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Review

Early clinical development of epidermal growth factor receptor targeted therapy in breast cancer

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Pages 463-479 | Received 22 Jul 2016, Accepted 22 Feb 2017, Published online: 08 Mar 2017

References

  • Chan TO, Rittenhouse SE, Tsichlis PN. Akt/pkb and other d3 phosphoinositide-regulated kinases: kinase activation by phosphoinositide-dependent phosphorylation. Annu Rev Biochem. 1999;68:965–1014.
  • Dickler MN, Rugo HS, Eberle CA, et al. A phase ii trial of erlotinib in combination with bevacizumab in patients with metastatic breast cancer. Clin Cancer Res. 2008;14(23):7878–7883.
  • Dickler MN, Cobleigh MA, Miller KD, et al. Efficacy and safety of erlotinib in patients with locally advanced or metastatic breast cancer. Breast Cancer Res Treat. 2009;115(1):115–121.
  • Von Minckwitz G, Jonat W, Fasching P, et al. A multicentre phase ii study on gefitinib in taxane- and anthracycline-pretreated metastatic breast cancer. Breast Cancer Res Treat. 2005;89(2):165–172.
  • Carey LA, Rugo HS, Marcom PK, et al. Tbcrc 001: randomized phase ii study of cetuximab in combination with carboplatin in stage iv triple-negative breast cancer. J Clin Oncol. 2012;30(21):2615–2623.
  • Cohen S. The epidermal growth factor (egf). Cancer. 1983;51(10):1787–1791.
  • Ushiro H, Cohen S. Identification of phosphotyrosine as a product of epidermal growth factor-activated protein kinase in a-431 cell membranes. J Biol Chem. 1980;255(18):8363–8365.
  • Ullrich A, Coussens L, Hayflick JS, et al. Human epidermal growth factor receptor cdna sequence and aberrant expression of the amplified gene in a431 epidermoid carcinoma cells. Nature. 1984;309(5967):418–425.
  • Downward J, Yarden Y, Mayes E, et al. Close similarity of epidermal growth factor receptor and v-erb-b oncogene protein sequences. Nature. 1984;307(5951):521–527.
  • Appert-Collin A, Hubert P, Cremel G, et al. Role of erbb receptors in cancer cell migration and invasion. Front Pharmacol. 2015;6:283.
  • Tebbutt N, Pedersen MW, Johns TG. Targeting the erbb family in cancer: couples therapy. Nat Rev Cancer. 2013;13(9):663–673.
  • Yarden Y, Pines G. The erbb network: at last, cancer therapy meets systems biology. Nat Rev Cancer. 2012;12(8):553–563.
  • Ceresa BP, Peterson JL. Cell and molecular biology of epidermal growth factor receptor. Int Rev Cell Mol Biol. 2014;313:145–178.
  • Ullrich A, Schlessinger J. Signal transduction by receptors with tyrosine kinase activity. Cell. 1990;61(2):203–212.
  • Burgess AW, Cho HS, Eigenbrot C, et al. An open-and-shut case? Recent insights into the activation of egf/erbb receptors. Mol Cell. 2003;12(3):541–552.
  • Zhang X, Gureasko J, Shen K, et al. An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor. Cell. 2006;125(6):1137–1149.
  • Kancha RK, Von Bubnoff N, Duyster J. Asymmetric kinase dimer formation is crucial for the activation of oncogenic egfrviii but not for erbb3 phosphorylation. Cell Commun Signal. 2013;11:39.
  • Rubin I, Yarden Y. The basic biology of her2. Ann Oncol. 2001;12(Suppl 1):S3–8.
  • Wallasch C, Weiss FU, Niederfellner G, et al. Heregulin-dependent regulation of her2/neu oncogenic signaling by heterodimerization with her3. Embo J. 1995;14(17):4267–4275.
  • Alimandi M, Romano A, Curia MC, et al. Cooperative signaling of erbb3 and erbb2 in neoplastic transformation and human mammary carcinomas. Oncogene. 1995;10(9):1813–1821.
  • Schulze WX, Deng L, Mann M. Phosphotyrosine interactome of the erbb-receptor kinase family. Mol Syst Biol. 2005;1:E1-E13.
  • Saito Y, Haendeler J, Hojo Y, et al. Receptor heterodimerization: essential mechanism for platelet-derived growth factor-induced epidermal growth factor receptor transactivation. Mol Cell Biol. 2001;21(19):6387–6394.
