Combining lapatinib and pertuzumab to overcome lapatinib resistance due to NRG1-mediated signalling in HER2-amplified breast cancer

Oncotarget

Volumn 6, Issue 8, 2015, Pages 5678-5694

  Leung, Wing Yin ^a   Roxanis, Ioannis ^b   Sheldon, Helen ^a   Buffa, Francesca M ^a   Li, Ji Liang ^a   Harris, Adrian L ^a   Kong, Anthony ^a,c  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b OXFORD UNIVERSITY HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

HER2; Lapatinib; NRG1; Pertuzumab; Resistance

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; LAPATINIB; NEUROGENIN 1; PERTUZUMAB; ANTINEOPLASTIC AGENT; ERBB2 PROTEIN, HUMAN; MONOCLONAL ANTIBODY; NEU DIFFERENTIATION FACTOR; NRG1 PROTEIN, HUMAN; QUINAZOLINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CANCER COMBINATION CHEMOTHERAPY; CANCER RESISTANCE; CONTROLLED STUDY; DRUG EFFICACY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LOADING DRUG DOSE; MONOTHERAPY; MOUSE; NONHUMAN; PROTEIN DEPHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR REGRESSION; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; BREAST NEOPLASMS; CELL PROLIFERATION; DRUG EFFECTS; DRUG POTENTIATION; DRUG RESISTANCE; DRUG SCREENING; FEMALE; GENETICS; METABOLISM; NUDE MOUSE; PATHOLOGY; RANDOMIZATION; TUMOR CELL LINE;

ANIMALS; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; FEMALE; HUMANS; MICE; MICE, INBRED BALB C; MICE, NUDE; NEUREGULIN-1; QUINAZOLINES; RANDOM ALLOCATION; RECEPTOR, ERBB-2; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84925652468     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3296     Document Type: Article

References (50)

1. Bazley LA, Gullick WJ. The epidermal growth factor receptor family. Endocrine-related cancer. 2005; 12 Suppl 1:S17-27.
2. Mendelsohn J, Baselga J. Epidermal growth factor receptor targeting in cancer. Seminars in oncology. 2006; 33:369-385.
3. Arteaga CL, Sliwkowski MX, Osborne CK, Perez EA, Puglisi F, Gianni L. Treatment of HER2-positive breast cancer: current status and future perspectives. Nature reviews Clinical oncology. 2012; 9:16-32.
4. Baselga J, Swain SM. Novel anticancer targets: revisiting ERBB2 and discovering ERBB3. Nature reviews Cancer. 2009; 9:463-475.
5. Yarden Y, Sliwkowski MX. Untangling the ErbB signalling network. Nature reviews Molecular cell biology. 2001; 2:127-137.
6. Capelan M, Pugliano L, De Azambuja E, Bozovic I, Saini KS, Sotiriou C, Loi S, Piccart-Gebhart MJ. Pertuzumab: new hope for patients with HER2-positive breast cancer. Annals of oncology: official journal of the European Society for Medical Oncology/ESMO. 2013; 24:273-282.
7. Johnson BE, Jänne PA. Rationale for a phase II trial of pertuzumab, a HER-2 dimerization inhibitor, in patients with non-small cell lung cancer. Clinical cancer research: an official journal of the American Association for Cancer Research. 2006; 12:4436s-4440s.
8. Agus DB, Akita RW, Fox WD, Lewis GD, Higgins B, Pisacane PI, Lofgren JA, Tindell C, Evans DP, Maiese K, Scher HI, Sliwkowski MX. Targeting ligand-activated ErbB2 signaling inhibits breast and prostate tumor growth. Cancer cell. 2002; 2:127-137.
9. Lee-Hoeflich ST, Crocker L, Yao E, Pham T, Munroe X, Hoeflich KP, Sliwkowski MX, Stern HM. A central role for HER3 in HER2-amplified breast cancer: implications for targeted therapy. Cancer research. 2008; 68:5878-5887.
