Decorin and its galactosaminoglycan chain: Extracellular regulator of cellular function?

IUBMB Life

Volumn 60, Issue 11, 2008, Pages 729-733

  Seidler, Daniela G ^a   Dreier, Rita ^a  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

Author keywords

Decorin; Extracellular matrix; Galactosaminoglycan chain; Sulfation patterns

Indexed keywords

CHONDROITIN; DECORIN; DERMATAN SULFATE; GALACTOSAMINOGLYCAN; LEUCINE; POLYSACCHARIDE; PROTEOGLYCAN; SCLEROPROTEIN;

CELL FUNCTION; EPIMERIZATION; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN SYNTHESIS; REVIEW; EXTRACELLULAR MATRIX; GENETICS; HUMAN; PHYSIOLOGY;

CELL PHYSIOLOGICAL PHENOMENA; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; HUMANS; POLYSACCHARIDES; PROTEOGLYCANS;

EID: 58149350127     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.115     Document Type: Review

References (55)

1. Boudreau N. and Bissell M. J. (1998) Extracellular matrix signaling: integration of form and function in normal and malignant cells. Curr. Opin. Cell Biol. 10, 640-646.
2. Hering, T. M. (1999) Regulation of chondrocyte gene expression. Front Biosci. 4, D743-D761.
3. Schwartz, M. A. and Baron, V. (1999) Interactions between mitogenic stimuli, or, a thousand and one connections. Curr. Opin. Cell. Biol. 11, 197-202.
4. Howe, A., Aplin, A. E., Alahari, S. K., and Juliano, R. L. (1998) Integrin signaling and cell growth control. Curr. Opin. Cell. Biol. 10, 220-231.
5. Itoh, Y. and Seiki, M. (2006) MT1-MMP: a potent modifier of pericellular microenvironment. J. Cell. Physiol. 206, 1-8.
6. Hornebeck, W. and Maquart, F.X. (2003) Proteolyzed matrix as a template for the regulation of tumor progression. Biomed. Pharmacother. 57, 223-230.
7. Hornebeck, W., Emonard, H., Monboisse, J. C., and Bellon, G. (2002) Matrix-directed regulation of pericellular proteolysis and tumor progression. Semin. Cancer Biol. 12, 231-241.
8. Prehm, P. (1984) Hyaluronate is synthesized at plasma membranes. Biochem. J. 220, 597-600.
9. Plaas, A. H., West, L. A., Thonar, E. J., Karcioglu, Z. A., Smith, C. J., Klintworth, G. K., and Hascall, V. C. (2001) Altered fine structures of corneal and skeletal keratan sulfate and chondroitin/dermatan sulfate in macular corneal dystrophy. J. Biol. Chem. 276, 39788-39796.
10. Bernfield, M., Götte, M., Park, P. W., Reizes, O., Fitzgerald, M. L., Lincecum, J., and Zako, M. (1999) Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68, 729-777.
11. Watanabe, H., Gao, L., Sugiyama, S., Doege, K., Kimata, K., and Yamada, Y. (1995) Mouse aggrecan, a large cartilage proteoglycan: protein sequence, gene structure and promoter sequence. Biochem. J. 308, 433-440.
12. Ito, K., Shinomura, T., Zako, M., Ujita, M., and Kimata, K. (1995) Multiple forms of mouse PG-M, a large chondroitin sulfate proteoglycan generated by alternative splicing. J. Biol. Chem. 270, 958-965.
13. Kusche-Gullberg, M. and Kjellen, L. (2003) Sulfotransferases in glycosaminoglycan biosynthesis. Curr. Opin. Struct. Biol. 13, 605-611.
14. Iozzo, R. V. (1997) The family of the small leucine-rich proteoglycans: key regulators of matrix assembly and cellular growth. Crit. Rev. Biochem. Mol. Biol. 32, 141-174.
15. Iozzo, R. V. (1999) The biology of the small leucine-rich proteoglycans. Functional network of interactive proteins. J. Biol. Chem. 274, 18843-18846.
16. Cheng, F., Heinegard, D., Malmström, A., Schmidtchen, A., Yoshida, K., and Fransson, L. A. (1994) Patterns of uronosyl epimerization and 4-/6-O-sulphation in chondroitin/dermatan sulphate from decorin and biglycan of various bovine tissues. Glycobiology 4, 685-696.
17. Kresse, H., Rosthoj, S., Quentin, E., Hollmann, J., Glössl, J., Okada, S., and Tonnesen, T. (1987) Glycosaminoglycan-free small proteoglycan core protein is secreted by fibroblasts from a patient with a syndrome resembling progeroid. Am. J. Hum. Genet. 41, 436-453.
18. Faiyaz-Ul-Haque, M. Zaidi, S. H., Al Ali, M., Al Mureikhi, M. S., Kennedy, S., Al Thani, G., Tsui, L. C., and Teebi, A. S. (2004) A novel missense mutation in the galactosyltransferase-I (B4GALT7) gene in a family exhibiting facioskeletal anomalies and Ehlers-Danlos syndrome resembling the progeroid type. Am. J. Med. Genet. A 128, 39-45.
