The internal region leucine-rich repeat 6 of decorin interacts with low density lipoprotein receptor-related protein-1, modulates Transforming Growth Factor (TGF)-β-dependent signaling, and inhibits TGF-β-dependent fibrotic response in skeletal muscles

Journal of Biological Chemistry

Volumn 287, Issue 9, 2012, Pages 6773-6787

  Cabello Verrugio, Claudio ^a,b   Santander, Cristian ^a   Cofré, Catalina ^a   Acuña, Maria José ^a   Melo, Francisco ^a   Brandan, Enrique ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b UNIVERSIDAD DEL DESARROLLO   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

DECORIN; DELETION MUTANTS; GROWTH FACTOR; IN-VIVO; LEUCINE-RICH REPEATS; LOW DENSITY LIPOPROTEINS; PATHOLOGICAL PROCESS; PROTEOGLYCANS; RECEPTOR-RELATED PROTEINS; SIGNALING PATHWAYS; SKELETAL MUSCLE; TRANSFORMING GROWTH FACTORS;

AMINO ACIDS; PEPTIDES; PHYSIOLOGICAL MODELS; SIGNALING; TISSUE;

GLYCOPROTEINS;

AMINO ACID; DECORIN; LEUCINE RICH REPEAT KINASE 2; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DELETION MUTANT; ENDOCYTOSIS; GENE DELETION; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SKELETAL MUSCLE;

ANIMALS; CELL LINE; CHO CELLS; CRICETINAE; DECORIN; ENDOCYTOSIS; FIBROSIS; GLYBURIDE; HUMANS; LEUCINE; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-1; MALE; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; MYOBLASTS, SKELETAL; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84857479041     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.312488     Document Type: Article

References (64)

