Structural basis and potential role of heparin/heparan sulfate binding to the angiogenesis inhibitor endostatin

EMBO Journal

Volumn 18, Issue 22, 1999, Pages 6240-6248

  Sasaki, Takako ^c   Larsson, Helena ^a   Kreuger, Johan ^a   Salmivirta, Markku ^a   Claesson Welsh, Lena ^a   Lindahl, Ulf ^a   Hohenester, Erhard ^b   Timpl, Rupert ^c  

^a UPPSALA UNIVERSITY   (Sweden)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

Angiogenesis; Endostatin inhibitor; Heparin binding epitope; Site directed mutagenesis

Indexed keywords

ALANINE; ENDOSTATIN; FIBROBLAST GROWTH FACTOR 2; FIBULIN; HEPARAN SULFATE; HEPARIN; RECOMBINANT PROTEIN; VASCULOTROPIN; ZINC;

ANGIOGENESIS; ARTICLE; BINDING AFFINITY; CHICKEN; CHORIOALLANTOIS; CONTROLLED STUDY; DOSE RESPONSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE;

ALLANTOIS; AMINO ACID SUBSTITUTION; ANGIOGENESIS INHIBITORS; ANIMALS; BINDING SITES; CALCIUM-BINDING PROTEINS; CHICK EMBRYO; CHORION; COLLAGEN; ENDOSTATINS; ENDOTHELIAL GROWTH FACTORS; EPITOPES; EXTRACELLULAR MATRIX PROTEINS; FIBROBLAST GROWTH FACTOR 2; HEPARIN; HEPARITIN SULFATE; HUMANS; KINETICS; LYMPHOKINES; MICE; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; NEOVASCULARIZATION, PHYSIOLOGIC; PEPTIDE FRAGMENTS; POINT MUTATION; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SWINE; TRANSFECTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTORS;

GALLUS GALLUS; MAMMALIA;

EID: 0033570910     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.22.6240     Document Type: Article

References (65)

