On the importance of being aromatic at an antibody-protein antigen interface: Mutagenesis of the extracellular interferon γ receptor and recognition by the neutralizing antibody A6

Journal of Molecular Biology

Volumn 285, Issue 2, 1999, Pages 805-815

  Hofstädter, Klaus ^a   Stuart, Fiona ^a   Jiang, Luyong ^a   Vrijbloed, Jan W ^a   Robinson, John A ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Cytokine; Epitope; Molecular recognition; pi cation interactions; Surface plasmon resonance biosensor

Indexed keywords

AROMATIC COMPOUND; GAMMA INTERFERON RECEPTOR; HISTIDINE; LYSINE; NEUTRALIZING ANTIBODY; TRYPTOPHAN; TYROSINE;

ANTIGEN ANTIBODY COMPLEX; ARTICLE; BIOSENSOR; ENZYME LINKED IMMUNOSORBENT ASSAY; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN BINDING; SITE DIRECTED MUTAGENESIS; SURFACE PLASMON RESONANCE;

EID: 0033555271     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2343     Document Type: Article

References (47)

1. Boteva R., Zlateva T., Dorovska-Taran V., Visser A. J. W. G., Tsanev R., Salvato B. Dissociation equilibrium of human recombinant interferon γ Biochemistry. 35:1996;14825-14830.
2. Braden B. C., Poljak R. J. Structural features of the reactions between antibodies and protein antigens. FASEB J. 9:1995;9-16.
3. Braden B. C., Poljak R. J. The structural and thermodynamic basis of antibody-protein antigen interactions. Zanetti M., Capra J. D. Antibodies. 1997;1-30 Harwood Academic Publishers.
4. Bridges A., Stuart F., Späth J., Lang S., Henke C., Birch A., Robinson J. A. Production and characterization of anti-human interferon γ receptor antibody fragments that inhibit cytokine binding to the receptor. Protein Eng. 9:1996;365-370.
5. Burley S. K., Petsko G. A. Aromatic-aromatic interaction: a mechanism of protein structure and stabilization. Science. 229:1985;23-28.
6. Burley S. K., Petsko G. A. Amino-aromatic interactions in proteins. FEBS Letters. 203:1986;139-143.
7. Chipot C., Jaffe R., Maigret B., Pearlman D. A., Kollman P. A. Benzene dimer: a good model for π-π interactions in protein? A comparison between the benzene and the toluene dimers in the gas phase and in an aqueous solution. J. Am. Chem. Soc. 118:1996;11217-11224.
8. Clackson T., Wells J. A. A hot spot of binding energy in a hormone-receptor interface. Science. 267:1995;383-386.
9. Covell D. G., Wallqvist A. Analysis of protein-protein interactions and the effects of amino acid mutations on their energetics. The importance of water molecules in the binding epitope. J. Mol. Biol. 269:1997;281-297.
10. Dall'Acqua W., Goldman E. R., Eisenstein E., Mariuzza R. A. A mutational analysis of the binding of two different proteins to the same antibody. Biochemistry. 35:1996;9667-9676.
11. Davies D. R., Cohen G. H. Interactions of protein antigens with antibodies. Proc. Natl Acad. Sci. USA. 93:1996;7-12.
12. Dougherty a. D. Cation-π interactions in chemistry and biology: a new view of benzene, Phe, Tyr, and Trp. Science. 271:1996;163-168.
13. England P., Brégégére F., Bedouelle H. Energetic and kinetic contributions of contact residues of antibody D1.3 in the interaction with lysozyme. Biochemistry. 36:1997;164-172.
14. Evan G. I., Lewis G. K., Ramsay G., Bishop J. M. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5:1985;3610-3616.
15. Fields B. A., Goldbaum F. A., Dall'Acqua W., Malchiodi E. L., Cauerhff A., Schwarz F. P., Ysern X., Poljak R. J., Mariuzza R. A. Hydrogen bonding and solvent structure in an antigen-antibody interface. Crystal structures and thermodynamic characterization of three Fv mutants complexed with lysozyme. Biochemistry. 35:1996;15494-15503.
16. Friguet B., Chaffotte A. F., Djavadi-Ohaniance L., Goldberg M. E. Measurements of the true affinity constant in solution of antigen-antibody complexes by enzyme-linked immunosorbent assay. J. Immunol. Methods. 77:1985;305-319.
17. Friguet B., Djavadi-Ohaniance L., Goldberg M. E. Creighton T. Protein Structure: A Practical Approach. 1989;287-310 IRL Press, Oxford.
18. Garotta G., Ozman L., Fountoulakis M., Dembic Z., Van Loon A. P. G. M., Stüber D. Human interferon-γ receptor. Mapping of epitopes recognized by neutralizing antibodies using native and recombinant proteins. J. Biol. Chem. 265:1990;6908-6915.
19. Goldman E. R., Dall'Acqua W., Braden B. C., Mariuzza R. A. Analysis of binding interactions in an idiotope-antiidiotope protein-protein complex by double mutant cycles. Biochemistry. 36:1997;49-56.
20. Hawkins R. E., Russell S. J., Baier M., Winter G. The contribution of contact and non-contact residues of antibody in the affinity of binding to antigen: the interaction of mutant D1.3 antibodies with lysozyme. J. Mol. Biol. 234:1993;958-964.
21. Hoogenboom H. R., Griffiths A. D., Johnson K. S., Chiswell D. J., Hudson P., Winter G. Multi-subunit proteins on the surface of filamentous phage: methodologies for displaying antibody (Fab) heavy and light chains. Nucl. Acids Res. 19:1991;4133-4137.