19. Seidler, D. G., Faiyaz-Ul-Haque, M., Hansen, U., Yip, G. W., Zaidi, S. H., Teebi, A. S., Kiesel, L., and Götte, M. (2006) Defective glycosylation of decorin and biglycan, altered collagen structure, and abnormal phenotype of the skin fibroblasts of an Ehlers-Danlos syndrome patient carrying the novel Arg270Cys substitution in galactosyltransferase I (beta4GalT-7). J. Mol. Med. 84, 583-594.
20. Scott, J. E. (1992) Supramolecular organization of extracellular matrix glycosaminoglycans, in vitro and in the tissues. FASEB J. 6, 2639-2645.
21. Vogel, K. G., Paulsson, M., and Heinegård, D. (1984) Specific inhibition of type I and type II collagen fibrillogenesis by the small proteoglycan of tendon. Biochem. J. 223, 587-597.
22. Hagg, R., Bruckner, P., and Hedbom, E. (1998) Cartilage fibrils of mammals are biochemically heterogeneous: differential distribution of decorin and collagen IX. J. Cell Biol. 142, 285-294.
23. Danielson, K. G., Baribault, H., Holmes, D. F., Graham, H., Kadler, K. E., and Iozzo, R. V. (1997) Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J. Cell Biol. 136, 729-743.
24. Seidler, D. G., Schaefer, L., Robenek, H., Iozzo, R. V., Kresse, H., and Schönherr, E. (2005) A physiologic three-dimensional cell culture system to investigate the role of decorin in matrix organisation and cell survival. Biochem. Biophys. Res. Commun. 332, 1162-1170.
25. Rühland, C., Schönherr, E., Robenek, H., Hansen, U., Iozzo, R. V., Bruckner, P., and Seidler, D. G. (2007) The glycosaminoglycan chain of decorin plays an important role in collagen fibril formation at the early stages of fibrillogenesis. FEBS J. 274, 4246-4255.
26. Nareyeck, G., Seidler, D. G., Troyer, D. Rauterberg, J., Kresse, H., and Schönherr, E. (2004) Differential interactions of decorin and decorin mutants with type I and type VI collagens. Eur. J. Biochem. 271, 3389-3398.
27. Fleischmajer, R., Fisher, L. W., MacDonald, E. D., Jacobs, L., Perlish, J. S., and Termine, J. D. (1991) Decorin interacts with fibrillar collagen of embryonic and adult human skin. J. Struct. Biol. 106, 82-90.
28. Takahashi, T., Cho, H.-I., Kublin, C. I., and Cintron, C. (1993) Keratan sulfate and dermatan sulfate proteoglycans associate with type VI collagen in fetal rabbit cornea. J. Histochem. Cytochem. 41, 1447-1457.
29. Wiberg, C., Klatt, A. R., Wagener, R., Paulsson, M., Bateman, J. F., Heinegard, D., and Morgelin, M. (2003) Complexes of matrilin-1 and biglycan or decorin connect collagen VI microfibrils to both collagen II and aggrecan. J. Biol. Chem. 278, 37698-37704.
30. 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.
31. 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.
32. Seidler, D.G., Goldoni, S., Agnew, C., Cardi, C., Thakur, M. L., Owens, R. T., McQuillan, D. J., and Iozzo, R. V. (2006) Decorin protein core inhibits in vivo cancer growth and metabolism by hindering epidermal growth factor receptor function and triggering apoptosis via caspase-3 activation. J. Biol. Chem. 281, 26408-26418.
33. Maccarana, M., Olander, B., Malmstrom, J., Tiedemann, K., Aebersold, R., Lindahl, U., Li, J. P., and Malmstrom, A. (2006) Biosynthesis of dermatan sulfate: chondroitin-glucuronate C5-epimerase is identical to SART2. J. Biol. Chem. 281: 11560-11568.
34. Nakao, M., Shichijo, S., Imaizumi, T., Inoue, Y., Matsunaga, K., Yamada, A., Kikuchi, M., Tsuda, N., Ohta, K., Takamori, S., Yamana, H., Fujita, H., and Itoh, K. (2000) Identification of a gene coding for a new squamous cell carcinoma antigen recognized by the CTL. J. Immunol. 164, 2565-2574.
35. Evers, M. R., Xia, G., Kang, H. G., Schachner, M., and Baenziger, J. U. (2001) Molecular cloning and characterization of a dermatan-specific N-acetylgalactosamine 4-O-sulfotransferase. J. Biol. Chem. 276, 36344-36353.
36. Hiraoka, N., Nakagawa, H., Ong, E., Akama, T. O., Fukuda, M. N., and Fukuda, M. (2000) Molecular cloning and expression of two distinct human chondroitin 4-O-sulfotransferases that belong to the HNK-1 sulfotransferase gene family. J. Biol. Chem. 275, 20188-20196.
