NMR solution structure of a potent cyclic nonapeptide inhibitor of ICAM-1-mediated leukocyte adhesion produced by homologous amino acid substitution

Journal of Peptide Research

Volumn 64, Issue 4, 2004, Pages 127-140

  Sillerud, L O ^a   Burks, E J ^a   Brown, W M ^a   Brown, D C ^a   Larson, R S ^a,b  

^a UNIVERSITY OF NEW MEXICO HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

Antagonists; Cyclic peptides; ICAM 1; Integrins; LFA 1; NMR

Indexed keywords

CYCLOPEPTIDE; INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MONOCLONAL ANTIBODY; NONAPEPTIDE; PROLINE;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; DISULFIDE BOND; LEUKOCYTE ADHERENCE; LIGAND BINDING; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; PROTON NUCLEAR MAGNETIC RESONANCE; REPERFUSION INJURY; SIMULATION; STRUCTURE ANALYSIS;

AMINO ACID MOTIFS; BINDING SITES; CELL LINE; DISULFIDES; HUMANS; INHIBITORY CONCENTRATION 50; INTERCELLULAR ADHESION MOLECULE-1; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; PEPTIDES; PEPTIDES, CYCLIC; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTONS; STRUCTURE-ACTIVITY RELATIONSHIP; TEMPERATURE;

MURINAE; RUMEX;

EID: 4744369163     PISSN: 1397002X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1399-3011.2004.00176.x     Document Type: Article

References (74)

