The structure of the anti-c-myc antibody 9E10 Fab fragment/epitope peptide complex reveals a novel binding mode dominated by the heavy chain hypervariable loops

Proteins: Structure, Function and Genetics

Volumn 73, Issue 3, 2008, Pages 552-565

  Krauß, Norbert ^a,d   Wessner, Helga ^a   Welfle, Karin ^b   Welfle, Heinz ^b   Scholz, Christa ^a   Seifert, Martina ^a   Zubow, Kristina ^a   Aÿ, Jacqueline ^a   Hahn, Michael ^a   Scheerer, Patrick ^a   Skerra, Arne ^c   Höhne, Wolfgang ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Antibody antigen interaction; Calorimetry; Conformation of complementarity determining regions; Crystal structure; Epitope peptide; myc tag

Indexed keywords

C MYC ANTIBODY 9E10; IMMUNOGLOBULIN F(AB) FRAGMENT; MYC PROTEIN; PROTEIN ANTIBODY; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANTIBODY TITER; ANTIGEN ANTIBODY REACTION; ARTICLE; BETA SHEET; CALORIMETRY; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; THERMODYNAMICS;

AMINO ACID SEQUENCE; ANTIBODIES; CALORIMETRY; CELL LINE; COMPLEMENTARITY DETERMINING REGIONS; CRYSTALLOGRAPHY, X-RAY; EPITOPES; HUMANS; HYDROGEN BONDING; IMMUNOGLOBULIN VARIABLE REGION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN STRUCTURE, SECONDARY; PROTO-ONCOGENE PROTEINS C-MYC; THERMODYNAMICS;

EID: 57349113010     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22080     Document Type: Article

References (60)