37. Kitagawa, H., Uyama, T., and Sugahara, K. (2001) Molecular cloning and expression of a human chondroitin synthase. J. Biol. Chem. 276, 38721-38726.
38. Faham, S., Hileman, R. E., Fromm, J. R., Linhardt, R. J., and Rees, D. C. (1996) Heparin structure and interactions with basic fibroblast growth factor. Science 271, 1116-1120.
39. Hildebrand, A., Romaris, M., Rasmussen, L. M., Heinegard, 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 beta. Biochem. J. 302, 527-534.
40. Tufvesson, E. and Westergren-Thorsson, G. (2002) Tumour necrosis factor-alpha interacts with biglycan and decorin. FEBS Lett. 530, 124-128.
41. Desnoyers, L., Arnott, D., and Pennica, D. (2001) WISP-1 binds to decorin and biglycan. J. Biol. Chem. 276, 47599-47607.
42. Venkataraman, G., Sasisekharan, V., Cooney, C. L., Langer, R., and Sasisekharan, R. (1994) A stereochemical approach to pyranose ring flexibility: its implications for the conformation of dermatan sulfate. Proc. Natl. Acad. Sci. USA 91, 6171-6175.
43. Pellegrini, L., Burke, D. F., von Delft, F., Mulloy, B., and Blundell, T. L. (2000) Crystal structure of fibroblast growth factor receptor ectodomain bound to ligand and heparin. Nature 407, 1029-1034.
44. Schlessinger, J., Plotnikov, A. N., Ibrahimi, O. A., Eliseenkova, A. V., Yeh, B. K., Yayon, A., Linhardt, R. J., and Mohammadi, M. (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.
45. Penc, S. F., Pomahac, B., Winkler, T., Dorschner, R. A., Eriksson, E., Herndon, M., and Gallo, R. L. (1998) Dermatan sulfate released after injury is a potent promoter of fibroblast growth factor-2 function. J. Biol. Chem. 273, 28116-28121.
46. Zamfir, A., Seidler, D. G., Kresse, H., and Peter-Katalinic, J. (2003) Structural investigation of chondroitin/dermatan sulfate oligosaccharides from human skin fibroblast decorin. Glycobiology 13, 733-742.
47. Zamfir, A., Seidler, D. G., Schönherr, E., Kresse, H., and Peter-Katalinic, J. (2004) On-line sheathless capillary electrophoresis/ nanoelectrospray ionization-tandem mass spectrometry for the analysis of glycosaminoglycan oligosaccharides. Electrophoresis 25, 2010-2016.
48. Taylor, K. R., Rudisill, J. A., and Gallo, R. L. (2005) Structural and sequence motifs in dermatan sulfate for promoting fibroblast growth factor-2 (FGF-2) and FGF-7 activity. J. Biol. Chem. 280, 5300-5306.
49. Koprivica, V., Cho, K. S., Park, J. B., Yiu, G., Atwal, J., Gore, B., Kim, J. A., Lin, E., Tessier-Lavigne, M., Chen, D. F., He Z (2005) EGFR activation mediates inhibition of axon regeneration by myelin and chondroitin sulfate proteoglycans. Science 310, 106-110.
50. Sirko, S., von, H. A., Wizenmann, A., Gotz, M., and Faissner, A. (2007) Chondroitin sulfate glycosaminoglycans control proliferation, radial glia cell differentiation and neurogenesis in neural stem/progenitor cells. Development 134, 2727-2738.
51. Hikino, M., Mikami, T., Faissner, A., Vilela-Silva, A. C., Pavao, M. S., and Sugahara, K. (2003) Oversulfated dermatan sulfate exhibits neurite outgrowth-promoting activity toward embryonic mouse hippocampal neurons: implications of dermatan sulfate in neuritogenesis in the brain. J. Biol. Chem. 278, 43744-43754.
52. Bao, X., Mikami, T., Yamada, S., Faissner, A., Muramatsu, T., and Sugahara, K. (2005) Heparin-binding growth factor, pleiotrophin, mediates neuritogenic activity of embryonic pig brain-derived chondroitin sulfate/dermatan sulfate hybrid chains. J. Biol. Chem. 280, 9180-9191.
53. Li, F., Shetty, A. K., and Sugahara, K. (2007) Neuritogenic activity of chondroitin/dermatan sulfate hybrid chains of embryonic pig brain and their mimicry from shark liver. Involvement of the pleiotrophin and hepatocyte growth factor signaling pathways. J. Biol. Chem. 282, 2956-2966.
54. Grzesik, W. J. Frazier, C. R., Shapiro, J. R., Sponseller, P. D., Robey, P. G., and Fedarko, N. S. (2002) Age-related changes in human bone proteoglycan structure. Impact of osteogenesis imperfecta. J. Biol. Chem. 277, 43638-43647.
55. Hayes, A. J., Tudor, D., Nowell, M. A., Caterson, B., and Hughes, C. E. (2008) Chondroitin sulfate sulfation motifs as putative biomarkers for isolation of articular cartilage progenitor cells. J. Histochem. Cytochem. 56, 125-138.