46
Views
87
CrossRef citations to date
0
Altmetric
Article

A Novel Mechanism of Sequestering Fibroblast Growth Factor 2 by Glypican in Lipid Rafts, Allowing Skeletal Muscle Differentiation

&
Pages 1634-1649 | Received 28 Aug 2009, Accepted 14 Jan 2010, Published online: 20 Mar 2023

REFERENCES

  • Akiyama, S., T. Katagiri, M. Namiki, N. Yamaji, N. Yamamoto, K. Miyama, H. Shibuya, N. Ueno, J. M. Wozney, and T. Suda. 1997. Constitutively active BMP type I receptors transduce BMP-2 signals without the ligand in C2C12 myoblasts. Exp. Cell Res. 235:362–369.
  • Anastasi, S., S. Giordano, O. Sthandier, G. Gambarotta, R. Maione, P. Comoglio, and P. Amati. 1997. 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. 137:1057–1068.
  • Ashikari, S., H. Habuchi, and K. Kimata. 1995. Characterization of heparan sulfate oligosaccharides that bind to hepatocyte growth factor. J. Biol. Chem. 270:29586–29593.
  • Beer, C., L. Pedersen, and M. Wirth. 2005. Amphotropic murine leukaemia virus envelope protein is associated with cholesterol-rich microdomains. Virol. J. 2:36.
  • Bernfield, M., M. Gotte, P. W. Park, O. Reizes, M. L. Fitzgerald, J. Lincecum, and M. Zako. 1999. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68:729–777.
  • Bernfield, M., and R. D. Sanderson. 1990. Syndecan, a developmentally regulated cell surface proteoglycan that binds extracellular matrix and growth factors. Philos. Trans. R. Soc. Lond. B Biol. Sci. 327:171–186.
  • Brady, J. D., T. C. Rich, X. Le, K. Stafford, C. J. Fowler, L. Lynch, J. W. Karpen, R. L. Brown, and J. R. Martens. 2004. Functional role of lipid raft microdomains in cyclic nucleotide-gated channel activation. Mol. Pharmacol. 65:503–511.
  • Brandan, E., D. J. Carey, J. Larrain, F. Melo, and A. Campos. 1996. Synthesis and processing of glypican during differentiation of skeletal muscle cells. Eur. J. Cell Biol. 71:170–176.
  • Brandan, E., and J. Larraín. 1998. Heparan sulfate proteoglycans during terminal skeletal muscle cell differentiation: possible functions and regulation of their expression. Basic Appl. Myol. 8:107–114.
  • Brandan, E., M. Maldonado, J. Garrido, and N. C. Inestrosa. 1985. Anchorage of collagen-tailed acetylcholinesterase to the extracellular matrix is mediated by heparan sulfate proteoglycans. J. Cell Biol. 101:985–992.
  • Brown, D. 1994. GPI-anchored proteins and detergent-resistant membrane domains. Braz. J. Med. Biol. Res. 27:309–315.
  • Brown, D. A., and E. London. 1998. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14:111–136.
  • Brunetti, A., and I. D. Goldfine. 1990. Role of myogenin in myoblast differentiation and its regulation by fibroblast growth factor. J. Biol. Chem. 265:5960–5963.
  • Campos, A., R. Nunez, C. S. Koenig, D. J. Carey, and E. Brandan. 1993. A lipid-anchored heparan sulfate proteoglycan is present in the surface of differentiated skeletal muscle cells. Isolation and biochemical characterization. Eur. J. Biochem. 216:587–595.
  • Capurro, M. I., Y. Y. Xiang, C. Lobe, and J. Filmus. 2005. Glypican-3 promotes the growth of hepatocellular carcinoma by stimulating canonical Wnt signaling. Cancer Res. 65:6245–6254.
  • Capurro, M. I., P. Xu, W. Shi, F. Li, A. Jia, and J. Filmus. 2008. Glypican-3 inhibits Hedgehog signaling during development by competing with patched for Hedgehog binding. Dev. Cell 14:700–711.
  • Casar, J. C., C. Cabello-Verrugio, H. Olguin, R. Aldunate, N. C. Inestrosa, and E. Brandan. 2004. Heparan sulfate proteoglycans are increased during skeletal muscle regeneration: requirement of syndecan-3 for successful fiber formation. J. Cell Sci. 117:73–84.