1. Larson, R.S. & Springer, T.A. (1990) Structure and function of leukocyte integrins. Immunol. Rev. 114, 181-217.
2. Winter, S.S., Sweatman, J.J., Lawrence, M.B., Rhoades, T.H., Hart, A.L. & Larson, R.S. (2001) Enhanced T-lineage acute lymphoblastic leukaemia cell survival on bone marrow stroma requires involvement of LFA-1 and de/title〉. Br. J. Haematol. 115, 862-871.
3. Umansky, V., Schirrmacher, V. & Rocha, M. (1996) New insights into tumor-host interactions in lymphoma metastasis. J. Mol. Med. 74, 353-363.
4. Zahalka, M.A., Okon, E. & Naor, D. (1993) Blocking lymphoma invasiveness with a monoclonal antibody directed against the beta-chain of the leukocyte adhesion molecule (CD18). J. Immunol. 150, 4466-4477.
5. Verrier, E.D. & Shen, I. (1993) Potential role of neutrophil anti-adhesion therapy in myocardial stunning, myocardial infarction, and organ dysfunction after cardiopulmonary bypass. J. Card. Surg. 8, 309-312.
6. Zhao, Z.Q., Lefer, D.J., Sato, H., Hart, K.K., Jefforda, P.R. & Vinten-Johansen, I. (1997) Monoclonal antibody to ICAM-1 preserves postischemic blood flow and reduces infarct size after ischemia-reperfusion in rabbit. J. Leukoc. Biol. 62, 292-300.
7. Tanaka, Y., Kobayashi, K., Takahashi, A., Arai, I., Higuchi, S., Otomo, S., Habu, S. & Nishimura, T. (1993) Inhibition of inflammatory liver injury by a monoclonal antibody against lymphocyte function-associated antigen-1. J. Immunol. 151, 5088-5095.
8. Clark, W.M., Madden, K.P., Rothlein, R. & Zivin, J.A. (1991) Reduction of central nervous system ischemic injury in rabbits using leukocyte adhesion antibody treatment. Stroke 22, 877-883.
9. Kawai, K., Kobayashi, Y., Shiratori, M., Sobue, G., Tamatani, T., Miyasaka, M. & Yoshikai, Y. (1996) Intrathecal administration of antibodies against LFA-1 and against ICAM-1 suppresses experimental allergic encephalomyelitis in rats. Cell. Immunol. 171, 262-268.
10. Kimura, T., Suzuki, K., Inada, S., Hayashi, A., Isobe, M., Matsuzaki, Y., Tanaka, N., Osuga, T. & Fujiwara, M. (1996) Monoclonal antibody against lymphocyte function-associated antigen 1 inhibits the formation of primary biliary cirrhosis-like lesions induced by murine graft-versus-host reaction. Hepatology 24, 888-894.
11. Nishikawa, K., Guo, Y.J., Miyasaka, M., Tamatani, T., Collins, A.B., Sy, M.S., McCluskey, R.T. & Andres, G. (1993) Abstract antibodies to intercellular adhesion molecule 1/lymphocyte function-associated antigen 1 prevent crescent formation in rat autoimmune glomerulonephritis. J. Exp. Med. 177, 667-677.
12. Cosimi, A.B., Conti, D., Delmonico, F.L., Preffer, F.I., Wee, S.L., Rothlein, R., Faanes, R. & Colvin, R.B. (1990) In vivo effects of monoclonal antibody to ICAM-1 (CD54) in nonhuman primates with renal allografts. J. Immunol. 144, 4604-4612.
13. Katz, S.M., Browne, B., Phan, T., Wang, M.E., Bennett, C.F., Stepkowski, S.M. & Kahan, B.D. (1995) Efficacy of ICAM-1 antisense oligonucleotide in pancreatic islet transplantation. Transplant. Proc. 27, 3214.
14. Isobe, M., Yagita, H., Okumura, K. & Ihara, A. (1992) Specific acceptance of cardiac allograft after treatment with antibodies to ICAM-1 and LFA-1. Science 255, 1125-1127.
15. Kato, Y., Yamataka, A., Yagita, H., Okumura, K., Fujiwara, T. & Miyano, T. (1996) Specific acceptance of fetal bowel allograft in mice after combined treatment with anti-intercellular adhesion molecule-1 and leukocyte function-associated antigen-1 antibodies. Ann. Surg. 223, 94-100.
16. Takei, Y., Nishimura, Y., Kawano, S., Nagai, H., Ohmae, A., Fusamoto, H. & Kamada, T. (1996) Expression of ICAM-1 is involved in the mechanism of liver injury during liver transplantation: therapeutic usefulness of the F(ab′)2 fragment of an anti-ICAM-1 monoclonal antibody. Transplant. Proc. 28, 1103-1105.
17. Wegner, C.D., Gundel, R.H., Reilly, P., Haynes, N., Letts, L.G. & Rothlein, R. (1990) Intercellular adhesion molecule-1 (ICAM-1) in the pathogenesis of asthma. Science 247, 456-459.
