The Antitumorigenic Function of EGFR in Metastatic Breast Cancer is Regulated by Expression of Mig6

Neoplasia (United States)

Volumn 17, Issue 1, 2015, Pages 124-133

  Wendt, Michael K ^a   Williams, Whitney K ^a   Pascuzzi, Pete E ^b   Balanis, Nikolas G ^c   Schiemann, Barbara J ^c   Carlin, Cathleen R ^c   Schiemann, William P ^c  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN INDUCED GENE 6 PROTEIN; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; ERLOTINIB; MIG-6 PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR; QUINAZOLINE DERIVATIVE; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CARCINOGENESIS; COMPUTER MODEL; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOBLOTTING; MDA-MB-231 CELL LINE; METASTATIC BREAST CANCER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; TUMOR CELL; ANIMAL; ANTAGONISTS AND INHIBITORS; BASAL CELL CARCINOMA; BREAST TUMOR; CELL TRANSFORMATION; DISEASE MODEL; DRUG RESISTANCE; FEMALE; GENE EXPRESSION; GENETICS; METABOLISM; METASTASIS; PATHOLOGY; TUMOR CELL LINE; TUMOR VOLUME; XENOGRAFT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; ERLOTINIB HYDROCHLORIDE; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; HETEROGRAFTS; HUMANS; MICE; NEOPLASM METASTASIS; NEOPLASMS, BASAL CELL; PROTEIN KINASE INHIBITORS; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; TUMOR BURDEN; TUMOR SUPPRESSOR PROTEINS;

EID: 84964694939     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1016/j.neo.2014.11.009     Document Type: Article

References (33)