  • Catlow, K. R., J. A. Deakin, Z. Wei, M. Delehedde, D. G. Fernig, E. Gherardi, J. T. Gallagher, M. S. Pavao, and M. Lyon. 2008. Interactions of hepatocyte growth factor/scatter factor with various glycosaminoglycans reveal an important interplay between the presence of iduronate and sulfate density. J. Biol. Chem. 283:5235–5248.
  • Chernousov, M. A., and D. J. Carey. 1993. N-syndecan (syndecan 3) from neonatal rat brain binds basic fibroblast growth factor. J. Biol. Chem. 268:16810–16814.
  • Choi, S. C., S. J. Kim, J. H. Choi, C. Y. Park, W. J. Shim, and D. S. Lim. 2008. Fibroblast growth factor-2 and -4 promote the proliferation of bone marrow mesenchymal stem cells by the activation of the PI3K-Akt and ERK1/2 signaling pathways. Stem Cells Dev. 17:725–736.
  • Cornelison, D., M. Filla, H. Stanley, A. Rapraeger, and B. Olwin. 2001. Syndecan-3 and syndecan-4 specifically mark skeletal muscle satellite cells and are implicated in satellite cell maintenance and muscle regeneration. Dev. Biol. 239:79–94.
  • Cornelison, D., and B. Wold. 1997. Single-cell analysis of regulatory gene expression in quiescent and activated mouse skeletal muscle satellite cells. Dev. Biol. 191:270–283.
  • Cornelison, D. D., B. B. Olwin, M. A. Rudnicki, and B. J. Wold. 2000. MyoD(-/-) satellite cells in single-fiber culture are differentiation defective and MRF4 deficient. Dev. Biol. 224:122–137.
  • Cornelison, D. D., S. A. Wilcox-Adelman, P. F. Goetinck, H. Rauvala, A. C. Rapraeger, and B. B. Olwin. 2004. Essential and separable roles for Syndecan-3 and Syndecan-4 in skeletal muscle development and regeneration. Genes Dev. 18:2231–2236.
  • Couchman, J. R. 2003. Syndecans: proteoglycan regulators of cell-surface microdomains? Nat. Rev. Mol. Cell Biol. 4:926–937.
  • Droguett, R., C. Cabello-Verrugio, C. Riquelme, and E. Brandan. 2006. Extracellular proteoglycans modifies TGF-beta bio-availability attenuating its signaling during skeletal muscle differentiation. Matrix Biol. 25:332–341.
  • Fico, A., F. Maina, and R. Dono. 18 December 2007, posting date. Fine-tuning of cell signalling by glypicans. Cell. Mol. Life Sci. [Epub ahead of print.]
  • Filla, M. S., P. Dam, and A. C. Rapraeger. 1998. The cell surface proteoglycan syndecan-1 mediates fibroblast growth factor-2 binding and activity. J. Cell. Physiol. 174:310–321.
  • Filmus, J., and M. Capurro. 2008. The role of glypican-3 in the regulation of body size and cancer. Cell Cycle 7:2787–2790.
  • Filmus, J., and S. B. Selleck. 2001. Glypicans: proteoglycans with a surprise. J. Clin. Investig. 108:497–501.
  • Fransson, L. A. 2003. Glypicans. Int. J. Biochem. Cell Biol. 35:125–129.
  • Fuentealba, L., D. J. Carey, and E. Brandan. 1999. Antisense inhibition of syndecan-3 expression during skeletal muscle differentiation accelerates myogenesis through a basic fibroblast growth factor-dependent mechanism. J. Biol. Chem. 274:37876–37884.
  • Galbiati, F., D. Volonte, J. A. Engelman, P. E. Scherer, and M. P. Lisanti. 1999. Targeted down-regulation of caveolin-3 is sufficient to inhibit myotube formation in differentiating C2C12 myoblasts. Transient activation of p38 mitogen-activated protein kinase is required for induction of caveolin-3 expression and subsequent myotube formation. J. Biol. Chem. 274:30315–30321.
  • García-Olivas, R., J. Hoebeke, S. Castel, M. Reina, G. Fager, F. Lustig, and S. Vilaro. 2003. Differential binding of platelet-derived growth factor isoforms to glycosaminoglycans. Histochem. Cell Biol. 120:371–382.
