Transgenic or tumor-induced expression of heparanase upregulates sulfation of heparan sulfate

Nature Chemical Biology

Volumn 3, Issue 12, 2007, Pages 773-778

  Escobar Galvis, Martha L ^a   Jia, Juan ^a   Zhang, Xiao ^b   Jastrebova, Nadja ^a   Spillmann, Dorothe ^a   Gottfridsson, Eva ^a   Van Kuppevelt, Toin H ^c   Zcharia, Eyal ^d   Vlodavsky, Israel ^d   Lindahl, Ulf ^a   Li, Jin Ping ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 1; GROWTH FACTOR; HEPARAN SULFATE; HEPARIN DERIVATIVE; HEPARIN LYASE; LIVER ENZYME; NITROGEN; OXYGEN; PROTEOHEPARAN SULFATE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; CORRELATION ANALYSIS; HUMAN; HUMAN TISSUE; LIVER; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN STRUCTURE; SULFATION; UPREGULATION;

ANIMALIA; MUS;

EID: 36248937194     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.2007.41     Document Type: Article

References (30)

1. Bernfield, M. et al. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68, 72-777 (1999).
2. Lin, X. & Perrimon, N. Role of heparan sulfate proteoglycans in cell-cell signaling in Drosophila. Matrix Biol. 19, 303-307 (2000).
3. Bishop, J.R., Schuksz, M. & Esko, J.D. Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446, 1030-1037 (2007).
4. Zcharia, E. et al. Transgenic expression of mammalian heparanase uncovers physiological functions of heparan sulfate in tissue morphogenesis, vascularization, and feeding behavior. FASEB J. 18, 252-263 (2004).
5. Li, J.P. et al. In vivo fragmentation of heparan sulfate by heparanase overexpression renders mice resistant to amyloid protein A amyloidosis. Proc. Natl. Acad. Sci. USA 102, 6473-6477 (2005).
6. Casu, B. & Lindahl, U. Structure and biological interactions of heparin and heparan sulfate. Adv. Carbohydr. Chem. Biochem. 57, 159-206 (2001).
7. Feyerabend, T.B., Li, J.P., Lindahl, U. & Rodewald, H.R. Heparan sulfate C5-epimerase is essential for heparin biosynthesis in mast cells. Nat. Chem. Biol. 2, 195-196 (2006).
8. Maccarana, M., Sakura, Y., Tawada, A., Yoshida, K. & Lindahl, U. Domain structure of heparan sulfates from bovine organs. J. Biol. Chem. 271, 17804-17810 (1996).
9. Stringer, S.E. & Gallagher, J.T. Molecules in focus: heparan sulphate. Int. J. Biochem. Cell Biol. 29, 709-714 (1997).
10. Ledin, J. et al. Heparan sulfate structure in mice with genetically modified heparan sulfate production. J. Biol. Chem. 279, 42732-42741 (2004).
11. Ögren, S. & Lindahl, U. Cleavage of macromolecular heparin by an enzyme from mouse mastocytoma. J. Biol. Chem. 250, 2690-2697 (1975).
12. Gong, F. et al. Processing of macromolecular heparin by heparanase. J. Biol. Chem. 278, 35152-35158 (2003).
13. Ilan, N., Elkin, M. & Vlodavsky, I. Regulation, function and clinical significance of heparanase in cancer metastasis and angiogenesis. Int. J. Biochem. Cell Biol. 38, 2018-2039 (2006).
14. Zetser, A. et al. Processing and activation of latent heparanase occurs in lysosomes. J. Cell Sci. 117, 2249-2258 (2004).
15. Guo, Y. & Conrad, H.E. The disaccharide composition of heparins and heparan sulfates. Anal. Biochem. 176, 96-104 (1989).
16. Pinhal, M.A. et al. Enzyme interactions in heparan sulfate biosynthesis: uronosyl 5-epimerase and 2-O-sulfotransferase interact in vivo. Proc. Natl. Acad. Sci. USA 98, 12984-12989 (2001).
17. Kurup, S. et al. Characterization of anti-heparan sulfate phage-display antibodies AO4B08 and HS4E4. J. Biol. Chem. 282, 21032-21042 (2007).
18. Jayson, G.C. et al. Heparan sulfate undergoes specific structural changes during the progression from human colon adenoma to carcinoma in vitro. J. Biol. Chem. 273, 51-57 (1998).
19. Vlodavsky, I. et al. Mammalian heparanase: gene cloning, expression and function in tumor progression and metastasis. Nat. Med. 5, 793-802 (1999).
20. Friedmann, Y. et al. Expression of heparanase in normal, dysplastic, and neoplastic human colonic mucosa and stroma. Evidence for its role in colonic tumorigenesis. Am. J. Pathol. 157, 1167-1175 (2000).
21. Jastrebova, N. et al. Heparan sulfate-related oligosaccharides in ternary complex formation with fibroblast growth factors 1 and 2 and their receptors. J. Biol. Chem. 281, 26884-26892 (2006).
22. Kreuger, J., Spillmann, D., Li, J.P. & Lindahl, U. Interactions between heparan sulfate and proteins: the concept of specificity. J. Cell Biol. 174, 323-327 (2006).
23. Jakobsson, L. et al. Heparan sulfate in trans potentiates VEGFR-mediated angiogenesis. Dev. Cell 10, 625-634 (2006).
24. Guimond, S., Maccarana, M., Olwin, B.B., Lindahl, U. & Rapraeger, A.C. Activating and inhibitory heparin sequences for FGF-2 (basic FGF). Distinct requirements for FGF-1, FGF-2, and FGF-4. J. Biol. Chem. 268, 23906-23914 (1993).
25. Reiland, J., Kempf, D., Roy, M., Denkins, Y. & Marchetti, D. FGF2 binding, signaling, and angiogenesis are modulated by heparanase in metastatic melanoma cells. Neoplasia 8, 596-606 (2006).
26. Gingis-Velitski, S., Ishai-Michaeli, R., Vlodavsky, I. & Ilan, N. Anti-heparanase monoclonal antibody enhances heparanase enzymatic activity and facilitates wound healing. FASEB J. (in the press).
27. 3H]Acetyl-labeling, a convenient method for radiolabeling of glycosaminoglycans. Anal. Biochem. 119, 236-245 (1982).
28. Blumenkrantz, N. & Asboe-Hansen, G. New method for quantitative determination of uronic acids. Anal. Biochem. 54, 484-489 (1973).
29. Pikas, D.S., Li, J.P., Vlodavsky, I. & Lindahl, U. Substrate specificity of heparanases from human hepatoma and platelets. J. Biol. Chem. 273, 18770-18777 (1998).
30. Maccarana, M. & Lindahl, U. Mode of interaction between platelet factor 4 and heparin. Glycobiology 3, 271-277 (1993).