10. Nahta R, Hung MC, Esteva FJ. The HER-2-targeting antibodies trastuzumab and pertuzumab synergistically inhibit the survival of breast cancer cells. Cancer research. 2004; 64:2343-2346.
11. Baselga J, Cortes J, Kim SB, Im SA, Hegg R, Im YH, Roman L, Pedrini JL, Pienkowski T, Knott A, Clark E, Benyunes MC, Ross G, Swain SM, Group CS. Pertuzumab plus trastuzumab plus docetaxel for metastatic breast cancer. The New England journal of medicine. 2012; 366:109-119.
12. Gianni L, Pienkowski T, Im YH, Roman L, Tseng LM, Liu MC, Lluch A, Staroslawska E, de la Haba-Rodriguez J, Im SA, Pedrini JL, Poirier B, Morandi P, Semiglazov V, Srimuninnimit V, Bianchi G et al. Efficacy and safety of neoadjuvant pertuzumab and trastuzumab in women with locally advanced, inflammatory, or early HER2-positive breast cancer (NeoSphere): a randomised multicentre, open-label, phase 2 trial. The lancet oncology. 2012; 13:25-32.
13. Rusnak DW, Lackey K, Affleck K, Wood ER, Alligood KJ, Rhodes N, Keith BR, Murray DM, Knight WB, Mullin RJ, Gilmer TM. The effects of the novel, reversible epidermal growth factor receptor/ErbB-2 tyrosine kinase inhibitor, GW2016, on the growth of human normal and tumor-derived cell lines in vitro and in vivo. Molecular cancer therapeutics. 2001; 1:85-94.
14. Konecny GE, Pegram MD, Venkatesan N, Finn R, Yang G, Rahmeh M, Untch M, Rusnak DW, Spehar G, Mullin RJ, Keith BR, Gilmer TM, Berger M, Podratz KC, Slamon DJ. Activity of the dual kinase inhibitor lapatinib (GW572016) against HER-2-overexpressing and trastuzumab-treated breast cancer cells. Cancer research. 2006; 66:1630-1639.
15. Xia W, Mullin RJ, Keith BR, Liu LH, Ma H, Rusnak DW, Owens G, Alligood KJ, Spector NL. Anti-tumor activity of GW572016: a dual tyrosine kinase inhibitor blocks EGF activation of EGFR/erbB2 and downstream Erk1/2 and AKT pathways. Oncogene. 2002; 21:6255-6263.
16. Cameron D, Casey M, Press M, Lindquist D, Pienkowski T, Romieu CG, Chan S, Jagiello-Gruszfeld A, Kaufman B, Crown J, Chan A, Campone M, Viens P, Davidson N, Gorbounova V, Raats JI et al. A phase III randomized comparison of lapatinib plus capecitabine versus capecitabine alone in women with advanced breast cancer that has progressed on trastuzumab: updated efficacy and biomarker analyses. Breast cancer research and treatment. 2008; 112:533-543.
17. Geyer CE, Forster J, Lindquist D, Chan S, Romieu CG, Pienkowski T, Jagiello-Gruszfeld A, Crown J, Chan A, Kaufman B, Skarlos D, Campone M, Davidson N, Berger M, Oliva C, Rubin SD et al. Lapatinib plus capecitabine for HER2-positive advanced breast cancer. The New England journal of medicine. 2006; 355:2733-2743.
18. Guarneri V, Frassoldati A, Bottini A, Cagossi K, Bisagni G, Sarti S, Ravaioli A, Cavanna L, Giardina G, Musolino A, Untch M, Orlando L, Artioli F, Boni C, Generali DG, Serra P et al. Preoperative chemotherapy plus trastuzumab, lapatinib, or both in human epidermal growth factor receptor 2-positive operable breast cancer: results of the randomized phase II CHER-LOB study. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2012; 30:1989-1995.