1. Massagué, J. (1998) TGF-β signal transduction. Annu. Rev. Biochem. 67, 753-791
2. Gray, P. C., Bilezikjian, L. M., and Vale, W. (2002) Antagonism of activin by inhibin and inhibin receptors. A functional role for betaglycan. Mol. Cell. Endocrinol. 188, 254-260
3. Massagué, J., and Gomis, R. R. (2006) The logic of TGF-β a signaling. FEBS Lett. 580, 2811-2820
4. Kang, J. S., Liu, C., and Derynck, R. (2009) New regulatory mechanisms of TGF-β receptor function. Trends Cell Biol. 19, 385-394
5. Brandan, E., Retamal, C., Cabello-Verrugio, C., and Marzolo, M. P. (2006) The low density lipoprotein receptor-related protein functions as an endocytic receptor for decorin. J. Biol. Chem. 281, 31562-31571 (Pubitemid 46041422)
6. Cabello-Verrugio, C., and Brandan, E. (2007) A novel modulatory mechanism of transforming growth factor-β signaling through decorin and LRP-1. J. Biol. Chem. 282, 18842-18850 (Pubitemid 47100183)
7. Herz, J., and Strickland, D. K. (2001) LRP, a multifunctional scavenger and signaling receptor. J. Clin. Invest. 108, 779-784 (Pubitemid 32880284)
8. Gonias, S. L., Wu, L., and Salicioni, A. M. (2004) Low density lipoprotein receptor-related protein. Regulation of the plasma membrane proteome. Thromb. Haemost. 91, 1056-1064 (Pubitemid 38821260)
9. Brandan, E., Cabello-Verrugio, C., and Vial, C. (2008) Novel regulatory mechanisms for the proteoglycans decorin and biglycan during muscle formation and muscular dystrophy. Matrix Biol. 27, 700-708
10. Riquelme, C., Larrain, J., Schonherr, E., Henriquez, J. P., Kresse, H., and 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
11. Derynck, R., and Zhang, Y. E. (2003) Smad-dependent and Smad-independent pathways in TGF-β family signaling. Nature 425, 577-584 (Pubitemid 37280136)
12. Iozzo, R. V. (1999) The biology of the small leucine-rich proteoglycans. Functional network of interactive proteins. J. Biol. Chem. 274, 18843-18846
13. McEwan, P. A., Scott, P. G., Bishop, P. N., and Bella, J. (2006) Structural correlations in the family of small leucine-rich repeat proteins and proteoglycans. J. Struct. Biol. 155, 294-305 (Pubitemid 44278663)
14. Schaefer, L., and Iozzo, R. V. (2008) Biological functions of the small leucine- rich proteoglycans. From genetics to signal transduction. J. Biol. Chem. 283, 21305-21309
15. Kobe, B., and Kajava, A. V. (2001) The leucine-rich repeat as a protein recognition motif. Curr. Opin. Struct. Biol. 11, 725-732 (Pubitemid 34076634)
16. Cáceres, S., Cuellar, C., Casar, J. C., Garrido, J., Schaefer, L., Kresse, H., and Brandan, E. (2000) Synthesis of proteoglycans is augmented in dystrophic mdx mouse skeletal muscle. Eur. J. Cell Biol. 79, 173-181 (Pubitemid 30179501)
17. Fadic, R., Mezzano, V., Alvarez, K., Cabrera, D., Holmgren, J., and Brandan, E. (2006) 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. 10, 758-769 (Pubitemid 44874284)
18. Droguett, R., Cabello-Verrugio, C., Riquelme, C., and Brandan, E. (2006) Extracellular proteoglycans modify TGF-β bioavailability attenuating its signaling during skeletal muscle differentiation. Matrix Biol. 25, 332-341 (Pubitemid 44202585)
19. Iozzo, R. V., and Schaefer, L. (2010) Proteoglycans in health and disease. Novel regulatory signaling mechanisms evoked by the small leucine-rich proteoglycans. FEBS J. 277, 3864-3875
20. Schönherr, E., Sunderkötter, C., Iozzo, R. V., and Schaefer, L. (2005) Decorin, a novel player in the insulin-like growth factor system. J. Biol. Chem. 280, 15767-15772 (Pubitemid 40616696)
21. Schaefer, L., Tsalastra, W., Babelova, A., Baliova, M., Minnerup, J., Sorokin, L., Gröne, H. J., Reinhardt, D. P., Pfeilschifter, J., Iozzo, R. V., and Schaefer, R. M. (2007) Decorin-mediated regulation of fibrillin-1 in the kidney involves the insulin-like growth factor-I receptor and mammalian target of rapamycin. Am. J. Pathol. 170, 301-315 (Pubitemid 47339209)
22. Moscatello, D. K., Santra, M., Mann, D. M., McQuillan, D. J., Wong, A. J., and Iozzo, R. V. (1998) Decorin suppresses tumor cell growth by activating the epidermal growth factor receptor. J. Clin. Invest. 101, 406-412 (Pubitemid 28067338)
23. Takeuchi, Y., Kodama, Y., and Matsumoto, T. (1994) Bone matrix decorin binds transforming growth factor-β and enhances its bioactivity. J. Biol. Chem. 269, 32634-32638
