Decorin enhances the proliferation and differentiation of myogenic cells through suppressing myostatin activity

Journal of Cellular Physiology

Volumn 215, Issue 3, 2008, Pages 856-867

  Kishioka, Yasuhiro ^a   Thomas, Mark ^b   Wakamatsu, Jun Ichi ^a   Hattori, Akihito ^a   Sharma, Mridula ^b   Kambadur, Ravi ^b   Nishimura, Takanori ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b RUAKURA RESEARCH CENTRE   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

DECORIN; MYOD PROTEIN; MYOSTATIN; MESSENGER RNA; PROTEOGLYCAN; SCLEROPROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; GENE EXPRESSION; MOUSE; MUSCLE DEVELOPMENT; MYOBLAST; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; WESTERN BLOTTING; ANIMAL; BIOASSAY; CELL CYCLE; CELL LINE; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUSCLE CELL;

ANIMALS; BIOLOGICAL ASSAY; CELL CYCLE; CELL DIFFERENTIATION; CELL LINE; CELL PROLIFERATION; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION; MICE; MUSCLE FIBERS; MYOBLASTS; PROTEOGLYCANS; RNA, MESSENGER; TRANSFORMING GROWTH FACTOR BETA;

EID: 42949096004     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21371     Document Type: Article

References (51)

