Stabilization of the activated αMβ2 integrin by a small molecule inhibits leukocyte migration and recruitment

Biochemistry

Volumn 45, Issue 9, 2006, Pages 2862-2871

  Björklund, Mikael ^a   Aitio, Olli ^a   Stefanidakis, Michael ^a   Suojanen, Juho ^b,c   Salo, Tuula ^c   Sorsa, Timo ^b   Koivunen, Erkki ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^c UNIVERSITY OF OULU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELLS; COMPUTATIONAL METHODS; DISEASES; FIBER OPTICS; ORGANIC COMPOUNDS;

ANTIINFLAMMATORY AGENTS; EMIGRATION; INTEGRIN-MEDIATED ADHESION; LEUKOCYTE MIGRATION; LEUKOCYTE RECRUITMENT; LIGAND-BINDING I; PEPTIDE BINDING;

FLAMMABILITY;

ALPHAMBETA2 INTEGRIN; BETA2 INTEGRIN; FIBRINOGEN; GELATINASE B; IMB 10; LATENT MATRIX METALLOPROTEINASE 9; LIGAND; THIAZOLIDINE DERIVATIVE; THIOXOTHIAZOLIDINE DERIVATIVE; UNCLASSIFIED DRUG; ANTIINFLAMMATORY AGENT; CD11B ANTIGEN; HYBRID PROTEIN; PEPTIDE LIBRARY; THIAZOLE DERIVATIVE;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL ADHESION; CONTROLLED STUDY; FEMALE; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; LEUKOCYTE MIGRATION; LIGAND BINDING; MIGRATION INHIBITION; MOUSE; NEUTROPHIL; NONHUMAN; PHAGE DISPLAY; PRIORITY JOURNAL; PROTEIN STABILITY; AMINO ACID SEQUENCE; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CELL MOTION; CHEMICAL STRUCTURE; DRUG EFFECT; LEUKOCYTE; METABOLISM; MOLECULAR GENETICS; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; ANTI-INFLAMMATORY AGENTS; CELL MOVEMENT; FEMALE; LEUKOCYTES; LIGANDS; MACROPHAGE-1 ANTIGEN; MICE; MICE, INBRED BALB C; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE LIBRARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; THIAZOLES; TUMOR CELLS, CULTURED;

EID: 33644682826     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi052238b     Document Type: Article

References (47)