1. Evan GI, Lewis GK, Ramsay G, Bishop JM. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol Cell Biol 1985;5:3610-3616.
2. Munro S, Pelham HRB. Use of peptide tagging to detect proteins expressed from cloned genes: deletion mapping functional domains of Drosophila hsp 70. EMBO J 1984;3:3087-3093.
3. Terpe K. Overview of tag protein fusions: from molecular and biochemical fundamentals to commercial systems. Appl Microbiol Biotechnol 2003;60:523-533.
4. Hoogenboom HR, Griffiths AD, Johnson KS, Chiswell DJ, Hudson P, Winter G. Multi-subunit proteins on the surface of filamentous phage: methodologies for displaying antibody (Fab) heavy and light chains. Nucleic Acids Res 1991;19:4133-4137.
5. Schiweck W, Buxbaum B, Schätzlein C, Neiss HG, Skerra A. Sequence analysis and bacterial production of the anti-c-myc antibody 9E10: the VH domain has an extended CDR-H3 and exhibits unusual solubility. FEBS Lett 1997;414:33-38.
6. Fuchs P, Breitling F, Little M, Dübel S. Primary structure and functional scFv antibody expression of an antibody against the human protooncogen c-myc. Hybridoma 1997;16:227-233.
7. Kabat EA, Wu TT, Perry HM, Gottesman KS, Foeller C. Sequences of proteins of immunological interest. Cambridge: Public Health Service; 1991. 2597 p.
8. Hilpert K, Hansen G, Wessner H, Küttner G, Welfle K, Seifert M, Höhne W. Anti-c-myc antibody 9E10: epitope key positions and variability characterized using peptide spot synthesis on cellulose. Protein Eng 2001;14:803-806.
9. Paschke M, Zahn G, Warsinke A, Höhne W. New series of vectors for phage display and prokaryotic expression of proteins. Biotechniques 2001;30:720-726.
10. Baggio R, Burgstaller P, Hale SP, Putney AR, Lane M, Lipovsek D, Wright MC, Roberts RW, Liu R, Szostak JW, Wagner RW. Identification of epitope-like consensus motifs using mRNA display. J Mol Recognit 2002;15:126-134.
11. Otwinowski Z, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 1997;276:307-326.
12. Navaza J. AMoRe: an automated package for molecular replacement. Acta Crystallogr 1994;A 50:157-163.
13. Collaborative Computational Project, Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D 1994;50:760-763.
14. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang J-S, Kuszewski J, Nilges N, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL. Crystallography and NMR system (CNS): a new software system for macromolecular structure determination. Acta Crystallogr D 1998;54:905-921.
15. Jones TA, Kjeldgaard M. Electron-density map interpretation. Methods Enzymol 1997;277:173-208.
16. Sanner MF, Olson AJ, Spehner J-C. Reduced surface: an efficient way to compute molecular surfaces. Biopolymers 1996;38:305-320.
17. Laskowski R, McArthur MW, Moss DS, Thornton JM. PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 1993;26:283-191.
18. Hooft RWW, Vriend G, Sander S, Abola EE. Errors in protein structures. Nature 1996;381:272-272.
19. Kraulis PJ. MOLSCRIPT. A program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 1991;24:946-950.
20. Merritt EA, Bacon DJ. Raster3D: photorealistic molecular graphics. Methods Enzymol 1997;277:505-524.
21. Lawrence MC, Bourke P. CONSCRIPT: a program for generating electron density isosurfaces for presentation in protein crystallography. J Appl Crystallogr 2000;33:990-991.
22. DeLano WL. The PyMOL Molecular Graphics System (DeLano Scientific), San Carlos; 2002. Available at: http://www.pymol.org
23. Christensen JJ, Hansen LD, Izatt RM. Handbook of proton ionization heats and related thermodynamic quantities. New York: Wiley; 1976. 286 p.
24. Fukada H, Takahashi K. Enthalpy and heat capacity changes for the proton dissociation of various buffer components in 0.1 M potassium chloride. Proteins 1998;33:159-166.
25. Al-Lazikani B, Lesk AM, Chothia C. Standard conformations for the canonical structures of immunoglobulins. J Mol Biol 1997;273:927-948.
26. Murphy KP, Freire E, Paterson Y. Configurational effects in antibody-antigen interactions studied by microcalorimetry. Proteins 1995;21:83-90.
27. Wibbenmeyer JA, Schuck P, Smith-Gill SJ, Willson RC. Salt links dominate affinity of antibody HyHEL-5 for lysozyme through enthalpic contributions. J Biol Chem 1999;274:26838-26842.
28. Hahn M, Winkler D, Welfle K, Misselwitz R, Welfle H, Wessner H, Zahn G, Scholz C, Seifert M, Harkins R, Schneider-Mergener J, Höhne W. Crossreactive binding of cyclic peptides to an anti-TGFα antibody Fab-fragment: an X-ray structural and thermodynamic analysis. J Mol Biol 2001;314:279-295.
29. Baker BM, Murphy KP. Evaluation of linked protonation effects in protein binding reactions using isothermal titration calorimetry. Biophys J 1996;71:2049-2055.
30. Murphy KP, Xie D, Thompson KS, Amzel LM, Freire E. Entropy in biological binding processes: estimation of translational entropy loss. Proteins 1994;18:63-67.
31. Hillig RC, Urlinger S, Fanghänel J, Brocks B, Haenel C, Stark Y, Sülzle D, Svergun DI, Baesler S, Malawski G, Moosmayer D, Menrad A, Schirner M, Licha K. Fab MOR03268 triggers absorption shift of a diagnostic dye via packaging in a solvent-shielded Fab dimer interface. J Mol Biol 2008;377:206-219.
32. Ramsland PA, Kaushik A, Marchalonis JJ, Edmundson AB. Incorporation of long CDR3s into V domains: implications for the structural evolution of the antibody-combining site. Exp Clin Immunogenet 2001;18:176-198.