  • García-Olivas, R., S. Vilaro, M. Reina, and S. Castel. 2007. PDGF-stimulated cell proliferation and migration of human arterial smooth muscle cells. Colocalization of PDGF isoforms with glycosaminoglycans. Int. J. Biochem. Cell Biol. 39:1915–1929.
  • Gutierrez, J., N. Osses, and E. Brandan. 2006. 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. 206:58–67.
  • Hartung, A., K. Bitton-Worms, M. M. Rechtman, V. Wenzel, J. H. Boergermann, S. Hassel, Y. I. Henis, and P. Knaus. 2006. Different routes of bone morphogenic protein (BMP) receptor endocytosis influence BMP signaling. Mol. Cell. Biol. 26:7791–7805.
  • Hering, H., C. C. Lin, and M. Sheng. 2003. Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. J. Neurosci. 23:3262–3271.
  • Itoh, N., T. Mima, and T. Mikawa. 1996. Loss of fibroblast growth factor receptors is necessary for terminal differentiation of embryonic limb muscle. Development 122:291–300.
  • Jenniskens, G. J., J. H. Veerkamp, and T. H. van Kuppevelt. 2006. Heparan sulfates in skeletal muscle development and physiology. J. Cell. Physiol. 206:283–294.
  • Kwiatkowski, B. A., I. Kirillova, R. E. Richard, D. Israeli, and Z. Yablonka-Reuveni. 2008. FGFR4 and its novel splice form in myogenic cells: Interplay of glycosylation and tyrosine phosphorylation. J. Cell. Physiol. 215:803–817.
  • Larraín, J., D. J. Carey, and E. Brandan. 1998. Syndecan-1 expression inhibits myoblast differentiation through a basic fibroblast growth factor-dependent mechanism. J. Biol. Chem. 273:32288–32296.
  • Larrain, J., G. Cizmeci-Smith, V. Troncoso, R. C. Stahl, D. J. Carey, and E. Brandan. 1997. Syndecan-1 expression is down-regulated during myoblast terminal differentiation. Modulation By growth factors and retinoic acid. J. Biol. Chem. 272:18418–18424.
  • Le Roy, C., and J. L. Wrana. 2005. Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat. Rev. Mol. Cell Biol. 6:112–126.
  • Liu, W., E. D. Litwack, M. J. Stanley, J. K. Langford, A. D. Lander, and R. D. Sanderson. 1998. Heparan sulfate proteoglycans as adhesive and anti-invasive molecules. Syndecans and glypican have distinct functions. J. Biol. Chem. 273:22825–22832.
  • Lyon, M., J. A. Deakin, K. Mizuno, T. Nakamura, and J. T. Gallagher. 1994. Interaction of hepatocyte growth factor with heparan sulfate. Elucidation of the major heparan sulfate structural determinants. J. Biol. Chem. 269:11216–11223.
  • Lyon, M., G. Rushton, and J. T. Gallagher. 1997. The interaction of the transforming growth factor-betas with heparin/heparan sulfate is isoform-specific. J. Biol. Chem. 272:18000–18006.
  • Mansukhani, A., P. Dell'Era, D. Moscatelli, S. Kornbluth, H. Hanafusa, and C. Basilico. 1992. Characterization of the murine BEK fibroblast growth factor (FGF) receptor: activation by three members of the FGF family and requirement for heparin. Proc. Natl. Acad. Sci. USA 89:3305–3309.
  • Massagué, J., S. Cheifetz, T. Endo, and B. Nadal-Ginard. 1986. Type beta transforming growth factor is an inhibitor of myogenic differentiation. Proc. Natl. Acad. Sci. USA 83:8206–8210.
  • McQuade, K. J., and A. C. Rapraeger. 2003. Syndecan-1 transmembrane and extracellular domains have unique and distinct roles in cell spreading. J. Biol. Chem. 278:46607–46615.
  • Melo, F., D. J. Carey, and E. Brandan. 1996. Extracellular matrix is required for skeletal muscle differentiation but not myogenin expression. J. Cell. Biochem. 62:227–239.
  • Midorikawa, Y., S. Ishikawa, H. Iwanari, T. Imamura, H. Sakamoto, K. Miyazono, T. Kodama, M. Makuuchi, and H. Aburatani. 2003. Glypican-3, overexpressed in hepatocellular carcinoma, modulates FGF2 and BMP-7 signaling. Int. J. Cancer 103:455–465.