  • Morgillo F, Hong WK, Lee H. Insulin-like growth factor-1 receptor/epidermal growth factor receptor (egfr) heterodimerization and resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small-cell lung cancer. J Clin Oncol. 2006;24(18_suppl):13032.
  • Tanizaki J, Okamoto I, Sakai K, et al. Differential roles of trans-phosphorylated egfr, her2, her3, and ret as heterodimerisation partners of met in lung cancer with met amplification. Br J Cancer. 2011;105(6):807–813.
  • Sarbassov DD, Ali SM, Sengupta S, et al. Prolonged rapamycin treatment inhibits mtorc2 assembly and akt/pkb. Mol Cell. 2006;22(2):159–168.
  • Maurer M, Su T, Saal LH, et al. 3-phosphoinositide-dependent kinase 1 potentiates upstream lesions on the phosphatidylinositol 3-kinase pathway in breast carcinoma. Cancer Res. 2009;69(15):6299–6306.
  • Tanaka K, Babic I, Nathanson D, et al. Oncogenic egfr signaling activates an mtorc2-nf-kappab pathway that promotes chemotherapy resistance. Cancer Discov. 2011;1(6):524–538.
  • Kapoor GS, Zhan Y, Johnson GR, et al. Distinct domains in the shp-2 phosphatase differentially regulate epidermal growth factor receptor/nf-kappab activation through gab1 in glioblastoma cells. Mol Cell Biol. 2004;24(2):823–836.
  • Roskoski R Jr. The erbb/her family of protein-tyrosine kinases and cancer. Pharmacological Res. 2014;79:34–74.
  • Caunt CJ, Sale MJ, Smith PD, et al. Mek1 and mek2 inhibitors and cancer therapy: the long and winding road. Nat Rev Cancer. 2015;15(10):577–592.
  • Citri A, Skaria KB, Yarden Y. The deaf and the dumb: the biology of erbb-2 and erbb-3. Exp Cell Res. 2003;284(1):54–65.
  • Nyati MK, Morgan MA, Feng FY, et al. Integration of egfr inhibitors with radiochemotherapy. Nat Rev Cancer. 2006;6(11):876–885.
  • Mukhopadhyay C, Zhao X, Maroni D, et al. Distinct effects of egfr ligands on human mammary epithelial cell differentiation. Plos One. 2013;8(10):e75907.
  • Zhang D, LaFortune TA, Krishnamurthy S, et al. Epidermal growth factor receptor tyrosine kinase inhibitor reverses mesenchymal to epithelial phenotype and inhibits metastasis in inflammatory breast cancer. Clin Cancer Res. 2009;15(21):6639–6648.
  • Yauch RL, Januario T, Eberhard DA, et al. Epithelial versus mesenchymal phenotype determines in vitro sensitivity and predicts clinical activity of erlotinib in lung cancer patients. Clin Cancer Res. 2005;11(24 Pt 1):8686–8698.
  • Frederick BA, Helfrich BA, Coldren CD, et al. Epithelial to mesenchymal transition predicts gefitinib resistance in cell lines of head and neck squamous cell carcinoma and non-small cell lung carcinoma. Mol Cancer Ther. 2007;6(6):1683–1691.
  • Barr S, Thomson S, Buck E, et al. Bypassing cellular egf receptor dependence through epithelial-to-mesenchymal-like transitions. Clin Exp Metastasis. 2008;25(6):685–693.
  • Wendt MK, Smith JA, Schiemann WP. Transforming growth factor-beta-induced epithelial-mesenchymal transition facilitates epidermal growth factor-dependent breast cancer progression. Oncogene. 2010;29(49):6485–6498.
  • Hay ED. An overview of epithelio-mesenchymal transformation. Acta Anat. 1995;154(1):8–20.
  • Kalluri R, Neilson EG. Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest. 2003;112(12):1776–1784.
  • Yang J, Mani SA, Donaher JL, et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 2004;117(7):927–939.
  • Lo HW, Hsu SC, Xia W, et al. Epidermal growth factor receptor cooperates with signal transducer and activator of transcription 3 to induce epithelial-mesenchymal transition in cancer cells via up-regulation of twist gene expression. Cancer Res. 2007;67(19):9066–9076.