18. Watanabe, S., Mukaida, N., Ikeda, N., Akiyama, M., Harada, A., Nakanishi, I., Nariuchi, H., Watanabe, Y. & Matsushima, K. (1995) Prevention of endotoxin shock by an antibody against leukocyte integrin beta 2 through inhibiting production and action of TNF. Int. Immunol. 7, 1037-1046.
19. Miyamoto, K., Khosrof, S., Bursell, S.E., Rohan, R., Murata, T., Clermont, A.C., Aiello, L.P., Ogura, Y. & Adamis, A.P. (1999) Prevention of leukostasis and vascular leakage in streptozotocin-induced diabetic retinopathy via intercellular adhesion molecule-1 inhibition. Proc. Natl Acad. Sci. U S A 96, 10836-10841.
20. Kavanaugh, A.F., Davis, L.S., Jain, R.I., Nichols, L.A., Norris, S.H. & Lipsky, P.E. (1996) A phase I/II open label study of the safety and efficacy of an anti-ICAM-1 (intercellular adhesion molecule-1; CD54) monoclonal antibody in early rheumatoid arthritis. J. Rheumatol. 23, 1338-1344.
21. Davis, L.S., Kavanaugh, A.F., Nichols, L.A. & Lipsky, P.E. (1995) Induction of persistent T cell hyporesponsiveness in vivo by monoclonal antibody to ICAM-1 in patients with rheumatoid arthritis. J. Immunol. 154, 3525-3537.
22. Haug, C.E., Colvin, R.B., Delmonico, F.L., Auchincloss, H. Jr, Tolkoff-Rubin, N., Preffer, F.I., Rothlein, R., Norris, S., Scharschmidt, L. & Cosimi, A.B. (1993) A phase I trial of immunosuppression with anti-ICAM-1 (CD54) mAb in renal allograft recipients. Transplantation 55, 766-772.
23. Kavanaugh, A.F., Davis, L.S., Nichols, L.A., Norris, S.H., Rothlein, R., Scharschmidt, L.A. & Lipsky, P.E. (1994) Treatment of refractory rheumatoid arthritis with a monoclonal antibody to intercellular adhesion molecule 1. Arthritis Rheum. 37, 992-999.
24. Kavanaugh, A.F., Schulze-Koops, H., Davis, L.S. & Lipsky, P.E. (1997) Repeat treatment of rheumatoid arthritis patients with a murine anti-intercellular adhesion molecule 1 monoclonal antibody. Arthritis Rheum. 40, 849-853.
25. Shannon, J.P., Silva, M.V., Brown, D.C. & Larson, R.S. (2001) Novel cyclic peptide inhibits intercellular adhesion molecule-1-mediated cell aggregation. J. Pept. Res. 58, 140-150.
26. Qu, A.D. & Leahy, D.J. (1995) Crystal structure of the I-domain from the CD11a/ CD18 (LFA-1, alpha L beta 2) integrin. Proc. Natl Acad. Sci. U S A 92, 10277-10281.
27. Kallen, J., Welzenbach, K., Ramage, P., Geyl, D., Kriwacki, R., Legge, G., Cottens, S., WeitzSchmidt, G. & Hommel, U. (1999) Structural basis for LFA-1 inhibition upon lovastatin binding to the CD11a I-domain. J. Mol. Biol. 292, 1-9.
28. Nakanishi, H., Ramurthy, S., Raktabutr, A., Shen, R. & Kahn, M. (1993) Peptidomimetics of the immunoglobulin supergene family - a review. Gene 137, 51-56.
29. Murali, R. & Greene, M.I. (1998) Structure-based design of immunologically active therapeutic peptides. Immunol. Res. 17, 163-169.
30. Koivunen, E., Ranta, T.M., Annila, A., Taube, S., Uppala, A., Jokinen, M., van Willigen, G., Ihanus, E. & 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.
31. Krause, K., Pineda, L.F., Peteranderl, R. & Reissmann, S. (2000) Conformational properties of a cyclic peptide bradykinin B2 receptor antagonist using experimental and theoretical methods. J. Pept. Res. 55, 63-71.
32. Viles, J.H., Mitchell, J.B., Gough, S.L., Doyle, P.M., Harris, C.J., Sadler, P.J. & Thornton, J.M. (1996) Multiple solution conformations of the integrin-binding cyclic pentapeptide cyclo(-Ser-D-Leu-Asp-Val-Pro-). Analysis of the (phi, psi) space available to cyclic pentapeptides. Eur. J. Biochem. 242, 352-362.
33. Lowman, H.B., Chen, Y.M., Skelton, N.J., Mortensen, D.L., Tomlinson, E.E., Sadick, M.D., Robinson, I.C. & Clark, R.G. (1998) Molecular mimics of insulin-like growth factor 1 (IGF-1) for inhibiting IGF-1: IGF-binding protein interactions. Biochemistry 37, 8870-8878.
