Therapeutically targeting ErbB3: A key node in ligand-induced activation of the ErbB receptor-PI3K axis

Science Signaling

Volumn 2, Issue 77, 2009, Pages

  Schoeberl, Birgit ^a   Pace, Emily A ^a   Fitzgerald, Jonathan B ^a   Harms, Brian D ^a   Xu, Lihui ^a   Nie, Lin ^a   Linggi, Bryan ^a   Kalra, Ashish ^a   Paragas, Violette ^a   Bukhalid, Raghida ^a   Grantcharova, Viara ^a   Kohli, Neeraj ^a   West, Kip A ^a   Leszczyniecka, Magdalena ^a   Feldhaus, Michael J ^a   Kudla, Arthur J ^a   Nielsen, Ulrik B ^a  

^a MERRIMACK PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETACELLULIN; CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 3; HEREGULIN 1 BETA; LAPATINIB; LIGAND; MM 121; MONOCLONAL ANTIBODY; NEU DIFFERENTIATION FACTOR; PERTUZUMAB; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TRASTUZUMAB; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INHIBITION; CONTROLLED STUDY; DRUG DOSE COMPARISON; DRUG MECHANISM; ENZYME ACTIVATION; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; KIDNEY CARCINOMA; LUNG ADENOCARCINOMA; MATHEMATICAL MODEL; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; SIMULATION; SOLID TUMOR; TUMOR XENOGRAFT; ANIMAL; IMMUNOLOGY; METABOLISM; MOUSE; PHOSPHORYLATION; XENOGRAFT;

MUS;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANTIBODIES, MONOCLONAL; HUMANS; LIGANDS; MICE; PHOSPHORYLATION; PROTEIN BINDING; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-3; SIGNAL TRANSDUCTION; TRANSPLANTATION, HETEROLOGOUS;

EID: 69849115198     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2000352     Document Type: Article

References (76)

1. N. E. Hynes, Targeting ERBB receptors in cancer. Recent Results Cancer Res. 172, 45-57 (2007).
2. T. Holbro, G. Civenni, N. E. Hynes, The ErbB receptors and their role in cancer progression. Exp. Cell Res. 284, 99-110 (2003).
3. S. Britsch, L. Li, S. Kirchhoff, F. Theuring, V. Brinkmann, C. Birchmeier, D. Riethmacher, The ErbB2 and ErbB3 receptors and their ligand, neuregulin-1, are essential for development of the sympathetic nervous system. Genes Dev. 12, 1825-1836 (1998).
4. E. M. Bublil, Y. Yarden, The EGF receptor family: Spearheading a merger of signaling and therapeutics. Curr. Opin. Cell Biol. 19, 124-134 (2007).
5. N. E. Hynes, H. A. Lane, ERBB receptors and cancer: The complexity of targeted inhibitors. Nat. Rev. Cancer 5, 341-354 (2005).
6. W. Pao, V. Miller, M. Zakowski, J. Doherty, K. Politi, I. Sarkaria, B. Singh, R. Heelan, V. Rusch, L. Fulton, E. Mardis, D. Kupfer, R. Wilson, M. Kris, H. Varmus, EGF receptor gene mutations are common in lung cancers from "never smokers" and are associated with sensitivity of tumors to gefitinib and erlotinib. Proc. Natl. Acad. Sci. U.S.A. 101, 13306-13311 (2004).
7. Y. Yarden, The EGFR family and its ligands in human cancer: Signalling mechanisms and therapeutic opportunities. Eur. J. Cancer 37 (Suppl. 4), S3-S8 (2001).
8. Y. Yarden, M. X. Sliwkowski, Untangling the ErbB signalling network, Nat. Rev. Mol. Cell Biol. 2, 127-137 (2001).
9. A. Citri, Y. Yarden, EGF-ERBB signalling: Towards the systems level. Nat. Rev. Mol. Cell Biol. 7, 505-516 (2006).
10. A. Citri, K. B. Skaria, Y. Yarden, The deaf and the dumb: The biology of ErbB-2 and ErbB-3. Exp. Cell Res. 284, 54-65 (2003).
11. T. Holbro, R. R. Beerli, F. Maurer, M. Koziczak, C. F. Barbas III, N. E. Hynes, 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. 100, 8933-8938 (2003).
12. H. S. Wiley, Trafficking of the ErbB receptors and its influence on signaling. Exp. Cell Res. 284, 78-88 (2003).
13. S. F. Wong, Cetuximab: An epidermal growth factor receptor monoclonal antibody for the treatment of colorectal cancer, Clin. Ther. 27, 684-694 (2005).
