295
Views
3
CrossRef citations to date
0
Altmetric
Review

Investigational ErbB-2 tyrosine kinase inhibitors for the treatment of breast cancer

, , , , , & show all
Pages 393-403 | Received 08 Nov 2015, Accepted 08 Feb 2016, Published online: 29 Feb 2016

References

  • Ferlay J, Soerjomataram I, Dikshit R, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–E386.
  • DeSantis CE, Bray F, Ferlay J, et al. International variation in female breast cancer incidence and mortality rates. Cancer Epidemiol Biomarkers Prev. 2015;24(10):1495–1506.
  • Slamon DJ, Clark GM, Wong SG, et al. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science. 1987;235(4785):177–182.
  • Ross JS, Fletcher JA. The HER-2/neu oncogene in breast cancer: prognostic factor, predictive factor, and target for therapy. Stem Cells. 1998;16(6):413–428.
  • Mustacchi G, Biganzoli L, Pronzato P, et al. HER2-positive metastatic breast cancer: a changing scenario. Crit Rev Oncol Hematol. 2015;95(1):78–87.
  • Yin W, Jiang Y, Shen Z, et al. Trastuzumab in the adjuvant treatment of HER2-positive early breast cancer patients: a meta-analysis of published randomized controlled trials. PLoS One. 2011;6(6):e21030.
  • Montemurro F, Valabrega G, Aglietta M. Lapatinib: a dual inhibitor of EGFR and HER2 tyrosine kinase activity. Expert Opin Biol Ther. 2007;7(2):257–268.
  • Swain SM, Baselga J, Kim SB, et al. Pertuzumab, trastuzumab, and docetaxel in HER2-positive metastatic breast cancer. N Engl J Med. 2015;372(8):724–734.
  • Verma S, Miles D, Gianni L, et al. Trastuzumab emtansine for HER2-positive advanced breast cancer. N Engl J Med. 2012;367(19):1783–1791.
  • Krop IE, Kim SB, Gonzalez-Martin A, et al. Trastuzumab emtansine versus treatment of physician’s choice for pretreated ErbB2-positive advanced breast cancer (TH3RESA): a randomised, open-label, phase 3 trial. Lancet Oncol. 2014;15(7):689–699.
  • Arteaga CL, Engelman JA. ERBB receptors: from oncogene discovery to basic science to mechanism-based cancer therapeutics. Cancer Cell. 2014;25(3):282–303.
  • Shi F, Telesco SE, Liu Y, et al. ErbB3/HER3 intracellular domain is competent to bind ATP and catalyze autophosphorylation. Proc Natl Acad Sci U S A. 2010;107(17):7692–7697.
  • Pinkas-Kramarski R, Soussan L, Waterman H, et al. Diversification of Neu differentiation factor and epidermal growth factor signaling by combinatorial receptor interactions. Embo J. 1996;15(10):2452–2467.
  • Ghosh R, Narasanna A, Wang SE, et al. Trastuzumab has preferential activity against breast cancers driven by HER2 homodimers. Cancer Res. 2011;71(5):1871–1882.
  • Montemurro F, Di Cosimo S, Arpino G. Human epidermal growth factor receptor 2 (HER2)-positive and hormone receptor-positive breast cancer: new insights into molecular interactions and clinical implications. Ann Oncol. 2013;24(11):2715–2724.
  • Montemurro F, Scaltriti M. Biomarkers of drugs targeting HER-family signalling in cancer. J Pathol. 2014;232(2):219–229.
  • Bose R, Kavuri SM, Searleman AC, et al. Activating HER2 mutations in HER2 gene amplification negative breast cancer. Cancer Discov. 2013;3(2):224–237.
  • Park YH, Shin HT, Jung HH, et al. Role of HER2 mutations in refractory metastatic breast cancers: targeted sequencing results in patients with refractory breast cancer. Oncotarget. 2015;6(31):32027–32038.
  • Ben-Baruch NE, Bose R, Kavuri SM, et al. HER2-mutated breast cancer responds to treatment with single-agent neratinib, a second-generation HER2/EGFR tyrosine kinase inhibitor. J Natl Compr Canc Netw. 2015;13(9):1061–1064.
  • Li D, Ambrogio L, Shimamura T, et al BIBW2992, an irreversible EGFR/HER2 inhibitor highly effective in preclinical lung cancer models. Oncogene. 2008;27(34):4702–4711.
  • Sequist LV, Yang JC, Yamamoto N, et al. Phase III study of afatinib or cisplatin plus pemetrexed in patients with metastatic lung adenocarcinoma with EGFR mutations. J Clin Oncol. 2013;31(27):3327–3334.
