NMR mapping of the IFNAR1-EC binding site on IFNα2 reveals allosteric changes in the IFNAR2-EC binding site

Biochemistry

Volumn 49, Issue 4, 2010, Pages 687-695

  Akabayov, Sabine Ruth ^a,c   Biron, Zohar ^a   Lamken, Peter ^b   Piehler, Jacob ^b,d   Anglister, Jacob ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b GOETHE UNIVERSITY   (Germany)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOSTERIC COMMUNICATION; BINARY COMPLEXES; CELL SURFACE RECEPTORS; CROSS PEAKS; EXTRACELLULAR DOMAINS; INTRACELLULAR SIGNALS; NMR STUDIES; SITE DIRECTED MUTAGENESIS; TYPE I INTERFERONS;

BINDING ENERGY; BIOCHEMISTRY; COMPLEXATION; ELECTRIC CONDUCTIVITY MEASUREMENT; ENZYME ACTIVITY; NUCLEAR MAGNETIC RESONANCE; SIGNAL TRANSDUCTION;

BINDING SITES;

ALPHA2 INTERFERON; INTERFERON RECEPTOR;

ALLOSTERISM; ARTICLE; BINDING SITE; CONTROLLED STUDY; HETERONUCLEAR SINGLE QUANTUM COHERENCE; NUCLEAR MAGNETIC RESONANCE; PH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS; SPECTROMETER;

AMINO ACID SEQUENCE; BINDING SITES; INTERFERON-ALPHA; KINETICS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN STRUCTURE, TERTIARY; RECEPTOR, INTERFERON ALPHA-BETA;

EID: 75149162520     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901313x     Document Type: Article

References (43)