14. E. E. Vokes, E. Chu, Anti-EGFR therapies: Clinical experience in colorectal, lung, and head and neck cancers. Oncology (Williston Park) 20, 15-25 (2006).
15. B. N. Kholodenko, O. V. Demin, G. Moehren, J. B. Hoek, Quantification of short termsignaling by the epidermal growth factor receptor. J. Biol. Chem. 274, 30169-30181 (1999).
16. M. Hatakeyama, S. Kimura, T. Naka, T. Kawasaki, N. Yumoto, M. Ichikawa, J. H. Kim, K. Saito, M. Saeki, M. Shirouzu, S. Yokoyama, A. Konagaya, A computational model on the modulation of mitogen-activated protein kinase (MAPK) and Akt pathways in heregulin-induced ErbB signalling. Biochem. J. 373, 451-463 (2003).
17. B. Schoeberl, C. Eichler-Jonsson, E. D. Gilles, G. Můller, Computational modeling of the dynamics of the MAP kinase cascade activated by surface and internalized EGF receptors. Nat. Biotechnol. 20, 370-375 (2002).
18. M. R. Birtwistle, M. Hatakeyama, N. Yumoto, B. A. Ogunnaike, J. B. Hoek, B. N. Kholodenko, Ligand-dependent responses of the ErbB signaling network: Experimental and modeling analyses. Mol. Syst. Biol. 3, 144 (2007).
19. B. S. Hendriks, J. Cook, J. M. Burke, J. M. Beusmans, D. A. Lauffenburger, D. de Graaf, Computational modelling of ErbB family phosphorylation dynamics in response to transforming growth factor alpha and heregulin indicates spatial compartmentation of phosphatase activity. Syst. Biol. (Stevenage) 153, 22-33 (2006).
20. H.S.Wiley, J. J. Herbst, B. J. Walsh, D. A. Lauffenburger, M.G.Rosenfeld,G.N.Gill, The role of tyrosine kinase activity in endocytosis, compartmentation, and down-regulation of the epidermal growth factor receptor. J. Biol. Chem. 266, 11083-11094 (1991).
21. W. W. Chen, B. Schoeberl, P. J. Jasper, M. Niepel, U. B. Nielsen, D. A. Lauffenburger, P. K. Sorger, Input-output behavior of ErbB signaling pathways as revealed by a mass action model trained against dynamic data. Mol. Syst. Biol. 5, 239 (2009).
22. S. Y. Shvartsman, M. P. Hagan, A. Yacoub, P. Dent, H. S. Wiley, D. A. Lauffenburger, Autocrine loops with positive feedback enable context-dependent cell signaling. Am. J. Physiol. Cell Physiol. 282, C545-C559 (2002).
23. K. Mayawala, D. G. Vlachos, J. S. Edwards, Computational modeling reveals molecular details of epidermal growth factor binding. BMC Cell Biol. 6, 41 (2005).
24. U. B. Nielsen, B. Schoeberl, Using computational modeling to drive the development of targeted therapeutics. IDrugs 8, 822-826 (2005).
25. W. W. Chen, B. Schoeberl, P. J. Jasper, M. Niepel, U. B. Nielsen, D. A. Lauffenburger, P. K. Sorger, Input-output behavior of ErbB signaling pathways as revealed by a mass action model trained against dynamic data. Mol. Syst. Biol. 5, 239 (2009).
26. M. Liscovitch, D. Ravid, A case study in misidentification of cancer cell lines: MCF-7/AdrR cells (re-designated NCI/ADR-RES) are derived from OVCAR-8 human ovarian carcinoma cells. Cancer Lett. 245, 350-352 (2007).
27. A. Monks, D. Scudiero, P. Skehan, R. Shoemaker, K. Paull, D. Vistica, C. Hose, J. Langley, P. Cronise, A. Vaigro-Wolff, M. Gray-Goodrich, H. Campbell, J. Mayo, M. Boyd, Feasibility of a high-flux anticancer drug screen using a diverse panel of cultured human tumor cell lines. J. Natl. Cancer Inst. 83, 757-766 (1991).
28. A. S. Clark, K. West, S. Streicher, P. A. Dennis, Constitutive and inducible Akt activity promotes resistance to chemotherapy, trastuzumab, or tamoxifen in breast cancer cells. Mol. Cancer Ther. 1, 707-717 (2002).