  • Wang XK, He JH, Xu JH, et al. Afatinib enhances the efficacy of conventional chemotherapeutic agents by eradicating cancer stem-like cells. Cancer Res. 2014;74(16):4431–4445.
  • Eskens FA, Mom CH, Planting AS, et al. A phase I dose escalation study of BIBW 2992, an irreversible dual inhibitor of epidermal growth factor receptor 1 (EGFR) and 2 (HER2) tyrosine kinase in a 2-week on, 2-week off schedule in patients with advanced solid tumours. Br J Cancer. 2008;98(1):80–85.
  • Marshall J, Hwang J, Eskens FA, et al. A Phase I, open-label, dose escalation study of afatinib, in a 3-week-on/1-week-off schedule in patients with advanced solid tumors. Invest New Drugs. 2013;31(2):399–408.
  • Marshall J, Shapiro GI, Uttenreuther-Fischer M, et al. Phase I dose-escalation study of afatinib, an ErbB family blocker, plus docetaxel in patients with advanced cancer. Future Oncol. 2013;9(2):271–281.
  • Ring A, Wheatley D, Hatcher H, et al. Phase I study to assess the combination of afatinib with trastuzumab in patients with advanced or metastatic HER2-positive breast cancer. Clin Cancer Res. 2015;21(12):2737–2744.
  • Lin NU, Winer EP, Wheatley D, et al. A phase II study of afatinib (BIBW 2992), an irreversible ErbB family blocker, in patients with HER2-positive metastatic breast cancer progressing after trastuzumab. Breast Cancer Res Treat. 2012;133(3):1057–1065.
  • Cortes J, Dieras V, Ro J, et al. Afatinib alone or afatinib plus vinorelbine versus investigator’s choice of treatment for HER2-positive breast cancer with progressive brain metastases after trastuzumab, lapatinib, or both (LUX-Breast 3): a randomised, open-label, multicentre, phase 2 trial. Lancet Oncol. 2015;16(16):1700–1710.
  • Rimawi MF, Aleixo SB, Rozas AA, et al. A neoadjuvant, randomized, open-label phase II trial of afatinib versus trastuzumab versus lapatinib in patients with locally advanced HER2-positive breast cancer. Clin Breast Cancer. 2015;15(2):101–109.
  • Hanusch C, Schneeweiss A, Loibl S, et al. Dual blockade with afatinib and trastuzumab as neoadjuvant treatment for patients with locally advanced or operable breast cancer receiving taxane-anthracycline containing chemotherapy-DAFNE (GBG-70). Clin Cancer Res. 2015;21(13):2924–2931.
  • Loibl S, Von Minckwitz G, Schneeweiss A, et al. PIK3CA mutations are associated with lower rates of pathologic complete response to anti-human epidermal growth factor receptor 2 (HER2) therapy in primary HER2-overexpressing breast cancer. J Clin Oncol. 2014;32(29):3212–3220.
  • Majewski IJ, Nuciforo P, Mittempergher L, et al. PIK3CA mutations are associated with decreased benefit to neoadjuvant human epidermal growth factor receptor 2-targeted therapies in breast cancer. J Clin Oncol. 2015;33(12):1334–1339.
  • Corkery B, Crown J, Clynes M, et al. Epidermal growth factor receptor as a potential therapeutic target in triple-negative breast cancer. Ann Oncol. 2009;20(5):862–867.
  • Schuler M, Awada A, Harter P, et al. A phase II trial to assess efficacy and safety of afatinib in extensively pretreated patients with HER2-negative metastatic breast cancer. Breast Cancer Res Treat. 2012;134(3):1149–1159.
  • Gunzer K, Joly F, Delozier T, et al. Addition of BIBW 2992, an irreversible inhibitor of EGFR/HER1 and HER2 inhibitor, to treatment continuation of letrozole in estrogen receptor (ER-) positive metastatic breast cancer progressing on letrozole. Cancer Res Dec. 2009;69(24 Supplement):4098–4098.
  • Harbeck N, Huang C-S, Hurvitz S, et al. Randomized Phase III trial of afatinib plus vinorelbine versus trastuzumab plus vinorelbine in patients with HER2-overexpressing metastatic breast cancer who had progressed on one prior trastuzumab treatment: LUX-Breast 1. Cancer Res. 2015;75(9 Supplement):Abstract P5-19-01.
  • 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.
  • Canonici A, Gijsen M, Mullooly M, et al Neratinib overcomes trastuzumab resistance in HER2 amplified breast cancer. Oncotarget. 2013;4(10):1592–1605.