24. Yamaguchi, Y., Mann, D. M., and Ruoslahti, E. (1990) Negative regulation of transforming growth factor-β by the proteoglycan decorin. Nature 346, 281-284
25. Vial, C., Gutiérrez, J., Santander, C., Cabrera, D., and Brandan, E. (2011) Decorin interacts with connective tissue growth factor (CTGF)/CCN2 by LRR12 inhibiting its biological activity. J. Biol. Chem. 286, 24242-24252
26. Goldoni, S., Humphries, A., Nyström, A., Sattar, S., Owens, R. T., McQuillan, D. J., Ireton, K., and Iozzo, R. V. (2009) Decorin is a novel antagonistic ligand of the Met receptor. J. Cell Biol. 185, 743-754
27. Olguin, H. C., Santander, C., and Brandan, E. (2003) Inhibition of myoblast migration via decorin expression is critical for normal skeletal muscle differentiation. Dev. Biol. 259, 209-224 (Pubitemid 36836141)
28. Bolster, M. B., and Silver, R. M. (1993) Lung disease in systemic sclerosis (scleroderma). Baillieres Clin. Rheumatol. 7, 79-97 (Pubitemid 23071215)
29. Ziyadeh, F. N. (1993) The extracellular matrix in diabetic nephropathy. Am. J. Kidney. Dis. 22, 736-744
30. Wynn, T. A. (2008) Cellular and molecular mechanisms of fibrosis. J. Pathol. 214, 199-210
31. Denton, C. P., and Abraham, D. J. (2001) Transforming growth factor-β and connective tissue growth factor. Key cytokines in scleroderma pathogenesis. Curr. Opin. Rheumatol. 13, 505-511 (Pubitemid 33070969)
32. Bernasconi, P., Di Blasi, C., Mora, M., Morandi, L., Galbiati, S., Confalonieri, P., Cornelio, F., and Mantegazza, R. (1999) Transforming growth factor-β 1 and fibrosis in congenital muscular dystrophies. Neuromusc. Disord. 9, 28-33 (Pubitemid 29079470)
33. Alvarez, K., Fadic, R., and Brandan, E. (2002) Augmented synthesis and differential localization of heparan sulfate proteoglycans in Duchenne muscular dystrophy. J. Cell. Biochem. 85, 703-713 (Pubitemid 34462781)
34. Schiaffino, S., and Partridge, T. (2008) Advances in Muscle Research, Vol. 3, pp. XIV-380, Springer, The Netherlands
35. Caldwell, C. J., Mattey, D. L., and Weller, R. O. (1990) Role of the basement membrane in the regeneration of skeletal muscle. Neuropathol. Appl. Neurobiol. 16, 225-238 (Pubitemid 20222898)
36. Casar, J. C., Cabello-Verrugio, C., Olguin, H., Aldunate, R., Inestrosa, N. C., and Brandan, E. (2004) Heparan sulfate proteoglycans are increased during skeletal muscle regeneration. Requirement of syndecan-3 for successful fiber formation. J. Cell Sci. 117, 73-84 (Pubitemid 38072122)
37. Gargioli, C., Coletta, M., De Grandis, F., Cannata, S. M., and Cossu, G. (2008) PlGF-MMP-9-expressing cells restore microcirculation and efficacy of cell therapy in aged dystrophic muscle. Nat. Med. 14, 973-978
38. Vial, C., Zúñiga, L. M., Cabello-Verrugio, C., Cañón, P., Fadic, R., and Brandan, E. (2008) Skeletal muscle cells express the profibrotic cytokine connective tissue growth factor (CTGF/CCN2), which induces their dedifferentiation. J. Cell. Physiol. 215, 410-421 (Pubitemid 351468953)
39. Brandan, E., Carey, D. J., Larraín, J., Melo, F., and Campos, A. (1996) Synthesis and processing of glypican during differentiation of skeletal muscle cells. Eur. J. Cell Biol. 71, 170-176 (Pubitemid 26348473)
40. Cabello-Verrugio, C., Córdova, G., Vial, C., Zúñiga, L. M., and Brandan, E. (2011) Connective tissue growth factor induction by lysophosphatidic acid requires transactivation of transforming growth factor type β receptors and the JNK pathway. Cell. Signal. 23, 449-457
41. Kresse, H., and Schönherr, E. (2001) Proteoglycans of the extracellular matrix and growth control. J. Cell. Physiol. 189, 266-274 (Pubitemid 33063294)
42. Giri, S. N. (2003) Novel pharmacological approaches to manage interstitial lung fibrosis in the twenty-first century. Annu. Rev. Pharmacol. Toxicol. 43, 73-95
43. Krusius, T., and Ruoslahti, E. (1986) Primary structure of an extracellular matrix proteoglycan core protein deduced from cloned cDNA. Proc. Natl. Acad. Sci. U.S.A. 83, 7683-7687 (Pubitemid 17183911)
44. Scott, P. G., McEwan, P. A., Dodd, C. M., Bergmann, E. M., Bishop, P. N., and Bella, J. (2004) Crystal structure of the dimeric protein core of decorin, the archetypal small leucine-rich repeat proteoglycan. Proc. Natl. Acad. Sci. U.S.A. 101, 15633-15638 (Pubitemid 39473539)
45. 260 interacts with TGF-β but does not compete for decorin binding to type I collagen. Arch. Biochem. Biophys. 355, 241-248