29. M. G. Kolonin, L. Bover, J. Sun, A. J. Zurita, K. A. Do, J. Lahdenranta, M. Cardó-Vila, R. J. Giordano, D. E. Jaalouk, M. G. Ozawa, C. A. Moya, G. R. Souza, F. I. Staquicini, A. Kunyiasu, D. A. Scudiero, S. L. Holbeck, E. A. Sausville, W. Arap, R. Pasqualini, Ligand-directed surface profiling of human cancer cells with combinatorial peptide libraries. Cancer Res. 66, 34-40 (2006).
30. J. N. Weinstein, Y. Pommier, Transcriptomic analysis of the NCI-60 cancer cell lines. C. R. Biol. 326, 909-920 (2003).
31. E. Atlas, M. Cardillo, I. Mehmi, H. Zahedkargaran, C. Tang, R. Lupu, Heregulin is sufficient for the promotion of tumorigenicity and metastasis of breast cancer cells in vivo. Mol. Cancer Res. 1, 165-175 (2003). (Pubitemid 36330198)
32. M. Breuleux, Role of heregulin in human cancer.Cell.Mol. LifeSci. 64, 2358-2377 (2007).
33. A. J. Dunbar, C. Goddard, Structure-function and biological role of betacellulin. Int. J. Biochem. Cell Biol. 32, 805-815 (2000).
34. S. A. Prigent, N. R. Lemoine, C. M. Hughes, G. D. Plowman, C. Selden, W. J. Gullick, Expression of the c-erbB-3 protein in normal human adult and fetal tissues. Oncogene 7, 1273-1278 (1992).
35. G. Hudelist, C. F. Singer, M. Manavi, K. Pischinger, E. Kubista, K. Czerwenka, Coexpression of ErbB-family members in human breast cancer: Her-2/neu is the preferred dimerization candidate in nodal-positive tumors. Breast Cancer Res. Treat. 80, 353-361 (2003).
36. C. P. Chuu, R. Y. Chen, J. L. Barkinge, M. F. Ciaccio, R. B. Jones, Systems-level analysis of ErbB4 signaling in breast cancer: A laboratory to clinical perspective. Mol. Cancer Res. 6, 885-891 (2008).
37. A. Sorkin, L. K. Goh, Endocytosis and intracellular trafficking of ErbBs. Exp. Cell Res. 314, 3093-3106 (2008).
38. M. Alimandi, L. M. Wang, D. Bottaro, C. C. Lee, A. Kuo, M. Frankel, P. Fedi, C. Tang, M. Lippman, J. H. Pierce, Epidermal growth factor and betacellulin mediate signal transduction through co-expressed ErbB2 and ErbB3 receptors. EMBO J. 16, 5608-5617 (1997).
39. R. Pinkas-Kramarski, A. E. Lenferink, S. S. Bacus, L. Lyass, M. L. van de Poll, L. N. Klapper, E. Tzahar, M. Sela, E. J. van Zoelen, Y. Yarden, The oncogenic ErbB-2/ErbB-3 heterodimer is a surrogate receptor of the epidermal growth factor and betacellulin. Oncogene 16, 1249-1258 (1998).
40. N. A. van Riel, Dynamic modelling and analysis of biochemical networks: Mechanismbased models and model-based experiments. Brief. Bioinform. 7, 364-374 (2006).
41. J. J. Hornberg, B. Binder, F. J. Bruggeman, B. Schoeberl, R. Heinrich, H. V. Westerhoff, Control of MAPK signalling: From complexity to what really matters. Oncogene 24, 5533-5542 (2005).
42. J. E. Shoemaker, F. J. Doyle III, Identifying fragilities in biochemical networks: Robust performance analysis of Fas signaling-induced apoptosis. Biophys. J. 95, 2610-2623 (2008).
43. C. Wofsy, B. Goldstein, Cross-linking of Fc gamma receptors and surface antibodies. Theory and application. J. Immunol. 145, 1814-1825 (1990).
44. G. Valabrega, F. Montemurro, M. Aglietta, Trastuzumab: Mechanism of action, resistance and future perspectives in HER2-overexpressing breast cancer. Ann. Oncol. 18, 977-984 (2007).
45. E. R. Wood, A. T. Truesdale, O. B. McDonald, D. Yuan, A. Hassell, S. H. Dickerson, B. Ellis, C. Pennisi, E. Horne, K. Lackey, K. J. Alligood, D. W. Rusnak, T. M. Gilmer, L. Shewchuk, A unique structure for epidermal growth factor receptor bound to GW572016 (Lapatinib): Relationships among protein conformation, inhibitor off-rate, and receptor activity in tumor cells. Cancer Res. 64, 6652-6659 (2004).
