Conformational nanobodies reveal tethered epidermal growth factor receptor involved in EGFR/ErbB2 predimers

ACS Nano

Volumn 9, Issue 2, 2015, Pages 1388-1399

  Nevoltris, Damien ^a,b,c,d,e   Lombard, Benjamin ^a,b,c,d   Dupuis, Elodie ^e   Mathis, Gérard ^e   Chames, Patrick ^a,b,c,d   Baty, Daniel ^a,b,c,d  

^a INSERM   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c CNRS   (France)

^d INSTITUT PAOLI CALMETTES   (France)

^e CisBio Bioassays   (France)

Author keywords

biosensors; conformational changes; epidermal growth factor receptor (EGFR); homogenous time resolved fluorescence; nanobodies; phage display; single domain antibodies

Indexed keywords

ACTIVATION ANALYSIS; AMINO ACIDS; BIOSENSORS; CELL MEMBRANES; CELL PROLIFERATION; ENZYMES; PHAGE DISPLAY;

CONFORMATIONAL CHANGE; EPIDERMAL GROWTH FACTOR RECEPTORS; NANOBODIES; SINGLE-DOMAIN ANTIBODIES; TIME-RESOLVED FLUORESCENCE;

LIGANDS;

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPITOPE; NANOBODY;

ANIMAL; ANTIBODY SPECIFICITY; BINDING SITE; CELL LINE; CHEMISTRY; GENETIC PROCEDURES; HUMAN; IMMUNOLOGY; MOUSE; NEW WORLD CAMELID; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE;

ANIMALS; ANTIBODY SPECIFICITY; BINDING SITES; BIOSENSING TECHNIQUES; CAMELIDS, NEW WORLD; CELL LINE; EPITOPES; HUMANS; MICE; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; SINGLE-DOMAIN ANTIBODIES;

EID: 84923408303     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn505752u     Document Type: Article

References (52)

