Conformational analysis of an α3β1 integrin-binding peptide from thrombospondin-1: Implications for antiangiogenic drug design

Journal of Medicinal Chemistry

Volumn 49, Issue 21, 2006, Pages 6324-6333

  Furrer, Julien ^a   Luy, Burkhard ^a   Basrur, Venkatesha ^b,e   Roberts, David D ^b,d   Barchi Jr , Joseph J ^c  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b NATIONAL CANCER INSTITUTE   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d Natl Heart Lung and Blood I   (United States)

^e UNIVERSITY OF TOLEDO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DODECYLPHOSPHORYLCHOLINE; PHENYLALANYLGLUTAMINYLGLYLCYLVALYLLEUCYLGLUTAMINYLASPARAGINYLVALYLARGINYLPHENYLALANYLVALYLPHENYLALANINE; SYNTHETIC PEPTIDE; THROMBOSPONDIN; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 3; WATER; ANGIOGENESIS INHIBITOR; DRUG DERIVATIVE; OLIGOPEPTIDE; PHOSPHORYLCHOLINE; THROMBOSPONDIN 1;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; DRUG CONFORMATION; DRUG STRUCTURE; MICELLE; MOLECULAR RECOGNITION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN MOTIF; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; CELL ADHESION; CHEMICAL STRUCTURE; CHEMISTRY; CIRCULAR DICHROISM; DRUG DESIGN; HUMAN; METABOLISM; PROTEIN SECONDARY STRUCTURE; SOLUTION AND SOLUBILITY; STRUCTURE ACTIVITY RELATION; SYNTHESIS; TUMOR CELL LINE;

ANGIOGENESIS INHIBITORS; CELL ADHESION; CELL LINE, TUMOR; CIRCULAR DICHROISM; DRUG DESIGN; HUMANS; INTEGRIN ALPHA3BETA1; MAGNETIC RESONANCE SPECTROSCOPY; MICELLES; MODELS, MOLECULAR; OLIGOPEPTIDES; PHOSPHORYLCHOLINE; PROTEIN STRUCTURE, SECONDARY; SOLUTIONS; STRUCTURE-ACTIVITY RELATIONSHIP; THROMBOSPONDIN 1; WATER;

EID: 33750101205     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm060833l     Document Type: Article

References (55)