  • Zhao XQ, Xie JD, Chen XG, et al. Neratinib reverses ATP-binding cassette B1-mediated chemotherapeutic drug resistance in vitro, in vivo, and ex vivo. Mol Pharmacol. 2012;82(1):47–58.
  • 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.
  • Vogel CL, Cobleigh MA, Tripathy D, et al. Efficacy and safety of trastuzumab as a single agent in first-line treatment of HER2-overexpressing metastatic breast cancer. J Clin Oncol. 2002;20(3):719–726.
  • Gomez HL, Doval DC, Chavez MA, et al. Efficacy and safety of lapatinib as first-line therapy for ErbB2-amplified locally advanced or metastatic breast cancer. J Clin Oncol. 2008;26(18):2999–3005.
  • 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.
  • Awada A, Dirix L, Manso SL, et al Safety and efficacy of neratinib (HKI-272) plus vinorelbine in the treatment of patients with ErbB2-positive metastatic breast cancer pretreated with anti-HER2 therapy. Ann Oncol. 2013;24(1):109–116.
  • Chow LW, Xu B, Gupta S, et al Combination neratinib (HKI-272) and paclitaxel therapy in patients with HER2-positive metastatic breast cancer. Br J Cancer. 2013;108(10):1985–1993.
  • Jankowitz RC, Abraham J, Tan AR, et al. Safety and efficacy of neratinib in combination with weekly paclitaxel and trastuzumab in women with metastatic HER2positive breast cancer: an NSABP foundation research program phase I study. Cancer Chemother Pharmacol. 2013;72(6):1205–1212.
  • Awada A, Colomer R, Bondarenko I, et al. Efficacy and CNS progression analysis from the randomized phase 2 trial of neratinib + paclitaxel vs trastuzumab + paclitaxel as first-line treatment for HER2+ metastatic breast cancer (NEfERTT). ASCO Meeting Abstracts. 2015;33(15_suppl):Abstract 610.
  • Gandhi L, Bahleda R, Tolaney SM, et al. Phase I study of neratinib in combination with temsirolimus in patients with human epidermal growth factor receptor 2-dependent and other solid tumors. J Clin Oncol. 2014;32(2):68–75.
  • Chan A, Delaloge S, Holmes FA, et al. Neratinib after adjuvant chemotherapy and trastuzumab in HER2-positive early breast cancer: Primary analysis at 2 years of a phase 3, randomized, placebo-controlled trial (ExteNET). J Clin Oncol. 2015;33(15_suppl):Abstract 508.
  • Goldhirsch A, Gelber RD, Piccart-Gebhart MJ, et al. 2 years versus 1 year of adjuvant trastuzumab for HER2-positive breast cancer (HERA): an open-label, randomised controlled trial. Lancet. 2013;382(9897):1021–1028.
  • Hickinson DM, Klinowska T, Speake G, et al. AZD8931, an equipotent, reversible inhibitor of signaling by epidermal growth factor receptor, ERBB2 (HER2), and ERBB3: a unique agent for simultaneous ERBB receptor blockade in cancer. Clin Cancer Res. 2010;16(4):1159–1169.
  • Tjulandin S, Moiseyenko V, Semiglazov V, et al. Phase I, dose-finding study of AZD8931, an inhibitor of EGFR (erbB1), HER2 (erbB2) and HER3 (erbB3) signaling, in patients with advanced solid tumors. Invest New Drugs. 2014;32(1):145–153.
  • Kurata T, Tsurutani J, Fujisaka Y, et al. Inhibition of EGFR, HER2 and HER3 signaling with AZD8931 alone and in combination with paclitaxel: phase i study in Japanese patients with advanced solid malignancies and advanced breast cancer. Invest New Drugs. 2014;32(5):946–954.
  • Baselga J, Hegg R, Losada MV, et al. A phase II randomized placebo-controlled study of AZD8931, an inhibitor of EGFR, HER2, and HER3 signaling, plus paclitaxel (P) vs P alone in patients (pts) with low HER2-expressing advanced breast cancer (BC) (THYME). Cancer Res. 2013;73(8 Supplement):LB-146.
  • Johnston SRD, Basik M, Hegg R, et al. Phase II randomized study of the EGFR, HER2, HER3 signaling inhibitor AZD8931 in combination with anastrozole (A) in women with endocrine therapy (ET) naive advanced breast cancer (MINT). J Clin Oncol. 2013;31(15_suppl):Abstract 531.
  • Smaill JB, Palmer BD, Rewcastle GW, et al. Tyrosine kinase inhibitors. 15. 4-(Phenylamino)quinazoline and 4-(phenylamino)pyrido[d]pyrimidine acrylamides as irreversible inhibitors of the ATP binding site of the epidermal growth factor receptor. J Med Chem. 1999;42(10):1803–1815.
