycan, decorin and fibromodulin with transforming growth factor beta. Biochem. J. 1994, 302:527-534.
56. Huang G., Brigstock D.R. Integrin expression and function in the response of primary culture hepatic stellate cells to connective tissue growth factor (CCN2). J. Cell. Mol. Med. 2011, 15:1087-1095.
57. Iozzo R.V. The family of the small leucine-rich proteoglycans: key regulators of matrix assembly and cellular growth. Crit. Rev. Biochem. Mol. Biol. 1997, 32:141-174.
58. Iozzo R.V. The biology of the small leucine-rich proteoglycans. Functional network of interactive proteins. J. Biol. Chem. 1999, 274:18843-18846.
59. Iozzo R.V., Schaefer L. Proteoglycans in health and disease: novel regulatory signaling mechanisms evoked by the small leucine-rich proteoglycans. FEBS J. 2010, 277:3864-3875.
60. Jen Y.H., Musacchio M., Lander A.D. Glypican-1 controls brain size through regulation of fibroblast growth factor signaling in early neurogenesis. Neural Dev. 2009, 4:33.
61. Jenniskens G.J., Hafmans T., Veerkamp J.H., van Kuppevelt T.H. Spatiotemporal distribution of heparan sulfate epitopes during myogenesis and synaptogenesis: a study in developing mouse intercostal muscle. Dev. Dyn. 2002, 225:70-79.
62. Jenniskens G.J., Veerkamp J.H., van Kuppevelt T.H. Heparan sulfates in skeletal muscle development and physiology. J. Cell. Physiol. 2006, 206:283-294.
63. Kamimura K., Ueno K., Nakagawa J., Hamada R., Saitoe M., Maeda N. Perlecan regulates bidirectional Wnt signaling at the Drosophila neuromuscular junction. J. Cell Biol. 2013, 200:219-233.
64. Kishioka Y., Thomas M., Wakamatsu J., Hattori A., Sharma M., Kambadur R., Nishimura T. Decorin enhances the proliferation and differentiation of myogenic cells through suppressing myostatin activity. J. Cell. Physiol. 2008, 215:856-867.
65. Kresse H., Hausser H., Schonherr E. Small proteoglycans. EXS 1994, 70:73-100.
66. Langsdorf A., Do A.T., Kusche-Gullberg M., Emerson C.P., Ai X. Sulfs are regulators of growth factor signaling for satellite cell differentiation and muscle regeneration. Dev. Biol. 2007, 311:464-477.
67. 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.
68. Larrain 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. 1997, 272:18418-18424.
69. 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.
70. Lechner B.E., Lim J.H., Mercado M.L., Fallon J.R. Developmental regulation of biglycan expression in muscle and tendon. Muscle Nerve 2006, 34:347-355.
71. Lin W., Burgess R.W., Dominguez B., Pfaff S.L., Sanes J.R., Lee K.F. Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse. Nature 2001, 410:1057-1064.
72. Lin W., Dominguez B., Yang J., Aryal P., Brandon E.P., Gage F.H., Lee K.F. Neurotransmitter acetylcholine negatively regulates neuromuscular synapse formation by a Cdk5-dependent mechanism. Neuron 2005, 46:569-579.
73. Litwack E.D., Ivins J.K., Kumbasar A., Paine-Saunders S., Stipp C.S., Lander A.D. Expression of the heparan sulfate proteoglycan glypican-1 in the developing rodent. Dev. Dyn. 1998, 211:72-87.
74. Liu X., Nestor K.E., McFarland D.C., Velleman S.G. Developmental expression of skeletal muscle heparan sulfate proteoglycans in turkeys with different growth rates. Poult. Sci. 2002, 81:1621-1628.
75. Liu X., McFarland D.C., Nestor K.E., Velleman S.G. Developmental regulated expression of syndecan-1 and glypican in pectoralis major muscle in turkeys with different growth rates. Dev. Growth Differ. 2004, 46:37-51.
76. Madhavan R., Peng H.B. HGF induction of postsynaptic specializations at the neuromuscular junction. J. Neurobiol. 2006, 66:134-147.