1. Pestka, S., Krause, C. D., and Walter, M. R. (2004) Interferons, interferon-like cytokines, and their receptors. Immunol. Rev. 202, 8-32.
2. Novick, D., Cohen, B., and Rubinstein, M. (1994) The human interferon α/β receptor: Characterization and molecular cloning. Cell 77, 391-400.
3. Uze,G., Lutfalla, G., and Mogensen, K. E. (1995) α and β interferons and their receptor and their friends and relations. J. Interferon Cytokine Res. 15, 3-26.
4. Piehler, J., and Schreiber, G. (1999) Mutational and structural analysis of the binding interface between type I interferons and their receptor Ifnar2. J. Mol. Biol. 294, 223-237.
5. Lamken, P., Gavutis, M., Peters, I., Van der Heyden, J., Uze, G., and Piehler, J. (2005) Functional cartography of the ectodomain of the type I interferon receptor subunit ifnar1. J. Mol. Biol. 350, 476-488.
6. Ozbek, S., Grotzinger, J., Krebs, B., Fischer, M., Wollmer, A., Jostock, T., Mullberg, J., and Rose-John, S. (1998) The membrane proximal cytokine receptor domain of the human interleukin-6 receptor is sufficient for ligand binding but not for gp130 association. J. Biol. Chem. 273, 21374-21379.
7. Cunningham, B. C., Ultsch, M., De Vos, A. M., Mulkerrin, M. G., Clauser, K. R., and Wells, J. A. (1991) Dimerization of the extracellular domain of the human growth hormone receptor by a single hormone molecule. Science 254, 821-825.
8. Gent, J., Van Kerkhof, P., and Strous, G. J. (2003) Dimerization and signal transduction of the growth hormone receptor. Mol. Endocrinol. 17, 967-975.
9. Krause, C. D., and Pestka, S. (2005) Evolution of the Class 2 cytokines and receptors, and discovery of new friends and relatives. Pharmacol. Ther. 106, 299-346.
10. Bernat, B., Pal, G., Sun, M., and Kossiakoff, A. A. (2003) Determination of the energetics governing the regulatory step in growth hormone-induced receptor homodimerization. Proc. Natl. Acad. Sci. U.S.A. 100, 952-957.
11. Remy, I., Wilson, I. A., and Michnick, S. W. (1999) Erythropoietin receptor activation by a ligand-induced conformation change. Science 283, 990-993.
12. Gavutis, M., Lata, S., Lamken, P., Muller, P., and Piehler, J. (2005) Lateral ligand-receptor interactions on membranes probed by simultaneous fluorescence-interference detection. Biophys. J. 88, 4289-4302.
13. Gavutis, M., Jaks, E., Lamken, P., and Piehler, J. (2006) Determination of the two-dimensional interaction rate constants of a cytokine receptor complex. Biophys. J. 90, 3345-3355.
14. Karpusas, M., Nolte, M., Benton, C. B., Meier, W., Lipscomb, W. N., and Goelz, S. (1997) The crystal structure of human interferon β at 2.2-Å resolution. Proc. Natl. Acad. Sci. U.S.A. 94, 11813-11818.
15. Senda, T., Shimazu, T., Matsuda, S., Kawano, G., Shimizu, H., Nakamura, K. T., and Mitsui, Y. (1992) Three-dimensional crystal structure of recombinant murine interferon-β. EMBO J. 11, 3193-3201.
16. Klaus, W., Gsell, B., Labhardt, A. M., Wipf, B., and Senn, H. (1997) The three-dimensional high resolution structure of human interferon α-2a determined by heteronuclear NMR spectroscopy in solution. J. Mol. Biol. 274, 661-675.
17. Radhakrishnan, R., Walter, L. J., Hruza, A., Reichert, P., Trotta, P. P., Nagabhushan, T. L., and Walter, M. R. (1996) Zinc mediated dimer of human interferon-α 2b revealed by X-ray crystallography. Structure 4, 1453-1463.
18. Radhakrishnan, R.,Walter, L. J., Subramaniam, P. S., Johnson, H. M., and Walter, M. R. (1999) Crystal structure of ovine interferon-τ at 2.1 Å resolution. J. Mol. Biol. 286, 151-162.
19. Chill, J. H., Quadt, S. R., Levy, R., Schreiber, G. E., and Anglister, J. (2003) NMR structure of the human type I interferon receptor reveals the molecular basis for ligand binding. Structure 11, 791-802.
20. Chill, J. H., Quadt, S. R., and Anglister, J. (2004) NMR backbone dynamics of the human type I interferon binding subunit, a representative cytokine receptor. Biochemistry 43, 10127-10137.
21. Chuntharapai, A., Gibbs, V., Lu, J., Ow, A., Marsters, S., Ashkenazi, A., De Vos, A., and Jin Kim, K. (1999) Determination of residues involved in ligand binding and signal transmission in the human IFNα receptor 2. J. Immunol. 163, 766-773.
22. Roisman, L. C., Piehler, J., Trosset, J.-Y., Scheraga, H. A., and Schreiber, G. E. (2001) Structure of the interferon-reeptor complex determined by distance constraints from double mutant cycles and flexible docking. Proc. Natl. Acad. Sci. U.S.A. 98, 13231-13236.