1. Hynes, R. O. (2002) Integrins: bidirectional, allosteric signaling machines, Cell 110, 673-687.
2. Xiong, J. P., Stehle, T., Diefenbach, B., Zhang, R., Dunker, R., Scott, D. L., Joachimiak, A., Goodman, S. L., and Arnaout, M. A. (2001) Crystal structure of the extracellular segment of integrin alpha Vbeta3, Science 294, 339-345.
3. Xiong, J. P., Stehle, T., Zhang, R., Joachimiak, A., Frech, M., Goodman, S. L., and Arnaout, M. A. (2002) Crystal structure of the extracellular segment of integrin alpha Vbeta3 in complex with an Arg-Gly-Asp ligand, Science 296, 151-155.
4. Salas, A., Shimaoka, M., Kogan, A. N., Harwood, C., von Andrian, U. H., and Springer, T. A. (2004) Rolling adhesion through an extended conformation of integrin alphaLbeta2 and relation to alpha I and beta I-like domain interaction, Immunity 20, 393-406.
5. Ruoslahti, E. (1996) RGD and other recognition sequences for integrins, Annu. Rev. Cell Dev. Biol. 12, 697-715.
6. Shimaoka, M., Salas, A., Yang, W., Weitz-Schmidt, G., and Springer, T. A. (2003) Small molecule integrin antagonists that bind to the beta2 subunit I-like domain and activate signals in one direction and block them in the other, Immunity 19, 391-402.
7. Luo, B. H., Takagi, J., and Springer, T. A. (2004) Locking the beta3 integrin I-like domain into high and low affinity conformations with disulfides, J. Biol. Chem. 279, 10215-10221.
8. Beglova, N., Blacklow, S. C., Takagi, J., and Springer, T. A. (2002) Cysteine-rich module structure reveals a fulcrum for integrin rearrangement upon activation, Nat. Struct. Biol. 9, 282-287.
9. Last-Barney, K., Davidson, W., Cardozo, M., Frye, L. L., Grygon, C. A., Hopkins, J. L., Jeanfavre, D. D., Pav, S., Qian, C., Stevenson, J. M., Tong, L., Zindell, R., and Kelly, T. A. (2001) Binding site elucidation of hydantoin-based antagonists of LFA-1 using multidisciplinary technologies: evidence for the allosteric inhibition of a protein-protein interaction, J. Am. Chem. Soc. 123, 5643-5650.
10. Liu, G., Huth, J. R., Olejniczak, E. T., Mendoza, R., DeVries, P., Leitza, S., Reilly, E. B., Okasinski, G. F., Fesik, S. W., and von Geldern, T. W. (2001) Novel p-arylthio cinnamides as antagonists of leukocyte function-associated antigen-1/intracellular adhesion molecule-1 interaction. 2. Mechanism of inhibition and structure-based improvement of pharmaceutical properties, J. Med. Chem. 44, 1202-1210.
11. Weitz-Schmidt, G., Welzenbach, K., Brinkmann, V., Kamata, T., Kallen, J., Bruns, C., Cottens, S., Takada, Y., and Hommel, U. (2001) Statins selectively inhibit leukocyte function antigen-1 by binding to a novel regulatory integrin site, Nat. Med. 7, 687-692.
12. Goodman, S. L., Holzemann, G., Sulyok, G. A., and Kessler, H. (2002) Nanomolar small molecule inhibitors for alphav(beta)6, alphav(beta)5, and alphav(beta)3 integrins, J. Med. Chem. 45, 1045-1051.
13. Bansal, V. S., Vaidya, S., Somers, E. P., Kanuga, M., Shevell, D., Weikel, R., and Detmers, P. A. (2003) Small molecule antagonists of complement receptor type 3 block adhesion and adhesion-dependent oxidative burst in human polymorphonuclear leukocytes, J. Pharmacol. Exp. Ther. 304, 1016-1024.
14. Stefanidakis, M., Ruohtula, T., Borregaard, N., Gahmberg, C. G., and Koivunen, E. (2004) Intracellular and cell surface localization of a complex between alphaMbeta2 integrin and promatrix metalloproteinase-9 progelatinase in neutrophils, J. Immunol. 172, 7060-7068.
15. Stefanidakis, M., Bjorklund, M., Ihanus, E., Gahmberg, C. G., and Koivunen, E. (2003) Identification of a negatively charged peptide motif within the catalytic domain of progelatinases that mediates binding to leukocyte beta 2 integrins, J. Biol. Chem. 278, 34674-34684.