1. Andac, Z., Sasaki, T., Mann, K., Brancaccio, A., Deutzmann, R. and Timpl, R. (1999) Analysis of heparin, α-dystroglycan and sulfatide binding to the G domain of laminin α1 chain by site-directed mutagenesis. J. Mol. Biol., 287, 253-264.
2. Beck, L. and D'Amore, P.A. (1997) Vascular development: cellular and molecular regulation. FASEB J., 11, 365-373.
3. Bitter, T. and Muir, H.M. (1962) A modified uronic acid carbazole reaction. Anal. Biochem., 4, 330-334.
4. Boehm, T., Forkman, J., Browder, T. and O'Reilly, M.S. (1997) Angiogenic therapy of cancer does not induce acquired drug resistance. Nature, 390, 404-407.
5. Boehm, T., O'Reilly, M.S., Keough, K., Shiloach, J., Shapiro, R. and Folkman, J. (1998) Zinc-binding of endostatin is essential for its antiangiogenic activity. Biochem. Biophys. Res. Commun., 252, 190-194.
6. Brooks, P.C., Clark, R.A.F. and Cheresh, D.A. (1994) Requirement of vascular integrin αvβ3 for angiogenesis. Science, 264, 569-571.
7. Cao, Y. (1998) Endogenous angiogenesis inhibitors: angiostatin, endostatin and other proteolytic fragments. In Macieira-Coelho, A. (ed.), Progress in Molecular and Subcellular Biology. Springer, Berlin, Germany, pp. 161-176.
8. Chang, Z., Choon, A. and Friedl, A. (1999) Endostatin binds to blood vessels in situ independent of heparan sulfate and does not compete for fibroblast growth factor-2 binding. Am. J. Pathol., 155, 71-76.
9. Dhanabal, M., Ramachandran, R., Volk, R., Stillman, I.E., Lombardo, M., Iruela-Arispe, M.L., Simons, M. and Sukhatme, V.P. (1999a) Endostatin: yeast production, mutants and antitumor effect in renal cell carcinoma. Cancer Res., 59, 189-197.
10. Dhanabal, M., Ramachandran, R., Waterman, M.J.F., Lu, H., Knebelmann, B., Segal, M. and Sukhatme, V.P. (1999b) Endostatin induces endothelial cell apoptosis. J. Biol. Chem., 274, 11721-11726.
11. DiGabriele, A.D., Lax, I., Chen, D.I., Svahn, C.M., Jaye, M., Schlessinger, J. and Hendrickson, W.A. (1998) Structure of a heparin-linked biologically active dimer of fibroblast growth factor. Nature, 393, 812-817.
12. Ding, Y.-H. et al. (1998) Zinc-dependent dimers observed in crystals of human endostatin. Proc. Natl Acad. Sci. USA, 95, 10443-10448.
13. Esnouf, R.M. (1997) An extensively modified version of MolScript which includes greatly enhanced colouring facilities. J. Mol. Graph., 15, 132-134.
14. 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.
15. Fairbrother, W.J., Champe, M.A., Christinger, H.W., Keyt, B.A. and Starovasnik, M.A. (1998) Solution structure of the heparin-binding domain of vascular endothelial growth factor. Structure, 6, 637-648.
16. Feyzi, E., Lustig, F., Fager, G., Spillmann, D., Lindahl, U. and Salmivirta, M. (1997a) Characterization of heparin and heparan sulfate domains binding to the long splice variant of platelet-derived growth factor A chain. J. Biol. Chem., 272, 5518-5524.
17. Feyzi, E., Trybala, E., Bergström, T., Lindahl, U. and Spillmann, D. (1997b) Structural requirement of heparan sulfate for interaction with herpes simplex virus type 1 virions and isolated glycoprotein C. J. Biol. Chem., 272, 24850-24857.
18. Feyzi, E., Saldeen, T., Larsson, E., Lindahl, U. and Salmivirta, M. (1998) Age-dependent modulation of heparan sulfate structure and function. J. Biol. Chem., 273, 13395-13398.
19. Friedlander, M., Brooks, P.C., Shaffer, R.W., Kincaid, C.M., Varner, J.A. and Cheresh, D.A. (1995) Definition of two angiogenic pathways by distinct αV integrins. Science, 270, 1500-1502.
20. Fry, E.E. et al. (1999). The structure and function of a foot-and-mouth disease virus-oligosaccharide receptor complex. EMBO J., 18, 543-554.
21. Galzie, Z., Kinsella, A.R. and Smith, J.A. (1997) Fibroblast growth factors and their receptors. Biochem. Cell Biol., 75, 669-685.
