ERBB3/HER2 signaling promotes resistance to EGFR blockade in head and neck and colorectal cancer models

Molecular Cancer Therapeutics

Volumn 13, Issue 5, 2014, Pages 1345-1355

  Zhang, Li ^a   Castanaro, Carla ^a   Luan, Bo ^a   Yang, Katie ^a   Fan, Liangfen ^a   Fairhurst, Jeanette L ^a   Rafique, Ashique ^a   Potocky, Terra B ^a   Shan, Jing ^a   Delfino, Frank J ^a   Shi, Ergang ^a   Huang, Tammy ^a   Martin, Joel H ^a   Chen, Gang ^a   MacDonald, Douglas ^a   Rudge, John S ^a   Thurston, Gavin ^a   Daly, Christopher ^a  

^a REGENERON PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BLOCKING ANTIBODY; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; NEU DIFFERENTIATION FACTOR; PROTEIN TYROSINE KINASE; REGN1400; REGN955; UNCLASSIFIED DRUG; MONOCLONAL ANTIBODY; PROTEIN BINDING; PROTEIN KINASE B;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER GROWTH; CANCER INHIBITION; CELL GROWTH ASSAY; CELL LYSATE; COLORECTAL CANCER; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; HUMAN CELL; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; COLORECTAL NEOPLASMS; DISEASE MODEL; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; HEAD AND NECK NEOPLASMS; METABOLISM; MOUSE; PATHOLOGY; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; ANTIBODIES, BLOCKING; ANTIBODIES, MONOCLONAL; ANTIBODIES, MONOCLONAL, HUMANIZED; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; HEAD AND NECK NEOPLASMS; HUMANS; MICE; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; RECEPTOR, ERBB-3; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84899808225     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-13-1033     Document Type: Article

References (38)

1. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW, 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;350:2129-39.
2. Paez JG, Janne PA, Lee JC, Tracy S, Greulich H, Gabriel S, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004;304:1497-500.
3. Bonner JA, Harari PM, Giralt J, Azarnia N, Shin DM, Cohen RB, et al. Radiotherapy plus cetuximab for squamous-cell carcinoma of the head and neck. N Engl J Med 2006;354:567-78.
4. Cunningham D, Humblet Y, Siena S, Khayat D, Bleiberg H, Santoro A, et al. Cetuximab monotherapy and cetuximab plus irinotecan in irinotecan- refractory metastatic colorectal cancer. N Engl J Med 2004; 351:337-45.
5. Jonker DJ, O'Callaghan CJ, Karapetis CS, Zalcberg JR, Tu D, Au HJ, et al. Cetuximab for the treatment of colorectal cancer. N Engl J Med 2007;357:2040-8.
6. Van Cutsem E, Kohne CH, Hitre E, Zaluski J, Chang Chien CR, Makhson A, et al. Cetuximab and chemotherapy as initial treatment for metastatic colorectal cancer. N Engl J Med 2009;360: 1408-17.
7. Van Cutsem E, Peeters M, Siena S, Humblet Y, Hendlisz A, Neyns B, et al. Open-label phase III trial of panitumumab plus best supportive care compared with best supportive care alone in patients with chemotherapy-refractory metastatic colorectal cancer. J Clin Oncol 2007;25:1658-64.
8. Douillard JY, Oliner KS, Siena S, Tabernero J, Burkes R, Barugel M, et al. Panitumumab-FOLFOX4 treatment and RAS mutations in colorectal cancer. N Engl J Med 2013;369:1023-34.
9. Vermorken JB, Trigo J, Hitt R, Koralewski P, Diaz-Rubio E, Rolland F, et al. Open-label, uncontrolled, multicenter phase II study to evaluate the efficacy and toxicity of cetuximab as a single agent in patients with recurrent and/or metastatic squamous cell carcinoma of the head and neck who failed to respond to platinum-based therapy. J Clin Oncol 2007;25:2171-7.
10. Abel EV, Basile KJ, Kugel CH 3rd, Witkiewicz AK, Le K, Amaravadi RK, et al. Melanoma adapts to RAF/MEK inhibitors through FOXD3-mediated upregulation of ERBB3. J Clin Invest 2013;123:2155-68.
11. Chakrabarty A, Sanchez V, Kuba MG, Rinehart C, Arteaga CL. Feedback upregulation of HER3 (ErbB3) expression and activity attenuates antitumor effect of PI3K inhibitors. Proc Natl Acad Sci U S A 2012;109:2718-23.
12. Engelman JA, Zejnullahu K, Mitsudomi T, Song Y, Hyland C, Park JO, et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007;316:1039-43.
13. Garrett JT, Olivares MG, Rinehart C, Granja-Ingram ND, Sanchez V, Chakrabarty A, et al. Transcriptional and posttranslational up-regulation of HER3 (ErbB3) compensates for inhibition of the HER2 tyrosine kinase. Proc Natl Acad Sci U S A 2011;108:5021-6.
14. Montero-Conde C, Ruiz-Llorente S, Dominguez JM, Knauf JA, Viale A, Sherman EJ, et al. Relief of feedback inhibition of HER3 transcription by RAF and MEK inhibitors attenuates their antitumor effects in BRAFmutant thyroid carcinomas. Cancer Discov 2013;3:520-33.
15. Schoeberl B, Faber AC, Li D, Liang MC, Crosby K, Onsum M, et al. An ErbB3 antibody, MM-121, is active in cancers with ligand-dependent activation. Cancer Res 2010;70:2485-94.
16. Sergina NV, Rausch M, Wang D, Blair J, Hann B, Shokat KM, et al. Escape from HER-family tyrosine kinase inhibitor therapy by the kinase-inactive HER3. Nature 2007;445:437-41.
17. Wheeler DL, Huang S, Kruser TJ, Nechrebecki MM, Armstrong EA, Benavente S, et al. Mechanisms of acquired resistance to cetuximab: role of HER (ErbB) family members. Oncogene 2008;27:3944-56.
18. Baselga J, Swain SM. Novel anticancer targets: revisiting ERBB2 and discovering ERBB3. Nat Rev Cancer 2009;9:463-75.
19. Yarden Y, Pines G. The ERBB network: at last, cancer therapy meets systems biology. Nat Rev Cancer 2012;12:553-63.
20. Engelman JA, Janne PA, Mermel C, Pearlberg J, Mukohara T, Fleet C, et al. ErbB-3 mediates phosphoinositide 3-kinase activity in gefitinibsensitive non-small cell lung cancer cell lines. Proc Natl Acad Sci U S A 2005;102:3788-93.
21. Holbro T, Beerli RR, Maurer F, Koziczak M, Barbas CF 3rd, Hynes NE. The ErbB2/ErbB3 heterodimer functions as an oncogenic unit: ErbB2 requires ErbB3 to drive breast tumor cell proliferation. Proc Natl Acad Sci U S A 2003;100:8933-8.
22. Soltoff SP, Carraway KL 3rd, Prigent SA, Gullick WG, Cantley LC. ErbB3 is involved in activation of phosphatidylinositol 3-kinase by epidermal growth factor. Mol Cell Biol 1994;14:3550-8.
23. Yonesaka K, Zejnullahu K, Okamoto I, Satoh T, Cappuzzo F, Souglakos J, et al. Activation of ERBB2 signaling causes resistance to the EGFR-directed therapeutic antibody cetuximab. Sci Transl Med 2011; 3:99ra86.
24. Schaefer G, Haber L, Crocker LM, Shia S, Shao L, Dowbenko D, et al. A two-in-one antibody against HER3 and EGFR has superior inhibitory activity compared with monospecific antibodies. Cancer Cell 2011; 20:472-86.
25. Garner AP, Bialucha CU, Sprague ER, Garrett JT, Sheng Q, Li S, et al. An antibody that locks HER3 in the inactive conformation inhibits tumor growth driven by HER2 or neuregulin. Cancer Res 2013;73: 6024-35.
26. Huang S, Li C, Armstrong EA, Peet CR, Saker J, Amler LC, et al. Dual targeting of EGFR and HER3 with MEHD7945A overcomes acquired resistancetoEGFRinhibitorsandradiation. CancerRes2013;73:824-33.
27. Wilson TR, Lee DY, Berry L, Shames DS, Settleman J. Neuregulin-1- mediated autocrine signaling underlies sensitivity to HER2 kinase inhibitors in a subset of human cancers. Cancer Cell 2011;20:158-72.
28. Shames DS, Carbon J, Walter K, Jubb AM, Kozlowski C, Januario T, et al. High heregulin expression is associated with activated HER3 and may define an actionable biomarker in patients with squamous cell carcinomas of the head and neck. PLoS ONE 2013;8:e56765.
29. Lemmon MA. Ligand-induced ErbB receptor dimerization. Exp Cell Res 2009;315:638-48.
30. Graus-Porta D, Beerli RR, Daly JM, Hynes NE. ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J 1997;16:1647-55.
31. Tzahar E, Waterman H, Chen X, Levkowitz G, Karunagaran D, Lavi S, et al. A hierarchical network of interreceptor interactions determines signal transduction by Neu differentiation factor/neuregulin and epidermal growth factor. Mol Cell Biol 1996;16:5276-87.
32. Adams CW, Allison DE, Flagella K, Presta L, Clarke J, Dybdal N, et al. Humanization of a recombinant monoclonal antibody to produce a therapeutic HER dimerization inhibitor, pertuzumab. Cancer Immunol Immunother 2006;55:717-27.
33. Zhang Q, Park E, Kani K, Landgraf R. Functional isolation of activated and unilaterally phosphorylated heterodimers of ERBB2 and ERBB3 as scaffolds in ligand-dependent signaling. Proc Natl Acad Sci U S A 2012;109:13237-42.
34. Cervantes A, Juric D, Hidalgo M, Messersmith W, Blumenschein G, Baselga J, et al. Aphase I study ofMEHD7945A(MEHD), a first-in-class HER3/EGFR dual-action antibody, in patients (pts) with refractory/ recurrent epithelial tumors: expansion cohorts. J Clin Oncol 2012; 30:15s.
35. Jaiswal BS, Kljavin NM, Stawiski EW, Chan E, Parikh C, Durinck S, et al. Oncogenic ERBB3 mutations in human cancers. Cancer Cell 2013; 23:603-17.
36. Mirschberger C, Schiller CB, Schraml M, Dimoudis N, Friess T, Gerdes CA, et al. RG7116, a therapeutic antibody that binds the inactive HER3 receptor and is optimized for immune effector activation. Cancer Res 2013;73:5183-94.
37. Schoeberl B, Pace EA, Fitzgerald JB, Harms BD, Xu L, Nie L, et al. Therapeutically targeting ErbB3: a key node in ligand-induced activation of the ErbB receptor-PI3K axis. Sci Signal 2009;2: ra31.
38. LoRusso P, Janne PA, Oliveira M, Rizvi N, Malburg L, Keedy V, et al. Phase I study of U3-1287, a fully human anti-HER3 monoclonal antibody, in patients with advanced solid tumors. Clin Cancer Res 2013;19:3078-87.