1. Wendt, MK, Smith, JA, Schiemann, WP, Transforming growth factor-beta-induced epithelial-mesenchymal transition facilitates epidermal growth factor-dependent breast cancer progression. Oncogene 29:49 (2010), 6485–6498.
2. Wendt, MK, Taylor, MA, Schiemann, BJ, Sossey-Alaoui, K, Schiemann, WP, Fibroblast growth factor receptor splice variants are stable markers of oncogenic transforming growth factor- beta1 signaling in metastatic breast cancers. Breast Cancer Res, 16(2), 2014, R24.
3. Tischkowitz, M, Brunet, J-S, Begin, L, Huntsman, D, Cheang, M, Akslen, L, Nielsen, T, Foulkes, W, Use of immunohistochemical markers can refine prognosis in triple negative breast cancer. BMC Cancer, 7(1), 2007, 134.
4. Dickler, MN, Cobleigh, MA, Miller, KD, Klein, PM, Winer, EP, Efficacy and safety of erlotinib in patients with locally advanced or metastatic breast cancer. Breast Cancer Res Treat 115:1 (2009), 115–121.
5. Dickler, MN, Rugo, HS, Eberle, CA, Brogi, E, Caravelli, JF, Panageas, KS, Boyd, J, Yeh, B, Lake, DE, et al. A phase II trial of erlotinib in combination with bevacizumab in patients with metastatic breast cancer. Clin Cancer Res 14:23 (2008), 7878–7883.
6. Tredan, O, Campone, M, Jassem, J, Vyzula, R, Coudert, B, Pacilio, C, Prausova, J, Hardy-Bessard, AC, Arance, A, et al. Ixabepilone Alone or With Cetuximab as First-Line Treatment for Advanced/Metastatic Triple-Negative Breast Cancer. Clin Breast Cancer, 2014 [pii: S1526-8209(14)00162-1].
7. Segatto, O, Anastasi, S, Alema, S, Regulation of epidermal growth factor receptor signalling by inducible feedback inhibitors. J Cell Sci 124:Pt 11 (2011), 1785–1793.
8. Anastasi, S, Baietti, MF, Frosi, Y, Alema, S, Segatto, O, The evolutionarily conserved EBR module of RALT/MIG6 mediates suppression of the EGFR catalytic activity. Oncogene 26:57 (2007), 7833–7846.
9. Zhang, YW, Staal, B, Su, Y, Swiatek, P, Zhao, P, Cao, B, Resau, J, Sigler, R, Bronson, R, et al. Evidence that MIG-6 is a tumor-suppressor gene. Oncogene 26:2 (2007), 269–276.
10. Ferby, I, Reschke, M, Kudlacek, O, Knyazev, P, Pante, G, Amann, K, Sommergruber, W, Kraut, N, Ullrich, A, et al. Mig6 is a negative regulator of EGF receptor-mediated skin morphogenesis and tumor formation. Nat Med 12:5 (2006), 568–573.
11. Hopkins, S, Linderoth, E, Hantschel, O, Suarez-Henriques, P, Pilia, G, Kendrick, H, Smalley, MJ, Superti-Furga, G, Ferby, I, Mig6 is a sensor of EGF receptor inactivation that directly activates c-Abl to induce apoptosis during epithelial homeostasis. Dev Cell 23:3 (2012), 547–559.
12. Xu, J, Keeton, AB, Wu, L, Franklin, JL, Cao, X, Messina, JL, Gene 33 inhibits apoptosis of breast cancer cells and increases poly(ADP-ribose) polymerase expression. Breast Cancer Res Treat 91:3 (2005), 207–215.
13. Jin, N, Cho, SN, Raso, MG, Wistuba, I, Smith, Y, Yang, Y, Kurie, JM, Yen, R, Evans, CM, et al. Mig-6 is required for appropriate lung development and to ensure normal adult lung homeostasis. Development 136:19 (2009), 3347–3356.
14. Ettenberg, SA, Rubinstein, YR, Banerjee, P, Nau, MM, Keane, MM, Lipkowitz, S, cbl-b inhibits EGF-receptor-induced apoptosis by enhancing ubiquitination and degradation of activated receptors. Mol Cell Biol Res Commun 2:2 (1999), 111–118.
15. Hyatt, DC, Ceresa, BP, Cellular localization of the activated EGFR determines its effect on cell growth in MDA-MB-468 cells. Exp Cell Res 314:18 (2008), 3415–3425.
16. Reinehr, R, Haussinger, D, CD95 death receptor and epidermal growth factor receptor (EGFR) in liver cell apoptosis and regeneration. Arch Biochem Biophys 518:1 (2012), 2–7.
17. Rush, JS, Quinalty, LM, Engelman, L, Sherry, DM, Ceresa, BP, Endosomal accumulation of the activated epidermal growth factor receptor (EGFR) induces apoptosis. J Biol Chem 287:1 (2012), 712–722.
18. Wendt, MK, Taylor, MA, Schiemann, BJ, Schiemann, WP, Down-regulation of epithelial cadherin is required to initiate metastatic outgrowth of breast cancer. Mol Biol Cell 22:14 (2011), 2423–2435.
19. Balanis, N, Wendt, MK, Schiemann, BJ, Wang, Z, Schiemann, WP, Carlin, CR, Epithelial-to-Mesenchymal Transition Promotes Breast Cancer Progression via a Fibronectin-Dependent Stat3 Signaling Pathway. J Biol Chem 288:25 (2013), 17954–17967.
20. Wendt, MK, Smith, JA, Schiemann, WP, p130Cas is required for mammary tumor growth and transforming growth factor-beta-mediated metastasis through regulation of Smad2/3 activity. J Biol Chem 284:49 (2009), 34145–34156.
21. Wendt, M, Schiemann, W, Therapeutic targeting of the focal adhesion complex prevents oncogenic TGF-beta signaling and metastasis. Breast Cancer Res, 11(5), 2009, R68.
22. Wendt, MK, Schiemann, BJ, Parvani, JG, Lee, YH, Kang, Y, Schiemann, WP, TGF-beta stimulates Pyk2 expression as part of an epithelial-mesenchymal transition program required for metastatic outgrowth of breast cancer. Oncogene 32:16 (2013), 2005–2015.
23. Richardson, AL, Wang, ZC, De Nicolo, A, Lu, X, Brown, M, Miron, A, Liao, X, Iglehart, JD, Livingston, DM, et al. X chromosomal abnormalities in basal-like human breast cancer. Cancer Cell 9:2 (2006), 121–132.
24. TCGA, Comprehensive molecular portraits of human breast tumours. Nature 490:7418 (2012), 61–70.
25. Balanis, N, Yoshigi, M, Wendt, MK, Schiemann, WP, Carlin, CR, beta3 integrin-EGF receptor cross-talk activates p190RhoGAP in mouse mammary gland epithelial cells. Mol Biol Cell 22:22 (2011), 4288–4301.
26. Wyckoff, J, Wang, W, Lin, EY, Wang, Y, Pixley, F, Stanley, ER, Graf, T, Pollard, JW, Segall, J, et al. A Paracrine Loop between Tumor Cells and Macrophages Is Required for Tumor Cell Migration in Mammary Tumors. Cancer Res 64:19 (2004), 7022–7029.
27. Cheang, MC, Voduc, D, Bajdik, C, Leung, S, McKinney, S, Chia, SK, Perou, CM, Nielsen, TO, Basal-like breast cancer defined by five biomarkers has superior prognostic value than triple-negative phenotype. Clin Cancer Res 14:5 (2008), 1368–1376.
28. Korpal, M, Ell, BJ, Buffa, FM, Ibrahim, T, Blanco, MA, Celia-Terrassa, T, Mercatali, L, Khan, Z, Goodarzi, H, et al. Direct targeting of Sec23a by miR-200s influences cancer cell secretome and promotes metastatic colonization. Nat Med 17:9 (2011), 1101–1108.
29. Kreike, B, Hart, G, Bartelink, H, van de Vijver, MJ, Analysis of breast cancer related gene expression using natural splines and the Cox proportional hazard model to identify prognostic associations. Breast Cancer Res Treat 122:3 (2010), 711–720.
30. Niikura, N, Liu, J, Hayashi, N, Mittendorf, EA, Gong, Y, Palla, SL, Tokuda, Y, Gonzalez-Angulo, AM, Hortobagyi, GN, et al. Loss of human epidermal growth factor receptor 2 (HER2) expression in metastatic sites of HER2-overexpressing primary breast tumors. J Clin Oncol 30:6 (2012), 593–599.
31. Hackel, PO, Gishizky, M, Ullrich, A, Mig-6 is a negative regulator of the epidermal growth factor receptor signal. Biol Chem 382:12 (2001), 1649–1662.
32. Armstrong, DK, Kaufmann, SH, Ottaviano, YL, Furuya, Y, Buckley, JA, Isaacs, JT, Davidson, NE, Epidermal growth factor-mediated apoptosis of MDA-MB-468 human breast cancer cells. Cancer Res 54:20 (1994), 5280–5283.
33. Xu, D, Makkinje, A, Kyriakis, JM, Gene 33 is an endogenous inhibitor of epidermal growth factor (EGF) receptor signaling and mediates dexamethasone-induced suppression of EGF function. J Biol Chem 280:4 (2005), 2924–2933.