  • Mohammadi, M., S. K. Olsen, and O. A. Ibrahimi. 2005. Structural basis for fibroblast growth factor receptor activation. Cytokine Growth Factor Rev. 16:107–137.
  • Olguin, H., and E. Brandan. 2001. Expression and localization of proteoglycans during limb myogenic activation. Dev. Dyn. 221:106–115.
  • Olwin, B. B., and A. Rapraeger. 1992. Repression of myogenic differentiation by aFGF, bFGF, and K-FGF is dependent on cellular heparan sulfate. J. Cell Biol. 118:631–639.
  • Ornitz, D. M., J. Xu, J. S. Colvin, D. G. McEwen, C. A. MacArthur, F. Coulier, G. Gao, and M. Goldfarb. 1996. Receptor specificity of the fibroblast growth factor family. J. Biol. Chem. 271:15292–15297.
  • Osses, N., and E. Brandan. 2002. ECM is required for skeletal muscle differentiation independently of muscle regulatory factor expression. Am. J. Physiol. Cell Physiol. 282:C383–C394.
  • Osterholm, C., M. M. Barczyk, M. Busse, M. Gronning, R. K. Reed, and M. Kusche-Gullberg. 2009. Mutation in the heparan sulfate biosynthesis enzyme EXT1 influences growth factor signaling and fibroblast interactions with the extracellular matrix. J. Biol. Chem. 284:34935–34943.
  • Ostermeyer, A. G., B. T. Beckrich, K. A. Ivarson, K. E. Grove, and D. A. Brown. 1999. Glycosphingolipids are not essential for formation of detergent-resistant membrane rafts in melanoma cells. Methyl-beta-cyclodextrin does not affect cell surface transport of a GPI-anchored protein. J. Biol. Chem. 274:34459–34466.
  • Patel, S. G., P. E. Funk, and J. X. DiMario. 1999. Regulation of avian fibroblast growth factor receptor 1 (FGFR-1) gene expression during skeletal muscle differentiation. Gene 237:265–276.
  • Pellegrini, L. 2001. Role of heparan sulfate in fibroblast growth factor signalling: a structural view. Curr. Opin. Struct. Biol. 11:629–634.
  • Peng, H., H. Xie, S. Rossi, and R. Rotundo. 1999. Acetylcholinesterase clustering at the neuromuscular junction involves perlecan and dystroglycan. J. Cell Biol. 145:911–921.
  • Plotnikov, A. N., J. Schlessinger, S. R. Hubbard, and M. Mohammadi. 1999. Structural basis for FGF receptor dimerization and activation. Cell 98:641–650.
  • Rapraeger, A. 2000. Syndecan-regulated receptor signaling. J. Cell Biol. 149:995–998.
  • Rapraeger, A. C., A. Krufka, and B. B. Olwin. 1991. Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 252:1705–1708.
  • Rider, C. C. 2006. Heparin/heparan sulphate binding in the TGF-beta cytokine superfamily. Biochem. Soc. Trans. 34:458–460.
  • Riquelme, C., J. Larrain, E. Schonherr, J. P. Henriquez, H. Kresse, and E. Brandan. 2001. Antisense inhibition of decorin expression in myoblasts decreases cell responsiveness to transforming growth factor beta and accelerates skeletal muscle differentiation. J. Biol. Chem. 276:3589–3596.
  • Rolny, C., D. Spillmann, U. Lindahl, and L. Claesson-Welsh. 2002. Heparin amplifies platelet-derived growth factor (PDGF)-BB-induced PDGF alpha-receptor but not PDGF beta-receptor tyrosine phosphorylation in heparan sulfate-deficient cells. Effects on signal transduction and biological responses. J. Biol. Chem. 277:19315–19321.
  • Rudnicki, M. A., and R. Jaenisch. 1995. The MyoD family of transcription factors and skeletal myogenesis. Bioessays 17:203–209.
  • Sabourin, L. A., and M. A. Rudnicki. 2000. The molecular regulation of myogenesis. Clin. Genet. 57:16–25.
  • Schlessinger, J., A. N. Plotnikov, O. A. Ibrahimi, A. V. Eliseenkova, B. K. Yeh, A. Yayon, R. J. Linhardt, and M. Mohammadi. 2000. Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol. Cell 6:743–750.
