ErbB3-ErbB2 complexes as a therapeutic target in a subset of wild-type BRAF/NRAS cutaneous melanomas

Cancer Research

Volumn 75, Issue 17, 2015, Pages 3554-3567

  Capparelli, Claudia ^a   Rosenbaum, Sheera ^a   Berman Booty, Lisa D ^a,f   Salhi, Amel ^b   Gaborit, Nadège ^c   Zhan, Tingting ^a   Chervoneva, Inna ^a   Roszik, Jason ^d   Woodman, Scott E ^d   Davies, Michael A ^d   Setiady, Yulius Y ^e   Osman, Iman ^b   Yarden, Yosef ^c   Aplin, Andrew E ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^d UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^e ImmunoGen   (United States)

^f BRISTOL MYERS SQUIBB   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B RAF KINASE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; N (2,3 DIHYDROXYPROPOXY) 3,4 DIFLUORO 2 (2 FLUORO 4 IODOANILINO)BENZAMIDE; NEU DIFFERENTIATION FACTOR; ONCOPROTEIN; PERTUZUMAB; PROTEIN KINASE B; PROTEIN NRAS; UNCLASSIFIED DRUG; BRAF PROTEIN, HUMAN; ERBB2 PROTEIN, HUMAN; ERBB3 PROTEIN, HUMAN; GUANOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; MONOCLONAL ANTIBODY; NRAS PROTEIN, HUMAN; NRG1 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOCRINE EFFECT; BINDING AFFINITY; CELL GROWTH; CELL SURVIVAL; CELL VIABILITY; COHORT ANALYSIS; CONTROLLED STUDY; CUTANEOUS MELANOMA; DIMERIZATION; DRUG POTENTIATION; FEMALE; HOMOZYGOSITY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LIGAND BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SHORT TANDEM REPEAT; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; CELL PROLIFERATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; MELANOMA; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY; TUMOR CELL LINE;

ANTIBODIES, MONOCLONAL, HUMANIZED; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; GENE EXPRESSION REGULATION, NEOPLASTIC; GTP PHOSPHOHYDROLASES; HUMANS; MAP KINASE SIGNALING SYSTEM; MELANOMA; MEMBRANE PROTEINS; MOLECULAR TARGETED THERAPY; NEUREGULIN-1; PROTO-ONCOGENE PROTEINS B-RAF; RECEPTOR, ERBB-2; RECEPTOR, ERBB-3;

EID: 84942843632     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-2959     Document Type: Article

References (47)

