Structural basis for eliciting a cytotoxic effect in HER2-overexpressing cancer cells via binding to the extracellular domain of HER2

Structure

Volumn 21, Issue 11, 2013, Pages 1979-1991

  Jost, Christian ^a   Schilling, Johannes ^a   Tamaskovic, Rastislav ^a   Schwill, Martin ^a   Honegger, Annemarie ^a   Plückthun, Andreas ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPITOPE; PERTUZUMAB; TRASTUZUMAB;

ARTICLE; CANCER CELL; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOTOXICITY; DIMERIZATION; DISSOCIATION CONSTANT; DISULFIDE BOND; EPITOPE MAPPING; GLYCOSYLATION; HYDROGEN BOND; INTERNALIZATION; PHAGE DISPLAY; PRIORITY JOURNAL; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION;

ANIMALS; ANKYRIN REPEAT; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS, HORMONAL; CELL LINE, TUMOR; CELL SURVIVAL; CRYSTALLOGRAPHY, X-RAY; EPITOPE MAPPING; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTOR, ERBB-2; RECOMBINANT FUSION PROTEINS; SF9 CELLS; SIGNAL TRANSDUCTION; SPODOPTERA;

EID: 84887412284     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.08.020     Document Type: Article

References (60)

1. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.W. Hung, G.J. Kapral, and R.W. Grosse-Kunstleve PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
2. K. Aertgeerts, R. Skene, J. Yano, B.C. Sang, H. Zou, G. Snell, A. Jennings, K. Iwamoto, N. Habuka, and A. Hirokawa Structural analysis of the mechanism of inhibition and allosteric activation of the kinase domain of HER2 protein J. Biol. Chem. 286 2011 18756 18765
3. A. Arkhipov, Y. Shan, R. Das, N.F. Endres, M.P. Eastwood, D.E. Wemmer, J. Kuriyan, and D.E. Shaw Architecture and membrane interactions of the EGF receptor Cell 152 2013 557 569
4. H.K. Binz, P. Amstutz, A. Kohl, M.T. Stumpp, C. Briand, P. Forrer, M.G. Grütter, and A. Plückthun High-affinity binders selected from designed ankyrin repeat protein libraries Nat. Biotechnol. 22 2004 575 582
5. E.V. Bocharov, M.L. Mayzel, P.E. Volynsky, M.V. Goncharuk, Y.S. Ermolyuk, A.A. Schulga, E.O. Artemenko, R.G. Efremov, and A.S. Arseniev Spatial structure and pH-dependent conformational diversity of dimeric transmembrane domain of the receptor tyrosine kinase EphA1 J. Biol. Chem. 283 2008 29385 29395
6. Y.L. Boersma, and A. Plückthun DARPins and other repeat protein scaffolds: advances in engineering and applications Curr. Opin. Biotechnol. 22 2011 849 857
7. J. Bostrom, S.F. Yu, D. Kan, B.A. Appleton, C.V. Lee, K. Billeci, W. Man, F. Peale, S. Ross, C. Wiesmann, and G. Fuh Variants of the antibody herceptin that interact with HER2 and VEGF at the antigen binding site Science 323 2009 1610 1614
8. S. Bouyain, P.A. Longo, S. Li, K.M. Ferguson, and D.J. Leahy The extracellular region of ErbB4 adopts a tethered conformation in the absence of ligand Proc. Natl. Acad. Sci. USA 102 2005 15024 15029
9. H.A. Burris III, J. Tibbitts, S.N. Holden, M.X. Sliwkowski, and G.D. Lewis Phillips Trastuzumab emtansine (T-DM1): a novel agent for targeting HER2+ breast cancer Clin. Breast Cancer 11 2011 275 282
10. CCP4 (Collaborative Computational Project, Number 4) The CCP4 suite: programs for protein crystallography Acta Crystallogr. D Biol. Crystallogr. 50 1994 760 763
11. H.S. Cho, and D.J. Leahy Structure of the extracellular region of HER3 reveals an interdomain tether Science 297 2002 1330 1333
