Crystal structure of the angiogenesis inhibitor endostatin at 1.5 Å resolution

EMBO Journal

Volumn 17, Issue 6, 1998, Pages 1656-1664

  Hohenester, Erhard ^a   Sasaki, Takako ^b   Olsen, Björn R ^c   Timpl, Rupert ^b  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Angiogenesis inhibitor; Collagen; Crystal structure; Heparin binding

Indexed keywords

ANGIOGENESIS INHIBITOR; CARBOHYDRATE BINDING PROTEIN; COLLAGEN; GROWTH FACTOR; HEPARIN; LECTIN; PROTEOHEPARAN SULFATE;

ANGIOGENESIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL PROLIFERATION; CRYSTAL STRUCTURE; ENDOTHELIUM CELL; EXPERIMENTAL NEOPLASM; MITOSIS INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; ARGININE; COLLAGEN; COLLAGEN TYPE XVIII; CRYSTALLOGRAPHY, X-RAY; ENDOSTATINS; HEPARIN; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEOVASCULARIZATION, PHYSIOLOGIC; PEPTIDE FRAGMENTS; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS;

EID: 0032536859     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.6.1656     Document Type: Article

References (49)

1. Beck, L., Jr and D'Amore, P.A. (1997) Vascular development: cellular and molecular regulation. FASEB J., 11, 365-373.
2. Bertrand, J.A., Pignol, D., Bernard, J.-P., Verdier, J.-M., Dagorn, J.-C. and Fontecilla-Camps, J.C. (1996) Crystal structure of human lithostathine, the pancreatic inhibitor of stone formation. EMBO J., 15, 2678-2684.
3. Boehm, T., Folkman, J., Browder, T. and O'Reilly, M.S. (1997) Antiangiogenic therapy of experimental cancer does not induce acquired drug resistance. Nature, 390, 404-407.
4. Bork, P., Downing, A.K., Kieffer, B. and Campbell, I.D. (1996) Structure and distribution of modules in extracellular proteins. Q. Rev. Biophys., 29, 119-167.
5. Brown, K.J. and Parish, C.P. (1994) Histidine-rich glycoprotein and platelet factor 4 mask heparan sulfate proteoglycans recognized by acidic and basic fibroblast growth factor. Biochemistry, 33, 13918-13927.
6. Brünger, A.T. (1992) X-PLOR version 3.1: A System for Crystallography and NMR. Yale University Press, New Haven, CT.
7. Bussolino, F., Mantovani, A. and Persico, G. (1997) Molecular mechanisms of blood vessel formation. Trends Biochem. Sci., 22, 251-256.
8. Clapp, C., Martial, J.A., Guzman, R.C., Rentier-Delrue, F. and Weiner, R.I. (1993) The 16 kDa N-terminal fragment of human prolactin is a potent inhibitor of angiogenesis. Endocrinology, 133, 1292-1299.
9. Collaborative Computing Project No. 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr., D50, 760-763.
10. Cowtan, K.D. and Main, P. (1996) Phase combination and cross validation in iterated density-modification calculations. Acta Crystallogr., D52, 43-48.
11. Dameron, K.M., Volpert, O.V., Tainsky, M.A. and Bouck, N. (1994) Control of angiogenesis in fibroblasts by p53 regulation of thrombospondin-1. Science, 265, 1582-1584.
12. 2+-dependent carbohydrate-recognition domains in animal proteins. Curr. Opin. Struct. Biol., 3, 393-400.
13. 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.
14. Ferrara, N., Clapp, C. and Weiner, R.I. (1991) The 16 kDa fragment of prolactin specifically inhibits basal or fibroblast growth factor-stimulated growth of capillary endothelial cells. Endocrinology, 129, 896-900.
15. Friesel, R.E. and Maciaq, T. (1995) Molecular mechanisms of angiogenesis: fibroblast growth factor signal. FASEB J., 9, 919-925.
16. Fromm, J.R., Hileman, R.E., Caldwell, E.E.O., Weiler, J.M. and Linhardt, R.J. (1997) Pattern and spacing of basic amino acids in heparin binding sites. Arch. Biochem. Biophys., 343, 92-100.
17. Good, D.J., Polversini, P.J., Rastinejad, F., Le Beau, M.M., Lemons, R.S., Frazier, W.A. and Bouck, N.P. (1990) A tumor suppressor-dependent inhibitor of angiogenesis is immunologically and functionally indistinguishable from a fragment of thrombospondin. Proc. Natl Acad. Sci. USA, 87, 6624-6628.
18. Graves, B.J. et al. (1994) Insight into E-selectin/ligand interaction from the crystal structure and mutagenesis of the lec/EGF domains. Nature, 367, 532-538.
19. Hanahan, D. and Folkman, J. (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell, 86, 353-364.
20. Herr, A.B., Ornitz, D.M., Sasisekharan, R., Venkataraman, G. and Waksman, G. (1997) Heparin-induced self-association of fibroblast orowth factor-2. Evidence for two oligomerization processes. J. Biol. Chem., 272, 16382-16389.
21. Holm, L. and Sander, C. (1993) Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123-138.
22. Holm, L. and Sander, C. (1994) The FSSP database of structurally aligned protein fold families. Nucleic Acids Res., 22, 3600-3609.