  • Seale, P., and M. Rudnicki. 2000. A new look at the origin, function, and “stem-cell” status of muscle satellite cells. Dev. Biol. 218:115–124.
  • Seveau, S., H. Bierne, S. Giroux, M. C. Prevost, and P. Cossart. 2004. Role of lipid rafts in E-cadherin- and HGF-R/Met-mediated entry of Listeria monocytogenes into host cells. J. Cell Biol. 166:743–753.
  • Sheehan, S., and R. Allen. 1999. Skeletal muscle satellite cell proliferation in response to members of the fibroblast growth factor family and hepatocyte growth factor. J. Cell. Physiol. 181:499–506.
  • Shi, Y., and J. Massague. 2003. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113:685–700.
  • Song, H. H., W. Shi, and J. Filmus. 1997. OCI-5/rat glypican-3 binds to fibroblast growth factor-2 but not to insulin-like growth factor-2. J. Biol. Chem. 272:7574–7577.
  • Spizz, G., J. S. Hu, and E. N. Olson. 1987. Inhibition of myogenic differentiation by fibroblast growth factor or type beta transforming growth factor does not require persistent c-myc expression. Dev. Biol. 123:500–507.
  • Steinfeld, R., H. Van Den Berghe, and G. David. 1996. Stimulation of fibroblast growth factor receptor-1 occupancy and signaling by cell surface-associated syndecans and glypican. J. Cell Biol. 133:405–416.
  • Stetzkowski-Marden, F., K. Gaus, M. Recouvreur, A. Cartaud, and J. Cartaud. 2006. Agrin elicits membrane lipid condensation at sites of acetylcholine receptor clusters in C2C12 myotubes. J. Lipid Res. 47:2121–2133.
  • Su, G., K. Meyer, C. D. Nandini, D. Qiao, S. Salamat, and A. Friedl. 2006. Glypican-1 is frequently overexpressed in human gliomas and enhances FGF-2 signaling in glioma cells. Am. J. Pathol. 168:2014–2026.
  • Tkachenko, E., and M. Simons. 2002. Clustering induces redistribution of syndecan-4 core protein into raft membrane domains. J. Biol. Chem. 277:19946–19951.
  • Tortorella, L. L., D. J. Milasincic, and P. F. Pilch. 2001. Critical proliferation-independent window for basic fibroblast growth factor repression of myogenesis via the p42/p44 MAPK signaling pathway. J. Biol. Chem. 276:13709–13717.
  • Villena, J., C. Berndt, F. Granes, M. Reina, and S. Vilaro. 2003. Syndecan-2 expression enhances adhesion and proliferation of stably transfected Swiss 3T3 cells. Cell Biol. Int. 27:1005–1010.
  • Yaffe, D., and O. Saxel. 1977. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270:725–727.
  • Yang, Y., M. Borset, J. K. Langford, and R. D. Sanderson. 2003. Heparan sulfate regulates targeting of syndecan-1 to a functional domain on the cell surface. J. Biol. Chem. 3:3.
  • Yayon, A., M. Klagsbrun, J. D. Esko, P. Leder, and D. M. Ornitz. 1991. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64:841–848.
  • Yu, S., L. Zheng, D. K. Trinh, S. L. Asa, and S. Ezzat. 2004. Distinct transcriptional control and action of fibroblast growth factor receptor 4 in differentiating skeletal muscle cells. Lab. Investig. 84:1571–1580.
  • Zhang, Y., J. Li, C. Partovian, F. W. Sellke, and M. Simons. 2003. Syndecan-4 modulates basic fibroblast growth factor 2 signaling in vivo. Am. J. Physiol. Heart Circ. Physiol. 284:H2078–H2082.
  • Zhao, P., G. Caretti, S. Mitchell, W. L. McKeehan, A. L. Boskey, L. M. Pachman, V. Sartorelli, and E. P. Hoffman. 2006. Fgfr4 is required for effective muscle regeneration in vivo. Delineation of a MyoD-Tead2-Fgfr4 transcriptional pathway. J. Biol. Chem. 281:429–438.
  • Zhu, D., W. C. Xiong, and L. Mei. 2006. Lipid rafts serve as a signaling platform for nicotinic acetylcholine receptor clustering. J. Neurosci. 26:4841–4851.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.