In-depth biophysical analysis of interactions between therapeutic antibodies and the extracellular domain of the epidermal growth factor receptor

Analytical Biochemistry

Volumn 421, Issue 1, 2012, Pages 138-151

  Alvarenga, Maria Leonor ^a,b   Kikhney, Judith ^a   Hannewald, Jens ^a   Metzger, Armin U ^a   Steffens, Klaus Juergen ^b   Bomke, Joerg ^a   Krah, Alexander ^a   Wegener, Ansgar ^a  

^a Merck Serono GmbH   (Germany)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

Antibodies; Biophysics; Cetuximab; EGFR; Isothermal titration calorimetry; Matuzumab; Protein protein interactions; Static light scattering; Surface plasmon resonance

Indexed keywords

ANTIBODIES; BINDING ENERGY; BIOPHYSICS; CALORIMETERS; CALORIMETRY; DRUG PRODUCTS; ISOTHERMS; LIGHT SCATTERING; MONOCLONAL ANTIBODIES; PLASMONS; SURFACE SCATTERING; TITRATION;

CETUXIMAB; EGFR; ISOTHERMAL TITRATION CALORIMETRY; MATUZUMAB; PROTEIN-PROTEIN INTERACTIONS; STATIC LIGHT SCATTERING;

SURFACE PLASMON RESONANCE;

CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR; MATUZUMAB; PANITUMUMAB;

ALLOSTERISM; ANTIGEN BINDING; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DRUG MECHANISM; DRUG RECEPTOR BINDING; ISOTHERMAL TITRATION CALORIMETRY; LIGHT SCATTERING; PRIORITY JOURNAL; PROTEIN DOMAIN; STOICHIOMETRY; SURFACE PLASMON RESONANCE; THERMODYNAMICS;

EID: 84855871754     PISSN: 00032697     EISSN: 10960309     Source Type: Journal    
DOI: 10.1016/j.ab.2011.10.039     Document Type: Article

References (54)