1. Oda, K.; Matsuoka, Y.; Funahashi, A.; Kitano, H. A Comprehensive Pathway Map of Epidermal Growth Factor Receptor Signaling Mol. Syst. Biol. 2005, 1 (2005 0010
2. Roskoski, R., Jr. The Erbb/Her Family of Protein-Tyrosine Kinases and Cancer Pharmacol. Res. 2014, 79, 34-74
3. Lemmon, M. A. Ligand-Induced Erbb Receptor Dimerization Exp. Cell Res. 2009, 315, 638-648
4. Cho, H. S.; Leahy, D. J. Structure of the Extracellular Region of Her3 Reveals an Interdomain Tether Science 2002, 297, 1330-1333
5. Ferguson, K. M.; Berger, M. B.; Mendrola, J. M.; Cho, H. S.; Leahy, D. J.; Lemmon, M. A. Egf Activates Its Receptor by Removing Interactions That Autoinhibit Ectodomain Dimerization Mol. Cell 2003, 11, 507-517
6. Garrett, T. P.; McKern, N. M.; Lou, M.; Elleman, T. C.; Adams, T. E.; Lovrecz, G. O.; Zhu, H. J.; Walker, F.; Frenkel, M. J.; Hoyne, P. A. Crystal Structure of a Truncated Epidermal Growth Factor Receptor Extracellular Domain Bound to Transforming Growth Factor Alpha Cell 2002, 110, 763-773
7. Ogiso, H.; Ishitani, R.; Nureki, O.; Fukai, S.; Yamanaka, M.; Kim, J. H.; Saito, K.; Sakamoto, A.; Inoue, M.; Shirouzu, M. Crystal Structure of the Complex of Human Epidermal Growth Factor and Receptor Extracellular Domains Cell 2002, 110, 775-787
8. Schlessinger, J. Ligand-Induced, Receptor-Mediated Dimerization and Activation of Egf Receptor Cell 2002, 110, 669-672
9. Zhang, X.; Gureasko, J.; Shen, K.; Cole, P. A.; Kuriyan, J. An Allosteric Mechanism for Activation of the Kinase Domain of Epidermal Growth Factor Receptor Cell 2006, 125, 1137-1149
10. Moriki, T.; Maruyama, H.; Maruyama, I. N. Activation of Preformed Egf Receptor Dimers by Ligand-Induced Rotation of the Transmembrane Domain J. Mol. Biol. 2001, 311, 1011-1026
11. Junttila, T. T.; Akita, R. W.; Parsons, K.; Fields, C.; Lewis Phillips, G. D.; Friedman, L. S.; Sampath, D.; Sliwkowski, M. X. Ligand-Independent Her2/Her3/Pi3k Complex Is Disrupted by Trastuzumab and Is Effectively Inhibited by the Pi3k Inhibitor Gdc-0941 Cancer Cell 2009, 15, 429-440
12. Kawashima, N.; Nakayama, K.; Itoh, K.; Itoh, T.; Ishikawa, M.; Biju, V. Reversible Dimerization of Egfr Revealed by Single-Molecule Fluorescence Imaging Using Quantum Dots Chemistry 2010, 16, 1186-1192
13. Gadella, T. W., Jr.; Jovin, T. M. Oligomerization of Epidermal Growth Factor Receptors on A431 Cells Studied by Time-Resolved Fluorescence Imaging Microscopy. A Stereochemical Model for Tyrosine Kinase Receptor Activation J. Cell Biol. 1995, 129, 1543-1558
14. Yu, X.; Sharma, K. D.; Takahashi, T.; Iwamoto, R.; Mekada, E. Ligand-Independent Dimer Formation of Epidermal Growth Factor Receptor (Egfr) Is a Step Separable from Ligand-Induced Egfr Signaling Mol. Biol. Cell 2002, 13, 2547-2557
15. Macdonald-Obermann, J. L.; Piwnica-Worms, D.; Pike, L. J. Mechanics of Egf Receptor/Erbb2 Kinase Activation Revealed by Luciferase Fragment Complementation Imaging Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 137-142
16. Jura, N.; Endres, N. F.; Engel, K.; Deindl, S.; Das, R.; Lamers, M. H.; Wemmer, D. E.; Zhang, X.; Kuriyan, J. Mechanism for Activation of the Egf Receptor Catalytic Domain by the Juxtamembrane Segment Cell 2009, 137, 1293-1307
17. Endres, N. F.; Das, R.; Smith, A. W.; Arkhipov, A.; Kovacs, E.; Huang, Y.; Pelton, J. G.; Shan, Y.; Shaw, D. E.; Wemmer, D. E. Conformational Coupling across the Plasma Membrane in Activation of the Egf Receptor Cell 2013, 152, 543-556
18. Mi, L. Z.; Lu, C.; Li, Z.; Nishida, N.; Walz, T.; Springer, T. A. Simultaneous Visualization of the Extracellular and Cytoplasmic Domains of the Epidermal Growth Factor Receptor Nat. Struct. Mol. Biol. 2011, 18, 984-989