16. Björklund, M., and Koivunen, E. (2005) Gelatinase-mediated migration and invasion of cancer cells, Biochim. Biophys. Acta 1755, 37-69.
17. Koivunen, E., Arap, W., Valtanen, H., Rainisalo, A., Medina, O. P., Heikkila, P., Kantor, C., Gahmberg, C. G., Salo, T., Konttinen, Y. T., Sorsa, T., Ruoslahti, E., and Pasqualini, R. (1999) Tumor targeting with a selective gelatinase inhibitor, Nat. Biotechnol. 17, 768-774.
18. Koivunen, E., Ranta, T. M., Annila, A., Taube, S., Uppala, A., Jokinen, M., van Willigen, G., Ihanus, E., and Gahmberg, C. G. (2001) Inhibition of beta(2) integrin-mediated leukocyte cell adhesion by leucine-leucine-glycine motif-containing peptides, J. Cell Biol. 153, 905-916.
19. Pasqualini, R., Koivunen, E., Kain, R., Lahdenranta, J., Sakamoto, M., Stryhn, A., Ashmun, R. A., Shapiro, L. H., Arap, W., and Ruoslahti, E. (2000) Aminopeptidase N is a receptor for tumor-homing peptides and a target for inhibiting angiogenesis, Cancer Res. 60, 722-727.
20. Kay, B., Kurakin, A., and Hyde-DeRuyscher, R. (1998) From peptides to drugs via phage display, Drug Discov. Today 3, 370-378.
21. Hyde-DeRuyscher, R., Paige, L. A., Christensen, D. J., Hyde-DeRuyscher, N., Lim, A., Fredericks, Z. L., Kranz, J., Gallant, P., Zhang, J., Rocklage, S. M., Fowlkes, D. M., Wendler, P. A., and Hamilton, P. T. (2000) Detection of small-molecule enzyme inhibitors with peptides isolated from phage-displayed combinatorial peptide libraries, Chem. Biol. 7, 17-25.
22. Michishita, M., Videm, V., and Arnaout, M. A. (1993) A novel divalent cation-binding site in the A domain of the beta 2 integrin CR3 (CD11b/CD18) is essential for ligand binding, Cell 72, 857-867.
23. Bjorklund, M., Heikkila, P., and Koivunen, E. (2004) Peptide inhibition of catalytic and noncatalytic activities of matrix metalloproteinase-9 blocks tumor cell migration and invasion, J. Biol. Chem. 279, 29589-29597.
24. Rowsell, S., Hawtin, P., Minshull, C. A., Jepson, H., Brockbank, S. M., Barratt, D. G., Slater, A. M., McPheat, W. L., Waterson, D., Henney, A. M., and Pauptit, R. A. (2002) Crystal structure of human MMP9 in complex with a reverse hydroxamate inhibitor, J. Mol. Biol. 319, 173-181.
25. Li, R., Xie, J., Kantor, C., Koistinen, V., Altieri, D. C., Nortamo, P., and Gahmberg, C. G. (1995) A peptide derived from the intercellular adhesion molecule-2 regulates the avidity of the leukocyte integrins CD11b/CD18 and CD11c/CD18, J. Cell Biol. 129, 1143-1153.
26. Xiong, J. P., Li, R., Essafi, M., Stehle, T., and Arnaout, M. A. (2000) An isoleucine-based allosteric switch controls affinity and shape shifting in integrin CD11b A-domain, J. Biol. Chem. 275, 38762-38767.
27. Lee, J. O., Bankston, L. A., Arnaout, M. A., and Liddington, R. C. (1995) Two conformations of the integrin A-domain (I-domain): a pathway for activation?, Structure 3, 1333-1340.
28. Morris, G. M., Goodsell, D. S., Halliday, R. S., Huey, R., Hart, W. E., Belew, R. K., and Olson, A. J. (1998) Automated docking using a lamarckian genetic algorithm and an empirical binding free energy function, J. Comput. Chem. 19, 1639-1662.
29. Shimaoka, M., Xiao, T., Liu, J. H., Yang, Y., Dong, Y., Jun, C. D., McCormack, A., Zhang, R., Joachimiak, A., Takagi, J., Wang, J. H., and Springer, T. A. (2003) Structures of the alpha LI domain and its complex with ICAM-1 reveal a shape-shifting pathway for integrin regulation, Cell 112, 99-111.
30. McCleverty, C. J., and Liddington, R. C. (2003) Engineered allosteric mutants of the integrin alphaMbeta2 I domain: structural and functional studies, Biochem. J. 372, 121-127.