46. D. B. Agus, R. W. Akita, W. D. Fox, G. D. Lewis, B. Higgins, P. I. Pisacane, J. A. Lofgren, C. Tindell, D. P. Evans, K. Maiese, H. I. Scher, M. X. Sliwkowski, Targeting ligandactivated ErbB2 signaling inhibits breast and prostate tumor growth. Cancer Cell 2, 127-137 (2002).
47. D. Patel, A. Lahiji, S. Patel, M. Franklin, X. Jimenez, D. J. Hicklin, X. Kang, Monoclonal antibody cetuximab binds to and down-regulates constitutively activated epidermal growth factor receptor vIII on the cell surface. Anticancer Res. 27, 3355-3366 (2007).
48. C. W. Adams, D. E. Allison, K. Flagella, L. Presta, J. Clarke, N. Dybdal, K. McKeever, M. X. Sliwkowski, Humanization of a recombinant monoclonal antibody to produce a therapeutic HER dimerization inhibitor, pertuzumab. Cancer Immunol. Immunother. 55, 717-727 (2006).
49. A. Ivascu, M. Kubbies, Rapid generation of single-tumor spheroids for high-throughput cell function and toxicity analysis. J. Biomol. Screen. 11, 922-932 (2006).
50. H. R. Xing, C. Cordon-Cardo, X. Deng, W. Tong, L. Campodonico, Z. Fuks, R. Kolesnick, Pharmacologic inactivation of kinase suppressor of ras-1 abrogates Ras-mediated pancreatic cancer. Nat. Med. 9, 1266-1268 (2003).
51. D. S. Salomon, R. Brandt, F. Ciardiello, N. Normanno, Epidermal growth factor-related peptides and their receptors in human malignancies. Crit. Rev. Oncol. Hematol. 19, 183-232 (1995).
52. J. L. Boerner, A. Danielsen, N. J. Maihle, Ligand-independent oncogenic signaling by the epidermal growth factor receptor: v-ErbB as a paradigm. Exp. Cell Res. 284, 111-121 (2003).
53. H. Greulich, T. H. Chen,W. Feng, P. A. Jänne, J. V. Alvarez, M. Zappaterra, S. E. Bulmer, D. A. Frank, W. C. Hahn, W. R. Sellers, M. Meyerson, Oncogenic transformation by inhibitor-sensitive and -resistant EGFR mutants. PLoS Med. 2, e313 (2005).
54. R. Chen, P. S. Rabinovitch, D. A. Crispin, M. J. Emond, M. P. Bronner, T. A. Brentnall, The initiation of colon cancer in a chronic inflammatory setting. Carcinogenesis 26, 1513-1519 (2005).
55. D. J. Riese II, Y. Bermingham, T. M. van Raaij, S. Buckley, G. D. Plowman, D. F. Stern, Betacellulin activates the epidermal growth factor receptor and erbB-4, and induces cellular response patterns distinct from those stimulated by epidermal growth factor or neuregulin-beta. Oncogene 12, 345-353 (1996).
56. R. R. Beerli, N. E. Hynes, Epidermal growth factor-related peptides activate distinct subsets of ErbB receptors and differ in their biological activities. J. Biol. Chem. 271, 6071-6076 (1996).
57. H. S. Kim, H. S. Shin, H. J. Kwak, C. H. Cho, C. O. Lee, G. Y. Koh, Betacellulin induces angiogenesis through activation of mitogen-activated protein kinase and phosphatidylinositol 3″-kinase in endothelial cell. FASEB J. 17, 318-320 (2003).
58. C. Xue, F. Liang, R. Mahmood, M. Vuolo, J. Wyckoff, H. Qian, K. L. Tsai, M. Kim, J. Locker, Z. Y. Zhang, J. E. Segall, ErbB3-dependent motility and intravasation in breast cancer metastasis. Cancer Res. 66, 1418-1426 (2006).
59. B. L. Smith, D. Chin, W. Maltzman, K. Crosby, G. N. Hortobagyi, S. S. Bacus, The efficacy of Herceptin therapies is influenced by the expression of other erbB receptors, their ligands and the activation of downstream signalling proteins. Br. J. Cancer 91, 1190-1194 (2004).
60. W. Dean-Colomb, F. J. Esteva, Her2-positive breast cancer: Herceptin and beyond. Eur. J. Cancer 44, 2806-2812 (2008).