1. Flaherty KT, Robert C, Hersey P, Nathan P, Garbe C, Milhem M, et al. Improved survival with MEK inhibition in BRAF-mutated melanoma. N Engl J Med 2012;367:107-14.
2. Flaherty KT, Infante JR, Daud A, Gonzalez R, Kefford RF, Sosman J, et al. Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations. N Engl J Med 2012;367:1694-703.
3. Das Thakur M, Stuart DD. Molecular pathways: response and resistance to BRAF and MEK inhibitors in BRAFV600E tumors. Clin Cancer Res 2013;20:1074-80.
4. Hartsough E, Shao Y, Aplin AE. Resistance to RAF inhibitors revisited. J Invest Dermatol 2014;134:319-25.
5. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with Ipilimumab in patients with metastatic melanoma. N Engl J Med 2010;363:711-23.
6. Hamid O, Robert C, Daud A, Hodi FS, Hwu WJ, Kefford R, et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma. N Engl J Med 2013;369:134-44.
7. Hodis E, Watson IR, Kryukov GV, Arold ST, Imielinski M, Theurillat JP, et al. A landscape of driver mutations in melanoma. Cell 2012;150:251-63.
8. Krauthammer M, Kong Y, Ha BH, Evans P, Bacchiocchi A, McCusker JP, et al. Exome sequencing identifies recurrent somatic RAC1 mutations in melanoma. Nat Genet 2012;44:1006-14.
9. Mar VJ, Wong SQ, Li J, Scolyer RA, McLean C, Papenfuss AT, et al. BRAF/ NRAS wild-type melanomas have a high mutation load correlating with histologic and molecular signatures of UV damage. Clin Cancer Res 2013; 19:4589-98.
10. Nissan MH, Pratilas CA, Jones AM, Ramirez R, Won H, Liu C, et al. Loss of NF1 in cutaneous melanoma is associated with RAS activation and MEK dependence. Cancer Res 2014;74:2340-50.
11. Guy PM, Platko JV, Cantley LC, Cerione RA, Carraway KL III. Insect cellexpressed p180erbB3 possesses an impaired tyrosine kinase activity. Proc Natl Acad Sci U S A 1994;91:8132-6.
12. Shi F, Telesco SE, Liu Y, Radhakrishnan R, Lemmon MA. ErbB3/HER3 intracellular domain is competent to bind ATP and catalyze autophosphorylation. Proc Natl Acad Sci U S A 2010;107:7692-7.
13. Berger MB, Mendrola JM, Lemmon MA. ErbB3/HER3 does not homodimerize upon neuregulin binding at the cell surface. FEBS Lett 2004; 569:332-6.
14. 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.
15. Pinkas-Kramarski R, Soussan L, Waterman H, Levkowitz G, Alroy I, Klapper L, et al. Diversification of Neu differentiation factor and epidermal growth factor signaling by combinatorial receptor interactions. EMBO J 1996;15: 2452-67.
16. Wallasch C, Weiss FU, Niederfellner G, Jallal B, Issing W, Ullrich A. Heregulin-dependent regulation of HER2/neu oncogenic signaling by heterodimerization with HER3. EMBO J 1995;14:4267-75.
17. 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.
18. Sheng Q, Liu X, Fleming E, Yuan K, Piao H, Chen J, et al. Anactivated ErbB3/ NRG1 autocrine loop supports in vivo proliferation in ovarian cancer cells. Cancer Cell 2010;17:298-310.
19. Yarden Y, Sliwkowski MX. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2001;2:127-37.
20. Buac K, Xu M, Cronin J, Weeraratna AT, Hewitt SM, Pavan WJ. NRG1 / ERBB3 signaling inmelanocyte development and melanoma: inhibition of differentiation and promotion of proliferation. Pigment Cell Melanoma Res 2009;22:773-84.
21. Reschke M, Mihic-Probst D, van der Horst EH, Knyazev P, Wild PJ, Hutterer M, et al. HER3 is a determinant for poor prognosis in melanoma. Clin Cancer Res 2008;14:5188-97.
22. Tworkoski K, Singhal G, Szpakowski S, Zito CI, Bacchiocchi A, Muthusamy V, et al. Phosphoproteomic screen identifies potential therapeutic targets in melanoma. Mol Cancer Res 2011;9:801-12.
23. Abel EV, Basile KJ, Kugel CH III, Witkiewicz AK, Le K, Amaravadi RK, et al. Melanoma adapts to RAF/MEK inhibitors by FOXD3-dependent upregulation of ERBB3 by FOXD3. J Clin Invest 2013;123:2155-68.
24. Wich LG, Hamilton HK, Shapiro RL, Pavlick A, Berman RS, Polsky D, et al. Developing a multidisciplinary prospective melanoma biospecimen repository to advance translational research. AmJ Trans Res 2009;1:35-43.
25. Gaborit N, Abdul-Hai A, Mancini M, Lindzen M, Lavi S, Leitner O, et al. Examination of HER3 targeting in cancer using monoclonal antibodies. Proc Natl Acad Sci U S A 2015;112:839-44.