31. Huth, J. R., Olejniczak, E. T., Mendoza, R., Liang, H., Harris, E. A., Lupher, M. L., Jr., Wilson, A. E., Fesik, S. W., and Staunton, D. E. (2000) NMR and mutagenesis evidence for an I domain allosteric site that regulates lymphocyte function-associated antigen 1 ligand binding, Proc. Natl. Acad. Sci. U.S.A. 97, 5231-5236.
32. Kallen, J., Welzenbach, K., Ramage, P., Geyl, D., Kriwacki, R., Legge, G., Cottens, S., Weitz-Schmidt, G., and Hommel, U. (1999) Structural basis for LFA-1 inhibition upon lovastatin binding to the CD11a I-domain, J. Mol. Biol. 292, 1-9.
33. Zhang, L., and Plow, E. F. (1999) Amino acid sequences within the alpha subunit of integrin alpha M beta 2 (Mac-1) critical for specific recognition of C3bi, Biochemistry 38, 8064-8071.
34. Lee, J. O., Rieu, P., Arnaout, M. A., and Liddington, R. (1995) Crystal structure of the A domain from the alpha subunit of integrin CR3 (CD11b/CD18), Cell 80, 631-638.
35. Shimaoka, M., Shifman, J. M., Jing, H., Takagi, J., Mayo, S. L., and Springer, T. A. (2000) Computational design of an integrin I domain stabilized in the open high affinity conformation, Nat. Struct. Biol. 7, 674-678.
36. Yakubenko, V. P., Lishko, V. K., Lam, S. C., and Ugarova, T. P. (2002) A molecular basis for integrin alpha Mbeta 2 ligand binding promiscuity, J. Biol. Chem. 107, 1.
37. Simon, D. I., Wei, Y., Zhang, L., Rao, N. K., Xu, H., Chen, Z., Liu, Q., Rosenberg, S., and Chapman, H. A. (2000) Identification of a urokinase receptor-integrin interaction site. Promiscuous regulator of integrin function, J. Biol. Chem. 275, 10228-10234.
38. Kelly, T. A., Jeanfavre, D. D., McNeil, D. W., Woska, J. R., Jr., Reilly, P. L., Mainolfi, E. A., Kishimoto, K. M., Nabozny, G. H., Zinter, R., Bormann, B. J., and Rothlein, R. (1999) Cutting edge: a small molecule antagonist of LFA-1-mediated cell adhesion, J. Immunol. 163, 5173-5177.
39. Lu, H., Smith, C. W., Perrard, J., Bullard, D., Tang, L., Shappell, S. B., Entman, M. L., Beaudet, A. L., and Ballantyne, C. M. (1997) LFA-1 is sufficient in mediating neutrophil emigration in Mac-1-deficient mice, J. Clin. Invest. 99, 1340-1350.
40. Ding, Z. M., Babensee, J. E., Simon, S. I., Lu, H., Perrard, J. L., Bullard, D. C., Dai, X. Y., Bromley, S. K., Dustin, M. L., Entman, M. L., Smith, C. W., and Ballantyne, C. M. (1999) Relative contribution of LFA-1 and Mac-1 to neutrophil adhesion and migration, J. Immunol. 163, 5029-5038.
41. Henderson, R. B., Lim, L. H., Tessier, P. A., Gavins, F. N., Mathies, M., Perretti, M., and Hogg, N. (2001) The use of lymphocyte function-associated antigen (LFA)-1-deficient mice to determine the role of LFA-1, Mac-1, and alpha4 integrin in the inflammatory response of neutrophils, J. Exp. Med. 194, 219-226.
42. Berlin-Rufenach, C., Otto, F., Mathies, M., Westermann, J., Owen, M. J., Hamann, A., and Hogg, N. (1999) Lymphocyte migration in lymphocyte function-associated antigen (LFA)-1-deficient mice, J. Exp. Med. 189, 1467-1478.
43. Yang, J. T., and Hynes, R. O. (1996) Fibronectin receptor functions in embryonic cells deficient in alpha 5 beta 1 integrin can be replaced by alpha V integrins, Mol. Biol. Cell 7, 1737-1748.
44. Palecek, S. P., Loftus, J. C., Ginsberg, M. H., Lauffenburger, D. A., and Horwitz, A. F. (1997) Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness, Nature 385, 537-540.
45. Geuijen, C. A., and Sonnenberg, A. (2002) Dynamics of the alpha6beta4 integrin in keratinocytes, Mol. Biol. Cell 13, 3845-3858.
46. Regen, C. M., and Horwitz, A. F. (1992) Dynamics of beta 1 integrin-mediated adhesive contacts in motile fibroblasts, J. Cell Biol. 119, 1347-1359.
47. Palecek, S. P., Huttenlocher, A., Horwitz, A. F., and Lauffenburger, D. A. (1998) Physical and biochemical regulation of integrin release during rear detachment of migrating cells, J. Cell Sci. 111, 929-940.