12. H.S. Cho, K. Mason, K.X. Ramyar, A.M. Stanley, S.B. Gabelli, D.W. Denney Jr., and D.J. Leahy Structure of the extracellular region of HER2 alone and in complex with the Herceptin Fab Nature 421 2003 756 760
13. M.A. Cobleigh, C.L. Vogel, D. Tripathy, N.J. Robert, S. Scholl, L. Fehrenbacher, J.M. Wolter, V. Paton, S. Shak, G. Lieberman, and D.J. Slamon Multinational study of the efficacy and safety of humanized anti-HER2 monoclonal antibody in women who have HER2-overexpressing metastatic breast cancer that has progressed after chemotherapy for metastatic disease J. Clin. Oncol. 17 1999 2639 2648
14. R.J. Craven, H. Lightfoot, and W.G. Cance A decade of tyrosine kinases: from gene discovery to therapeutics Surg. Oncol. 12 2003 39 49
15. I.W. Davis, A. Leaver-Fay, V.B. Chen, J.N. Block, G.J. Kapral, X. Wang, L.W. Murray, W.B. Arendall III, J. Snoeyink, J.S. Richardson, and D.C. Richardson MolProbity: all-atom contacts and structure validation for proteins and nucleic acids Nucleic Acids Res. 35 Web Server issue 2007 W375-83
16. J.P. Dawson, Z. Bu, and M.A. Lemmon Ligand-induced structural transitions in ErbB receptor extracellular domains Structure 15 2007 942 954
17. B. Dreier, A. Honegger, C. Hess, G. Nagy-Davidescu, P.R. Mittl, M.G. Grütter, N. Belousova, G. Mikheeva, V. Krasnykh, and A. Plückthun Development of a generic adenovirus delivery system based on structure-guided design of bispecific trimeric DARPin adapters Proc. Natl. Acad. Sci. USA 110 2013 E869 E877
18. C. Eigenbrot, M. Ultsch, A. Dubnovitsky, L. Abrahmsén, and T. Härd Structural basis for high-affinity HER2 receptor binding by an engineered protein Proc. Natl. Acad. Sci. USA 107 2010 15039 15044
19. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
20. N.F. Endres, R. Das, A.W. Smith, A. Arkhipov, E. Kovacs, Y. Huang, J.G. Pelton, Y. Shan, D.E. Shaw, and D.E. Wemmer Conformational coupling across the plasma membrane in activation of the EGF receptor Cell 152 2013 543 556
21. A.C. Faber, K.K. Wong, and J.A. Engelman Differences underlying EGFR and HER2 oncogene addiction Cell Cycle 9 2010 851 852
22. K.M. Ferguson, M.B. Berger, J.M. Mendrola, H.S. Cho, D.J. Leahy, and M.A. Lemmon EGF activates its receptor by removing interactions that autoinhibit ectodomain dimerization Mol. Cell 11 2003 507 517
23. R.S. Finn, and D.J. Slamon Monoclonal antibody therapy for breast cancer: herceptin Cancer Chemother. Biol. Response Modif. 21 2003 223 233
24. R.D. Fisher, M. Ultsch, A. Lingel, G. Schaefer, L. Shao, S. Birtalan, S.S. Sidhu, and C. Eigenbrot Structure of the complex between HER2 and an antibody paratope formed by side chains from tryptophan and serine J. Mol. Biol. 402 2010 217 229
25. D.J. Fitzgerald, P. Berger, C. Schaffitzel, K. Yamada, T.J. Richmond, and I. Berger Protein complex expression by using multigene baculoviral vectors Nat. Methods 3 2006 1021 1032
26. M.C. Franklin, K.D. Carey, F.F. Vajdos, D.J. Leahy, A.M. de Vos, and M.X. Sliwkowski Insights into ErbB signaling from the structure of the ErbB2-pertuzumab complex Cancer Cell 5 2004 317 328
27. D. Gajria, and S. Chandarlapaty HER2-amplified breast cancer: mechanisms of trastuzumab resistance and novel targeted therapies Expert Rev. Anticancer Ther. 11 2011 263 275
28. T.P. Garrett, N.M. McKern, M. Lou, T.C. Elleman, T.E. Adams, G.O. Lovrecz, M. Kofler, R.N. Jorissen, E.C. Nice, A.W. Burgess, and C.W. Ward The crystal structure of a truncated ErbB2 ectodomain reveals an active conformation, poised to interact with other ErbB receptors Mol. Cell 11 2003 495 505