61. F. E. von Eyben, Epidermal growth factor receptor inhibition and non-small cell lung cancer. Crit. Rev. Clin. Lab. Sci. 43, 291-323 (2006).
62. R. Jefferis, Antibody therapeutics: Isotype and glycoform selection. Expert Opin. Biol. Ther. 7, 1401-1413 (2007).
63. A. W. Hamburger, The role of ErbB3 and its binding partners in breast cancer progression and resistance to hormone and tyrosine kinase directed therapies. J. Mammary Gland Biol. Neoplasia 13, 225-233 (2008).
64. V. Folgiero, P. Avetrani, G. Bon, S. E. Di Carlo, A. Fabi, C. Nisticò, P. Vici, E. Melucci, S. Buglioni, L. Perracchio, I. Sperduti, L. Rosanò, A. Sacchi, M. Mottolese, R. Falcioni, Induction of ErbB-3 expression by a6b4 integrin contributes to tamoxifen resistance in ERb1-negative breast carcinomas. PLoS ONE 3, e1592 (2008).
65. B. Liu, D. Ordonez-Ercan, Z. Fan, S. M. Edgerton, X. Yang, A. D. Thor, Downregulation of erbB3 abrogates erbB2-mediated tamoxifen resistance in breast cancer cells. Int. J. Cancer 120, 1874-1882 (2007).
66. E. H. van der Horst, M. Murgia, M. Treder, A. Ullrich, Anti-HER-3 MAbs inhibit HER-3-mediated signaling in breast cancer cell lines resistant to anti-HER-2 antibodies. Int. J. Cancer 115, 519-527 (2005).
67. N. V. Sergina, M. Rausch, D. Wang, J. Blair, B. Hann, K. M. Shokat, M. M. Moasser, Escape from HER-family tyrosine kinase inhibitor therapy by the kinase-inactive HER3. Nature 445, 437-441 (2007).
68. J. A. Engelman, K. Zejnullahu, T. Mitsudomi, Y. Song, C. Hyland, J. O. Park, N. Lindeman, C. M. Gale, X. Zhao, J. Christensen, T. Kosaka, A. J. Holmes, A. M. Rogers, F. Cappuzzo, T. Mok, C. Lee, B. E. Johnson, L. C. Cantley, P. A. Jänne, MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 316, 1039-1043 (2007).
69. J. B. Fitzgerald, B. Schoeberl, U. B. Nielsen, P. K. Sorger, Systems biology and combination therapy in the quest for clinical efficacy. Nat. Chem. Biol. 2, 458-466 (2006).
70. E. Horak, T. Heitner, M. K. Robinson, H. H. Simmons, J. Garrison, M. Russeva, P. Furmanova, J. Lou, Y. Zhou, Q. A. Yuan, L. M. Weiner, G. P. Adams, J. D. Marks, Isolation of scFvs to in vitro produced extracellular domains of EGFR family members. Cancer Biother. Radiopharm. 20, 603-613 (2005).
71. A. Schwartz, E. Fernández-Repollet, Development of clinical standards for flow cytometry. Ann. N. Y. Acad. Sci. 677, 28-39 (1993).
72. D. Wassaf, G. Kuang, K. Kopacz, Q. L. Wu, Q. Nguyen, M. Toews, J. Cosic, J. Jacques, S. Wiltshire, J. Lambert, C. C. Pazmany, S. Hogan, R. C. Ladner, A. E. Nixon, D. J. Sexton, High-throughput affinity ranking of antibodies using surface plasmon resonance microarrays. Anal. Biochem. 351, 241-253 (2006).
73. K. Sakai, H. Yokote, K. Murakami-Murofushi, T. Tamura, N. Saijo, K. Nishio, Pertuzumab, a novel HER dimerization inhibitor, inhibits the growth of human lung cancer cells mediated by the HER3 signaling pathway. Cancer Sci. 98, 1498-1503 (2007).
74. R. Herrmann, W. Fayad, S. Schwarz, M. Berndtsson, S. Linder, Screening for compounds that induce apoptosis of cancer cells grown as multicellular spheroids. J. Biomol. Screen. 13, 1-8 (2008).
75. J. T. Jones, R. W. Akita, M. X. Sliwkowski, Binding specificities and affinities of egf domains for ErbB receptors. FEBS Lett. 447, 227-231 (1999).
76. B. B. Aldridge, J. M. Burke, D. A. Lauffenburger, P. K. Sorger, Physicochemical modelling of cell signalling pathways. Nat. Cell Biol. 8, 1195-1203 (2006).