Structure, function and tissue forms of the C-terminal globular domain of collagen XVIII containing the angiogenesis inhibitor endostatin

EMBO Journal

Volumn 17, Issue 15, 1998, Pages 4249-4256

  Sasaki, Takako ^a   Fukai, Naomi ^b   Mann, Karlheinz ^a   Göhring, Walter ^a   Olsen, Björn R ^b   Timpl, Rupert ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Binding properties; Collagen; Proteolysis; Recombinant production; Serum form

Indexed keywords

ANGIOGENESIS INHIBITOR; COLLAGEN; ENDOSTATIN; EPITOPE; FIBULIN; HEPARIN; LAMININ; PERLECAN; RECOMBINANT PROTEIN; SULFATIDE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; DNA TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOASSAY; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN STRUCTURE; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; ANIMALS; CARBOHYDRATE METABOLISM; CELL LINE; COLLAGEN; COLLAGEN TYPE XVIII; ENDOPEPTIDASES; ENDOSTATINS; GENETIC VECTORS; HUMANS; HYDROLYSIS; LIGANDS; MICE; MOLECULAR SEQUENCE DATA; NEOVASCULARIZATION, PATHOLOGIC; ORGAN SPECIFICITY; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 0032479999     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.15.4249     Document Type: Article

References (44)