22. Huang M. D., Syed R., Stura E. A., Stone M. J., Stefanko R. S., Ruf W., Edgington T. S., Wilson I. A. The mechanism of an inhibitory antibody on TF-initiated blood coagulation revealed by the crystal structures of human tissue factor, Fab5G9 and TF center dot 5G9 complex. J. Mol. Biol. 275:1998;873-894.
23. Hunter C. A., Singh J., Thornton J. M. π-π Interactions: the geometry and energetics of phenylalanine-phenylalanine interactions in proteins. J. Mol. Biol. 218:1991;837-846.
24. Johnson D. L., Farrell F. X., Barbone F. P., McMahon F. J., Tullai J., Hoey K., Livnah O., Wrighton N. C., Middleton S. A., Loughney D. A., Stura E. A., Dower W. J., Mulcahy L. S., Wilson I. A., Jolliffe L. K. Identification of a 13 amino acid peptide mimetic of erythropoietin and description of amino acids critical for the mimetic activity of EMP1. Biochemistry. 37:1998;3699-3710.
25. Jones S., Thornton J. M. Principles of protein-protein interactions. Proc. Natl Acad. Sci. USA. 93:1996;13-20.
26. Karlsson R., Faelt A. Experimental design for kinetic analysis of protein-protein interactions with surface plasmon resonance biosensors. J. Immunol. Methods. 200:1997;121-133.
27. Karlsson R., Michaelsson A., Mattsson L. Kinetic analysis of monoclonal antibody-antigen interactions with a new biosensor based analytical system. J. Immunol. Methods. 145:1991;229-240.
28. Karlsson R., Fägerstam L., Nilshans H., Persson B. Analysis of active antibody concentrations. Separation of affinity and concentration parameters. J. Immunol. Methods. 166:1993;75-84.
29. Koradi R., Billeter M., Wüthrich K. MOLMOL: A program for display and analysis of macromolecular structures. J. Mol. Graph. 14:1996;51-55.
30. Levitt M., Perutz M. F. Aromatic rings as hydrogen bond acceptors. J. Mol. Biol. 201:1988;751-754.
31. Mian I. S., Bradwell A. R., Olson A. J. Structure, function and properties of antibody binding sites. J. Mol. Biol. 217:1991;133-151.
32. Nuss J. M., Bossart Whitaker P., Air G. M. Identification of critical contact residues in the NC41 epitope of a subtype N9 influenza virus neuraminidase. Proteins: Struct. Funct. Genet. 15:1993;121-132.
33. O'Shannessy D. J., Brigham-Burke M., Soneson K. K., Hensley P., Brooks I. Determination of rate and equilibrium constants for macromolecular interactions using surface plasmon resonance: Use of nonlinear least squares analysis methods. Anal. Biochem. 212:1993;457-468.
34. Padlan E. A. On the nature of antibody combining sites: unusual structural features that may confer on these sites an enhanced capacity for binding ligands. Proteins: Struct. Funct. Genet. 7:1990;112-124.
35. Pearce K. H., Ultsch M. H., Kelley R. F., Devos A. M., Wells J. A. Structural and mutational analysis of affinity-inert contact residues at the growth hormone-receptor interface. Biochemistry. 35:1996;10300-10307.
36. Randal M., Kossiakoff A. A. Crystallization and preliminary X-ray analysis of 1:1 complex between a designed monomeric interferon-gamma and its soluble receptor. Protein Sci. 7:1998;1057-1060.
37. Serrano L., Bycroft M., Fersht A. R. Aromatic-aromatic interactions and protein stability. Investigations by double-mutant cycles. J. Mol. Biol. 218:1991;465-475.
38. Silvennoinen O., Ihle J. N. Signaling by the Hematopoietic Cytokine Receptors. 1996;R. G. Landes & Co. Austin.
39. 1-108complex. J. Mol. Biol. 273:1997;882-897.
40. Stevens F. J. Modification of an ELISA-based procedure for affinity determination: correction necessary for use with bivalent antibody. Mol. Immunol. 24:1987;1055-1060.
41. Thomas K. A., Smith G. M., Thomas T. B., Feldmann R. J. Electronic distributions within protein phenylalanine aromatic rings are reflected by the three-dimensional oxygen atom environments. Proc. Natl Acad. Sci. USA. 79:1982;4843-4847.
42. Tsumoto K., Ogasahara K., Ueda Y., Watanabe K., Yutani K., Kumagai I. Role of Tyr residues in the contact region of anti-lysozyme monoclonal antibody HyHEL10 for antigen binding. J. Biol. Chem. 270:1995;18551-18557.
43. Walter M. R., Windsor W., Nagabhushan T. L., Lundell D. J., Lunn C. A., Zauodny P. J., Narula S. K. Crystal structure of a complex between interferon-gamma and its soluble high-affinity receptor. Nature. 376:1995;230-235.
44. Williams G., Ruegg N., Birch A., Weber C., Hofstadter K., Robinson J. A., Aguet M., Garotta G., Schlatter D., Huber W. Dissection of the extracellular human interferon gamma receptor alpha-chain into two immunoglobulin-like domains. Production in an Escherichia coli thioredoxin gene fusion expression system and recognition by neutralizing antibodies. Biochemistry. 34:1995;1787-1797.
45. Wilson I. A., Stanfield R. L. Antibody-antigen interactions: new structures and new conformational changes. Curr. Opin. Struct. Biol. 4:1994;857-867.
46. Worth G. A., Wade R. C. The aromatic-(i+2) amine interaction in peptides. J. Phys. Chem. 99:1995;17473-17482.
47. Xu D., Lin S. L., Nussinov R. Protein binding versus protein folding: the role of hydrophilic bridges in protein associations. J. Mol. Biol. 265:1997;68-84.