1. Hynes, R. O. Integrins: bidirectional, allosteric signaling machines. Cell 2002, 110, 673-687.
2. Hood, J. D.; Cheresh, D. A. Role of integrins in cell invasion and migration. Nat. Rev. Cancer 2002, 2, 91-100.
3. Arnaout, M. A.; Goodman, S. L.; Xiong, J. P.; Stehle, T.; Zhang, R.; Joachimiak, A.; Frech, M. Coming to grips with integrin binding to ligands. Curr. Opin. Cell Biol. 2002, 14, 641-651.
4. Xiong, J. P.; Stehle, T.; Zhang, R.; Joachimiak, A.; Frech, M.; Goodman, S. L.; Arnaout, M. A. Crystal structure of the extracellular segment of integrin alpha Vbeta3 in complex with an Arg-Gly-Asp ligand. Science 2002, 296, 151-155.
5. Springer, T. A. Predicted and experimental structures of integrins and beta-propellers. Curr. Opin. Struct. Biol. 2002, 12, 802-813.
6. Pierschbacher, M. D.; Ruoslahti, E. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature 1984, 309, 30-33.
7. Main, A. L.; Harvey, T. S.; Baron, M.; Boyd, J.; Campbell, I. D. The three-dimensional structure of the tenth type III module of fibronectin: an insight into RGD-mediated interactions. Cell 1992, 71, 671-678.
8. Pierschbacher, M. D.; Ruoslahti, E. Influence of stereochemistry of the sequence Arg-Gly-Asp-Xaa on binding specificity in cell adhesion. J. Biol. Chem. 1987, 262, 17294-17298.
9. Emsley, J.; Knight, C. G.; Farndale, R. W.; Barnes, M. J.; Liddington, R. C. Structural basis of collagen recognition by integrin alpha2beta1. Cell 2000, 101, 47-56.
10. Ruoslahti, E. RGD and other recognition sequences for integrins. Ann. Rev. Cell Dev. Biol. 1996, 12, 697-715.
11. Loftus, J. C.; Liddington, R. C. New insights into integrin-ligand interaction. J. Clin. Invest 1997, 100, 77-81.
12. Gehlsen, K. R.; Sriramarao, P.; Furcht, L. T.; Skubitz, A. P. A synthetic peptide derived from the carboxy terminus of the laminin A chain represents a binding site for the alpha 3 beta 1 integrin. J. Cell Biol. 1992, 117, 449-459.
13. Krutzsch, H. C.; Choe, B.; Sipes, J. M.; Guo, N.; Roberts, D. D. Identification of an α3β1 integrin recognition sequence in thrombospondin-1. J. Biol. Chem. 1999, 274, 24080-24086.
14. Guo, N.; Templeton, N. S.; Al-Barazi, H.; Cashel, J. A.; Sipes, J. M.; Krutzsch, H. C.; Roberts, D. D. Thrombospondin-1 promotes α3β1 integrin-mediated adhesion and neurite-like outgrowth and inhibits proliferation of small cell lung carcinoma cells. Cancer Res. 2000, 60, 457-466.
15. Chandrasekaran, L.; He, C.-Z.; Al-Barazi, H. O.; Krutzsch, H. C.; Iruela-Arispe, M. L.; Roberts, D. D. Cell contact-dependent activation of α3β1 integrin modulates endothelial cell responses to thrombospondin-1. Mol. Biol. Cell 2000, 11, 2885-2900.
16. Tan, K.; Duquette, M.; Liu, J. H.; Zhang, R. G.; Joachimiak, A.; Wang, J. H.; Lawler, J. The structures of the thrombospondin-1 N-terminal domain and its complex with a synthetic pentameric heparin. Structure 2006, 14, 33-42.
17. Beckmann, G.; Hanke, J.; Bork, P.; Reich, J. G. Merging extracellular domains: fold prediction for laminin G-like and amino-terminal thrombospondin-like modules based on homology to pentraxins. J. Mol. Biol. 1998, 275, 725-730.
18. Hohenester, E.; Tisi, D.; Talts, J. F.; Timpl, R. The crystal structure of a laminin G-like module reveals the molecular basis of alpha-dystroglycan binding to laminins, perlecan, and agrin. Mol. Cell 1999, 4, 783-792.
19. Marion, D.; Ikura, M.; Tschudin, R.; Bax, A. Rapid Recording of 2D NMR Spectra without Phase Cycling. Application to the Study of Hydrogen Exchange in Proteins. J. Magn. Reson. 1989, 85, 393-399.
20. Palmer, A. G.; Cavanagh, J.; Wright, P. E.; Ranee, M. Sensitivity Improvement in Proton-Detected 2-Dimensional Heteronuclear Correlation Nmr-Spectroscopy. J. Magn. Reson. 1991, 93, 151-170.