  • Allen LF, Eiseman IA, Fry DW, et al. CI-1033, an irreversible pan-erbB receptor inhibitor and its potential application for the treatment of breast cancer. Semin Oncol. 2003;30(5 Suppl 16):65–78.
  • Nemunaitis J, Eiseman I, Cunningham C, et al Phase 1 clinical and pharmacokinetics evaluation of oral CI-1033 in patients with refractory cancer. Clin Cancer Res. 2005;11(10):3846–3853.
  • Rixe O, Franco SX, Yardley DA, et al. A randomized, phase II, dose-finding study of the pan-ErbB receptor tyrosine-kinase inhibitor CI-1033 in patients with pretreated metastatic breast cancer. Cancer Chemother Pharmacol. 2009;64(6):1139–1148.
  • Jani JP, Finn RS, Campbell M, et al Discovery and pharmacologic characterization of CP-724,714, a selective ErbB2 tyrosine kinase inhibitor. Cancer Res. 2007;67(20):9887–9893.
  • Munster PN, Britten CD, Mita M, et al. First study of the safety, tolerability, and pharmacokinetics of CP-724,714 in patients with advanced malignant solid HER2-expressing tumors. Clin Cancer Res. 2007;13(4):1238–1245.
  • Feng B, Xu JJ, Bi YA, et al. Role of hepatic transporters in the disposition and hepatotoxicity of a HER2 tyrosine kinase inhibitor CP-724,714. Toxicol Sci. 2009;108(2):492–500.
  • Kim HJ, Kim HP, Yoon YK, et al. Antitumor activity of HM781-36B, a pan-HER tyrosine kinase inhibitor, in HER2-amplified breast cancer cells. Anticancer Drugs. 2012;23(3):288–297.
  • Cha MY, Lee KO, Kim M, et al. Antitumor activity of HM781-36B, a highly effective pan-HER inhibitor in erlotinib-resistant NSCLC and other EGFR-dependent cancer models. Int J Cancer. 2012;130(10):2445–2454.
  • Kim Y, Oh J, Kim TM, et al. Phase I study to evaluate the safety and to assess the food effect of HM781-36B, a novel pan-HER inhibitor continuously given in patients with advanced solid tumors. J Clin Oncol. 2013;31(15_suppl):Abstract 2565.
  • Xu B, Ma F, Chen S, et al. A phase I study for tolerability, safety, and pharmacokinetics of pyrotinib, a novel irreversible HER2 and EGFR inhibitor, in Chinese patients with HER2+ metastatic breast cancer. J Clin Oncol. 2015;33(15_suppl):Abstract e11596.
  • Wong TW, Lee FY, Emanuel S, et al. Antitumor and antiangiogenic activities of BMS-690514, an inhibitor of human EGF and VEGF receptor kinase families. Clin Cancer Res. 2011;17(12):4031–4041.
  • Nokihara H, Yamamoto N, Yamada Y, et al. A phase I study of BMS-690514 in Japanese patients with advanced or metastatic solid tumors. Cancer Chemother Pharmacol. 2012;70(4):559–565.
  • Chow LQ, Jonker DI, Dy GK, et al. A phase I trial to determine the safety, pharmacokinetics, and pharmacodynamics of intercalated BMS-690514 with paclitaxel/carboplatin (PC) in advanced or metastatic solid malignancies. Cancer Chemother Pharmacol. 2013;71(5):1273–1285.
  • Wang DS, Patel A, Sim HM, et al. ARRY-334543 reverses multidrug resistance by antagonizing the activity of ATP-binding cassette subfamily G member 2. J Cell Biochem. 2014;115(8):1381–1391.
  • Ellard S, Rothenberg M, Cohen R, et al. ARRY-334543 in ErbB2 positive metastatic breast cancer and other ErbB expressing cancers: experience from expansion cohorts on a phase I study. Cancer Res. 2009;69:Abstract 3603.
  • Dy GK, Adjei AA. Understanding, recognizing, and managing toxicities of targeted anticancer therapies. CA Cancer J Clin. 2013;63(4):249–279.
  • Giordano SH, Temin S, Kirshner JJ, et al. Systemic therapy for patients with advanced human epidermal growth factor receptor 2-positive breast cancer: American society of clinical oncology clinical practice guideline. J Clin Oncol. 2014;32(19):2078–2099.
  • Koutras AK, Fountzilas G, Kalogeras KT, et al. The upgraded role of HER3 and HER4 receptors in breast cancer. Crit Rev Oncol Hematol. 2010;74(2):73–78.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.