A Two-in-One Antibody against HER3 and EGFR Has Superior Inhibitory Activity Compared with Monospecific Antibodies

Cancer Cell

Volumn 20, Issue 4, 2011, Pages 472-486

  Schaefer, Gabriele ^a   Haber, Lauric ^a   Crocker, Lisa M ^a   Shia, Steven ^a   Shao, Lily ^a   Dowbenko, Donald ^a   Totpal, Klara ^a   Wong, Anne ^a   Lee, Chingwei V ^a   Stawicki, Scott ^a   Clark, Robyn ^a   Fields, Carter ^a   Lewis Phillips, Gail D ^a   Prell, Rodney A ^a   Danilenko, Dimitry M ^a   Franke, Yvonne ^a   Stephan, Jean Philippe ^a   Hwang, Jiyoung ^a   Wu, Yan ^a   Bostrom, Jenny ^a   Sliwkowski, Mark X ^a   Fuh, Germaine ^a   Eigenbrot, Charles ^a   more..

^a GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPITOPE; GEMCITABINE; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G1 MEHD 7945A; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY SPECIFICITY; ANTIGEN RECOGNITION; ARTICLE; BINDING AFFINITY; CELL GROWTH; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOTOXICITY; MACACA FASCICULARIS; MALE; MOUSE; NONHUMAN; PHAGE DISPLAY; PRIORITY JOURNAL; TUMOR XENOGRAFT;

EID: 80054765331     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2011.09.003     Document Type: Article

References (51)