29. R. Ghosh, A. Narasanna, S.E. Wang, S. Liu, A. Chakrabarty, J.M. Balko, A.M. González-Angulo, G.B. Mills, E. Penuel, and J. Winslow Trastuzumab has preferential activity against breast cancers driven by HER2 homodimers Cancer Res. 71 2011 1871 1882
30. M. Hollmén, P. Liu, K. Kurppa, H. Wildiers, I. Reinvall, T. Vandorpe, A. Smeets, K. Deraedt, T. Vahlberg, and H. Joensuu Proteolytic processing of ErbB4 in breast cancer PLoS ONE 7 2012 e39413
31. G. Interlandi, S.K. Wetzel, G. Settanni, A. Plückthun, and A. Caflisch Characterization and further stabilization of designed ankyrin repeat proteins by combining molecular dynamics simulations and experiments J. Mol. Biol. 375 2008 837 854
32. T. Ishikawa, M. Seto, H. Banno, Y. Kawakita, M. Oorui, T. Taniguchi, Y. Ohta, T. Tamura, A. Nakayama, and H. Miki Design and synthesis of novel human epidermal growth factor receptor 2 (HER2)/epidermal growth factor receptor (EGFR) dual inhibitors bearing a pyrrolo[3,2-d]pyrimidine scaffold J. Med. Chem. 54 2011 8030 8050
33. T.T. Junttila, R.W. Akita, K. Parsons, C. Fields, G.D. Lewis Phillips, L.S. Friedman, D. Sampath, and M.X. Sliwkowski Ligand-independent HER2/HER3/PI3K complex is disrupted by trastuzumab and is effectively inhibited by the PI3K inhibitor GDC-0941 Cancer Cell 15 2009 429 440
34. W. Kabsch Xds Acta Crystallogr. D Biol. Crystallogr. 66 2010 125 132
35. 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
36. P. Liu, S. Bouyain, C. Eigenbrot, and D.J. Leahy The ErbB4 extracellular region retains a tethered-like conformation in the absence of the tether Protein Sci. 21 2012 152 155
37. P. Martin-Killias, N. Stefan, S. Rothschild, A. Plückthun, and U. Zangemeister-Wittke A novel fusion toxin derived from an EpCAM-specific designed ankyrin repeat protein has potent antitumor activity Clin. Cancer Res. 17 2011 100 110
38. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Cryst. 40 2007 658 674
39. L.Z. Mi, C. Lu, Z. Li, N. Nishida, T. Walz, and T.A. Springer Simultaneous visualization of the extracellular and cytoplasmic domains of the epidermal growth factor receptor Nat. Struct. Mol. Biol. 18 2011 984 989
40. M.M. Moasser The oncogene HER2: its signaling and transforming functions and its role in human cancer pathogenesis Oncogene 26 2007 6469 6487
41. R.C. Münch, M.D. Mühlebach, T. Schaser, S. Kneissl, C. Jost, A. Plückthun, K. Cichutek, and C.J. Buchholz DARPins: an efficient targeting domain for lentiviral vectors Mol. Ther. 19 2011 686 693
42. H. Ogiso, R. Ishitani, O. Nureki, S. Fukai, M. Yamanaka, J.H. Kim, K. Saito, A. Sakamoto, M. Inoue, M. Shirouzu, and S. Yokoyama Crystal structure of the complex of human epidermal growth factor and receptor extracellular domains Cell 110 2002 775 787
43. V. Ramamurthy, S.R. Krystek Jr., A. Bush, A. Wei, S.L. Emanuel, R. Das Gupta, A. Janjua, L. Cheng, M. Murdock, and B. Abramczyk Structures of adnectin/protein complexes reveal an expanded binding footprint Structure 20 2012 259 269
44. G. Schaefer, V.D. Fitzpatrick, and M.X. Sliwkowski Gamma-heregulin: a novel heregulin isoform that is an autocrine growth factor for the human breast cancer cell line, MDA-MB-175 Oncogene 15 1997 1385 1394
45. N.V. Sergina, M. Rausch, D. Wang, J. Blair, B. Hann, K.M. Shokat, and M.M. Moasser Escape from HER-family tyrosine kinase inhibitor therapy by the kinase-inactive HER3 Nature 445 2007 437 441