34. Scherf, T., Kasher, R., Balass, M., Fridkin, M., Fuchs, S. & Katchalski-Katzir, E. (2001) A beta -hairpin structure in a 13-mer peptide that binds alpha-bungarotoxin with high affinity and neutralizes its toxicity. Proc. Natl Acad. Sci. U S A 98, 6629-6634.
35. Skelton, N.J., Chen, Y.M., Dubree, N., Quan, C., Jackson, D.Y., Cochran, A., Zobel, K., Deshayes, K., Baca, M., Pisabarro, M.T. & Lowman, H.B. (2001) Structure-function analysis of a phage display-derived peptide that binds to insulin-like growth factor binding protein 1. Biochemistry 40, 8487-8498.
36. Sem, D.S., Baker, B.L., Victoria, E.J., Jones, D.S., Marquis, D., Yu, L., Parks, J. & Coutts, S.M. (1998) Structural characterization and optimization of antibody-selected phage library mimotopes of an antigen associated with autoimmune recurrent thrombosis. Biochemistry 37, 16069-16081.
37. Lin, K.C. & Castro, A.C. (1998) Very late antigen 4 (VLA4) antagonists as antiinflammatory agents. Curr. Opin. Chem. Biol. 2, 453-457.
38. Souers, A.J., Virgilio, A.A., Schurer, S.S., Ellman, J.A., Kogan, T.P., West, H.E., Ankener, W. & Vanderslice, P. (1998) Novel inhibitors of alpha 4 beta 1 integrin receptor interactions through library synthesis and screening. Bioorg. Med. Chem. Lett. 8, 2297-2302.
39. Krebs, S. & Rognan, D. (1998) From peptides to peptidomimetics: design of nonpeptide ligands for major histocompatibility proteins. Pharm. Acta Helv. 73, 173-181.
40. Henlin, J.M., Boutin, J.A., Kucharczyk, N., Desmet-Beaufort, C., Loynel, A., Bertrand, M., Genton, A., Tucker, G.C., Atassi, G. & Fauchere, J.L. (2001) From peptide libraries to optimized nonpeptide ligands in the search for S-farnesyltransferase inhibitors. J. Pept. Res. 57, 85-96.
41. Kieber-Emmons, T., Murali, R. & Greene, M.I. (1997) Therapeutic peptides and peptidomimetics. Curr. Opin. Biotechnol. 8, 435-441.
42. Sillerud, L.O., Burks, E.J., Wester, M.J., Brown, D.C., Vijayan, S. & Larson, R.S. NMR-derived model of interconverting conformations of an ICAM-1 inhibitory cyclic-nonapeptide. J. Pept. Res. 62, 97-116.
43. Wiesmann, C., Christinger, H.W., Cochran, A.G., Cunningham, B.C., Fairbrother, W.J., Keenan, C.J., Meng, G. & de Vos, A.M. (1998) Crystal structure of the complex between VEGF and a receptor-blocking peptide. Biochemistry 37, 17765-17772.
44. Kessler, H. (1982) Peptide conformations: 19. Conformation and biological-activity of cyclic peptides. Angew. Chem. Int. Ed. Engl. 21, 512-523.
45. Kurogi, Y. & Guner, O.F. (2001) Pharmacophore modeling and three-dimensional database searching for drug design using catalyst. Curr. Med. Chem. 8, 1035-1055.
46. Merchant, S.H., Gurule, D.M. & Larson, R.S. (2003) Amelioration of ischemia-reperfusion injury with cyclic peptide blockade of de/ title〉. Am. J. Physiol. Heart Circ. 284, H1260-1268.
47. Oj, V.T. & Herzenberg, T. (1980) Immunoglobulin-producing hybrid cell lines. In: Selected Methods in Cellular Immunology. (Mishell, B.B. & Shiigi, S.M., eds), pp 351-372. W.H. Freeman, New York.
48. Larson, R.S., Brown, D.C. & Sklar, L.A. (1997) Retinoic acid induces aggregation of the acute promyelocytic leukemia cell line NB-4 by utilization of LFA-1 and ICAM-2. Blood 90, 2747-2756.
49. Rothlein, R. & Springer, T.A. (1986) The requirement for lymphocyte function-associated antigen 1 in homotypic leukocyte adhesion stimulated by phorbol ester. J. Exp. Med. 163, 1132-1149.
50. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J. & Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293.
51. Farrar, T.C. & Becker, E.D. (1971) Pulse and Fourier transform NMR: Introduction to Theory and Methods. Academic Press, New York.
52. Lee, B. & Richards, F.M. (1971) The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55, 379-400.
53. Shrake, A. & Rupley, J.A. (1973) Environment and exposure to solvent of protein atoms. Lysozyme and insulin. J. Mol. Biol. 79, 351-371.
54. Casasnovas, J.M., Stehle, T., Liu, J.H., Wang, J.H. & Springer, T.A. (1998) A dimeric crystal structure for the N-terminal two domains of intercellular adhesion molecule-1. Proc. Natl Acad. Sci. U S A 95, 4134-4139.
55. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291.
56. McLachlan, A.D. (1982) Rapid comparison of protein structures. Acta Crystallogr. A 38, 871-873.
57. 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. & Springer, T.A. (2003) Structures of the alpha L I domain and its complex with ICAM-1 reveal a shape-shifting pathway for integrin regulation. Cell 112, 99-111.
58. Gabb, H.A., Jackson, R.M. & Sternberg, M.J. (1997) Modelling protein docking using shape complementarity, electrostatics and biochemical information. J. Mol. Biol. 272, 106-120.
59. Jackson, R.M., Gabb, H.A. & Sternberg, M.J. (1998) Rapid refinement of protein interfaces incorporating solvation: application to the docking problem. J. Mol. Biol. 276, 265-285.
60. Morris, G.M., Goodsell, D.S., Halliday, R.S., Huey, R., Hart, W.E., Belew, R.K. & Olson, A.J. (1998) Automated docking using a Lamarckian genetic algorithm and empirical binding free energy function. J. Comput. Chem. 19, 1639-1662.
61. Plaxco, K.W., Morton, C.J., Grimshaw, S.B., Jones, J.A., Pitkeathly, M., Campbell, I.D. & Dobson, C.M. (1997) The effects of guanidine hydrochloride on the 'random coil' conformations and NMR chemical shifts of the peptide series GGXGG. J. Biomol. NMR 10, 221-230.
62. Smith, L.J., Bolin, K.A., Schwalbe, H., MacArthur, M.W., Thornton, J.M. & Dobson, C.M. (1996) Analysis of main chain torsion angles in proteins: prediction of NMR coupling constants for native and random coil conformations. J. Mol. Biol. 255, 494-506.
63. Chou, K.C. (2000) Prediction of tight turns and their types in proteins. Anal. Biochem. 286, 1-16.
64. Moont, G., Gabb, H.A. & Sternberg, M.J. (1999) Use of pair potentials across protein interfaces in screening predicted docked complexes. Proteins 35, 364-373.
65. Pontius, J., Richelle, J. & Wodak, S.J. (1996) Deviations from standard atomic volumes as a quality measure for protein crystal structures. J. Mol. Biol. 264, 121-136.
66. Chen, C., Hsu, C.H., Su, N.Y., Lin, Y.C., Chiou, S.H. & Wu, S.H. (2001) Solution structure of a Kunitz-type chymotrypsin inhibitor isolated from the elapid snake Bungarus faciatus. J. Biol. Chem. 276, 45079-45087.
67. Tamamura, H., Sugioka, M., Odagaki, Y., Omagari, A., Kan, Y., Oishi, S., Nakashima, H., Yamamoto, N., Peiper, S.C., Hamanaka, N., Otaka, A. & Fujii, N. (2001) Conformational study of a highly specific CXCR4 inhibitor, T140, disclosing the close proximity of its intrinsic pharmacophores associated with strong anti-HIV activity. Bioorg. Med. Chem. Lett. 11, 359-362.
68. Brauer, A.B., Kelly, G., McBride, J.D., Cooke, R.M., Matthews, S.J. & Leatherbarrow, R.J. (2001) The Bowman-Birk inhibitor reactive site loop sequence represents an independent structural beta-hairpin motif. J. Mol. Biol. 306, 799-807.
69. 2 bound to farnesyl-protein transferase. J. Pept. Res. 54, 66-73.
70. Casasnovas, J.M., Pieroni, C. & Springer, T.A. (1999) 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 96, 3017-3022.
71. Staunton, D.E., Dustin, M.L., Erickson, H.P. & Springer, T.A. (1990) The arrangement of the immunoglobulin-like domains of ICAM-1 and the binding sites for LFA-1 and rhinovirus. Cell 61, 243-254.
72. Fairbrother, W.J., Christinger, H.W., Cochran, A.G., Fuh, G., Keenan, C.J., Quan, C., Shriver, S.K., Tom, J.Y., Wells, J.A. & Cunningham, B.C. (1998) Novel peptides selected to bind vascular endothelial growth factor target the receptor-binding site. Biochemistry 37, 17754-17764.
73. Katz, B.A. (1997) Structural and mechanistic determinants of affinity and specificity of ligands discovered or engineered by phage display. Annu. Rev. Biophys. Biomol. Struct. 26, 27-45.
74. Schulz, A., Escher, S., Marx, U.C., Meyer, M., Rösch, P., Forssmann, W.-G. & Adermann, K. (1998) Carboxy-terminal extension stabilizes the topological stereoisomers of guanylin. J. Pept. Res. 52, 518-525.