33. Collis AVJ, Brouwer AP, Martin ACR. Analysis of the antigen combining site: correlations between length and sequence composition of the hypervariable loops and the nature of the antigen. J Mol Biol 2003;325:337-354.
34. Stanfield RL, Wilson IA. Structural studies of human HIV-1 V3 antibodies. Hum Antibodies 2005;14:73-80.
35. Webster DM, Henry AH, Rees AR. Antibody-antigen interactions. Curr Opin Struct Biol 1994;4:123-129.
36. Saphire EO, Parren, PWHI, Pantophlet R, Zwick MB, Morris GM, Rudd PM, Dwek RA, Stanfield RL, Burton DR, Wilson IA. Crystal structure of a neutralizing human IgG against HIV-1: a template for vaccine design. Science 2001;293:1155-1159.
37. Rossmann MG. The canyon hypothesis. J Biol Chem 1989;264: 14587-14590.
38. Guddat LW, Shan L, Broomell C, Ramsland PA, Fan ZC, Anchin JM, Linthicum DS, Edmundson AB. The three-dimensional structure of a complex of a murine Fab (NC10.14) with a potent sweetener (NC174): an illustration of structural diversity in antigen recognition by immunoglobulins. J Mol Biol 2000;302:853-872.
39. Stanfield RL, Cabezas E, Satterthwait AC, Stura EA, Profy AT, Wilson IA. Dual conformations for the HIV-1 gp120 V3 loop in complexes with different neutralizing Fabs. Structure 1999;7:131-142.
40. Stanfield RL, Gorny MK, Williams C, Zolla-Pazner S, Wilson IA. Structural rationale for the broad neutralization of HIV-1 by human monoclonal antibody 447-52D. Structure 2004;12:193-204.
41. He XM, Rüker F, Casale E, Carter DC. Structure of a human monoclonal antibody fab fragment against gp41 of human immunodeficiency virus type 1. Proc Natl Acad Sci USA 1992;89:7154-7158.
42. Chi, S-W, Maeng, C-Y, Kim SJ, Oh MS, Ryu CJ, Kim SJ, Han ,K-H, Hong HJ, Ryu, SE. Broadly neutralizing anti-hepatitis B virus antibody reveals a complementarity determining region H3 lid-opening mechanism. Proc Natl Acad Sci USA. 2007;104:9230-9235.
43. Momany C, Kovari LC, Prongay AJ, Keller W, Gitti RK, Lee BM, Gorbalenya AE, Tong L, McClure J, Ehrlich LS, Summers MF, Carter C, Rossman MG. Crystal structure of dimeric HIV-1 capsid protein. Nat Struct Biol 1996;3:763-770.
44. Lescar J, Stouracova R, Riottot MM, Chitarra V, Brynda J, Fabry M, Horejsi M, Sedlacek J, Bentley GA. Three-dimensional structure of an fab-peptide complex: structural basis of HIV-1 protease inhibition by a monoclonal antibody. J Mol Biol 1997;267:1207-1222.
45. Chavali G, Papageorgiou A, Olson K, Fett J, Hu G, Shapiro R, Acharya KR. The crystal structure of human angiogenin in complex with an antitumor neutralizing antibody. Structure 2003;11:875-885.
46. Yang PL, Schultz PG. Mutational analysis of the affinity maturation of antibody 48G7. J Mol Biol 1999;294:1191-1201.
47. Foote J, Winter G. Antibody framework residues affecting the conformation of the hypervariable loops. J Mol Biol 1992;224:487-499.
48. Li Y, Li H, Yang F, Smith-Gill SJ, Mariuzza RA. X-ray snapshots of the maturation of an antibody response to a protein antigen. Nat Struct Biol 2003;10:482-488.
49. Acierno JP, Braden BC, Klinke S, Goldbaum FA, Cauerhff A. Affinity maturation increases the stability and plasticity of the Fv domain of anti-protein antibodies. J Mol Biol 2007;374:130-146.
50. 1HNMR solution structure of the c-myc heterodimeric leucine zipper. J Mol Biol 1998;281:165-181.
51. Nair SK, Burley SK. X-ray structures of myc-max and mad-max recognizing DNA: molecular bases of regulation by proto-oncogenic transcription factors. Cell 2003;112:193-205.
52. Fan H, Villegas C, Chan AK, Wright JA. Myc-epitope tagged proteins detected with the 9E10 antibody in immunofluorescence and immunoprecipitation assays but not in western blot analysis. Biochem Cell Biol 1998;76:125-128.
53. Murphy KP, Xie D, Garcia KC, Amzel LM, Freire E. Structural energetics of peptide recognition: angiotensin II/antibody binding. Proteins 1993;15:113-120.
54. Shick KA, Xavier KA, Rajpal A, Smith-Gill SJ, Willson RC. Association of the anti-hen egg lysozyme antibody HyHEL-5 with avian species variant and mutant lysozymes. Biochim Biophys Acta 1997;1340:205-214.
55. Xavier KA, Shick KA, Smith-Gill SJ, Willson RC. Involvement of water molecules in the association of monoclonal antibody HyHEL-5 with bobwhite quail lysozyme. Biophys J 1997;73:2116-2125.
56. Welfle K, Misselwitz R, Höhne W, Welfle H. Interaction of epitope-related and -unrelated peptides with anti-p24 (HIV-1) monoclonal antibody CB4-1 and its fab fragment. J Mol Recognit 2003;16:54-62.
57. Cooper A, Johnson CM, Lakey JH, Nöllmann M. Heat does not come in different colours: entropy-enthalpy compensation, free energy windows, quantum confinement, pressure perturbation calorimetry, solvation and the multiple causes of heat capacity effects in biomolecular interactions. Biophys Chem 2001;93:215-230.
58. Lumry R, Rajender S. Enthalpy-entropy compensation phenomena in water solutions of proteins and small molecules: a ubiquitous property of water. Biopolymers 1970;9:1125-1127.
59. Dunitz JD. Win some, lose some. Enthalpy-entropy compensation in weak intermolecular interactions. Chem Biol 1995;2:709-712.
60. Haun MF, Wirth M, Rüterjahns H. Calorimetric investigation of thermal stability and ligand-binding characteristics of disulfide-bond-cleaved ribonuclease T1. Eur J Biochem 1995;227:516-523.