46. M. Simon, U. Zangemeister-Wittke, and A. Plückthun Facile double-functionalization of designed ankyrin repeat proteins using click and thiol chemistries Bioconjug. Chem. 23 2012 279 286
47. M.X. Sliwkowski, G. Schaefer, R.W. Akita, J.A. Lofgren, V.D. Fitzpatrick, A. Nuijens, B.M. Fendly, R.A. Cerione, R.L. Vandlen, and K.L. Carraway III Coexpression of erbB2 and erbB3 proteins reconstitutes a high affinity receptor for heregulin J. Biol. Chem. 269 1994 14661 14665
48. M.X. Sliwkowski, J.A. Lofgren, G.D. Lewis, T.E. Hotaling, B.M. Fendly, and J.A. Fox Nonclinical studies addressing the mechanism of action of trastuzumab (Herceptin) Semin. Oncol. 26 4, Suppl 12 1999 60 70
49. D. Steiner, P. Forrer, and A. Plückthun Efficient selection of DARPins with sub-nanomolar affinities using SRP phage display J. Mol. Biol. 382 2008 1211 1227
50. R. Tamaskovic, M. Simon, N. Stefan, M. Schwill, and A. Plückthun Designed ankyrin repeat proteins (DARPins) from research to therapy Methods Enzymol. 503 2012 101 134
51. J.P. Theurillat, B. Dreier, G. Nagy-Davidescu, B. Seifert, S. Behnke, U. Zürrer-Härdi, F. Ingold, A. Plückthun, and H. Moch Designed ankyrin repeat proteins: a novel tool for testing epidermal growth factor receptor 2 expression in breast cancer Mod. Pathol. 23 2010 1289 1297
52. S. Verma, D. Miles, L. Gianni, I.E. Krop, M. Welslau, J. Baselga, M. Pegram, D.Y. Oh, V. Diéras, E. Guardino EMILIA Study Group Trastuzumab emtansine for HER2-positive advanced breast cancer N. Engl. J. Med. 367 2012 1783 1791
53. S.E. Webb, S.K. Roberts, S.R. Needham, C.J. Tynan, D.J. Rolfe, M.D. Winn, D.T. Clarke, R. Barraclough, and M.L. Martin-Fernandez Single-molecule imaging and fluorescence lifetime imaging microscopy show different structures for high- and low-affinity epidermal growth factor receptors in A431 cells Biophys. J. 94 2008 803 819
54. S.K. Wetzel, C. Ewald, G. Settanni, S. Jurt, A. Plückthun, and O. Zerbe Residue-resolved stability of full-consensus ankyrin repeat proteins probed by NMR J. Mol. Biol. 402 2010 241 258
55. W. Xia, L.H. Liu, P. Ho, and N.L. Spector Truncated ErbB2 receptor (p95ErbB2) is regulated by heregulin through heterodimer formation with ErbB3 yet remains sensitive to the dual EGFR/ErbB2 kinase inhibitor GW572016 Oncogene 23 2004 646 653
56. Y. Yarden, and M.X. Sliwkowski Untangling the ErbB signalling network Nat. Rev. Mol. Cell Biol. 2 2001 127 137
57. C. Zahnd, E. Wyler, J.M. Schwenk, D. Steiner, M.C. Lawrence, N.M. McKern, F. Pecorari, C.W. Ward, T.O. Joos, and A. Plückthun A designed ankyrin repeat protein evolved to picomolar affinity to Her2 J. Mol. Biol. 369 2007 1015 1028
58. C. Zahnd, M. Kawe, M.T. Stumpp, C. de Pasquale, R. Tamaskovic, G. Nagy-Davidescu, B. Dreier, R. Schibli, H.K. Binz, R. Waibel, and A. Plückthun Efficient tumor targeting with high-affinity designed ankyrin repeat proteins: effects of affinity and molecular size Cancer Res. 70 2010 1595 1605
59. Q. Zhang, E. Park, K. Kani, and R. Landgraf Functional isolation of activated and unilaterally phosphorylated heterodimers of ERBB2 and ERBB3 as scaffolds in ligand-dependent signaling Proc. Natl. Acad. Sci. USA 109 2012 13237 13242
60. H. Zhou, Z. Zha, Y. Liu, H. Zhang, J. Zhu, S. Hu, G. Shen, L. Cheng, L. Niu, and M.I. Greene Structural insights into the down-regulation of overexpressed p185(her2/neu) protein of transformed cells by the antibody chA21 J. Biol. Chem. 286 2011 31676 31683