1. Abe, N., Muragaki, Y., Yoshioka, H., Inoue, H. and Ninomiya, Y. (1993) Identification of a novel collagen chain represented by extensive interruptions in the triple-helical region. Biochem. Biophys. Res. Commun., 196, 576-582.
2. Boehm, T., Folkman, J., Browder, T. and O'Reilly, M.S. (1997) Anti-angiogenic therapy of cancer does not induce acquired drug resistance. Nature, 390, 404-407.
3. Cao, Y. et al. (1996) Kringle domains of human angiostatin: characterization of the anti-proliferative activity on endothelial cells. J. Biol. Chem., 271, 29461-29467.
4. Cao, Y., Chen, A., An, S.S.A., Ji, R.-W., Davidson, D., Cao, Y. and Llinas, M. (1997) Kringle 5 of plasminogen is a novel inhibitor of endothelial cell growth. J. Biol. Chem., 272, 22924-22928.
5. Clapp, C., Martial, J.A., Guzman, R.C., Rentier-Delrue, F. and Weiner, R.I. (1993) The 16-kilodalton N-terminal fragment of human prolactin is a potent inhibitor of angiogenesis. Endocrinology, 133, 1292-1299.
6. Costell, M., Mann, K., Yamada, Y. and Timpl, R. (1997) Characterization of recombinant perlecan domain I and its substitution by glycosaminoglycans and oligosaccharides. Eur. J. Biochem., 243, 115-121.
7. Dawson, D.W., Pearce, S.F.A., Zhong, R., Silverstein, R.L., Frazier, W.A. and Bouck, N.P. (1997) CD36 mediates the in vitro inhibitory effects of thrombospondin-1 on endothelial cells. J. Cell Biol., 138, 707-717.
8. Folkman, J. (1995) Clinical applications of research on angiogenesis. N. Engl. J. Med., 333, 1757-1763.
9. Fraenkel-Conrat, H. (1957) Methods for investigating the essential groups for enzyme activity. Methods Enzymol., 4, 247-269.
10. Funk, S.E. and Sage, E.H. (1993) Differential effects of SPARC and cationic SPARC peptides on DNA synthesis by endothelial cells and fibroblasts. J. Cell. Physiol., 154, 53-63.
11. Good, D.J., Polverini, 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.
12. Gupta, S.K., Hassel, T. and Singh, J.P. (1995) A potent inhibitor of endothelial cell proliferation is generated by proteolytic cleavage of the chemokine platelet factor 4. Proc. Natl Acad. Sci. USA, 92, 7799-7803.
13. Hanahan, D. and Folkman, J. (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell, 86, 353-364.
14. 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.
15. Homandberg, G.A., Williams, J.E., Grant, D., Schumacher, B. and Eisenstein, R. (1985) Heparin-binding fragments of fibronectin are potent inhibitors of endothelial cell growth. Am. J. Pathol., 120, 327-332.
16. Iruela-Arispe, M.L., Bornstein, P. and Sage, H. (1991) Thrombospondin exerts an antiangiogenic effect on cord formation by endothelial cells in vitro. Proc. Natl Acad. Sci. USA, 88, 5026-5030.
17. 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.
18. Lees, J.F., Tasab, M. and Bulleid, N.J. (1997) Identification of the molecular recognition sequence which determines the type-specific assembly of procollagen. EMBO J., 16, 908-916.
19. Maione, T.E., Gray, G.S., Petro, J., Hunt, A.J., Donner, A.L., Bauer, S.I., Carson, H.F. and Sharpe, R.J. (1990) Inhibition of angiogenesis by recombinant human platelet factor-4 and related peptides. Science, 247, 77-79.
20. Mann, K., Mechling, D.E., Bächinger, H.P., Eckerskorn, C., Gaill, F. and Timpl, R. (1996) Glycosylated threonine but not 4-hydroxyproline dominates the triple helix stabilizing positions in the sequence of a hydrothermal vent worm cuticle collagen. J. Mol. Biol., 261, 255-266.
21. 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.
22. Müller, G., Behrens, J., Nussbaumer, U., Böhlen, P. and Birchmeier, W. (1987) Inhibitory action of transforming growth factor beta on endothelial cells. Proc. Natl Acad. Sci. USA, 84, 5600-5604.
23. 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.
24. 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-XaaYaa repeats identify a distinct family of collagenous proteins. Proc. Natl Acad. Sci. USA, 91, 4229-4233.
25. 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.
26. 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.
27. 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.
28. O'Reilly, M.S. et al. (1997) Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell, 88, 277-285.
29. Pan, T.C., Sasaki, T., Zhang, R.-Z., Fässler, R., Timpl, R. and Chu, M.-L. (1993) Structure and expression of fibulin-2, a novel extracellular matrix protein with multiple EGF-like repeats and consensus motifs for calcium-binding. J. Cell Biol., 123, 1269-1277.
30. Rehn, M. and Pihlajaniemi, T. (1994) α1(XVIII), a collagen chain with frequent interruptions in the collagenous sequence, a distinct tissue distribution, and homology with type XV collagen. Proc. Natl Acad. Sci. USA, 91, 4234-4238.
31. Rehn, M., Hintikka, E. and Pihlajaniemi, T. (1994) Primary structure of the α1 chain of mouse type XVIII collagen, partial structure of the corresponding gene, and comparison of the α1(XVIII) chain with its homologue, the α1(XV) collagen chain. J. Biol. Chem., 269, 13929-13935.
32. Rehn, M., Hintikka, E. and Pihlajaniemi, T. (1996) Characterization of the mouse gene for the α1 chain of type XVIII collagen (Col 18a1) reveals that three variant N-terminal polypeptides forms are transcribed from two widely separated promoters. Genomics, 32, 436-446.
33. Reinhardt, D.P., Sasaki, T., Dzamba, B.J., Keene, D.R., Chu, M.-L., Göhring, W., Timpl, R. and Sakai, L.Y. (1996) Fibrillin-1 and fibulin-2 interact and are colocalized in some tissues. J. Biol. Chem., 271, 19489-19496.
34. Sasaki, T., Göhring, W., Pan, T.-C., Chu, M.-L. and Timpl, R. (1995) Binding of mouse and human fibulin-2 to extracellular matrix ligands. J. Mol. Biol., 254, 892-899.
35. Sasaki, T., Wiedemann, H., Matzner, M., Chu, M.-L. and Timpl, R. (1996) Expression of fibulin-2 by fibroblasts and deposition with fibronectin into a fibrillar matrix. J. Cell Sci., 109, 2895-2904.
36. Sasaki, T., Hohenester, E., Göhring, W. and Timpl, R. (1998) Crystal structure and mapping by site-directed mutagenesis of the collagen-binding epitope of an activated form of BM-40/SPARC/osteonectin. EMBO J., 17, 1625-1634.
37. Schulze, B., Mann, K., Battistutta, R., Wiedemann, H. and Timpl, R. (1995) Structural properties of recombinant domain III-3 of perlecan containing a globular domain inserted into an epidermal-growth-factor-like motif. Eur. J. Biochem., 231, 551-556.
38. Standker, L., Schrader, M., Kanse, S.M., Jürgens, M., Forssmann,W.-G. and Preissner, K.T. (1997) Isolation and characterization of the circulating form of human endostatin. FEBS Lett., 420, 129-133.
39. Takahashi, K. (1968) The reaction of phenylglyoxal with arginine residues in proteins. J. Biol. Chem., 243, 6171-6179.
40. Taraboletti, G., Roberts, D., Liotta, L.A. and Giavazzi, R. (1990a) Platelet thrombospondin modulates endothelial cell adhesion, mobility and growth: a potential angiogenesis regulatory factor. J. Cell Biol., 111, 765-772.
41. Taraboletti, G., Rao, C.N., Krutzsch, H.C., Liotta, L.A. and Roberts, D.D. (1990b) Sulfatide-binding domain of the laminin A chain. J. Biol. Chem., 265, 12253-12258.
42. Timpl, R. (1982) Antibodies to collagens and procollagens. Methods Enzymol., 82, 472-498.
43. 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 anti-angiogenic activity. J. Cell Biol., 122, 497-511.
44. Vogel, T., Guo, N., Krutzsch, H.C., Blake, D.A., Hartmann, J., Mendelovitz, S., Panet, A. and Roberts, D.D. (1993) Modulation of endothelial cell proliferation, adhesion and motility by recombinant heparin-binding domain and synthetic peptides from the type I repeats of thrombospondin. J. Cell. Biochem., 53, 74-84.