Dermatan sulfate domains defined by the novel antibody GD3A12, in normal tissues and ovarian adenocarcinomas
Tóm tắt
Dermatan sulfate (DS) expression in normal tissue and ovarian cancer was investigated using the novel, phage display-derived antibody GD3A12 that was selected against embryonic glycosaminoglycans (GAGs). Antibody GD3A12 was especially reactive with DS rich in IdoA-GalNAc4S disaccharide units. IdoA residues are important for antibody recognition as DS polymers with low numbers of IdoA residues were less reactive, and expression of the DS epimerase in ovarian carcinoma cells was associated with expression of the GD3A12 epitope. Moreover, staining of antibody GD3A12 was abolished by chondroitinase-B lyase digestion. Expression of DS domains defined by antibody GD3A12 was confined to connective tissue of most organs examined and presented as a typical fibrillar-type of staining. Differential expression of the DS epitopes recognized by antibodies GD3A12 and LKN1 (4/2,4 di-O-sulfated DS) was best seen in thymus and spleen, indicating differential expression of various DS domains in these organs. In ovarian carcinomas strong DS expression was found in the stromal parts, and occasionally on tumor cells. Partial co-localization in ovarian carcinomas was observed with decorin, versican and type I collagen suggesting a uniform distribution of this specific DS epitope. This unique anti-DS antibody may be instrumental to investigate the function, expression, and localization of specific DS domains in health and disease.
Tài liệu tham khảo
Bao X, Mikami T, Yamada S, Faissner A, Muramatsu T, Sugahara K (2005a) 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
Bao X, Pavao MS, Dos Santos JC, Sugahara K (2005b) A functional dermatan sulfate epitope containing iduronate(2-O-sulfate)alpha1–3GalNAc(6-O-sulfate) disaccharide in the mouse brain: demonstration using a novel monoclonal antibody raised against dermatan sulfate of ascidian Ascidia nigra. J Biol Chem 280:23184–23193
Dennissen MA, Jenniskens GJ, Pieffers M, Versteeg EM, Petitou M, Veerkamp JH, van Kuppevelt TH (2002) Large, tissue-regulated domain diversity of heparan sulfates demonstrated by phage display antibodies. J Biol Chem 277:10982–10986
Hikino M, Mikami T, Faissner A, Vilela-Silva AC, Pavao MS, 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
Iozzo RV (1998) Matrix proteoglycans: from molecular design to cellular function. Annu Rev Biochem 67:609–652
Jenniskens GJ, Oosterhof A, Brandwijk R, Veerkamp JH, van Kuppevelt TH (2000) Heparan sulfate heterogeneity in skeletal muscle basal lamina: demonstration by phage display-derived antibodies. J Neurosci 20:4099–4111
Lensen JF, Wijnhoven TJ, Kuik LH, Versteeg EM, Hafmans T, Rops AL, Pavao MS, van der Vlag J, van den Heuvel LP, Berden JH, van Kuppevelt TH (2006) Selection and characterization of a unique phage display-derived antibody against dermatan sulfate. Matrix Biol 25:457–461
Li F, Yamada S, Basappa ShettyAK, Sugiura M, Sugahara K (2008) Determination of iduronic acid and glucuronic acid in sulfated chondroitin/dermatan hybrid chains by (1)H-nuclear magnetic resonance spectroscopy. Glycoconj J 25:603–610
Maccarana M, Olander B, Malmstrom J, Tiedemann K, Aebersold R, Lindahl U, Li JP, Malmstrom A (2006) Biosynthesis of dermatan sulfate: chondroitin-glucuronate C5-epimerase is identical to SART2. J Biol Chem 281:11560–11568
Miller MJ, Costello CE, Malmstrom A, Zaia J (2006) A tandem mass spectrometric approach to determination of chondroitin/dermatan sulfate oligosaccharide glycoforms. Glycobiology 16:502–513
Nash MA, Deavers MT, Freedman RS (2002) The expression of decorin in human ovarian tumors. Clin Cancer Res 8:1754–1760
Nissim A, Hoogenboom HR, Tomlinson IM, Flynn G, Midgley C, Lane D, Winter G (1994) Antibody fragments from a ‘single pot’ phage display library as immunochemical reagents. EMBO J 13:692–698
Pavao MS, Mourao PA, Mulloy B, Tollefsen DM (1995) A unique dermatan sulfate-like glycosaminoglycan from ascidian Its structure and the effect of its unusual sulfation pattern on anticoagulant activity. J Biol Chem 270:31027–31036