19. Robidoux A, Tang G, Rastogi P, Geyer CE, Jr., Azar CA, Atkins JN, Fehrenbacher L, Bear HD, Baez-Diaz L, Sarwar S, Margolese RG, Farrar WB, Brufsky AM, Shibata HR, Bandos H, Paik S et al. Lapatinib as a component of neoadjuvant therapy for HER2-positive operable breast cancer (NSABP protocol B-41): an open-label, randomised phase 3 trial. The lancet oncology. 2013; 14:1183-1192.
20. Baselga J, Bradbury I, Eidtmann H, Di Cosimo S, de Azambuja E, Aura C, Gomez H, Dinh P, Fauria K, Van Dooren V, Aktan G, Goldhirsch A, Chang TW, Horvath Z, Coccia-Portugal M, Domont J et al. Lapatinib with trastuzumab for HER2-positive early breast cancer (NeoALTTO): a randomised, open-label, multicentre, phase 3 trial. Lancet. 2012; 379:633-640.
21. Valachis A, Nearchou A, Lind P, Mauri D. Lapatinib, trastuzumab or the combination added to preoperative chemotherapy for breast cancer: a meta-analysis of randomized evidence. Breast cancer research and treatment. 2012; 135:655-662.
22. Gelmon KA, Boyle F, Kaufman B, Huntsman D, Manikhas A, Leo AD, Martin M, Schwartzberg L, Dent SF, Ellard S, Tonkin KS, Nagarwala YM, Pritchard KI, Whelan TJ, Nomikos D, Chapman JW et al: Open-label phase III randomized controlled trial comparing taxane-based chemotherapy (Tax) with lapatinib (L) or trastuzumab (T) as first-line therapy for women with HER2+ metastatic breast cancer: Interim analysis (IA) of NCIC CTG MA.31/GSK EGF 108919. In: ASCO Annual Meeting: June 20 2012 2012; Chicago, IL: Journal of Clinical Oncology; 2012: suppl, LBA671.
23. Xia W, Bacus S, Hegde P, Husain I, Strum J, Liu L, Paulazzo G, Lyass L, Trusk P, Hill J, Harris J, Spector NL. A model of acquired autoresistance to a potent ErbB2 tyrosine kinase inhibitor and a therapeutic strategy to prevent its onset in breast cancer. Proceedings of the National Academy of Sciences of the United States of America. 2006; 103:7795-7800.
24. Liu L, Greger J, Shi H, Liu Y, Greshock J, Annan R, Halsey W, Sathe GM, Martin AM, Gilmer TM. Novel mechanism of lapatinib resistance in HER2-positive breast tumor cells: activation of AXL. Cancer research. 2009; 69:6871-6878.
25. Garrett JT, Olivares MG, Rinehart C, Granja-Ingram ND, Sanchez V, Chakrabarty A, Dave B, Cook RS, Pao W, McKinely E, Manning HC, Chang J, Arteaga CL. Transcriptional and posttranslational up-regulation of HER3 (ErbB3) compensates for inhibition of the HER2 tyrosine kinase. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108:5021-5026.
26. Xia W, Bacus S, Husain I, Liu L, Zhao S, Liu Z, Moseley MA, 3rd, Thompson JW, Chen FL, Koch KM, Spector NL. Resistance to ErbB2 tyrosine kinase inhibitors in breast cancer is mediated by calcium-dependent activation of RelA. Molecular cancer therapeutics. 2010; 9:292-299.
27. Xia W, Petricoin EF, 3rd, Zhao S, Liu L, Osada T, Cheng Q, Wulfkuhle JD, Gwin WR, Yang X, Gallagher RI, Bacus S, Lyerly HK, Spector NL. An heregulin-EGFR-HER3 autocrine signaling axis can mediate acquired lapatinib resistance in HER2+ breast cancer models. Breast cancer research: BCR. 2013; 15:R85.
28. Blackburn E, Zona S, Murphy ML, Brown IR, Chan SK, Gullick WJ. A monoclonal antibody to the human HER3 receptor inhibits Neuregulin 1-beta binding and co-operates with Herceptin in inhibiting the growth of breast cancer derived cell lines. Breast cancer research and treatment. 2012; 134:53-59.