1. Agus D.B., Akita R.W., Fox W.D., Lewis G.D., Higgins B., Pisacane P.I., Lofgren J.A., Tindell C., Evans D.P., Maiese K., et al. Targeting ligand-activated ErbB2 signaling inhibits breast and prostate tumor growth. Cancer Cell 2002, 2:127-137.
2. Bleeker W.K., Lammerts van Bueren J.J., van Ojik H.H., Gerritsen A.F., Pluyter M., Houtkamp M., Halk E., Goldstein J., Schuurman J., van Dijk M.A., et al. Dual mode of action of a human anti-epidermal growth factor receptor monoclonal antibody for cancer therapy. J. Immunol. 2004, 173:4699-4707.
3. Bostrom J., Yu S.F., Kan D., Appleton B.A., Lee C.V., Billeci K., Man W., Peale F., Ross S., Wiesmann C., Fuh G. Variants of the antibody herceptin that interact with HER2 and VEGF at the antigen binding site. Science 2009, 323:1610-1614.
4. Buck E., Eyzaguirre A., Haley J.D., Gibson N.W., Cagnoni P., Iwata K.K. Inactivation of Akt by the epidermal growth factor receptor inhibitor erlotinib is mediated by HER-3 in pancreatic and colorectal tumor cell lines and contributes to erlotinib sensitivity. Mol. Cancer Ther. 2006, 5:2051-2059.
5. Campbell M.R., Amin D., Moasser M.M. HER3 comes of age: new insights into its functions and role in signaling, tumor biology, and cancer therapy. Clin. Cancer Res. 2010, 16:1373-1383.
6. Carraway K.L., Sliwkowski M.X., Akita R., Platko J.V., Guy P.M., Nuijens A., Diamonti A.J., Vandlen R.L., Cantley L.C., Cerione R.A. The erbB3 gene product is a receptor for heregulin. J. Biol. Chem. 1994, 269:14303-14306.
7. Chames P., Baty D. Bispecific antibodies for cancer therapy. Curr. Opin. Drug Discov. Devel. 2009, 12:276-283.
8. Cho H.S., Leahy D.J. Structure of the extracellular region of HER3 reveals an interdomain tether. Science 2002, 297:1330-1333.
9. Chou T.C., Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv. Enzyme Regul. 1984, 22:27-55.
10. Ciardiello F., Tortora G. EGFR antagonists in cancer treatment. N. Engl. J. Med. 2008, 358:1160-1174.
11. Engelman J.A., Settleman J. Acquired resistance to tyrosine kinase inhibitors during cancer therapy. Curr. Opin. Genet. Dev. 2008, 18:73-79.
12. Engelman J.A., Jänne P.A., Mermel C., Pearlberg J., Mukohara T., Fleet C., Cichowski K., Johnson B.E., Cantley L.C. ErbB-3 mediates phosphoinositide 3-kinase activity in gefitinib-sensitive non-small cell lung cancer cell lines. Proc. Natl. Acad. Sci. USA 2005, 102:3788-3793.
13. Folprecht G., Tabernero J., Köhne C.H., Zacharchuk C., Paz-Ares L., Rojo F., Quinn S., Casado E., Salazar R., Abbas R., et al. Phase I pharmacokinetic/pharmacodynamic study of EKB-569, an irreversible inhibitor of the epidermal growth factor receptor tyrosine kinase, in combination with irinotecan, 5-fluorouracil, and leucovorin (FOLFIRI) in first-line treatment of patients with metastatic colorectal cancer. Clin. Cancer Res. 2008, 14:215-223.
14. Gessner J.E., Heiken H., Tamm A., Schmidt R.E. The IgG Fc receptor family. Ann. Hematol. 1998, 76:231-248.
15. Giaccone G. The role of gefitinib in lung cancer treatment. Clin. Cancer Res. 2004, 10:4233s-4237s.
16. Grothey A. EGFR antibodies in colorectal cancer: where do they belong?. J. Clin. Oncol. 2010, 28:4668-4670.
17. Herbst R.S., Prager D., Hermann R., Fehrenbacher L., Johnson B.E., Sandler A., Kris M.G., Tran H.T., Klein P., Li X., et al. TRIBUTE: a phase III trial of erlotinib hydrochloride (OSI-774) combined with carboplatin and paclitaxel chemotherapy in advanced non-small-cell lung cancer. J. Clin. Oncol. 2005, 23:5892-5899. TRIBUTE Investigator Group.
18. Hickinson D.M., Marshall G.B., Beran G.J., Varella-Garcia M., Mills E.A., South M.C., Cassidy A.M., Acheson K.L., McWalter G., McCormack R.M., et al. Identification of biomarkers in human head and neck tumor cell lines that predict for in vitro sensitivity to gefitinib. Clin. Transl. Sci. 2009, 2:183-192.
19. Hynes N.E., MacDonald G. ErbB receptors and signaling pathways in cancer. Curr. Opin. Cell Biol. 2009, 21:177-184.
20. Jain A., Penuel E., Mink S., Schmidt J., Hodge A., Favero K., Tindell C., Agus D.B. HER kinase axis receptor dimer partner switching occurs in response to EGFR tyrosine kinase inhibition despite failure to block cellular proliferation. Cancer Res. 2010, 70:1989-1999.
21. Jones R.B., Gordus A., Krall J.A., MacBeath G. A quantitative protein interaction network for the ErbB receptors using protein microarrays. Nature 2006, 439:168-174.
22. Junttila T.T., Parsons K., Olsson C., Lu Y., Xin Y., Theriault J., Crocker L., Pabonan O., Baginski T., Meng G., et al. Superior in vivo efficacy of afucosylated trastuzumab in the treatment of HER2-amplified breast cancer. Cancer Res. 2010, 70:4481-4489.
23. 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.
24. Jura N., Shan Y., Cao X., Shaw D.E., Kuriyan J. Structural analysis of the catalytically inactive kinase domain of the human EGF receptor 3. Proc. Natl. Acad. Sci. USA 2009, 106:21608-21613.
25. Kong A., Calleja V., Leboucher P., Harris A., Parker P.J., Larijani B. HER2 oncogenic function escapes EGFR tyrosine kinase inhibitors via activation of alternative HER receptors in breast cancer cells. PLoS ONE 2008, 3:e2881.
26. Lee C.V., Hymowitz S.G., Wallweber H.J., Gordon N.C., Billeci K.L., Tsai S.P., Compaan D.M., Yin J., Gong Q., Kelley R.F., et al. Synthetic anti-BR3 antibodies that mimic BAFF binding and target both human and murine B cells. Blood 2006, 108:3103-3111.
27. Lee C.V., Liang W.C., Dennis M.S., Eigenbrot C., Sidhu S.S., Fuh G. High-affinity human antibodies from phage-displayed synthetic Fab libraries with a single framework scaffold. J. Mol. Biol. 2004, 340:1073-1093.