23. Homandberg, G.A., Williams, J.E., Grant, D., Schuhmacher, B. and Eisenstein, R. (1985) Heparin-binding fragments of fibronectin are potent inhibitors of endothelial cell growth. Am. J. Pathol., 120, 327-332.
24. Jones, T.A., Zou, J.-Y., Cowan, S.W. and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr., A47, 110-119.
25. Kohda, D., Morton, C.J., Parkar, A.A., Hatanaka, H., Inagaki, F.M., Campbell, I.D. and Day, A.J. (1996) Solution structure of the Link module: a hyaluronan-binding domain involved in extracellular matrix stability and cell migration. Cell, 86, 767-775.
26. Kohfeldt, E., Maurer, P., Vannahme, C. and Timpl, R. (1997) Properties of the extracellular calcium binding module of the proteoglycan testican. FEBS Lett., 414, 557-561.
27. Kraulis, P.J. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr., 24, 946-950.
28. Laskowski, R.A., MacArthur, M.W., Moss, D.S. and Thornton, J.M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr., 26, 283-291.
29. Leslie, A.G.W. (1994) MOSFLM Users Guide. MRC-LMB, Cambridge, UK.
30. Mayer, U., Nischt, R., Pöschl, E., Mann, K., Fukuda, K., Gerl, M., Yamada, Y. and Timpl, R. (1993) A single EGF-like motif of laminin is responsible for high-affinity nidogen binding. EMBO J., 12, 1879-1885.
31. 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.
32. Muragaki, Y., Timmons, S., Griffith, C.M., Oh, S.P., Fadel, B., Quertermous, T. and Olsen, B.R. (1995) Mouse Col18a1 is expressed in a tissue-specific manner as three alternative variants and is localized in basement membrane zones. Proc. Natl Acad. Sci. USA, 92, 8763-8767.
33. Myers, J.C., Kivirikko, S., Gordon, M.K., Dion, A.S. and Pihlajaniemi, T. (1992) Identification of a previously unknown human collagen chain, α1(XV), characterized by extensive interruptions in the triple-helical region. Proc. Natl Acad. Sci. USA, 89, 10144-10148.
34. Nicholls, A. (1992) GRASP: Graphical Representation and Analysis of Surface Properties. Columbia University, NY.
35. Oh, S.P., Kamagata, Y., Muragaki, Y., Timmons, S., Ooshima, A. and Olsen, B.R. (1994a) Isolation and sequencing of cDNAs for proteins with multiple domains of Gly-Xaa-Yaa repeats identify a distinct family of collageneous proteins. Proc. Natl Acad. Sci. USA, 91, 4229-4233.
36. Oh, S.P., Warman, M.L., Seldin, M.F., Cheng, S.-D., Knoll, J.H.M., Timmons, S. and Olsen, B.R. (1994b) Cloning of cDNA and genomic DNA encoding human type XVIII collagen and localization of the α1(XVIII) collagen gene to mouse chromosome 10 and human chromosome 21. Genomics, 19, 494-499.
37. 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.
38. O'Reilly, M.S. et al. (1997) Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell, 88, 277-285.
39. Read, R.J. (1986) Improved Fourier coefficients for maps using phases from partial structure factors with errors. Acta Crystallogr., A42, 140-149.
40. Rehn, M. and Pihlajaniemi, T. (1994) α1(XVIII), a collagen chain with frequent interruptions in the collageneous sequence, a distinct distribution and homology with type XV collagen. Proc. Natl Acad. Sci. USA, 91, 4234-4238.
41. Rehn, M. and Pihlajaniemi, T. (1995) Identification of three N-terminal ends of type XVIII collagen chains and tissue-specific differences in the expression of the corresponding transcripts. J. Biol. Chem., 270, 4705-4711.
42. Rehn, M., Hintikka, E. and Pihlajaniemi, T. (1996) Characterization of the mouse gene for the α1 chain of type XVIII collagen (Col18a1) reveals that the three variant N-terminal polypeptide forms are transcribed from two widely separated promoters. Genomics, 32, 436-446.
43. Risau, W. (1997) Mechanisms of angiogenesis. Nature, 386, 671-674.
44. Sage, E.H. (1997) Pieces of eight: bioactive fragments of extracellular proteins as regulators of angiogenesis. Trends Cell Biol., 7, 182-186.
45. Thompson, L.D., Pantoliano, M.W. and Springer, B.A. (1994) Energetic characterization of the basic fibroblast growth factor-heparin interaction: identification of the heparin-binding domain. Biochemistry, 33, 3831-3840.
46. Tolsma, S.S., Volpert, O.V., Good, D.J., Frazier, W.A., Polverini, P.J. and Bouck, N. (1993) Peptides derived from two separate domains of the matrix protein thrombospondin-1 have antiangiogenic activity. J. Cell Biol., 122, 497-511.
47. Weis, W.I., Kahn, R., Fourme, R., Drickamer, K. and Hendrickson, W.A. (1991) Structure of the calcium-dependent lectin domain from a rat mannose-binding protein determined by MAD phasing. Science, 254, 1608-1615.
48. Weis, W.I., Drickamer, K. and Hendrickson, W.A. (1992) Structure of a C-type mannose-binding protein complexed with an oligosaccharide. Nature, 360, 127-134.
49. Yayon, A., Klagsbrun, M., Esko, J.D., Leder, P. and Ornitz, D.M. (1991) Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell, 64, 841-848.