Dermatan sulfate remodeling associated with advanced Dupuytren's contracture
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Dermatan sulfate (DS) widespread as a component of extracellular matrix proteoglycans, is characterized by great bio-reactivity and remarkable structural heterogeneity due to distinct degrees of sulfation and glucuronosyl epimerization and different polymerization degrees. However, DS metabolism under various biological conditions is poorly known. Dupuytren's contracture is a benign fibromatosis leading to complex remodeling of the palmar fascia structure and properties. However, it remains unclear whether the disease affects the structure of DS, which is the major tissue glycosaminoglycan. Thus the aim of the study was to examine the structure of the total DS in Dupuytren's fascia. DS chains were extracted from 5 samples of normal fascia and 7 specimens of Dupuytren's tissue by papain digestion followed by fractionation with cetylpyridinium chloride. Then, DS structure analysis was performed comprising the evaluation of its molecular masses and sensitivity to hyaluronidase and chondroitinase B. Dupuytren's contracture is associated with significant remodeling of DS chain structure revealed by (1) a distinct profile of chain molecular masses characterized by the appearance of long size components as well as the increase in the content of small size chains; (2) a different glucuronosyl epimerization pattern connected with the enhanced content of glucuronate disaccharide blocks; (3) chain oversulfation. These structural alterations in total DS may modify the GAG interactions especially affecting collagen fibrillogenesis and growth factor availability. Thus, Dupuytren's contracture associated DS remodeling may promote the phenomena typical for advanced disease: apoptosis and reduction in cell number as well as the appearance of dense pseudotendinous collagen matrix.
- Badalamente MA, Hurst LC (1999) The biochemistry of Dupuytren's disease. Hand Clin 15: 35-42.
- Blumenkrantz N, Asboe-Hansen G (1973) New method for determination of uronic acids. Anal Biochem 54: 484-489.
- Casu B, Ferro DR, Ragazzi M, Torri G (1993) Conformation of iduronic acid-containing glycosaminoglycans. In Dermatan sulphate proteoglycans chemistry, biology, chemical pathology. Scott JE, ed, pp 41-53. Portland Press, London, Chapel Hill.
- Corsi A, Xu T, Chen X-D, Boyde A, Liang J, Mankani M, Sommer B, Iozzo VR, Eichstetter I, Robey PG, Bianco P, Young MF (2002) Phenotypic effects of biglycan deficiency are linked to collagen fibril abnormalities, are synergized by decorin deficiency, and mimic Ehlers-Danlos-like changes in bone and other connective tissues. J Bone Miner Res 17: 1180-1189.
- Cowman MK, Slahetka MF, Hittner DM, Kim J, Forino M, Gadelrab G (1984) Polyacrylamide-gel electrophoresis and Alcian blue staining of sulphated glycosaminoglycan oligosaccharides. Biochem J 221: 707-716.
- Dal Cin P, De Smet L, Sciot R, Van Damme B, Van den Berghe H (1999) Trisomy 7 and trisomy 8 in dividing and non-dividing tumor cells in Dupuytren's disease. Cancer Genet Cytogenet 108: 137-140.
- Flint MH, Gillard GC, Reilly HC (1982) The glycosaminoglycans of Dupuytren's disease. Connect Tissue Res 9: 173-179.
- Garcia-Olivas R, Hoebeke J, Castel S, Reina M, Fager G, Lustig F, Vilaro S (2003) Differential binding of platelet-derived growth factor isoforms to glycosaminoglycans. Histochem Cell Biol 120: 371-382.
- Gaździk T, Januszewski K, Jędrysik M (1984) Micromorphological studies in Dupuytren's contracture. Chir Narzadow Ruchu Ortop Pol 49: 345-349 (in polish).
- Gendelman R, Burton-Wurster NI, MacLeod JN, Lust G (2003) The cartilage-specific fibronectin isoform has a high affinity binding site for the small proteoglycan decorin. J Biol Chem 278: 11175-11181.
- Głowacki A, Olczyk K, Sonecki P, Koźma E, Najmiec T (1994) Glycosaminoglycans of normal and scarred fascia. Acta Biochim Polon 41: 166-169.
- Gu K, Linhardt RJ, Laliberte M, Gu K, Zimmermann DR (1995) Purification, characterization and specificity of chondroitin lyases and glucuronidases from Flavobacterium heparinum. Biochem J 312: 569-577.
- Gudmundsson KG, Arngrimsson R, Sigfusson N, Bjornsson A, Jonsson T (2000) Epidemiology of Dupuytren's disease: clinical, serological, and social assessment. J Clin Epidemiol 53: 291-296.
- Hamai A, Hashimoto N, Mochizuki H, Kato F, Makiguchi Y, Horie K, Suzuki S (1997) Two distinct chondroitin sulfate ABC lyases. An endoeliminase yielding tetrasaccharides and an exoeliminase preferentially acting on oligosaccharides. J Biol Chem 272: 9123-9130.
- Hampson IN, Gallagher JT (1984) Separation of radiolabelled glycosaminoglycan oligosaccharides by polyacrylamide-gel electrophoresis. Biochem J 221: 697-705.
- Hinek A, Wilson SE (2000) Impaired elastogenesis in Hurler disease. Dermatan sulfate accumulation linked to deficiency in elastin-binding protein and elastic fiber assembly. Am J Pathol 156: 925-938.
- Jung Y, Hohmann TC, Gerneth JA, Novak J, Wasserman RC, D'Andrea BJ, Newton RH, Danowski TS (1971) Diabetic hand syndrome. Metabolism 20: 1008-1015.