1. 2+-dependent phosphorylation of Smad2 at serine-240. Biochem J 362:643-649.
2. Amthor H, Nicholas G, McKinnell I, Kemp CF, Sharma M, Kambadur R, Patel K. 2004. Follistatin complexes Myostatin and antagonises Myostatin-mediated inhibition of myogenesis. Dev Biol 270:19-30.
3. Berkes CA, Tapscott SJ. 2005. MyoD and the transcriptional control of myogenesis. Semin Cell Dev Biol 16:585-595.
4. Bidanset DJ, Guidry C, Rosenberg LC, Choi HU, Timpl R, Hook M. 1992. Binding of the proteoglycan decorin to collagen type VI. J Biol Chem 267:5250-5256.
5. Brandan E, Fuentes ME, Andrade W. 1991. The proteoglycan decorin is synthesized and secreted by differentiated myotubes. Eur J Cell Biol 55:209-216.
6. Cabello-Verrugio C, Brandan E. 2007. A novel modulatory mechanism of TGF-beta signaling through decorin and LRP-I. J Biol Chem 282:18842-18850.
7. Danielson KG, Baribault H, Holmes DF, Graham H, Kadler KE, Iozzo RV. 1997. Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J Cell Biol 136:729-743.
8. Droguett R, Cabello-Verrugio C, Riquelme C, Brandan E. 2006. Extracellular proteoglycans modify TGF-beta bio-availability attenuating its signaling during skeletal muscle differentiation. Matrix Biol 25:332-341.
9. Grobet L, Martin LJ, Poncelet D, Pirottin D, Brouwers B, Riquet J, Schoeberlein A, Dunner S, Menissier F, Massabanda J., et al. 1997. A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nat Genet 17:71-74.
10. Guo K, Wang J, Andres V, Smith RC, Walsh K. 1995. MyoD-induced expression of p21 inhibits cyclin-dependent kinase activity upon myocyte terminal differentiation. Mol Cell Biol 15:3823-3829.
11. Halevy O, Novitch BG, Spicer DB, Skapek SX, Rhee J, Hannon GJ, Beach D, Lassar AB. 1995. Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science 267:1018-1021.
12. Hausser H, Gröning A, Hasilik A, Schönherr E, Kresse H. 1994. Selective inactivity of TGF-beta/decorin complexes. FEBS Lett 353:243-245.
13. Hill JJ, Davies MV, Pearson AA, Wang JH, Hewick RM, Wolfman NM, Qiu Y. 2002. The myostatin propeptide and the follistatin-related gene are inhibitory binding proteins of myostatin in normal serum. J Biol Chem 277:40735-40741.
14. Iozzo RV, Moscatello DK, McQuillan DJ, Eichstetter I. 1999. Decorin is a biological ligand for the epidermal growth factor receptor. J Biol Chem 274:4489-4492.
15. Joulia D, Bernardi H, Garandel V, Rabenoelina F, Vernus B, Cabello G. 2003. Mechanisms involved in the inhibition of myoblast proliferation and differentiation by myostatin. Exp Cell Res 286:263-275.
16. Kambadur R, Sharma M, Smith TP, Bass JJ. 1997. Mutations in myostatin (GDF8) in double-muscled Belgian Blue and Piedmontese cattle. Genome Res 7:910-916.
17. Kitzmann M, Carnac G, Vandromme M, Primig M, Lamb NJ, Fernandez A. 1998. The muscle regulatory factors MyoD and myf-5 undergo distinct cell cycle-specific expression in muscle cells. J Cell Biol 142:1447-1459.
18. Krusius T, Ruoslahti E. 1986. Primary structure of an extracellular matrix proteoglycan core protein deduced from cloned cDNA. Proc Nat Acad Sci USA 83:7683-7687.
19. Langley B, Thomas M, Bishop A, Sharma M, Gilmour S, Kambadur R. 2002. Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. J Biol Chem 277:49831-49840.
20. Langley B, Thomas M, McFarlane C, Gilmour S, Sharma M, Kambadur R. 2004. Myostatin inhibits rhabdomyosarcoma cell proliferation through an Rb-independent pathway. Oncogene 23:524-534.
21. Lathrop B, Thomas K, Glaser L. 1985. Control of myogenic differentiation by fibroblast growth factor is mediated by position in the G1 phase of the cell cycle. J Cell Biol 101:2194-2198.
22. Li Y, Li J, Zhu J, Sun B, Branca M, Tang Y, Foster W, Xiao X, Huard J. 2007. Decorin gene transfer promotes muscle cell differentiation and muscle regeneration. Mol Ther 15:1616-1622.
23. McCroskery S, Thomas M, Maxwell L, Sharma M, Kambadur R. 2003. Myostatin negatively regulates satellite cell activation and self-renewal. J Cell Biol 162:1135-1147.
24. McPherron AC, Lee SJ. 1997. Double muscling in cattle due to mutations in the myostatin gene. Proc Natl Acad Sci USA 94:12457-12461.
25. McPherron AC, Lawler AM, Lee SJ. 1997. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387:83-90.
26. Miura T, Kishioka Y, Wakamatsu J, Hattori A, Hennebry A, Berry CJ, Sharma M, Kambadur R, Nishimura T. 2006. Decorin binds myostatin and modulates its activity to muscle cells. Biochem Biophys Res Commun 340:675-680.
27. Nicholas G, Thomas M, Langley B, Somers W, Patel K, Kemp CF, Sharma M, Kambadur R. 2002. Titin-cap associates with, and regulates secretion of, Myostatin. J Cell Physiol 193:120-131.