  • Huber MA, Kraut N, Beug H. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol. 2005;17(5):548–558.
  • Kotiyal S, Bhattacharya S. Breast cancer stem cells, emt and therapeutic targets. Biochem Biophys Res Commun. 2014;453(1):112–116.
  • Vaupel P, Kallinowski F, Okunieff P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res. 1989;49(23):6449–6465.
  • Klopp AH, Gupta A, Spaeth E, et al. Concise review: dissecting a discrepancy in the literature: do mesenchymal stem cells support or suppress tumor growth? Stem Cells. 2011;29(1):11–19.
  • Lacerda L, Debeb BG, Smith D, et al. Mesenchymal stem cells mediate the clinical phenotype of inflammatory breast cancer in a preclinical model. Breast Cancer Res. 2015;17:42.
  • Condeelis J, Pollard JW. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell. 2006;124(2):263–266.
  • Wang D, Dubois RN. The role of cox-2 in intestinal inflammation and colorectal cancer. Oncogene. 2010;29(6):781–788.
  • Kim HS, Moon HG, Han W, et al. Cox2 overexpression is a prognostic marker for stage iii breast cancer. Breast Cancer Res Treat. 2012;132(1):51–59.
  • Rolland PH, Martin PM, Jacquemier J, et al. Prostaglandin in human breast cancer: evidence suggesting that an elevated prostaglandin production is a marker of high metastatic potential for neoplastic cells. J Natl Cancer Inst. 1980;64(5):1061–1070.
  • Bennett A, Charlier EM, McDonald AM, et al. Prostaglandins and breast cancer. Lancet. 1977;2(8039):624–626.
  • Reis-Filho JS, Milanezi F, Steele D, et al. Metaplastic breast carcinomas are basal-like tumours. Histopathology. 2006;49(1):10–21.
  • Cho EY, Choi YL, Han JJ, et al. Expression and amplification of her2, egfr and cyclin d1 in breast cancer: immunohistochemistry and chromogenic in situ hybridization. Pathol Int. 2008;58(1):17–25.
  • Sassen A, Rochon J, Wild P, et al. Cytogenetic analysis of her1/egfr, her2, her3 and her4 in 278 breast cancer patients. Breast Cancer Res. 2008;10(1):R2.
  • Park AK, Francis JM, Park WY, et al. Constitutive asymmetric dimerization drives oncogenic activation of epidermal growth factor receptor carboxyl-terminal deletion mutants. Oncotarget. 2015;6(11):8839–8850.
  • Cancer Genome Atlas N. Comprehensive molecular portraits of human breast tumours. Nature. 2012;490(7418):61–70.
  • Weber F, Fukino K, Sawada T, et al. Variability in organ-specific egfr mutational spectra in tumour epithelium and stroma may be the biological basis for differential responses to tyrosine kinase inhibitors. Br J Cancer. 2005;92(10):1922–1926.
  • Dent R, Trudeau M, Pritchard KI, et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res. 2007;13(15 Pt 1):4429–4434.
  • Masuda H, Baggerly KA, Wang Y, et al. Differential response to neoadjuvant chemotherapy among 7 triple-negative breast cancer molecular subtypes. Clin Cancer Res. 2013;19(19):5533–5540.
  • Siziopikou KP, Ariga R, Proussaloglou KE, et al. The challenging estrogen receptor-negative/progesterone receptor-negative/her-2-negative patient: a promising candidate for epidermal growth factor receptor-targeted therapy? Breast J. 2006;12(4):360–362.
  • Viale G, Rotmensz N, Maisonneuve P, et al. Invasive ductal carcinoma of the breast with the “triple-negative” phenotype: prognostic implications of egfr immunoreactivity. Breast Cancer Res Treat. 2009;116(2):317–328.
  • Gonzalez-Angulo AM, Timms KM, Liu S, et al. Incidence and outcome of brca mutations in unselected patients with triple receptor-negative breast cancer. Clin Cancer Res. 2011;17(5):1082–1089.
  • Muller PA, Trinidad AG, Timpson P, et al. Mutant p53 enhances met trafficking and signalling to drive cell scattering and invasion. Oncogene. 2013;32(10):1252–1265.
  • Cabioglu N, Gong Y, Islam R, et al. Expression of growth factor and chemokine receptors: new insights in the biology of inflammatory breast cancer. Ann Oncol. 2007;18(6):1021–1029.