46. Varga, J., Rosenbloom, J., and Jimenez, S. A. (1987) Transforming growth factor β (TGF-β) causes a persistent increase in steady-state amounts of type I and type III collagen and fibronectin mRNAs in normal human dermal fibroblasts. Biochem. J. 247, 597-604 (Pubitemid 17158405)
47. Hildebrand, A., Romarís, M., Rasmussen, L. M., Heinegård, D., Twardzik, D. R., Border, W. A., and Ruoslahti, E. (1994) Interaction of the small interstitial proteoglycans biglycan, decorin, and fibromodulin with transforming growth factor β. Biochem. J. 302, 527-534 (Pubitemid 24280108)
48. Kalamajski, S., Aspberg, A., and Oldberg, A. (2007) The decorin sequence SYIRIADTNIT binds collagen type I. J. Biol. Chem. 282, 16062-16067
49. 2-macroglobulin receptor is a receptor for connective tissue growth factor. J. Biol. Chem. 276, 40659-40667
50. Iozzo, R. V., and Karamanos, N. (2010) Proteoglycans in health and disease. Emerging concepts and future directions. FEBS J. 277, 3863
51. Santra, M., Reed, C. C., and Iozzo, R. V. (2002) Decorin binds to a narrow region of the epidermal growth factor (EGF) receptor, partially overlapping but distinct from the EGF-binding epitope. J. Biol. Chem. 277, 35671-35681
52. Orgel, J. P., Eid, A., Antipova, O., Bella, J., and Scott, J. E. (2009) Decorin core protein (decoron) shape complements collagen fibril surface structure and mediates its binding. PloS One 4, e7028
53. Huang, S. S., Ling, T. Y., Tseng, W. F., Huang, Y. H., Tang, F. M., Leal, S. M., and Huang, J. S. (2003) Cellular growth inhibition by IGFBP-3 and TGF-β1 requires LRP-1. FASEB J. 17, 2068-2081 (Pubitemid 37392451)
54. Abreu, J. G., Ketpura, N. I., Reversade, B., and De Robertis, E. M. (2002) Connective tissue growth factor (CTGF) modulates cell signaling by BMP and TGF-β. Nat. Cell Biol. 4, 599-604
55. Prud'homme, G. J. (2007) Pathobiology of transforming growth factorß in cancer, fibrosis, and immunologic disease, and therapeutic considerations. Lab. Invest. 87, 1077-1091
56. Duncan, M. R., Frazier, K. S., Abramson, S., Williams, S., Klapper, H., Huang, X., and Grotendorst, G. R. (1999) Connective tissue growth factor mediates transforming growth factor β-induced collagen synthesis. Down-regulation by cAMP. FASEB J. 13, 1774-1786 (Pubitemid 29473339)
57. Frazier, K., Williams, S., Kothapalli, D., Klapper, H., and Grotendorst, G. R. (1996) Stimulation of fibroblast cell growth, matrix production, and granulation tissue formation by connective tissue growth factor. J. Invest. Dermatol. 107, 404-411 (Pubitemid 26284351)
58. Shinozaki, M., Kawara, S., Hayashi, N., Kakinuma, T., Igarashi, A., and Takehara, K. (1997) Induction of subcutaneous tissue fibrosis in newborn mice by transforming growth factor β. Simultaneous application with basic fibroblast growth factor causes persistent fibrosis. Biochem. Biophys. Res. Commun. 240, 292-297
59. Pohlers, D., Brenmoehl, J., Löffler, I., Müller, C. K., Leipner, C., Schultze- Mosgau, S., Stallmach, A., Kinne, R. W., and Wolf, G. (2009) TGF-β and fibrosis in different organs. Molecular pathway imprints. Biochim. Biophys. Acta 1792, 746-756
60. Desmoulière, A., Geinoz, A., Gabbiani, F., and Gabbiani, G. (1993) Transforming growth factor-β1 induces α-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J. Cell Biol. 122, 103-111 (Pubitemid 23188802)
61. Folger, P. A., Zekaria, D., Grotendorst, G., and Masur, S. K. (2001) Transforming growth factor-β-stimulated connective tissue growth factor expression during corneal myofibroblast differentiation. Invest. Ophthalmol. Vis. Sci. 42, 2534-2541 (Pubitemid 32958560)
62. McLennan, I. S., and Koishi, K. (1997) Cellular localization of transforming growth factor-β2 and -β3 (TGF-β2, TGF-β3) in damaged and regenerating skeletal muscles. Dev. Dyn. 208, 278-289
63. Casar, J. C., McKechnie, B. A., Fallon, J. R., Young, M. F., and Brandan, E. (2004) Transient up-regulation of biglycan during skeletal muscle regeneration. Delayed fiber growth along with decorin increase in biglycandeficient mice. Dev. Biol. 268, 358-371 (Pubitemid 38519849)
64. Hu, K., Wu, C., Mars, W. M., and Liu, Y. (2007) Tissue-type plasminogen activator promotes murine myofibroblast activation through LDL receptor- related protein 1-mediated integrin signaling. J. Clin. Invest. 117, 3821-3832 (Pubitemid 350224092)