19. Liu, P.; Cleveland, T. E., IV; Bouyain, S.; Byrne, P. O.; Longo, P. A.; Leahy, D. J. A Single Ligand Is Sufficient to Activate EGFR Dimers Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 10861-10866
20. Macdonald-Obermann, J. L.; Adak, S.; Landgraf, R.; Piwnica-Worms, D.; Pike, L. J. Dynamic Analysis of the Epidermal Growth Factor (Egf) Receptor-Erbb2-Erbb3 Protein Network by Luciferase Fragment Complementation Imaging J. Biol. Chem. 2013, 288, 30773-30784
21. Arkhipov, A.; Shan, Y.; Das, R.; Endres, N. F.; Eastwood, M. P.; Wemmer, D. E.; Kuriyan, J.; Shaw, D. E. Architecture and Membrane Interactions of the Egf Receptor Cell 2013, 152, 557-569
22. Muyldermans, S. Nanobodies: Natural Single-Domain Antibodies Annu. Rev. Biochem. 2013, 82, 775-797
23. Perez, J. M.; Renisio, J. G.; Prompers, J. J.; van Platerink, C. J.; Cambillau, C.; Darbon, H.; Frenken, L. G. Thermal Unfolding of a Llama Antibody Fragment: A Two-State Reversible Process Biochemistry 2001, 40, 74-83
24. Gueorguieva, D.; Li, S.; Walsh, N.; Mukerji, A.; Tanha, J.; Pandey, S. Identification of Single-Domain, Bax-Specific Intrabodies That Confer Resistance to Mammalian Cells against Oxidative-Stress-Induced Apoptosis FASEB J. 2006, 20, 2636-2638
25. Muyldermans, S. Single Domain Camel Antibodies: Current Status J. Biotechnol. 2001, 74, 277-302
26. De Genst, E.; Silence, K.; Decanniere, K.; Conrath, K.; Loris, R.; Kinne, J.; Muyldermans, S.; Wyns, L. Molecular Basis for the Preferential Cleft Recognition by Dromedary Heavy-Chain Antibodies Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 4586-4591
27. Irannejad, R.; Tomshine, J. C.; Tomshine, J. R.; Chevalier, M.; Mahoney, J. P.; Steyaert, J.; Rasmussen, S. G.; Sunahara, R. K.; El-Samad, H.; Huang, B. Conformational Biosensors Reveal Gpcr Signalling from Endosomes Nature 2013, 495, 534-538
28. Staus, D. P.; Wingler, L. M.; Strachan, R. T.; Rasmussen, S. G.; Pardon, E.; Ahn, S.; Steyaert, J.; Kobilka, B. K.; Lefkowitz, R. J. Regulation of Beta2-Adrenergic Receptor Function by Conformationally Selective Single-Domain Intrabodies Mol. Pharmacol. 2014, 85, 472-481
29. Ho-Pun-Cheung, A.; Bazin, H.; Gaborit, N.; Larbouret, C.; Garnero, P.; Assenat, E.; Castan, F.; Bascoul-Mollevi, C.; Ramos, J.; Ychou, M. Quantification of Her Expression and Dimerization in Patients' Tumor Samples Using Time-Resolved Forster Resonance Energy Transfer PLoS One 2012, 7 e37065
30. Mathis, G. Probing Molecular Interactions with Homogeneous Techniques Based on Rare Earth Cryptates and Fluorescence Energy Transfer Clin Chem. 1995, 41, 1391-1397
31. Juillerat, A.; Gronemeyer, T.; Keppler, A.; Gendreizig, S.; Pick, H.; Vogel, H.; Johnsson, K. Directed Evolution of O6-Alkylguanine-DNA Alkyltransferase for Efficient Labeling of Fusion Proteins with Small Molecules in Vivo Chem. Biol. 2003, 10, 313-317
32. Gautier, A.; Juillerat, A.; Heinis, C.; Correa, I. R., Jr.; Kindermann, M.; Beaufils, F.; Johnsson, K. An Engineered Protein Tag for Multiprotein Labeling in Living Cells Chem. Biol. 2008, 15, 128-136
33. Maurel, D.; Comps-Agrar, L.; Brock, C.; Rives, M. L.; Bourrier, E.; Ayoub, M. A.; Bazin, H.; Tinel, N.; Durroux, T.; Prezeau, L. Cell-Surface Protein-Protein Interaction Analysis with Time-Resolved Fret and Snap-Tag Technologies: Application to Gpcr Oligomerization Nat. Methods 2008, 5, 561-567
34. Cochran, J. R.; Kim, Y. S.; Olsen, M. J.; Bhandari, R.; Wittrup, K. D. Domain-Level Antibody Epitope Mapping through Yeast Surface Display of Epidermal Growth Factor Receptor Fragments J. Immunol. Methods 2004, 287, 147-158
35. Rodeck, U.; Herlyn, M.; Herlyn, D.; Molthoff, C.; Atkinson, B.; Varello, M.; Steplewski, Z.; Koprowski, H. Tumor Growth Modulation by a Monoclonal Antibody to the Epidermal Growth Factor Receptor: Immunologically Mediated and Effector Cell-Independent Effects Cancer Res. 1987, 47, 3692-3696