23. Piehler, J., Roisman, L. C., and Schreiber, G. (2000) New structural and functional aspects of the IFN-receptor interaction revealed by comprehensive mutational analysis of the binding interface. J. Biol. Chem. 275, 40425-40433.
24. Quadt-Akabayov, S. R., Chill, J. H., Levy, R., Kessler, N., and Anglister, J. (2006) Determination of the human type I interferon receptor binding site on human interferon-α2 by cross saturation and an NMR-based model of the complex. Protein Sci. 15, 2656-2668.
25. Roisman, L. C., Jaitin, D. A., Baker, D. P., and Schreiber, G. (2005) Mutational analysis of the IFNAR1 binding site on IFNα2 reveals the architecture of a weak ligand-receptor binding-site. J. Mol. Biol. 353, 271-281.
26. Stroud, R. M., and Wells, J. A. (2004) Mechanistic diversity of cytokine receptor signaling across cell membranes. Sci. STKE 2004, re7.
27. Hu, R., Bekisz, J., Schmeisser, H., McPhie, P., and Zoon, K. (2001) Human IFN-α protein engineering: The amino acid residues at positions 86 and 90 are important for antiproliferative activity. J. Immunol. 167, 1482-1489.
28. Runkel, L., deDios, C., Karpusas, M., Betzenhauser, M., Muldowney, C., Zafari,M., Benjamin,C.D.,Miller, S.,Hochman,P. S., andWhitty, A. (2000) Systematic mutational mapping of sites on human interferon-β-1a that are important for receptor binding and functional activity. Biochemistry 39, 2538-2551.
29. Pan, M., Kalie, E., Scaglione, B. J., Raveche, E. S., Schreiber, G., and Langer, J. A. (2008) Mutation of the IFNAR-1 receptor binding site of human IFN-α2 generates type I IFN competitive antagonists. Biochemistry 47, 12018-12027.
30. Jaitin, D. A., Roisman, L. C., Jaks, E., Gavutis, M., Piehler, J., Van der Heyden, J., Uze, G., and Schreiber, G. (2006) Inquiring into the differential action of interferons (IFNs): An IFN-α2 mutant with enhanced affinity to IFNAR1 is functionally similar to IFN-β. Mol. Cell. Biol. 26, 1888-1897.
31. Kalie, E., Jaitin, D. A., Abramovich, R., and Schreiber, G. (2007) An interferon α2 mutant optimized by phage display for IFNAR1 binding confers specifically enhanced antitumor activities. J. Biol. Chem. 282, 11602-11611.
32. Cutrone, E. C., and Langer, J. A. (2001) Identification of critical residues in bovine IFNAR-1 responsible for interferon binding. J. Biol. Chem. 276, 17140-17148.
33. Cajean-Feroldi, C., Nosal, F., Nardeux, P. C., Gallet, X., Guymarho, J., Baychelier, F., Sempe, P., Tovey, M. G., Escary, J. L., and Eid, P. (2004) Identification of residues of the IFNAR1 chain of the type I human interferon receptor critical for ligand binding and biological activity. Biochemistry 43, 12498-12512.
34. Li, Z., Strunk, J. J., Lamken, P., Piehler, J., and Walz, T. (2008) The EM structure of a type I interferon-receptor complex reveals a novel mechanism for cytokine signaling. J. Mol. Biol. 377, 715-724.
35. Chill, J. H., Nivasch, R., Levy, R., Albeck, S., Schreiber, G. E., and Anglister, J. (2002) The human interferon receptor: NMR-based modeling of the IFN-a2 binding site, and observed ligand-induced tightening. Biochemistry 41, 3575-3585.
36. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) Nmrpipe: A Multidimensional Spectral Processing System Based On Unix Pipes. J. Biomol. NMR 6, 277-293.
37. Johnson, B. A., and Blevins, R. A. (1994) NMRView: A computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4, 603-614.
38. Larkin,M. A., Blackshields,G., Brown, N. P., Chenna, R.,McGettigan, P. A.,McWilliam,H., Valentin, F., Wallace, I. M.,Wilm, A., Lopez, R., Thompson, J. D.,Gibson, T. J., and Higgins, D. G. (2007)ClustalWand Clustal X version 2.0. Bioinformatics 23, 2947-2948.
39. Shindyalov, I. N., and Bourne, P. E. (1998) Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. Protein Eng. 11, 739-747.
40. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, Palo Alto, CA.
41. Uze, G., Schreiber, G., Piehler, J., and Pellegrini, S. (2007) The receptor of the type I interferon family. Curr. Top. Microbiol. Immunol. 316, 71-95.
42. Slutzki, M., Jaitin, D. A., Yehezkel, T. B., and Schreiber, G. (2006) Variations in the unstructured C-terminal tail of interferons contribute to differential receptor binding and biological activity. J. Mol. Biol. 360, 1019-1030.
43. Goldman, L. A., Cutrone, E. C., Dang, A., Hao, X., Lim, J. K., and Langer, J. A. (1998) Mapping human interferon-α (IFN-α2) binding determinants of the type I interferon receptor subunit IFNAR-1 with human/bovine IFNAR-1 chimeras. Biochemistry 37, 13003-13010.