- Kähäri VM, Larjava H, Uitto J (1991) Differential regulation of extracellular matrix proteoglycan (PG) gene expression. Transforming growth factor-beta 1 up-regulates biglycan (PGI), and versican (large fibroblast PG) but down-regulates decorin (PGII) mRNA levels in human fibroblasts in culture. J Biol Chem 266: 10608-10615.
- Kinsella MG, Bressler SL, Wight TN (2004) The regulated synthesis of versican, decorin, and biglycan: extracellular matrix proteoglycans that influence cellular phenotype. Crit Rev Eukaryot Gene Expr 14: 203-234.
- Kinsella MG, Fischer JW, Mason DP, Wight TN (2000) Retrovirally mediated expression of decorin by macrovascular endothelial cells. Effects on cellular migration and fibronectin fibrillogenesis in vitro. J Biol Chem 275: 13924-13932.
- Kinsella MG, Wight TN (1990) Formation of high molecular weight dermatan sulfate proteoglycan in bovine aortic endothelial cell cultures. Evidence for transglutaminase-catalyzed cross-linking to fibronectin. J Biol Chem 265: 17891-17898.
- Koshiishi I, Hasegawa T, Imanari T (2002) Quantitative and qualitative alterations of chondroitin/dermatan sulfates accompanied with development of tubulointerstitial nephritis. Arch Biochem Biophys 401: 38-43.
- Koshiishi I, Takenouchi M, Imanari T (1999) Structural characteristics of oversulfated chondroitin/dermatan sulfates in the fibrous lesions of the liver with cirrhosis. Arch Biochem Biophys 370: 151-155.
- Koźma EM, Olczyk K, Głowacki A (2001) Dermatan sulfates of normal and scarred fascia. Comp Biochem Physiol B 128: 221-232.
- Koźma EM, Olczyk K, Głowacki A, Bobiński R (2000) An accumulation of proteoglycans in scarred fascia. Mol Cell Biochem 203: 103-112.
- Koźma EM, Olczyk K, Wisowski G, Głowacki A, Bobiński R (2005) Alterations in the extracellular matrix proteoglycan profile in Dupuytren's contracture affect the palmar fascia. J Biochem 137: 463-476.
- Lennox IAC, Murali SR, Porter R (1993) A study of the repeatability of the diagnosis of Dupuytren's contracture and its prevalence in the Grampian Region. J Hand Surg Br 18: 258-261.
- Lyon M, Gallagher JT (1990) A general method for the detection and mapping of submicrogram quantities of glycosaminoglycan oligosaccharides on polyacrylamide gels by sequential staining with azur A and ammoniacal silver. Anal Biochem 185: 63-70.
- Nandini CD, Itoh N, Sugahara K (2005) Novel 70-kDa chondroitin sulfate/dermatan sulfate hybrid chains with a unique heterogenous sulfation pattern from shark skin, which exhibit neuritogenic activity and binding activities for growth factors and neurotrophic factors. J Biol Chem 280: 4058-4069.
- Nandini CD, Mikami T, Ohta M, Itoh N, Akiyama-Nambu F, Sugahara K (2004) Structural and functional characterization of oversulfated chondroitin sulfate/dermatan sulfate hybrid chains from the notochord of hagfish. J Biol Chem 279: 50799-50809.
- Prydz K, Dalen KT (2000) Synthesis and sorting of proteoglycans. J Cell Sci 113: 193-205.
- Rayan GM (1999) Clinical presentation and types of Dupuytren's disease. Hand Clin 15: 87-96.
- Roden L, Baker JR, Cifonelli JA, Mathews MB (1972) Isolation and characterization of connective tissue polysaccharides. Methods Enzymol 28: 73-140.
- Rombouts JJ, Noel H, Legrain Y, Munting E (1989) Prediction of recurrence in the treatment of Dupuytren's disease: Evaluation of a histologic classification. J Hand Surg Am 14: 644-652.
- Schönherr E, Kinsella MG, Wight TN (1997) Genistein selectively inhibits platelet-derived growth factor stimulated versican biosynthesis in monkey arterial smooth muscle cells. Arch Biochem Biophys 339: 353-361.
- Scott JE (2003) Elasticity in extracellular matrix 'shape modules' of tendon, cartilage, etc. A sliding proteoglycan-filament model. J Physiol 553: 335-343.
- Sottile J, Hocking DC (2002) Fibronectin polymerization regulates the composition and stability of extracellular matrix fibrils and cell-matrix adhesion. Mol Biol Cell 13: 3546-3559.
- Taylor KR, Rudisill JA, Gallo RL (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.
- Tiedemann K, Olander B, Eklund E, Todorova L, Bengtsson M, Maccarana M, Westergren-Thorsson G, Malmstrom A (2005) Regulation of the chondroitin/dermatan fine structure by transforming growth factor-β1 through effects on polymer-modifying enzymes. Glycobiology 15: 1277-1285.
- Tomasek JJ, Schultz RJ, Episalla CW, Newman SA (1986) The cytoskeleton and extracellular matrix of the Dupuytren's disease 'myofibroblast': An immunofluorescence study of a nonmuscle cell type. J Hand Surg Am 11: 365-371.
- Tomasek JJ, Vaughan MB, Haaksma CJ (1999) Cellular structure and biology of Dupuytren's disease. Hand Clin 15: 21-34.
- Tunn S, Gurr E, Delbruck A, Buhr T, Flory J (1988) The distribution of unsulphated and sulphated glycosaminoglycans in palmar fascia from patients with Dupuytren's disease and healthy subjects. J Clin Chem Clin Biochem 26: 7-14.
- Wegrowski Y, Maquart FX (2004) Involvement of stromal proteoglycans in tumor progression. Crit Rev Oncol Hematol 49: 259-268.
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