Ricciardelli C, Rodgers RJ (2006) Extracellular matrix of ovarian tumors. Semin Reprod Med 24:270–282
Shirk RA, Parthasarathy N, San Antonio JD, Church FC, Wagner WD (2000) Altered dermatan sulfate structure and reduced heparin cofactor II-stimulating activity of biglycan and decorin from human atherosclerotic plaque. J Biol Chem 275:18085–18092
Skandalis SS, Kletsas D, Kyriakopoulou D, Stavropoulos M, Theocharis DA (2006a) The greatly increased amounts of accumulated versican and decorin with specific post-translational modifications may be closely associated with the malignant phenotype of pancreatic cancer. Biochim Biophys Acta 1760:1217–1225
Skandalis SS, Theocharis AD, Papageorgakopoulou N, Vynios DH, Theocharis DA (2006b) The increased accumulation of structurally modified versican and decorin is related with the progression of laryngeal cancer. Biochimie 88:1135–1143
Sugahara K, Nadanaka S, Takeda K, Kojima T (1996) Structural analysis of unsaturated hexasaccharides isolated from shark cartilage chondroitin sulfate D that are substrates for the exolytic action of chondroitin ABC lyase. Eur J Biochem 239:871–880
Sugahara K, Mikami T, Uyama T, Mizuguchi S, Nomura K, Kitagawa H (2003) Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate. Curr Opin Struct Biol 13:612–620
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
ten Dam GB, Hafmans T, Veerkamp JH, van Kuppevelt TH (2003) Differential expression of heparan sulfate domains in rat spleen. J Histochem Cytochem 51:727–739
ten Dam GB, Kurup S, van de Westerlo EM, Versteeg EM, Lindahl U, Spillmann D, van Kuppevelt TH (2006) 3-O-sulfated oligosaccharide structures are recognized by anti-heparan sulfate antibody HS4C3. J Biol Chem 281:4654–4662
ten Dam GB, van de Westerlo EM, Purushothaman A, Stan RV, Bulten J, Sweep FC, Massuger LF, Sugahara K, van Kuppevelt TH (2007) Antibody GD3G7 selected against embryonic glycosaminoglycans defines chondroitin sulfate-E domains highly up-regulated in ovarian cancer and involved in vascular endothelial growth factor binding. Am J Pathol 171:1324–1333
Theocharis AD (2002) Human colon adenocarcinoma is associated with specific post-translational modifications of versican and decorin. Biochim Biophys Acta 1588:165–172
Theocharis AD, Vynios DH, Papageorgakopoulou N, Skandalis SS, Theocharis DA (2003) Altered content composition and structure of glycosaminoglycans and proteoglycans in gastric carcinoma. Int J Biochem Cell Biol 35:376–390
Timar J, Lapis K, Dudas J, Sebestyen A, Kopper L, Kovalszky I (2002) Proteoglycans and tumor progression: janus-faced molecules with contradictory functions in cancer. Semin Cancer Biol 12:173–186
Tovar AM, de Mattos DA, Stelling MP, Sarcinelli-Luz BS, Nazareth RA, Mourao PA (2005) Dermatan sulfate is the predominant antithrombotic glycosaminoglycan in vessel walls: implications for a possible physiological function of heparin cofactor II. Biochim Biophys Acta 1740:45–53
Trowbridge JM, Gallo RL (2002) Dermatan sulfate: new functions from an old glycosaminoglycan. Glycobiology 12:117R–125R
van de Lest CH, Versteeg EM, Veerkamp JH, van Kuppevelt TH (1994) Quantification and characterization of glycosaminoglycans at the nanogram level by a combined azure A-silver staining in agarose gels. Anal Biochem 221:356–361
van Kuppevelt TH, Dennissen MA, van Venrooij WJ, Hoet RM, Veerkamp JH (1998) Generation and application of type-specific anti-heparan sulfate antibodies using phage display technology Further evidence for heparan sulfate heterogeneity in the kidney. J Biol Chem 273:12960–12966
Voutilainen K, Anttila M, Sillanpaa S, Tammi R, Tammi M, Saarikoski S, Kosma VM (2003) Versican in epithelial ovarian cancer: relation to hyaluronan, clinicopathologic factors and prognosis. Int J Cancer 107:359–364
Wegrowski Y, Maquart FX (2004) Involvement of stromal proteoglycans in tumour progression. Crit Rev Oncol Hematol 49:259–268
Werneck CC, Cruz MS, Silva LC, Villa-Verde DM, Savino W, Mourao PA (2000) Is there a glycosaminoglycan-related heterogeneity of the thymic epithelium? J Cell Physiol 185:68–79