21. Cavanagh, J.; Palmer, A. G.; Wright, P. E.; Ranee, M. Sensitivity Improvement in Proton-Detected 2-Dimensional Heteronuclear Relay Spectroscopy. J. Magn. Reson. 1991, 91, 429-436.
22. Liu, M. L.; Mao, X. A.; Ye, C. H.; Huang, H.; Nicholson, J. K.; Lindon, J. C. Improved WATERGATE pulse sequences for solvent suppression in NMR spectroscopy. J. Magn. Reson. 1998, 132, 125-129.
23. Hwang, T. L.; Shaka, A. J. Multiple-pulse mixing sequences that selectively enhance chemical exchange or cross-relaxation peaks in high-resolution NMR spectra. J. Magn. Reson. 1998, 135, 280-287.
24. Kneller, D. G.; Kuntz, I. D. Ucsf Sparky - an NMR Display, Annotation and Assignment Tool. J. Cell. Biochem. 1993, 254.
25. Braunschweiler, L.; Ernst, R. R. Coherence Transfer by Isotropic Mixing: Application to Proton Correlation Spectroscopy. J. Magn. Reson. 1983, 53, 521-528.
26. Bax, A.; Davis, D. G. MLEV-17-based 2D homonuclear magnetization transfer spectroscopy. J. Magn. Reson. 1985, 65, 355-360.
27. Shaka, A. J.; Lee, C. J.; Pines, A. Iterative Schemes for Bilinear Operators; Application to Spin Decoupling. J. Magn. Reson. 1988, 77, 274-293.
28. Bothner-By, A. A.; Stevens, R. L.; Lee, J.; Warren, C. D.; Jeanloz, R. W. Structure Determination of a Tetrasaccharide: Transient Nuclear Overhauser Effects in the Rotating Frame. J. Am. Chem. Soc. 1984, 106, 811-813.
29. Bax, A.; Davis, D. G. Practical Aspects of Two-Dimensional Transverse NOE Spectroscopy. J. Magn. Reson. 1985, 63, 207-213.
30. Wishart, D. S.; Bigam, C. G.; Yao, J.; Abildgaard, F.; Dyson, H. J.; Oldfield, E.; Markley, J. L.; Sykes, B. D. H-1, C-13 and N-15 Chemical-Shift Referencing in Biomolecular Nmr. J. Biomol. NMR 1995, 6, 135-140.
31. Furrer, J.; Kramer, F.; Marino, J. P.; Glaser, S. J.; Luy, B. Homonuclear Hartmann-Hahn transfer with reduced relaxation losses by use of the MOCCA-XY16 multiple pulse sequence. J. Magn. Reson. 2004, 166, 39-46.
32. Nilges, M.; Gronenborn, A. M.; Brunger, A. T.; Clore, G. M. Determination of 3-Dimensional Structures of Proteins by Simulated Annealing with Interproton Distance Restraints - Application to Crambin, Potato Carboxypeptidase Inhibitor and Barley Serine Proteinase Inhibitor-2. Protein Eng. 1988, 2, 27-38.
33. Wilson, K. E.; Li, Z.; Kara, M.; Gardner, K. L.; Roberts, D. D. β1 integrin- and proteoglycan-mediated stimulation of T lymphoma cell adhesion and mitogen-activated protein kinase signaling by thrombospondin-1 and thrombospondin-1 peptides. J. Immunol. 1999, 163, 3621-3628.
34. Koivunen, E.; Wang, B. C.; Ruoslahti, E. Isolation of A Highly Specific Ligand for the Alpha(5)Beta(1) Integrin from A Phage Display Library. J. Cell Biol. 1994, 124, 373-380.
35. Katabami, K.; Kato, T.; Sano, R.; Ogura, M.; Mizuno, H.; Itoh, S.; Tsuji, T. Characterization of the promoter for the alpha 3 integrin gene in various tumor cell lines: Roles of the Ets- and Sp-family of transcription factors. J. Cell. Biochem. 2006, 97, 530-543.
36. Calzada, M. J.; Sipes, J. M.; Krutzsch, H. C.; Yurchenco, P. D.; Annis, D. S.; Mosher, D. F.; Roberts, D. D. Recognition of the N-terminal modules of thrombospondin-1 and thrombospondin-2 by alpha6beta1 integrin. J. Biol. Chem. 2003, 278, 40679-40687.
37. Woody; R. W. Theory of Circular Dichroism in Proteins. In Circular Dichroism and the Conformational Analysis of Biomolecules; Gerald D Fasman Ed.; Plenum Press: New York, 1996; pp 25-67.
38. Timpl, R.; Tisi, D.; Talts, J. F.; Andac, Z.; Sasaki, T.; Hohenester, E. Structure and function of laminin LG modules. Matrix Biol. 2000, 19, 309-317.