28. Nili N, Cheema AN, Giordano FJ, Barolet AW, Babaei S, Hickey R, Eskandarian MR, Smeets M, Butany J, Pasterkamp G., et al. 2003. Decorin inhibition of PDGF-stimulated vascular smooth muscle cell function: Potential mechanism for inhibition of intimal hyperplasia after balloon angioplasty. Am J Pathol 163:869-878.
29. Olguin HC, Santander C, Brandan E. 2003. Inhibition of myoblast migration via decorin expression is critical for normal skeletal muscle differentiation. Dev Biol 259:209-224.
30. Oliver MH, Harrison NK, Bishop JE, Cole PJ, Laurent GJ. 1989. A rapid and convenient assay for counting cells cultured in microwell plates: Application for assessment of growth factors. J Cell Sci 92:513-518.
31. Patel S, Santra M, McQuillan DJ, Iozzo RV, Thomas AP. 1998. Decorin activates the epidermal growth factor receptor and elevates cytosolic Ca2+ in A431 carcinoma cells. J Biol Chem 273:3121-3124.
32. Philip B, Lu Z, Gao Y. 2005. Regulation of GDF-8 signaling by the p38 MAPK. Cell Signal 17:365-375.
33. Rada JA, Cornuet PK, Hassell JR. 1993. Regulation of corneal collagen fibrillogenesis in vitro by corneal proteoglycan (lumican and decorin) core proteins. Exp Eye Res 56:635-648.
34. Ríos R, Fernandez-Nocelos S, Carneiro I, Arce VM, Devesa J. 2004. Differential response to exogenous and endogenous myostatin in myoblasts suggests that myostatin acts as an autocrine factor in vivo. Endocrinology 145:2795-2803.
35. Riquelme C, Larrain J, Schönherr E, Henriquez JP, Kresse H, Brandan E. 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.
36. Rosenthal SM, Cheng ZQ. 1995. Opposing early and late effects of insulin-like growth factor I on differentiation and the cell cycle regulatory retinoblastoma protein in skeletal myoblasts. Proc Natl Acad Sci USA 92:10307-10311.
37. Santra M, Mann DM, Mercer EW, Skorski T, Calabretta B, Iozzo RV. 1997. Ectopic expression of decorin protein core causes a generalized growth suppression in neoplastic cells of various histogenetic origin and requires endogenous p21, an inhibitor of cyclin-dependent kinases. J Clin Invest 100:149-157.
38. Schaefer L, Tsalastra W, Babelova A, Baliova M, Minnerup J, Sorokin L, Grone HJ, Reinhardt DP, Pfeilschifter J, Iozzo RV. et al., 2007. Decorin-mediated regulation of fibrillin-1 in the kidney involves the insulin-like growth factor-1 receptor and Mammalian target of rapamycin. Am J Pathol 170:301-315.
39. Schönherr E, Hausser H, Beavan L, Kresse H. 1995. Decorin-type I collagen interaction. Presence of separate core protein-binding domains. J Biol Chem 270:8877-8883.
40. Schönherr E, Broszat M, Brandan E, Bruckner P, Kresse H. 1998. Decorin core protein fragment Leu 155-Val260 interacts with TGF-beta but does not compete for decorin binding to type I collagen. Arch Biochem Biophys 355:241-248.
41. Schönherr E, Sunderkotter C, Iozzo RV, Schaefer L. 2005. Decorin, a novel player in the insulin-like growth factor system. J Biol Chem 280:15767-15772.
42. Sharma M, Kambadur R, Matthews KG, Somers WG, Devlin GP, Conaglen JV, Fowke PJ, Bass JJ. 1999. Myostatin, a transforming growth factor-beta super-family member, is expressed in heart muscle and is upregulated in cardiomyocytes after infarct. J Cell Physiol 180:1-9.
43. Shen X, Collier JM, Hlaing M, Zhang L, Delshad EH, Bristow J, Bernstein HS. 2003. Genome-wide examination of myoblast cell cycle withdrawal during differentiation. Dev Dyn 226:128-138.
44. Takeuchi Y, Kodama Y, Matsumoto T. 1994. Bone matrix decorin binds transforming growth factor-beta and enhances its bioactivity. J Biol Chem 269:32634-32638.
45. Thies RS, Chen T, Davies MV, Tomkinson KN, Pearson AA, Shakey QA, Wolfman NM. 2001. GDF-8 propeptide binds to GDF-8 and antagonizes biological activity by inhibiting GDF-8 receptor binding. Growth Factors 18:251-259.
46. Thomas M, Langley B, Berry C, Sharma M, Kirk S, Bass J, Kambadur R. 2000. Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J Biol Chem 275:40235-10243.
47. Villena J, Brandan E. 2004. Dermatan sulfate exerts an enhanced growth factor response on skeletal muscle satellite cell proliferation and migration. J Cell Physiol 198:169-178.
48. Yaffe D, Saxel O. 1977. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270:725-727.
49. Yamaguchi Y, Ruoslahti E. 1988. Expression of human proteoglycan in Chinese hamster ovary cells inhibits cell proliferation. Nature 336:244-246.
50. Yamaguchi Y, Mann DM, Ruoslahti E. 1990. Negative regulation of transforming growth factor-beta by the proteoglycan decorin. Nature 346:281-284.
51. Zhu J, Li Y, Shen W, Qiao C, Ambrosio F, Lavasani M, Nozaki M, Branca MF, Huard J. 2007. Relationships between TGF-beta-1, myostatin, and decorin: Implications for skeletal muscle fibrosis. J Biol Chem 282:25852-25863.