29. Scaltriti M1, Verma C, Guzman M, Jimenez J, Parra JL, Pedersen K, Smith DJ, Landolfi S, Ramon y Cajal S, Arribas J, Baselga J. Lapatinib, a HER2 tyrosine kinase inhibitor, induces stabilization and accumulation of HER2 and potentiates trastuzumab-dependent cell cytotoxicity. Oncogene. 2009;28:803-14.
30. Jackson JG, St Clair P, Sliwkowski MX, Brattain MG. Blockade of epidermal growth factor-or heregulin-dependent ErbB2 activation with the anti-ErbB2 monoclonal antibody 2C4 has divergent downstream signaling and growth effects. Cancer research. 2004; 64:2601-2609.
31. Kramer-Marek G, Gijsen M, Kiesewetter DO, Bennett R, Roxanis I, Zielinski R, Kong A, Capala J. Potential of PET to predict the response to trastuzumab treatment in an ErbB2-positive human xenograft tumor model. Journal of nuclear medicine: official publication, Society of Nuclear Medicine. 2012; 53:629-637.
32. Kong A, Calleja V, Leboucher P, Harris A, Parker PJ, Larijani B. HER2 oncogenic function escapes EGFR tyrosine kinase inhibitors via activation of alternative HER receptors in breast cancer cells. PloS one. 2008; 3:e2881.
33. Gijsen M, King P, Perera T, Parker PJ, Harris AL, Larijani B, Kong A. HER2 phosphorylation is maintained by a PKB negative feedback loop in response to anti-HER2 herceptin in breast cancer. PLoS Biol. 2010; 8:e1000563.
34. Toi M, Iwata H, Fujiwara Y, Ito Y, Nakamura S, Tokuda Y, Taguchi T, Rai Y, Aogi K, Arai T, Watanabe J, Wakamatsu T, Katsura K, Ellis CE, Gagnon RC, Allen KE et al. Lapatinib monotherapy in patients with relapsed, advanced, or metastatic breast cancer: efficacy, safety, and biomarker results from Japanese patients phase II studies. British journal of cancer. 2009; 101:1676-1682.
35. Feldinger K, Generali D, Kramer-Marek G, Gijsen M, Ng TB, Wong JH, Strina C, Cappelletti M, Andreis D, Li JL, Bridges E, Turley H, Leek R, Roxanis I, Capala J, Murphy G et al. ADAM10 mediates trastuzumab resistance and is correlated with survival in HER2 positive breast cancer. Oncotarget. 2014; 5:6633-6646.
36. Waterhouse BR, Gijsen M, Barber PR, Tullis ID, Vojnovic B, Kong A. Assessment of EGFR/HER2 dimerization by FRET-FLIM utilizing Alexa-conjugated secondary antibodies in relation to targeted therapies in cancers. Oncotarget. 2011; 2:728-736.
37. Canonici A, Gijsen M, Mullooly M, Bennett R, Bouguern N, Pedersen K, O'Brien NA, Roxanis I, Li JL, Bridge E, Finn R, Siamon D, McGowan P, Duffy MJ, O'Donovan N, Crown J et al. Neratinib overcomes trastuzumab resistance in HER2 amplified breast cancer. Oncotarget. 2013; 4:1592-1605.
38. Koutras AK, Fountzilas G, Kalogeras KT, Starakis I, Iconomou G, Kalofonos HP. The upgraded role of HER3 and HER4 receptors in breast cancer. Critical reviews in oncology/hematology. 2010; 74:73-78.
39. Sundvall M, Veikkolainen V, Kurppa K, Salah Z, Tvorogov D, van Zoelen EJ, Aqeilan R, Elenius K. Cell death or survival promoted by alternative isoforms of ErbB4. Molecular biology of the cell. 2010; 21:4275-4286.