39. Srinivasan, N.; White, H. E.; Emsley, J.; Wood, S. P.; Pepys, M. B.; Blundell, T. L. Comparative analyses of pentraxins: implications for protomer assembly and ligand binding. Structure 1994, 2, 1017-1027.
40. Hamburger, Z. A.; Brown, M. S.; Isberg, R. R.; Bjorkman, P. J. Crystal structure of invasin: a bacterial integrin-binding protein. Science 1999, 286, 291-295.
41. Paz Moreno-Murciano, M.; Monleon, D.; Marcinkiewicz, C.; Calvete, J. J.; Celda, B. NMR solution structure of the non-RGD disintegrin obtustatin. J. Mol. Biol. 2003, 329, 135-145.
42. Casasnovas, J. M.; Pieroni, C.; Springer, T. A. Lymphocyte function-associated antigen-1 binding residues in intercellular adhesion molecule-2 (ICAM-2) and the integrin binding surface in the ICAM subfamily. Proc. Natl. Acad. Sci. U. S. A. 1999, 96, 3017-3022.
43. Wang, J.; Springer, T. A. Structural specializations of immunoglobulin superfamily members for adhesion to integrins and viruses. Immunol. Rev. 1998, 163, 197-215.
44. Li, Z.; Calzada, M. J.; Sipes, J. M.; Cashel, J. A.; Krutzsch, H. C.; Annis, D.; Mosher, D. F.; Roberts, D. D. Interactions of thrombospondins with α4β1 integrin and CD47 differentially modulate T cell behavior. J Cell Biol. 2002, 157, 509-519.
45. Aplin, A. E.; Short, S. M.; Juliano, R. L. Anchorage-dependent regulation of the mitogen-activated protein kinase cascade by growth factors is supported by a variety of integrin alpha chains. J. Biol. Chem. 1999, 274, 31223-31228.
46. Morini, M.; Mottolese, M.; Ferrari, N.; Ghiorzo, F.; Buglioni, S.; Mortarini, R.; Noonan, D. M.; Natali, P. G.; Albini, A. The alpha 3 beta 1 integrin is associated with mammary carcinoma cell metastasis, invasion, and gelatinase B (MMP-9) activity. Int. J. Cancer 2000, 87, 336-342.
47. van der Pluijm, G.; Vloedgraven, H.; Papapoulos, S.; Lowick, C.; Grzesik, W.; Kerr, J.; Robey, P. G. Attachment characteristics and involvement of integrins in adhesion of breast cancer cell lines to extracellular bone matrix components. Lab Invest. 1997, 77, 665-675.
48. Aina, O.; Marik, J.; Candour-Edwards, R.; Lam, K. Near-infrared optical imaging of ovarian cancer xenografts with novel alpha 3-integrin binding peptide "OA02". Mol. Imaging 2005, 4, 439-447.
49. O'Shea, J. C.; Tcheng, J. E. Eptifibatide: a potent inhibitor of the platelet receptor integrin glycoprotein IIb/IIIa. Expert Opin. Pharmacother. 2002, 3, 1199-1210.
50. Miller, W. H.; Keenan, R. M.; Willette, R. N.; Lark, M. W. Identification and in vivo efficacy of small-molecule antagonists of integrin alphavbeta3 (the vitronectin receptor). Drug Discovery Today 2000, 5, 397-408.
51. Jackson, D. Y. α4 integrin antagonists. Curr. Pharm. Des. 2002, 8, 1229-1253.
52. Fischer, P. M. The design, synthesis and application of stereochemical and directional peptide isomers: A critical review. Current Protein Pept. Sci. 2003, 4, 339-356.
53. Le, G. T.; Abbenante, G.; Becker, B.; Grathwohl, M.; Halliday, J.; Tometzki, G.; Zuegg, J.; Meutermans, W. Molecular diversity through sugar scaffolds. Drug Discovery Today 2003, 8, 701-709.
54. Boer, J.; Gottschling, D.; Schuster, A.; Holzmann, B.; Kessler, H. Design, synthesis, and biological evaluation of alpha(4)beta(1) integrin antagonists based on beta-d-mannose as rigid scaffold. Angew. Chem.-Int. Ed. 2001, 40, 3870-3873.
55. Locardi, E.; Boer, J.; Modlinger, A.; Schuster, A.; Holzmann, B.; Kessler, H. Synthesis and structure - Activity relationship of mannose-based peptidomimetics selectively blocking integrin alpha 4 beta 7 binding to mucosal addressin cell adhesion molecule-1. J. Med. Chem. 2003, 46, 5752-5762.