22. Guimond, S., Maccarana, M., Olwin, B.B., Lindahl, U. and Rapraeger, A.C. (1993) 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.
23. Habuchi, H., Suzuki, S., Saito, T., Tamura, T., Harada, T., Yoshida, K. and Kimata, K. (1992) Structure of a heparan sulphate oligosaccharide that binds to basic fibroblast growth factor. Biochem. J., 285, 805-813.
24. Hanahan, D. and Folkman, J. (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell, 86, 353-364.
25. Herr, A.B., Ornitz, D.M., Sasisekharan, R., Venkataraman, G. and Waksman, G. (1997) Heparin-induced self association of fibroblast growth factor-2. Evidence for two oligomerization processes. J. Biol. Chem., 272, 16382-16389.
26. Hohenester, E., Sasaki, T., Olsen, B.R. and Timpl, R. (1998) Crystal structure of the angiogenesis inhibitor endostatin at 1.5 Å resolution. EMBO J., 17, 1656-1664.
27. 3H]Acetyl-labeling, a convenient method for radiolabeling of glycosaminoglycans. Anal. Biochem., 119, 236-245.
28. Huhtala, M.T., Pentikäinen, O.T. and Johnson, M.S. (1999) A dimeric ternary complex of FGFR1, heparin and FGF-1 leads to an 'electrostatic sandwich' model for heparin binding. Structure, 7, 699-709.
29. Ishihara, M., Tyrrell, D., Stauber, G.B., Brown, S., Cousens, L.S. and Stack, R.J. (1993) Preparation of affinity-fractioned, heparin-derived oligosccharides and their effects on selected biological activities mediated by basic fibroblast growth factor. J. Biol. Chem., 268, 4675-4683.
30. Klint, P. and Claesson-Welsh, C. (1999) Signal transduction by fibroblast growth factor receptors. Front. Biosci., 4, 165-177.
31. Kreuger, J., Prydz, K., Petterson, R.F., Lindahl, U. and Salmivirta, M. (1999) Characterization of fibroblast growth factor 1 binding heparan sulfate domain. Glycobiology, 9, 723-729.
32. Lander, A.D. (1994) Targeting the glycosaminoglycan-binding sites on proteins. Chem. Biol., 1, 73-78.
33. Lander, A.D. (1998) Proteoglycans: master regulators of molecular encounter? Matrix Biol., 17, 456-472.
34. Lindahl, U., Kusche-Gullberg, M. and Kjellén, L. (1998) Regulated diversity of heparan sulfate. J. Biol. Chem., 273, 24979-24982.
35. Lyon, M. and Gallagher, J.T. (1998) Bio-specific sequences and domains in heparan sulphate and the regulation of cell growth and adhesion. Matrix Biol., 17, 485-493.
36. Maccarana, M. and Lindahl, U. (1993) Mode of interaction between platelet factor 4 and heparin. Glycobiology, 3, 271-277.
37. Maccarana, M., Casu, B. and Lindahl, U. (1993) Minimal sequence in heparin/heparan sulfate required for binding of basic fibroblast growth factor. J. Biol. Chem., 268, 23898-23905.
38. Maione, T.E., Gray, G.S., Hunt, A.J. and Sharpe, A.J. (1991) Inhibition of tumor growth in mice by an analogue of platelet factor-4 that lacks affinity for heparin and retains potent angiostatic activity. Cancer Res., 51, 2077-2083.
39. Merritt, E.A. and Murphy, M.E.P. (1994) Raster3D version 2.0. A program for photorealistic molecular graphics. Acta Crystallogr. D, 50,869-873.
40. Miosge, N., Sasaki, T. and Timpl, R. (1999) Angiogenesis inhibitor endostatin is a distinct component of elastic fibers in vessel walls. FASEB J., 13, 1743-1750.
41. Moy, F.J., Safran, M., Seddon, A.P., Kitchen, D., Böhlen, P., Aviezer, D., Yayon, A. and Powers, R. (1997) Properly oriented heparin-decasaccharide-induced dimers are the biologically active form of basic fibroblast growth factor Biochemistry, 36, 4782-4791.
42. Neufeld, G., Cohen, T., Gengrinovitch, S. and Poltorak, Z. (1999) Vascular endothelial growth factor (VEGF) and its receptor. FASEB J., 13, 9-22.
43. Nicholls, A., Sharp, K.A. and Honig, B. (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins, 11, 281-296.
44. O'Reilly, M.S. et al. (1994) Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell, 79, 315-328.
45. O'Reilly, M.S., Holmgren, L., Chen, C.C. and Folkman, J. (1996) Angiostatin induces and sustains dormancy of human primary tumors in mice. Nature Med., 2, 689-692.