36. Li, S.; Schmitz, K. R.; Jeffrey, P. D.; Wiltzius, J. J.; Kussie, P.; Ferguson, K. M. Structural Basis for Inhibition of the Epidermal Growth Factor Receptor by Cetuximab Cancer Cell 2005, 7, 301-311
37. Voigt, M.; Braig, F.; Gothel, M.; Schulte, A.; Lamszus, K.; Bokemeyer, C.; Binder, M. Functional Dissection of the Epidermal Growth Factor Receptor Epitopes Targeted by Panitumumab and Cetuximab Neoplasia 2012, 14, 1023-1031
38. Schmiedel, J.; Blaukat, A.; Li, S.; Knochel, T.; Ferguson, K. M. Matuzumab Binding to Egfr Prevents the Conformational Rearrangement Required for Dimerization Cancer Cell 2008, 13, 365-373
39. Kowal, J.; Chami, M.; Baumgartner, P.; Arheit, M.; Chiu, P. L.; Rangl, M.; Scheuring, S.; Schroder, G. F.; Nimigean, C. M.; Stahlberg, H. Ligand-Induced Structural Changes in the Cyclic Nucleotide-Modulated Potassium Channel Mlok1 Nat. Commun. 2014, 5 3106
40. Remy, I.; Wilson, I. A.; Michnick, S. W. Erythropoietin Receptor Activation by a Ligand-Induced Conformation Change Science 1999, 283, 990-993
41. Roovers, R. C.; Vosjan, M. J.; Laeremans, T.; El Khoulati, R.; de Bruin, R. C.; Ferguson, K. M.; Verkleij, A. J.; van Dongen, G. A.; van Bergen en Henegouwen, P. M. A Biparatopic Anti-EGFR Nanobody Efficiently Inhibits Solid Tumour Growth Int. J. Cancer 2011, 129, 2013-2024
42. Schmitz, K. R.; Bagchi, A.; Roovers, R. C.; van Bergen en Henegouwen, P. M.; Ferguson, K. M. Structural Evaluation of Egfr Inhibition Mechanisms for Nanobodies/Vhh Domains Structure 2013, 21, 1214-1224
43. Sako, Y.; Minoghchi, S.; Yanagida, T. Single-Molecule Imaging of Egfr Signalling on the Surface of Living Cells Nat. Cell Biol. 2000, 2, 168-172
44. Clayton, A. H.; Orchard, S. G.; Nice, E. C.; Posner, R. G.; Burgess, A. W. Predominance of Activated EGFR Higher-Order Oligomers on the Cell Surface Growth Factors 2008, 26, 316-324
45. Hofman, E. G.; Bader, A. N.; Voortman, J.; van den Heuvel, D. J.; Sigismund, S.; Verkleij, A. J.; Gerritsen, H. C.; van Bergen en Henegouwen, P. M. Ligand-Induced EGF Receptor Oligomerization Is Kinase-Dependent and Enhances Internalization J. Biol. Chem. 2010, 285, 39481-39489
46. Teramura, Y.; Ichinose, J.; Takagi, H.; Nishida, K.; Yanagida, T.; Sako, Y. Single-Molecule Analysis of Epidermal Growth Factor Binding on the Surface of Living Cells EMBO J. 2006, 25, 4215-4222
47. Chung, I.; Akita, R.; Vandlen, R.; Toomre, D.; Schlessinger, J.; Mellman, I. Spatial Control of EGF Receptor Activation by Reversible Dimerization on Living Cells Nature 2010, 464, 783-787
48. Holbro, T.; Civenni, G.; Hynes, N. E. The Erbb Receptors and Their Role in Cancer Progression Exp. Cell Res. 2003, 284, 99-110
49. Behar, G.; Chames, P.; Teulon, I.; Cornillon, A.; Alshoukr, F.; Roquet, F.; Pugniere, M.; Teillaud, J. L.; Gruaz-Guyon, A.; Pelegrin, A. Llama Single-Domain Antibodies Directed against Nonconventional Epitopes of Tumor-Associated Carcinoembryonic Antigen Absent from Nonspecific Cross-Reacting Antigen FEBS J. 2009, 276, 3881-3893
50. Alvarez-Rueda, N.; Behar, G.; Ferre, V.; Pugniere, M.; Roquet, F.; Gastinel, L.; Jacquot, C.; Aubry, J.; Baty, D.; Barbet, J. Generation of Llama Single-Domain Antibodies against Methotrexate, a Prototypical Hapten Mol. Immunol. 2007, 44, 1680-1690
51. Even-Desrumeaux, K.; Baty, D.; Chames, P. Strong and Oriented Immobilization of Single Domain Antibodies from Crude Bacterial Lysates for High-Throughput Compatible Cost-Effective Antibody Array Generation Mol. BioSyst. 2010, 6, 2241-2248
52. Mathis, G. Rare Earth Cryptates and Homogeneous Fluoroimmunoassays with Human Sera Clin Chem. 1993, 39, 1953-1959