1. C.M. West, L. Joseph, and S. Bhana Epidermal growth factor receptor-targeted therapy Br. J. Radiol. 81 Spec. No. 1 2008 S36 S44
2. N. Normanno, L.A. De, C. Bianco, L. Strizzi, M. Mancino, M.R. Maiello, A. Carotenuto, F.G. De, F. Caponigro, and D.S. Salomon Epidermal growth factor receptor (EGFR) signaling in cancer Gene 366 2006 2 16 (Pubitemid 43199589)
3. J. Mendelsohn, and J. Baselga Epidermal growth factor receptor targeting in cancer Semin. Oncol. 33 2006 369 385 (Pubitemid 44142736)
4. D.J. Leahy A molecular view of anti-ErbB monoclonal antibody therapy Cancer Cell 13 2008 291 293 (Pubitemid 351446199)
5. K.R. Schmitz, and K.M. Ferguson Interaction of antibodies with ErbB receptor extracellular regions Exp. Cell Res. 315 2009 659 670
6. M. Peipp, M. Dechant, and T. Valerius Effector mechanisms of therapeutic antibodies against ErbB receptors Curr. Opin. Immunol. 20 2008 436 443
7. S. Li, K.R. Schmitz, P.D. Jeffrey, J.J. Wiltzius, P. Kussie, and K.M. Ferguson Structural basis for inhibition of the epidermal growth factor receptor by cetuximab Cancer Cell 7 2005 301 311 (Pubitemid 40544648)
8. S. Li, P. Kussie, and K.M. Ferguson Structural basis for EGF receptor inhibition by the therapeutic antibody IMC-11F8 Structure 16 2008 216 227 (Pubitemid 351215209)
9. J.J. Lammerts van Bueren, W.K. Bleeker, A. Brannstrom, E.A. von, M. Jansson, M. Peipp, T. Schneider-Merck, T. Valerius, J.G. van de Winkel, and P.W. Parren The antibody zalutumumab inhibits epidermal growth factor receptor signaling by limiting intra- and intermolecular flexibility Proc. Natl. Acad. Sci. USA 105 2008 6109 6114 (Pubitemid 351758407)
10. D. Freeman, J. Sun, R. Bass, K. Jung, S. Ogbagabriel, G. Elliott, R. Radinsky, Panitumumab and cetuximab epitope mapping and in vitro activity, 2008 ASCO Annual Meeting, May 20, suppl., abstr. 14536. J. Clin. Oncol. 26 (2008).
11. J. Schmiedel, A. Blaukat, S. Li, T. Knochel, and K.M. Ferguson Matuzumab binding to EGFR prevents the conformational rearrangement required for dimerization Cancer Cell 13 2008 365 373 (Pubitemid 351446197)
12. V. Kamat, J.M. Donaldson, C. Kari, M.R. Quadros, P.I. Lelkes, I. Chaiken, S. Cocklin, J.C. Williams, E. Papazoglou, and U. Rodeck Enhanced EGFR inhibition and distinct epitope recognition by EGFR antagonistic mAbs C225 and 425 Cancer Biol. Ther. 7 2008 726 733
13. R. Karlsson SPR for molecular interaction analysis: a review of emerging application areas J. Mol. Recognit. 17 2004 151 161 (Pubitemid 38688875)
14. L.C. Santora, Z. Kaymakcalan, P. Sakorafas, I.S. Krull, and K. Grant Characterization of noncovalent complexes of recombinant human monoclonal antibody and antigen using cation exchange, size exclusion chromatography, and BIAcore Anal. Biochem. 299 2001 119 129 (Pubitemid 34053400)
15. P.S. Katsamba, I. Navratilova, M. Calderon-Cacia, L. Fan, K. Thornton, M. Zhu, T.V. Bos, C. Forte, D. Friend, I. Laird-Offringa, G. Tavares, J. Whatley, E. Shi, A. Widom, K.C. Lindquist, S. Klakamp, A. Drake, D. Bohmann, M. Roell, L. Rose, J. Dorocke, B. Roth, B. Luginbuhl, and D.G. Myszka Kinetic analysis of a high-affinity antibody/antigen interaction performed by multiple Biacore users Anal. Biochem. 352 2006 208 221
16. R. Patel, and B.A. Andrien Jr. Kinetic analysis of a monoclonal therapeutic antibody and its single-chain homolog by surface plasmon resonance Anal. Biochem. 396 2010 59 68
17. R.A. Copeland, D.L. Pompliano, and T.D. Meek Drug-target residence time and its implications for lead optimization Nat. Rev. Drug Discov. 5 2006 730 739 (Pubitemid 44323700)
18. Y.S. Day, C.L. Baird, R.L. Rich, and D.G. Myszka Direct comparison of binding equilibrium, thermodynamic, and rate constants determined by surface- and solution-based biophysical methods Protein Sci. 11 2002 1017 1025 (Pubitemid 34441221)
19. I. Jelesarov, L. Leder, and H.R. Bosshard Probing the energetics of antigen-antibody recognition by titration microcalorimetry Methods 9 1996 533 541 (Pubitemid 26273474)
20. I. Jelesarov, and H.R. Bosshard Isothermal titration calorimetry and differential scanning calorimetry as complementary tools to investigate the energetics of biomolecular recognition J. Mol. Recognit. 12 1999 3 18 (Pubitemid 29160432)
21. R. Perozzo, G. Folkers, and L. Scapozza Thermodynamics of protein-ligand interactions: history, presence, and future aspects J. Recept. Signal. Transduct. Res. 24 2004 1 52 (Pubitemid 39011288)
22. A. Velazquez-Campoy, Y. Kiso, and E. Freire The binding energetics of first- and second-generation HIV-1 protease inhibitors: implications for drug design Arch. Biochem. Biophys. 390 2001 169 175 (Pubitemid 32568478)
23. S. Leavitt, and E. Freire Direct measurement of protein binding energetics by isothermal titration calorimetry Curr. Opin. Struct. Biol. 11 2001 560 566 (Pubitemid 32972017)
24. J.M. Sturtevant Heat capacity and entropy changes in processes involving proteins Proc. Natl. Acad. Sci. USA 74 1977 2236 2240 (Pubitemid 8110685)
25. J. Gomez, and E. Freire Thermodynamic mapping of the inhibitor site of the aspartic protease endothiapepsin J. Mol. Biol. 252 1995 337 350
26. W.H. Ward, and G.A. Holdgate Isothermal titration calorimetry in drug discovery Prog. Med. Chem. 38 2001 309 376