40. Mohd Nafi SN, Generali D, Kramer-Marek G, Gijsen M, Strina C, Cappelletti M, Andreis D, Haider S, Li JL, Bridges E, Capala J, Ioannis R, Harris AL, Kong A. Nuclear HER4 mediates acquired resistance to trastuzumab and is associated with poor outcome in HER2 positive breast cancer. Oncotarget. 2014; 5:5934-5949.
41. Scheuer W, Friess T, Burtscher H, Bossenmaier B, Endl J, Hasmann M. Strongly enhanced antitumor activity of trastuzumab and pertuzumab combination treatment on HER2-positive human xenograft tumor models. Cancer research. 2009; 69:9330-9336.
42. Dupouy S, Doan VK, Wu Z, Mourra N, Liu J, De Wever O, Llorca FP, Cayre A, Kouchkar A, Gompel A, Forgez P. Activation of EGFR, HER2 and HER3 by neurotensin/neurotensin receptor 1 renders breast tumors aggressive yet highly responsive to lapatinib and metformin in mice. Oncotarget. 2014;5:8235-51.
43. Noto A, De Vitis C, Roscilli G, Fattore L, Malpicci D, Marra E, Luberto L, D'Andrilli A, Coluccia P, Giovagnoli MR, Normanno N, Ruco L, Aurisicchio L, Mancini R, Ciliberto G. Combination therapy with anti-ErbB3 monoclonal antibodies and EGFR TKIs potently inhibits non-small cell lung cancer. Oncotarget. 2013;4:1253-65.
44. Axelrod M, Gordon VL, Conaway M, Tarcsafalvi A, Neitzke DJ, Gioeli D, Weber MJ. Combinatorial drug screening identifies compensatory pathway interactions and adaptive resistance mechanisms. Oncotarget. 2013;4(4):622-35.
45. Verma S, Miles D, Gianni L, Krop IE, Welslau M, Baselga J, Pegram M, Oh DY, Dieras V, Guardino E, Fang L, Lu MW, Olsen S, Blackwell K. Trastuzumab emtansine for HER2-positive advanced breast cancer. N Engl J Med. 2012; 367:1783-1791.
46. Li JL, Sainson RC, Shi W, Leek R, Harrington LS, Preusser M, Biswas S, Turley H, Heikamp E, Hainfellner JA, Harris AL. Delta-like 4 Notch ligand regulates tumor angiogenesis, improves tumor vascular function, and promotes tumor growth in vivo. Cancer research. 2007; 67:11244-11253.
47. Gril B, Palmieri D, Bronder JL, Herring JM, Vega-Valle E, Feigenbaum L, Liewehr DJ, Steinberg SM, Merino MJ, Rubin SD, Steeg PS. Effect of lapatinib on the outgrowth of metastatic breast cancer cells to the brain. Journal of the National Cancer Institute. 2008; 100:1092-1103.
48. Rimawi MF, Wiechmann LS, Wang YC, Huang C, Migliaccio I, Wu MF, Gutierrez C, Hilsenbeck SG, Arpino G, Massarweh S, Ward R, Soliz R, Osborne CK, Schiff R. Reduced dose and intermittent treatment with lapatinib and trastuzumab for potent blockade of the HER pathway in HER2/neu-overexpressing breast tumor xenografts. Clinical cancer research: an official journal of the American Association for Cancer Research. 2011; 17:1351-1361.
49. Arpino G, Gutierrez C, Weiss H, Rimawi M, Massarweh S, Bharwani L, De Placido S, Osborne CK, Schiff R. Treatment of human epidermal growth factor receptor 2-overexpressing breast cancer xenografts with multiagent HER-targeted therapy. Journal of the National Cancer Institute. 2007; 99:694-705.
50. Friess T, Scheuer W, Hasmann M. Combination treatment with erlotinib and pertuzumab against human tumor xenografts is superior to monotherapy. Clinical cancer research: an official journal of the American Association for Cancer Research. 2005; 11:5300-5309.