  • Lee MJ, Ye AS, Gardino AK, et al. Sequential application of anticancer drugs enhances cell death by rewiring apoptotic signaling networks. Cell. 2012;149(4):780–794.
  • Imai K, Takaoka A. Comparing antibody and small-molecule therapies for cancer. Nat Rev Cancer. 2006;6(9):714–727.
  • Segovia-Mendoza M, Diaz L, Gonzalez-Gonzalez ME, et al. Calcitriol and its analogues enhance the antiproliferative activity of gefitinib in breast cancer cells. J Steroid Biochem Mol Biol. 2015;148:122–131.
  • Nechushtan H, Vainer G, Stainberg H, et al. A phase 1/2 of a combination of cetuximab and taxane for “triple negative” breast cancer patients. Breast. 2014;23(4):435–438.
  • Baselga J, Gomez P, Greil R, et al. Randomized phase ii study of the anti-epidermal growth factor receptor monoclonal antibody cetuximab with cisplatin versus cisplatin alone in patients with metastatic triple-negative breast cancer. J Clin Oncol. 2013;31(20):2586–2592.
  • Real PJ, Benito A, Cuevas J, et al. Blockade of epidermal growth factor receptors chemosensitizes breast cancer cells through up-regulation of bnip3l. Cancer Res. 2005;65(18):8151–8157.
  • Tredan O, Campone M, Jassem J, et al. Ixabepilone alone or with cetuximab as first-line treatment for advanced/metastatic triple-negative breast cancer. Clin Breast Cancer. 2015;15(1):8–15.
  • Modi S, D’Andrea G, Norton L, et al. A phase i study of cetuximab/paclitaxel in patients with advanced-stage breast cancer. Clin Breast Cancer. 2006;7(3):270–277.
  • Yang XD, Jia XC, Corvalan JR, et al. Eradication of established tumors by a fully human monoclonal antibody to the epidermal growth factor receptor without concomitant chemotherapy. Cancer Res. 1999;59(6):1236–1243.
  • Cowherd S, Miller LD, Melin SA, et al. A phase ii clinical trial of weekly paclitaxel and carboplatin in combination with panitumumab in metastatic triple negative breast cancer. Cancer Biol Ther. 2015;16(5):678–683.
  • Nabholtz JM, Abrial C, Mouret-Reynier MA, et al. Multicentric neoadjuvant phase ii study of panitumumab combined with an anthracycline/taxane-based chemotherapy in operable triple-negative breast cancer: identification of biologically defined signatures predicting treatment impact. Ann Oncol. 2014;25(8):1570–1577.
  • Monteverde M, Milano G, Strola G, et al. The relevance of adcc for egfr targeting: a review of the literature and a clinically-applicable method of assessment in patients. Crit Rev Oncol Hematol. 2015;95(2):179–190.
  • Moulder SL, Yakes FM, Muthuswamy SK, et al. Epidermal growth factor receptor (her1) tyrosine kinase inhibitor zd1839 (iressa) inhibits her2/neu (erbb2)-overexpressing breast cancer cells in vitro and in vivo. Cancer Res. 2001;61(24):8887–8895.
  • Anido J, Matar P, Albanell J, et al. Zd1839, a specific epidermal growth factor receptor (egfr) tyrosine kinase inhibitor, induces the formation of inactive egfr/her2 and egfr/her3 heterodimers and prevents heregulin signaling in her2-overexpressing breast cancer cells. Clin Cancer Res. 2003;9(4):1274–1283.
  • Campiglio M, Locatelli A, Olgiati C, et al. Inhibition of proliferation and induction of apoptosis in breast cancer cells by the epidermal growth factor receptor (egfr) tyrosine kinase inhibitor zd1839 (‘iressa’) is independent of egfr expression level. J Cell Physiol. 2004;198(2):259–268.
  • Baselga J, Albanell J, Ruiz A, et al. Phase ii and tumor pharmacodynamic study of gefitinib in patients with advanced breast cancer. J Clin Oncol. 2005;23(23):5323–5333.
  • Polychronis A, Sinnett HD, Hadjiminas D, et al. Preoperative gefitinib versus gefitinib and anastrozole in postmenopausal patients with oestrogen-receptor positive and epidermal-growth-factor-receptor-positive primary breast cancer: a double-blind placebo-controlled phase ii randomised trial. Lancet Oncol. 2005;6(6):383–391.