26. Vasudevan KM, Barbie DA, Davies MA, Rabinovsky R, McNear CJ, Kim JJ, et al. AKT-independent signaling downstream of oncogenic PIK3CA mutations in human cancer. Cancer Cell 2009;16:21-32.
27. Park ES, Rabinovsky R, Carey M, Hennessy BT, Agarwal R, Liu W, et al. Integrative analysis of proteomic signatures, mutations, and drug responsiveness in theNCI 60 cancer cell line set. Mol Cancer Therap 2010;9:257-67.
28. Gopal YN, Deng W, Woodman SE, Komurov K, Ram P, Smith PD, et al. Basal and treatment-induced activation of AKT mediates resistance to cell death by AZD6244 (ARRY-142886) in Braf-mutant human cutaneous melanoma cells. Cancer Res 2010;70:8736-47.
29. Kaplan FM, Kugel CH, Dadpey N, Shao Y, Abel EV, Aplin AE. SHOC2 and CRAF mediate ERK1/2 reactivation inmutant NRAS-mediated resistance to RAF inhibitor. J Biol Chem 2012;287:41797-807.
30. Prickett TD, Agrawal NS, Wei X, Yates KE, Lin JC, Wunderlich JR, et al. Analysis of the tyrosine kinome in melanoma reveals recurrent mutations in ERBB4. Nat Genet 2009;41:1127-32.
31. Setiady YY, Skaletskaya A, Coccia J, Moreland J, Carrigan C, Rui L, et al. huHER3-8, a novel humanized anti-HER3 antibody that inhibits exogeneous ligand-independent proliferation of tumor cells [abstract]. In: Proceedings of the 102nd Annual Meeting of the American Association for Cancer Research; 2011 Apr 2-6; Orlando, FL. Philadelphia (PA): AACR; Cancer Res 2011;71(8 Suppl):Abstract nr 4564.
32. Sithanandam G, Anderson LM. The ERBB3 receptor in cancer and cancer gene therapy. Cancer Gene Ther 2008;15:413-48.
33. Silva JM, Bulman C, McMahon M. BRAFV600E cooperates with PI3K signaling, independent of AKT, to regulate melanoma cell proliferation. Mol Cancer Res 2014;12:447-63.
34. Kugel CH III, Hartsough EJ, Davies MA, Setiady YY, Aplin AE. Functionblocking ERBB3 antibody inhibits the adaptive response to RAF inhibitor. Cancer Res 2014;74:4122-32.
35. Hoek KS, Eichhoff OM, Schlegel NC, Dobbeling U, Kobert N, Schaerer L, et al. In vivo switching of humanmelanoma cells between proliferative and invasive states. Cancer Res 2008;68:650-6.
36. Zhang K, Wong P, Zhang L, Jacobs B, Borden EC, Aster JC, et al. A Notch1-neuregulin1 autocrine signaling loop contributes to melanoma growth. Oncogene 2012;31:4609-18.
37. 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 BRAF-mutant thyroid carcinomas. Cancer Discov 2013;3:520-33.
38. Mei L, Xiong WC. Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat Rev Neurosci 2008;9:437-52.
39. Soltoff SP, Carraway KL III, 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.
40. Kim HH, Vijapurkar U, Hellyer NJ, Bravo D, Koland JG. Signal transduction by epidermal growth factor and heregulin via the kinase-deficient ErbB3 protein. Biochem J 1998;334:189-95.
41. 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.
42. 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.
43. 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.
44. Liu J, Ray-Coquard IL, Selle F, Poveda A, Cibula D,Hirte HW, et al. A phase II randomized open-label study of MM-121, a fully human monoclonal antibody targeting ErbB3, in combination with weekly paclitaxel versus weekly paclitaxel in patients with platinum-resistant/ refractory ovarian cancers. J Clin Oncol 2014;32(suppl):5519.
45. Sequist LV, Chavez A, Doebele RC, Gray JE, Harb WA, Modiano MR, et al. A randomized phase 2 trial of MM-121, a fully human monoclonal antibody targeting ErbB3, in combination with erlotinib in EGFR wild-type NSCLC patients. J Clin Oncol 2014;32(suppl):8051.
46. Higgins MJ, Doyle C, Paepke S, Azaro A, Martin M, Semiglazov V, et al. A randomized, double-blind phase II trial of exemestane plus MM-121 (a monoclonal antibody targeting ErbB3) or placebo in postmenopausal women with locally advanced or metastatic ER+/PR+, HER2-negative breast cancer. J Clin Oncol 2014;32(suppl):587.
47. Baselga J, Cortes J, Kim SB, Im SA, Hegg R, Im YH, et al. Pertuzumab plus trastuzumab plus docetaxel for metastatic breast cancer. N Engl J Med 2012;366:109-19.