27. P.D. Kwong, M.L. Doyle, D.J. Casper, C. Cicala, S.A. Leavitt, S. Majeed, T.D. Steenbeke, M. Venturi, I. Chaiken, M. Fung, H. Katinger, P.W. Parren, J. Robinson, R.D. Van, L. Wang, D.R. Burton, E. Freire, R. Wyatt, J. Sodroski, W.A. Hendrickson, and J. Arthos HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites Nature 420 2002 678 682 (Pubitemid 36764500)
28. N.V. Prabhu, and K.A. Sharp Heat capacity in proteins Annu. Rev. Phys. Chem. 56 2005 521 548 (Pubitemid 41156887)
29. G.A. Holdgate, and W.H. Ward Measurements of binding thermodynamics in drug discovery Drug Discov. Today 10 2005 1543 1550 (Pubitemid 41527197)
30. T. Arakawa, J. Wen, Size-exclusion chromatography with on-line light scattering, Curr. Protoc. Protein Sci. Chapter 20 (2001) Unit 20.6.
31. R.L. Qian, R. Mhatre, and I.S. Krull Characterization of antigen-antibody complexes by size-exclusion chromatography coupled with low-angle light-scattering photometry and viscometry J. Chromatogr. A 787 1997 101 109 (Pubitemid 27515129)
32. D.S. Rehder, D. Chelius, A. McAuley, T.M. Dillon, G. Xiao, J. Crouse-Zeineddini, L. Vardanyan, N. Perico, V. Mukku, D.N. Brems, M. Matsumura, and P.V. Bondarenko Isomerization of a single aspartyl residue of anti-epidermal growth factor receptor immunoglobulin gamma2 antibody highlights the role avidity plays in antibody activity Biochemistry 47 2008 2518 2530 (Pubitemid 351304557)
33. X.D. Yang, X.C. Jia, J.R. Corvalan, P. Wang, C.G. Davis, and A. Jakobovits Eradication of established tumors by a fully human monoclonal antibody to the epidermal growth factor receptor without concomitant chemotherapy Cancer Res. 59 1999 1236 1243 (Pubitemid 29136253)
34. W. Weber, G.N. Gill, and J. Spiess Production of an epidermal growth factor receptor-related protein Science 224 1984 294 297 (Pubitemid 14172514)
35. A. Ullrich, L. Coussens, J.S. Hayflick, T.J. Dull, A. Gray, A.W. Tam, J. Lee, Y. Yarden, T.A. Libermann, and J. Schlessinger Human epidermal growth factor receptor cDNA sequence and aberrant expression of the amplified gene in A431 epidermoid carcinoma cells Nature 309 1984 418 425 (Pubitemid 14102443)
36. H. Edelhoch Spectroscopic determination of tryptophan and tyrosine in proteins Biochemistry 6 1967 1948 1954
37. Biacore, Biacore T100 Instrument Handbook, Biacore AB, Uppsala, 2005.
38. Biacore, Biacore T100 Software Handbook, Biacore AB, Uppsala, 2006.
39. T. Wiseman, S. Williston, J.F. Brandts, and L.N. Lin Rapid measurement of binding constants and heats of binding using a new titration calorimeter Anal. Biochem. 179 1989 131 137 (Pubitemid 19149635)
40. J.E. Ladbury, and B.Z. Chowdhry Biocalorimetry: Applications of Calorimetry in the Biological Sciences 1998 Wiley Chichester
41. Microcal Tutorial Guide on ITC Data Analysis in Origin®. Using Origin® Scientific Plotting Software to Analyze Calorimetric Data from All MicroCal Isothermal Titration Calorimeters, V7.0(MAU130010 Rev. D), Northampton, MA, MicroCal, LLC, 2004.
42. M.A. Lemmon, Z. Bu, J.E. Ladbury, M. Zhou, D. Pinchasi, I. Lax, D.M. Engelman, and J. Schlessinger Two EGF molecules contribute additively to stabilization of the EGFR dimer EMBO J. 16 1997 281 294 (Pubitemid 27049386)
43. M.A. Lemmon Ligand-induced ErbB receptor dimerization Exp. Cell Res. 315 2009 638 648
44. J.L. Macdonald, and L.J. Pike Heterogeneity in EGF-binding affinities arises from negative cooperativity in an aggregating system Proc. Natl. Acad. Sci. USA 105 2008 112 117
45. C.J. Stroop, W. Weber, G.J. Gerwig, M. Nimtz, J.P. Kamerling, and J.F. Vliegenthart Characterization of the carbohydrate chains of the secreted form of the human epidermal growth factor receptor Glycobiology 10 2000 901 917
46. R.L. Stanfield, and I.A. Wilson Antibody molecular structure Z. An, Therapeutic Monoclonal Antibodies - From Bench to Clinic 2009 Wiley NJ 51 66
47. D.H. Williams, E. Stephens, D.P. O'Brien, and M. Zhou Understanding noncovalent interactions: ligand binding energy and catalytic efficiency from ligand-induced reductions in motion within receptors and enzymes Angew. Chem. Int. Ed. Engl. 43 2004 6596 6616 (Pubitemid 40018986)
48. A. Cooper, and D.T. Dryden Allostery without conformational change. A plausible model Eur. Biophys. J. 11 1984 103 109
49. S. Otto Reinforced molecular recognition as an alternative to rigid receptors Dalton Trans. 2006 2861 2864 (Pubitemid 43856592)
50. C.J. Tsai, S.A. del, and R. Nussinov Protein allostery, signal transmission and dynamics: a classification scheme of allosteric mechanisms Mol. Biosyst. 5 2009 207 216
51. M.R. Eftink, A.C. Anusiem, and R.L. Biltonen Enthalpy-entropy compensation and heat capacity changes for protein-ligand interactions: general thermodynamic models and data for the binding of nucleotides to ribonuclease A Biochemistry 22 1983 3884 3896
52. X. Zhang, J. Gureasko, K. Shen, P.A. Cole, and J. Kuriyan An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor Cell 125 2006 1137 1149 (Pubitemid 43866200)
53. L.M. Friedman, A. Rinon, B. Schechter, L. Lyass, S. Lavi, S.S. Bacus, M. Sela, and Y. Yarden Synergistic down-regulation of receptor tyrosine kinases by combinations of mAbs: implications for cancer immunotherapy Proc. Natl. Acad. Sci. USA 102 2005 1915 1920 (Pubitemid 40261987)
54. M. Dechant, W. Weisner, S. Berger, M. Peipp, T. Beyer, T. Schneider-Merck, J.J. Lammerts van Bueren, W.K. Bleeker, P.W. Parren, J.G. van de Winkel, and T. Valerius Complement-dependent tumor cell lysis triggered by combinations of epidermal growth factor receptor antibodies Cancer Res. 68 2008 4998 5003