77. McMahan U. The agrin hypothesis. Cold Spring Harb. Symp. Quant. Biol. 1990, 55:407-418.
78. Melo F., Brandan E. Decorin is specifically solubilized by heparin from the extracellular matrix of rat skeletal muscles. FEBS Lett. 1993, 319:249-252.
79. Mercado M.L., Amenta A.R., Hagiwara H., Rafii M.S., Lechner B.E., Owens R.T., McQuillan D.J., Froehner S.C., Fallon J.R. Biglycan regulates the expression and sarcolemmal localization of dystrobrevin, syntrophin, and nNOS. FASEB J. 2006, 20:1724-1726.
80. Mishina M., Takai T., Imoto K., Noda M., Takahashi T., Numa S., Methfessel C., Sakmann B. Molecular distinction between fetal and adult forms of muscle acetylcholine receptor. Nature 1986, 321:406-411.
81. Miura T., Kishioka Y., Wakamatsu J., Hattori A., Hennebry A., Berry C.J., Sharma M., Kambadur R., Nishimura T. Decorin binds myostatin and modulates its activity to muscle cells. Biochem. Biophys. Res. Commun. 2006, 340:675-680.
82. Nishimura T., Oyama K., Kishioka Y., Wakamatsu J., Hattori A. Spatiotemporal expression of decorin and myostatin during rat skeletal muscle development. Biochem. Biophys. Res. Commun. 2007, 361:896-902.
83. Nishimura T., Nozu K., Kishioka Y., Wakamatsu J., Hattori A. Decorin expression in quiescent myogenic cells. Biochem. Biophys. Res. Commun. 2008, 370:383-387.
84. Olguin H., Brandan E. Expression and localization of proteoglycans during limb myogenic activation. Dev. Dyn. 2001, 221:106-115.
85. Olguin H., Santander C., Brandan E. Inhibition of myoblast migration, via decorin expression is critical for normal skeletal muscle differentiation. Dev. Biol. 2013, (in press).
86. Olwin B.B., Rapraeger A. Repression of myogenic differentiation by aFGF, bFGF, and K-FGF is dependent on cellular heparan sulfate. J. Cell Biol. 1992, 118:631-639.
87. Ontell M., Kozeka K. Organogenesis of the mouse extensor digitorum logus muscle: a quantitative study. Am. J. Anat. 1984, 171:149-161.
88. Peng H., Ali A., Daggett D., Rauvala H., Hassell J., Smalheiser N. The relationship between perlecan and dystroglycan and its implication in the formation of the neuromuscular junction. Cell Adhes. Commun. 1998, 5:475-489.
89. Pisconti A., Cornelison D.D., Olguin H.C., Antwine T.L., Olwin B.B. Syndecan-3 and Notch cooperate in regulating adult myogenesis. J. Cell Biol. 2010, 190:427-441.
90. Rafii M.S., Hagiwara H., Mercado M.L., Seo N.S., Xu T., Dugan T., Owens R.T., Hook M., McQuillan D.J., Young M.F., Fallon J.R. Biglycan binds to alpha- and gamma-sarcoglycan and regulates their expression during development. J. Cell. Physiol. 2006, 209:439-447.
91. Rapraeger A.C., Krufka A., Olwin B.B. Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 1991, 252:1705-1708.
92. Riquelme C., Larrain J., Schonherr E., Henriquez J.P., Kresse H., Brandan E. Antisense inhibition of decorin expression in myoblasts decreases cell responsiveness to transforming growth factor beta and accelerates skeletal muscle differentiation. J. Biol. Chem. 2001, 276:3589-3596.
93. Rudnicki M.A., Jaenisch R. The MyoD family of transcription factors and skeletal myogenesis. Bioessays 1995, 17:203-209.
94. Samuel M.A., Valdez G., Tapia J.C., Lichtman J.W., Sanes J.R. Agrin and synaptic laminin are required to maintain adult neuromuscular junctions. PLoS One 2012, 7:e46663.
95. Sarrazin S., Lamanna W.C., Esko J.D. Heparan sulfate proteoglycans. Cold Spring Harb. Perspect. Biol. 2011, 3.
96. Schaefer L., Iozzo R.V. Biological functions of the small leucine-rich proteoglycans: from genetics to signal transduction. J. Biol. Chem. 2008, 283:21305-21309.