  • Ciardiello F, Troiani T, Caputo F, et al. Phase ii study of gefitinib in combination with docetaxel as first-line therapy in metastatic breast cancer. Br J Cancer. 2006;94(11):1604–1609.
  • Osborne CK, Neven P, Dirix LY, et al. Gefitinib or placebo in combination with tamoxifen in patients with hormone receptor-positive metastatic breast cancer: a randomized phase ii study. Clin Cancer Res. 2011;17(5):1147–1159.
  • Rabindran SK, Discafani CM, Rosfjord EC, et al. Antitumor activity of hki-272, an orally active, irreversible inhibitor of the her-2 tyrosine kinase. Cancer Res. 2004;64(11):3958–3965.
  • Wissner A, Overbeek E, Reich MF, et al. Synthesis and structure-activity relationships of 6,7-disubstituted 4-anilinoquinoline-3-carbonitriles. The design of an orally active, irreversible inhibitor of the tyrosine kinase activity of the epidermal growth factor receptor (egfr) and the human epidermal growth factor receptor-2 (her-2). J Med Chem. 2003;46(1):49–63.
  • Schaefer G, Fitzpatrick VD, Sliwkowski MX. 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(12):1385–1394.
  • Canonici A, Gijsen M, Mullooly M, et al. Neratinib overcomes trastuzumab resistance in her2 amplified breast cancer. Oncotarget. 2013;4(10):1592–1605.
  • Feldinger K, Kong A. Profile of neratinib and its potential in the treatment of breast cancer. Breast Cancer (Dove Med Press). 2015;7:147–162.
  • Wong KK, Fracasso PM, Bukowski RM, et al. A phase i study with neratinib (hki-272), an irreversible pan erbb receptor tyrosine kinase inhibitor, in patients with solid tumors. Clin Cancer Res. 2009;15(7):2552–2558.
  • Burstein HJ, Sun Y, Dirix LY, et al. Neratinib, an irreversible erbb receptor tyrosine kinase inhibitor, in patients with advanced erbb2-positive breast cancer. J Clin Oncol. 2010;28(8):1301–1307.
  • Martin M, Bonneterre J, Geyer CE Jr., et al. A phase two randomised trial of neratinib monotherapy versus lapatinib plus capecitabine combination therapy in patients with her2+ advanced breast cancer. Eur J Cancer. 2013;49(18):3763–3772.
  • Ma CX, Bose R, Gao F, et al. Phase ii trial of neratinib for her2 mutated, non-amplified metastatic breast cancer (her2mut mbc). Poster session presented at: 2016 ASCO Annual Meeting; 2016 Jun 3–7; Chicago, IL.
  • Inoue K, Torimura T, Nakamura T, et al. Vandetanib, an inhibitor of vegf receptor-2 and egf receptor, suppresses tumor development and improves prognosis of liver cancer in mice. Clin Cancer Res. 2012;18(14):3924–3933.
  • Ferrara N, Kerbel RS. Angiogenesis as a therapeutic target. Nature. 2005;438(7070):967–974.
  • Miller KD, Trigo JM, Wheeler C, et al. A multicenter phase ii trial of zd6474, a vascular endothelial growth factor receptor-2 and epidermal growth factor receptor tyrosine kinase inhibitor, in patients with previously treated metastatic breast cancer. Clin Cancer Res. 2005;11(9):3369–3376.
  • Boer K, Lang I, Llombart-Cussac A, et al. Vandetanib with docetaxel as second-line treatment for advanced breast cancer: A double-blind, placebo-controlled, randomized phase ii study. Invest New Drugs. 2012;30(2):681–687.
  • Clemons MJ, Cochrane B, Pond GR, et al. Randomised, phase ii, placebo-controlled, trial of fulvestrant plus vandetanib in postmenopausal women with bone only or bone predominant, hormone-receptor-positive metastatic breast cancer (mbc): the OCOG Zamboney study. Breast Cancer Res Treat. 2014;146(1):153–162.
  • Morabito A, Piccirillo MC, Falasconi F, et al. Vandetanib (zd6474), a dual inhibitor of vascular endothelial growth factor receptor (vegfr) and epidermal growth factor receptor (egfr) tyrosine kinases: current status and future directions. Oncologist. 2009;14(4):378–390.

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