The structures of the thrombospondin-1 N-terminal domain and its complex with a synthetic pentameric heparin

Structure

Volumn 14, Issue 1, 2006, Pages 33-42

  Tan, Kemin ^a,c   Duquette, Mark ^b   Liu, Jin Huan ^a,c   Zhang, Rongguang ^d   Joachimiak, Andrzej ^d   Wang, Jia Huai ^a,c   Lawler, Jack ^b,c  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALRETICULIN; COLLAGEN; CONCANAVALIN A; FIBRINOGEN; FONDAPARINUX; GLUCAN GLUCOSIDASE; GLYCOSAMINOGLYCAN; HEPARIN; INTEGRIN; LAMININ; LECTIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; THROMBOSPONDIN 1;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; COMPLEX FORMATION; CRYSTAL STRUCTURE; DISULFIDE BOND; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; THROMBOCYTE AGGREGATION;

AMINO ACID SEQUENCE; BINDING SITES; CONCANAVALIN A; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; HUMANS; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; POLYSACCHARIDES; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY, PROTEIN; THROMBOSPONDIN 1;

EID: 33644807623     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2005.09.017     Document Type: Article

References (51)

1. J.C. Adams, and J. Lawler The thrombospondins Int. J. Biochem. Cell Biol. 36 2004 961 968
2. J.C. Adams, R. Monk, A.L. Taylor, S. Ozbek, N. Fascetti, S. Baumgartner, and J. Engel Characterisation of Drosophila thrombospondin defines an early origin of pentameric thrombospondins J. Mol. Biol. 328 2003 479 494
3. K.A. Bauer New pentasaccharides for prophylaxis of deep vein thrombosis: pharmacology Chest 124 2003 364S 370S
4. G. Beckmann, J. Hanke, P. Bork, and J.G. Reich Merging extracellular domains: fold prediction for laminin G-like and amino-terminal thrombospondin-like modules based on homology to pentraxins J. Mol. Biol. 275 1998 725 730
5. A. Bonnefoy, R. Hantgan, C. Legrand, and M.M. Frojmovic A model of platelet aggregation involving multiple interactions of thrombospondin-1, fibrinogen, and GPIIbIIIa receptor J. Biol. Chem. 276 2001 5605 5612
6. P. Bork, A.K. Downing, B. Kieffer, and I.D. Campbell Structure and distribution of modules in extracellular proteins Q. Rev. Biophys. 29 1996 119 167
7. P. Bornstein, and E.H. Sage Matricellular proteins: extracellular modulators of cell function Curr. Opin. Cell Biol. 14 2002 608 616
8. P. Bornstein, A. Agah, and T.R. Kyriakides The role of thrombospondins 1 and 2 in the regulation of cell-matrix interactions, collagen fibril formation, and the response to injury Int. J. Biochem. Cell Biol. 36 2004 1115 1125
9. A.T. Brunger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, R.W. Grosse-Kunstleve, J.S. Jiang, J. Kuszewski, M. Nilges, and N.S. Pannu Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallogr. D Biol Crystallogr. 54 1998 905 921
10. M.J. Calzada, J.M. Sipes, H.C. Krutzsch, P.D. Yurchenco, D.S. Annis, D.F. Mosher, and D.D. Roberts Recognition of the N-terminal modules of thrombospondin-1 and thrombospondin-2 by α6β1 integrin J. Biol. Chem. 278 2003 40679 40687
11. M.J. Calzada, L. Zhou, J.M. Sipes, J. Zhang, H.C. Krutzsch, M.L. Iruela-Arispe, D.S. Annis, D.F. Mosher, and D.D. Roberts α4β1 integrin mediates selective endothelial cell responses to thrombospondins 1 and 2 in vitro and modulates angiogenesis in vivo Circ. Res. 94 2004 462 470
12. CCP4 (Collaborative Computational Project, Number 4) The CCP4 suite: programs for protein crystallography Acta Crystallogr. D Biol. Crystallogr. 50 1994 760 763
13. H. Chen, M.E. Herndon, and J. Lawler The cell biology of thrombospondin-1 Matrix Biol. 19 2000 597 614
14. K.S. Christopherson, E.M. Ullian, C.C. Stokes, C.E. Mullowney, J.W. Hell, A. Agah, J. Lawler, D.F. Mosher, P. Bornstein, and B.A. Barres Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis Cell 120 2005 421 433