97. Schiaffino S., Partridge T. Skeletal muscle repair and regeneration. Advances in Muscle Research 2008, 3. Springer, Netherlands, (pp. XIV-380).
98. Schonherr E., Broszat M., Brandan E., Bruckner P., Kresse H. Decorin core protein fragment Leu155-Val260 interacts with TGF-beta but does not compete for decorin binding to type I collagen. Arch. Biochem. Biophys. 1998, 355:241-248.
99. Serrano A.L., Munoz-Canoves P. Regulation and dysregulation of fibrosis in skeletal muscle. Exp. Cell Res. 2010, 316:3050-3058.
100. Sogos V., Balaci L., Ennas M.G., Dell'era P., Presta M., Gremo F. Developmentally regulated expression and localization of fibroblast growth factor receptors in the human muscle. Dev. Dyn. 1998, 211:362-373.
101. Ugarte G., Santander C., Brandan E. Syndecan-4 and beta1 integrin are regulated by electrical activity in skeletal muscle: implications for cell adhesion. Matrix Biol. 2010, 29:383-392.
102. Velleman S.G., Patterson R.A., Nestor K.E. Identification of decorin and chondroitin sulfate proteoglycans in turkey skeletal muscle. Poult. Sci. 1997, 76:506-510.
103. Velleman S.G., Liu X., Coy C.S., McFarland D.C. Effects of syndecan-1 and glypican on muscle cell proliferation and differentiation: implications for possible functions during myogenesis. Poult. Sci. 2004, 83:1020-1027.
104. Vial C., Zuniga L.M., Cabello-Verrugio C., Canon P., Fadic R., Brandan E. Skeletal muscle cells express the profibrotic cytokine connective tissue growth factor (CTGF/CCN2), which induces their dedifferentiation. J. Cell. Physiol. 2008, 215:410-421.
105. Vial C., Gutiérrez J., Santander C., Cabrera D., Brandan E. Decorin interacts with CTGF/CCN2 through LRR12 inhibiting its biological activity. J. Biol. Chem. 2011, 286:24242-24252.
106. Villar M.J., Hassell J.R., Brandan E. Interaction of skeletal muscle cells with collagen type IV is mediated by perlecan associated with the cell surface. J. Cell. Biochem. 1999, 75:665-674.
107. Winzen U., Cole G.J., Halfter W. Agrin is a chimeric proteoglycan with the attachment sites for heparan sulfate/chondroitin sulfate located in two multiple serine-glycine clusters. J. Biol. Chem. 2003, 278:30106-30114.
108. Wynn T.A. Cellular and molecular mechanisms of fibrosis. J. Pathol. 2008, 214:199-210.
109. Xu Z., Ichikawa N., Kosaki K., Yamada Y., Sasaki T., Sakai L.Y., Kurosawa H., Hattori N., Arikawa-Hirasawa E. Perlecan deficiency causes muscle hypertrophy, a decrease in myostatin expression, and changes in muscle fiber composition. Matrix Biol. 2010, 29:461-470.
110. Yamaguchi Y. Glycobiology of the synapse: the role of glycans in the formation, maturation, and modulation of synapses. Biochim. Biophys. Acta 2002, 1573:369-376.
111. Yang X., Arber S., William C., Li L., Tanabe Y., Jessell T.M., Birchmeier C., Burden S.J. Patterning of muscle acetylcholine receptor gene expression in the absence of motor innervation. Neuron 2001, 30:399-410.
112. Yayon A., Klagsbrun M., Esko J.D., Leder P., Ornitz D.M. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 1991, 64:841-848.
113. Zanotti S., Negri T., Cappelletti C., Bernasconi P., Canioni E., Di Blasi C., Pegoraro E., Angelini C., Ciscato P., Prelle A., Mantegazza R., Morandi L., Mora M. Decorin and biglycan expression is differentially altered in several muscular dystrophies. Brain 2005, 128:2546-2555.
114. Zhang W., Coldefy A.S., Hubbard S.R., Burden S.J. Agrin binds to the N-terminal region of Lrp4 protein and stimulates association between Lrp4 and the first immunoglobulin-like domain in muscle-specific kinase (MuSK). J. Biol. Chem. 2011, 286:40624-40630.