46. O'Reilly, M.S. et al. (1997) Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell, 88, 277-285.
47. Perollet, C., Han, Z.C., Savona, C., Caen, J.P. and Bikfalvi, A. (1998) Platelet factor 4 modulates fibroblast growth factor 2 (FGF-2) activity and inhibits FGF-2 dimerization. Blood, 9, 1-11.
48. Pöschl, E., Mayer, U., Stetefeld, J., Baumgartner, R., Holak, T.A., Huber, R. and Timpl, R. (1996) Site-directed mutagenesis and structural interpretation of the nidogen binding site of laminin γl chain. EMBO J., 15, 5154-5159.
49. Pye, D.A., Vives, R.R., Turnbull, J.E., Hyde, P. and Gallagher, J.T. (1998) Heparan sulfate oligosaccharides require 6-O-sulfation for promotion of basic fibroblast growth factor mitogenic activity. J. Biol. Chem., 273, 22936-22942.
50. Rahmoune, H., Chen, H.-L., Gallagher, J.T., Rudland, P.S. and Fernig, D.G. (1998) Interaction of heparan sulfate from mammary cells with acidic fibroblast growth factor (FGF) and basic FGF. Regulation of the activity of basic FGF by high and low affinity binding sites in heparan sulfate. J. Biol. Chem., 273, 7303-7310.
51. Risau, W. (1995) Differentiation of endothelium. FASEB J., 9, 926-933.
52. Risau, W. (1997) Mechanisms of angiogenesis. Nature, 386, 671-674.
53. Safaiyan, F., Lindahl, U. and Salmivirta, M. (1998) Selective reduction of 6-O-sulfation in heparan sulfate from transformed mammary epithelial cells. Eur. J. Biochem., 252, 576-582.
54. Salmivirta, M., Lidholt, K. and Lindahl, U. (1996) Heparan sulfate - a piece of information. FASEB J., 10, 1270-1279.
55. Sasaki, J., Fukai, N., Mann, K., Göhring, W., Olsen, B.R. and Timpl, R. (1998) Structure, function and tissue forms of the C-terminal globular domain of collagen XVIII containing the angiogenesis inhibitor endostatin. EMBO J., 17, 4249-4256.
56. Sato, Y., Abe, M. and Takai, R. (1990) Platelet factor 4 blocks the binding of basic fibroblast growth factor to the receptor and inhibits the spontaneous migration of vascular endothelial cells. Biochem. Biophys. Res. Commun., 172, 595-600.
57. Sharma, A., Askari, J.A., Humphries, M.J., Jones, E.Y. and Stuart, D.I. (1999) Crystal structure of a heparin- and integrin-binding segment of human fibronectin. EMBO J., 18, 1468-1479.
58. Spillmann, D. and Lindahl, U. (1994) Glycosaminoglycan-protein interactions: a question of specificity. Curr. Opin. Struct. Biol., 4, 677-682.
59. Spillmann, D., Witt, D. and Lindahl, U. (1998) Defining the interleukin-8-binding domain of heparan sulfate. J. Biol. Chem., 273, 15487-15493.
60. Taraboletti, G., Belotti, D., Borsotti, P., Rusnati, M., Presta, M. and Giavazzi, R. (1997) The 140-kilodalton antiangiogenic fragment of thrombospondin-1 binds to basic fibroblast growth factor Cell Growth Differ., 8, 471-479.
61. Tyrrell, D.J., Ishihara, M., Rao, N., Horne, A., Kiefer, M.C., Stauber, G.B., Lam, L.H. and Stack, R.J. (1993) Structure and biological activities of a heparin-derived hexasaccharide with high affinity for basic fibroblast growth factor. J. Biol. Chem., 268, 4684-4689.
62. Vallejo, A.N., Pogulis, R.J. and Pease, L.R. (1994) In vitro synthesis of novel genes: mutagenesis and recombination by PCR. PCR Methods Appl., 4, 123-130.
63. Venkataraman, G., Raman, R., Sasisekharan, V. and Sasisekharan, R. (1999) Molecular characteristics of fibroblast growth factor-fibroblast growth factor receptor-heparin-like glycosaminoglycan complex. Proc. Natl Acad. Sci. USA, 96, 3658-3663.
64. Watson, J.B., Getzler, S.B. and Mosher, D.F. (1994) Platelet factor-4 modulates the mitogenic activity of basic fibroblast growth factor. J. Clin. Invest., 94, 261-268.
65. Yamaguchi, N. et al. (1999) Endostatin inhibits VEGF-induced endothelial cell migration and tumor growth independently of zinc binding. EMBO J., 18, 4414-4423.