28. 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.
29. Li T., Perez-Soler R. Skin toxicities associated with epidermal growth factor receptor inhibitors. Targeted Oncol. 2009, 4:107-119.
30. Lutterbuese R., Raum T., Kischel R., Hoffmann P., Mangold S., Rattel B., Friedrich M., Thomas O., Lorenczewski G., Rau D., et al. T cell-engaging BiTE antibodies specific for EGFR potently eliminate KRAS- and BRAF-mutated colorectal cancer cells. Proc. Natl. Acad. Sci. USA 2010, 107:12605-12610.
31. Lynch D.H., Yang X.D. Therapeutic potential of ABX-EGF: a fully human anti-epidermal growth factor receptor monoclonal antibody for cancer treatment. Semin. Oncol. 2002, 29(Suppl 4):47-50.
32. Lynch T.J., Bell D.W., Sordella R., Gurubhagavatula S., Okimoto R.A., Brannigan B.W., Harris P.L., Haserlat S.M., Supko J.G., Haluska F.G., et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N. Engl. J. Med. 2004, 350:2129-2139.
33. Moasser M.M. Targeting the function of the HER2 oncogene in human cancer therapeutics. Oncogene 2007, 26:6577-6592.
34. Olayioye M.A., Neve R.M., Lane H.A., Hynes N.E. The ErbB signaling network: receptor heterodimerization in development and cancer. EMBO J. 2000, 19:3159-3167.
35. Paez J.G., Janne P.A., Lee J.C., Tracy S., Greulich H., Gabriel S., Herman P., Kaye F.J., Lindeman N., Boggon T.J., et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004, 304:1497-1500.
36. Presta L.G. Engineering of therapeutic antibodies to minimize immunogenicity and optimize function. Adv. Drug Deliv. Rev. 2006, 58:640-656.
37. Prigent S.A., Gullick W.J. Identification of c-erbB-3 binding sites for phosphatidylinositol 3'-kinase and SHC using an EGF receptor/c-erbB-3 chimera. EMBO J. 1994, 13:2831-2841.
38. Ritter C.A., Perez-Torres M., Rinehart C., Guix M., Dugger T., Engelman J.A., Arteaga C.L. Human breast cancer cells selected for resistance to trastuzumab in vivo overexpress epidermal growth factor receptor and ErbB ligands and remain dependent on the ErbB receptor network. Clin. Cancer Res. 2007, 13:4909-4919.
39. Robak T. GA-101, a third-generation, humanized and glyco-engineered anti-CD20 mAb for the treatment of B-cell lymphoid malignancies. Curr. Opin. Investig. Drugs 2009, 10:588-596.
40. Schaefer G., Fitzpatrick V.D., Sliwkowski M.X. Gamma-heregulin: a novel heregulin isoform that is an autocrine growth factor for the human breast cancer cell line, MDA-MB-175. Oncogene 1997, 15:1385-1394.
41. Schaefer G., Shao L., Totpal K., Akita R.W. Erlotinib directly inhibits HER2 kinase activation and downstream signaling events in intact cells lacking epidermal growth factor receptor expression. Cancer Res. 2007, 67:1228-1238.
42. Schneider-Merck T., Lammerts van Bueren J.J., Berger S., Rossen K., van Berkel P.H., Derer S., Beyer T., Lohse S., Bleeker W.K., Peipp M., et al. Human IgG2 antibodies against epidermal growth factor receptor effectively trigger antibody-dependent cellular cytotoxicity but, in contrast to IgG1, only by cells of myeloid lineage. J. Immunol. 2010, 184:512-520.
43. Schoeberl B., Faber A.C., Li D., Liang M.C., Crosby K., Onsum M., Burenkova O., Pace E., Walton Z., Nie L., et al. An ErbB3 antibody, MM-121, is active in cancers with ligand-dependent activation. Cancer Res. 2010, 70:2485-2494.
44. Schoeberl B., Pace E.A., Fitzgerald J.B., Harms B.D., Xu L., Nie L., Linggi B., Kalra A., Paragas V., Bukhalid R., et al. Therapeutically targeting ErbB3: a key node in ligand-induced activation of the ErbB receptor-PI3K axis. Sci. Signal. 2009, 2:ra31.
45. Sliwkowski M.X., Schaefer G., Akita R.W., Lofgren J.A., Fitzpatrick V.D., Nuijens A., Fendly B.M., Cerione R.A., Vandlen R.L., Carraway K.L. Coexpression of erbB2 and erbB3 proteins reconstitutes a high affinity receptor for heregulin. J. Biol. Chem. 1994, 269:14661-14665.
46. Soltoff S.P., Carraway K.L., Prigent S.A., Gullick W.G., Cantley L.C. ErbB3 is involved in activation of phosphatidylinositol 3-kinase by epidermal growth factor. Mol. Cell. Biol. 1994, 14:3550-3558.
47. Tabernero J., Cervantes A., Rivera F., Martinelli E., Rojo F., von Heydebreck A., Macarulla T., Rodriguez-Braun E., Eugenia Vega-Villegas M., Senger S., et al. Pharmacogenomic and pharmacoproteomic studies of cetuximab in metastatic colorectal cancer: biomarker analysis of a phase I dose-escalation study. J. Clin. Oncol. 2010, 28:1181-1189.
48. Taylor R.J., Chan S.L., Wood A., Voskens C.J., Wolf J.S., Lin W., Chapoval A., Schulze D.H., Tian G., Strome S.E. FcgammaRIIIa polymorphisms and cetuximab induced cytotoxicity in squamous cell carcinoma of the head and neck. Cancer Immunol. Immunother. 2009, 58:997-1006.
49. Wheeler D.L., Huang S., Kruser T.J., Nechrebecki M.M., Armstrong E.A., Benavente S., Gondi V., Hsu K.T., Harari P.M. Mechanisms of acquired resistance to cetuximab: role of HER (ErbB) family members. Oncogene 2008, 27:3944-3956.
50. Yonesaka K., Zejnullahu K., Okamoto I., Satoh T., Cappuzzo F., Souglakos J., Ercan D., Rogers A., Roncalli M., Takeda M., et al. Activation of ERBB2 signaling causes resistance to the EGFR-directed therapeutic antibody cetuximab. Sci. Transl. Med. 2011, 3:99ra86.
51. Zhou B.B., Peyton M., He B., Liu C., Girard L., Caudler E., Lo Y., Baribaud F., Mikami I., Reguart N., et al. Targeting ADAM-mediated ligand cleavage to inhibit HER3 and EGFR pathways in non-small cell lung cancer. Cancer Cell 2006, 10:39-50.