15. C. Damas, T. Vink, H.K. Nieuwenhuis, and J.J. Sixma The 33-kDa platelet α-granule membrane protein (GMP-33) is an N-terminal proteolytic fragment of thrombospondin Thromb. Haemost. 86 2001 887 893
16. M.A. Ferrari do Outeiro-Bernstein, S.S. Nunes, A.C. Andrade, T.R. Alves, C. Legrand, and V. Morandi A recombinant NH(2)-terminal heparin-binding domain of the adhesive glycoprotein, thrombospondin-1, promotes endothelial tube formation and cell survival: a possible role for syndecan-4 proteoglycan Matrix Biol. 21 2002 311 324
17. W.A. Hendrickson Determination of macromolecular structures from anomalous diffraction of synchrotron radiation Science 254 1991 51 58
18. M.E. Herndon, C.S. Stipp, and A.D. Lander Interactions of neural glycosaminoglycans and proteoglycans with protein ligands: assessment of selectivity, heterogeneity and the participation of core proteins in binding Glycobiology 9 1999 143 155
19. T.A. Jones, J.Y. Zou, S.W. Cowan, and Kjeldgaard Improved methods for building protein models in electron density maps and the location of errors in these models Acta Crystallogr. A 47 1991 110 119
20. P.J. Kraulis Molscript: a program to produce both detailed and schematic plots of proetin structures J. Appl. Crystallogr. 24 1991 946 950
21. H.C. Krutzsch, B.J. Choe, J.M. Sipes, N. Guo, and D.D. Roberts Identification of an α(3)β(1) integrin recognition sequence in thrombospondin-1 J. Biol. Chem. 274 1999 24080 24086
22. S. Kuroda, M. Oyasu, M. Kawakami, N. Kanayama, K. Tanizawa, N. Saito, T. Abe, S. Matsuhashi, and K. Ting Biochemical characterization and expression analysis of neural thrombospondin-1-like proteins NELL1 and NELL2 Biochem. Biophys. Res. Commun. 265 1999 79 86
23. M. Kvansakul, J.C. Adams, and E. Hohenester Structure of a thrombospondin C-terminal fragment reveals a novel calcium core in the type 3 repeats EMBO J. 23 2004 1223 1233
24. J. Lawler, and M. Detmar Tumor progression: the effects of thrombospondin-1 and -2 Int. J. Biochem. Cell Biol. 36 2004 1038 1045
25. J. Lawler, L.H. Derick, J.E. Connolly, J.H. Chen, and F.C. Chao The structure of human platelet thrombospondin J. Biol. Chem. 260 1985 3762 3772
26. J. Lawler, P. Ferro, and M. Duquette Expression and mutagenesis of thrombospondin Biochemistry 31 1992 1173 1180
27. J. Lawler, M. Sunday, V. Thibert, M. Duquette, E.L. George, H. Rayburn, and R.O. Hynes Thrombospondin-1 is required for normal murine pulmonary homeostasis and its absence causes pneumonia J. Clin. Invest. 101 1998 982 992
28. S.S. Li, A. Forslow, and K.G. Sundqvist Autocrine regulation of T cell motility by calreticulin-thrombospondin-1 interaction J. Immunol. 174 2005 654 661
29. L. Lo Conte, C. Chothia, and J. Janin The atomic structure of protein-protein recognition sites J. Mol. Biol. 285 1999 2177 2198
30. M. Matsui, K. Mizuseki, J. Nakatani, S. Nakanishi, and Y. Sasai Xenopus kielin: a dorsalizing factor containing multiple chordin-type repeats secreted from the embryonic midline Proc. Natl. Acad. Sci. USA 97 2000 5291 5296
31. B. Merle, L. Malaval, J. Lawler, P. Delmas, and P. Clezardin Decorin inhibits cell attachment to thrombospondin-1 by binding to a KKTR-dependent cell adhesive site present within the N-terminal domain of thrombospondin-1 J. Cell. Biochem. 67 1997 75 83
32. W.M. Miao, W.L. Seng, M. Duquette, P. Lawler, C. Laus, and J. Lawler Thrombospondin-1 type 1 repeat recombinant proteins inhibit tumor growth through transforming growth factor-beta-dependent and -independent mechanisms Cancer Res. 61 2001 7830 7839
33. I. Mikhailenko, D. Krylov, K.M. Argraves, D.D. Roberts, G. Liau, and D.K. Strickland Cellular internalization and degradation of thrombospondin-1 is mediated by the amino-terminal heparin binding domain (HBD). High affinity interaction of dimeric HBD with the low density lipoprotein receptor-related protein J. Biol. Chem. 272 1997 6784 6791
34. M. Moradi-Ameli, G. Deleage, C. Geourjon, and M. van der Rest Common topology within a non-collagenous domain of several different collagen types Matrix Biol. 14 1994 233 239
35. C. Mulatero, M. Lyon, J. Lawler, G. Jayson, and J. Gallagher Novel approaches to investigate glycoaminoglycan (GAG) binding to the N terminal region of thrombospondin-1 (NTSP) Proc. Am. Assoc. Cancer Res. 44 2003 1430
36. J.E. Murphy-Ullrich, S. Gurusiddappa, W.A. Frazier, and M. Hook Heparin-binding peptides from thrombospondins 1 and 2 contain focal adhesion-labilizing activity J. Biol. Chem. 268 1993 26784 26789
37. A.G. Murzin, S.E. Brenner, T. Hubbard, and C. Chothia SCOP: a structural classification of proteins database for the investigation of sequences and structures J. Mol. Biol. 247 1995 536 540
38. A. Nicholls, K.A. Sharp, and B. Honig Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons Proteins 11 1991 281 296
39. J.M. O'Leary, J.M. Hamilton, C.M. Deane, N.V. Valeyev, L.J. Sandell, and A.K. Downing Solution structure and dynamics of a prototypical chordin-like cysteine-rich repeat (von Willebrand Factor type C module) from collagen IIA J. Biol. Chem. 279 2004 53857 53866
40. A.W. Orr, M.A. Pallero, and J.E. Murphy-Ullrich Thrombospondin stimulates focal adhesion disassembly through Gi- and phosphoinositide 3-kinase-dependent ERK activation J. Biol. Chem. 277 2002 20453 20460
41. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode C.W. Carter Jr. R.M. Sweet Methods in Enzymology 1997 Academic Press New York 307 326
42. T. Pihlajamaa, H. Lankinen, J. Ylostalo, L. Valmu, J. Jaalinoja, F. Zaucke, L. Spitznagel, S. Gosling, A. Puustinen, and M. Morgelin Characterization of recombinant amino-terminal NC4 domain of human collagen IX: interaction with glycosaminoglycans and cartilage oligomeric matrix protein J. Biol. Chem. 279 2004 24265 24273
43. K. Rothblum, R.C. Stahl, and D.J. Carey Constitutive release of α4 type V collagen N-terminal domain by Schwann cells and binding to cell surface and extracellular matrix heparan sulfate proteoglycans J. Biol. Chem. 279 2004 51282 51288
44. G. Rudenko, E. Hohenester, and Y.A. Muller LG/LNS domains: multiple functions-one business end? Trends Biochem. Sci. 26 2001 363 368
45. H. Scheel, S. Tomiuk, and K. Hofmann A common protein interaction domain links two recently identified epilepsy genes Hum. Mol. Genet. 11 2002 1757 1762
46. K. Tan, M. Duquette, J.H. Liu, Y. Dong, R. Zhang, A. Joachimiak, J. Lawler, and J.H. Wang Crystal structure of the TSP-1 type 1 repeats: a novel layered fold and its biological implication J. Cell Biol. 159 2002 373 382
47. T.C. Terwilliger SOLVE and RESOLVE: automated structure solution and density modification C.W. Carter Jr. R.M. Sweet Methods in Enzymology 2003 Academic Press New York 22 37
48. C. Voland, C.M. Serre, P. Delmas, and P. Clezardin Platelet-osteosarcoma cell interaction is mediated through a specific fibrinogen-binding sequence located within the N-terminal domain of thrombospondin 1 J. Bone Miner. Res. 15 2000 361 368
49. S. Wang, M.E. Herndon, S. Ranganathan, S. Godyna, J. Lawler, W.S. Argraves, and G. Liau Internalization but not binding of thrombospondin-1 to low density lipoprotein receptor-related protein-1 requires heparan sulfate proteoglycans J. Cell. Biochem. 91 2004 766 776
50. Z. Yang, D.K. Strickland, and P. Bornstein Extracellular matrix metalloproteinase 2 levels are regulated by the low density lipoprotein-related scavenger receptor and thrombospondin 2 J. Biol. Chem. 276 2001 8403 8408
51. H. Yu, D. Tyrrell, J. Cashel, N.H. Guo, T. Vogel, J.M. Sipes, L. Lam, H.M. Fillit, J. Hartman, and S. Mendelovitz Specificities of heparin-binding sites from the amino-terminus and type 1 repeats of thrombospondin-1 Arch. Biochem. Biophys. 374 2000 13 23