Resistance to human epidermal growth factor receptor type 2-targeted therapies

European Journal of Cancer

Volumn 50, Issue 5, 2014, Pages 892-901

  Thery, Jean Christophe ^a   Spano, Jean Philippe ^a   Azria, David ^b   Raymond, Eric ^c   Penault Llorca, Frédérique ^d  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b CENTRE VAL D AURELLE   (France)

^c BEAUJON HOSPITAL   (France)

^d UNIVERSITÉ CLERMONT AUVERGNE   (France)

Author keywords

Breast cancer; HER 2; Resistance

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; LAPATINIB; PERTUZUMAB; TRASTUZUMAB; TRASTUZUMAB EMTANSINE;

BREAST CANCER; CANCER RESISTANCE; CANCER SURVIVAL; DRUG MECHANISM; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; REGISTRATION; REVIEW;

BREAST CANCER; HER-2; RESISTANCE;

ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; DISEASE-FREE SURVIVAL; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; MAYTANSINE; RECEPTOR, ERBB-2;

EID: 84896696101     PISSN: 09598049     EISSN: 18790852     Source Type: Journal    
DOI: 10.1016/j.ejca.2014.01.003     Document Type: Review

References (82)

1. D.J. Slamon, G.M. Clark, S.G. Wong, W.J. Levin, A. Ullrich, and W.L. McGuire Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene Science 235 4785 1987 177 182
2. M. Marty, F. Cognetti, and D. Maraninchi et al. Randomized phase II trial of the efficacy and safety of trastuzumab combined with docetaxel in patients with human epidermal growth factor receptor 2-positive metastatic breast cancer administered as first-line treatment: the M77001 study group J Clin Oncol 23 19 2005 4265 4274
3. D.J. Slamon, B. Leyland-Jones, and S. Shak et al. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2 N Engl J Med 344 11 2001 783 792
4. D. Cameron, M. Casey, and M. Press 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 Res Treat 112 3 2008 533 543
5. S. Verma, D. Miles, and L. Gianni et al. Trastuzumab emtansine for HER2-positive advanced breast cancer N Engl J Med 367 19 2012 1783 1791
6. S. Zhang, W.C. Huang, and P. Li et al. Combating trastuzumab resistance by targeting SRC, a common node downstream of multiple resistance pathways Nat Med 17 4 2011 461 469
7. P.C. Liu, X. Liu, and Y. Li et al. Identification of ADAM10 as a major source of HER2 ectodomain sheddase activity in HER2 overexpressing breast cancer cells Cancer Biol Ther 5 6 2006 657 664
8. M. Scaltriti, F. Rojo, and A. Ocana et al. Expression of p95HER2, a truncated form of the HER2 receptor, and response to anti-HER2 therapies in breast cancer J Natl Cancer Inst 99 8 2007 628 638
9. M. Scaltriti, S. Chandarlapaty, and L. Prudkin et al. Clinical benefit of lapatinib-based therapy in patients with human epidermal growth factor receptor 2-positive breast tumors coexpressing the truncated p95HER2 receptor Clin Cancer Res 16 9 2010 2688 2695
10. S. Friedman, R. Levy, and P. Scherle et al. Clinical benefit of INCB7839, a potent and selective inhibitor of ADAM10 and ADAM17, in combination with trastuzumab in metastatic HER2 positive breast cancer patients Cancer Res 69 24 2009 12345 [abstract N 5056, thirty-second annual CTRC-AACR San Antonio Breast Cancer Symposium]
11. K. Pedersen, P.D. Angelini, and S. Laos et al. A naturally occurring HER2 carboxy-terminal fragment promotes mammary tumor growth and metastasis Mol Cell Biol 29 12 2009 3319 3331
12. J. Arribas, J. Baselga, K. Pedersen, and J.L. Parra-Palau P95HER2 and breast cancer Cancer Res 71 5 2011 1515 1519
13. K. Leitzel, Y. Teramoto, and E. Sampson et al. Elevated soluble c-erbB-2 antigen levels in the serum and effusions of a proportion of breast cancer patients J Clin Oncol 10 9 1992 1436 1443
14. J. Sperinde, X. Jin, and J. Banerjee et al. Quantitation of p95HER2 in paraffin sections by using a p95-specific antibody and correlation with outcome in a cohort of trastuzumab-treated breast cancer patients Clin Cancer Res 16 16 2010 4226 4235
15. S. loibl, J. Bruey, G. Von Minckwitz, J.B. Huober, M.F. Press, and S. Darb-Esfahani et al. Validation of p95 as a predictive marker for trastuzumab-based therapy in primary HER2-positive breast cancer: a translational investigation from the neoadjuvant GeparQuattro study J Clin Oncol 29 Suppl. 2011 530 [abstr. 530]
16. D. Recupero, L. Daniele, and C. Marchio et al. Spontaneous and pronase-induced HER2 truncation increases the trastuzumab binding capacity of breast cancer tissues and cell lines J Pathol 229 3 2013 390 399
17. S.W. Han, Y. Cha, and A. Paquet et al. Correlation of HER2, p95HER2 and HER3 expression and treatment outcome of lapatinib plus capecitabine in her2-positive metastatic breast cancer PLoS One 7 7 2012 e39943
18. P. Carter Improving the efficacy of antibody-based cancer therapies Nat Rev Cancer 1 2 2001 118 129
19. L. Arnould, M. Gelly, and F. Penault-Llorca et al. Trastuzumab-based treatment of HER2-positive breast cancer: an antibody-dependent cellular cytotoxicity mechanism? Br J Cancer 94 2 2006 259 267
20. H.R. Koene, M. Kleijer, J. Algra, D. Roos, A.E. von dem Borne, and M. de Haas Fc gammaRIIIa-158V/F polymorphism influences the binding of IgG by natural killer cell Fc gammaRIIIa, independently of the Fc gammaRIIIa-48L/R/H phenotype Blood 90 3 1997 1109 1114
21. R.L. Shields, A.K. Namenuk, and K. Hong et al. High resolution mapping of the binding site on human IgG1 for Fc gamma RI, Fc gamma RII, Fc gamma RIII, and FcRn and design of IgG1 variants with improved binding to the Fc gamma R J Biol Chem 276 9 2001 6591 6604
22. A. Musolino, N. Naldi, and B. Bortesi et al. Immunoglobulin G fragment C receptor polymorphisms and clinical efficacy of trastuzumab-based therapy in patients with HER-2/neu-positive metastatic breast cancer J Clin Oncol 26 11 2008 1789 1796
23. Hurvitz SA, Betting D, Stern HM, et al. Analysis of Fcγ receptor IIA & IIIA polymorphisms: correlation with outcome in trastuzumab-treated HER2/Neu amplified early and metastatic breast cancer patients. In: 32nd annual San Antonio Breast Cancer Symposium, San Antonio, Texas, USA; December 9-13, 2009 [abstract 64].
24. K. Berns, H.M. Horlings, and B.T. Hennessy et al. A functional genetic approach identifies the PI3K pathway as a major determinant of trastuzumab resistance in breast cancer Cancer Cell 12 4 2007 395 402
25. Y. Nagata, K.H. Lan, and X. Zhou et al. PTEN activation contributes to tumor inhibition by trastuzumab, and loss of PTEN predicts trastuzumab resistance in patients Cancer Cell 6 2 2004 117 127
26. G. Jerusalem, A. Fasolo, and V. Dieras et al. Phase I trial of oral mTOR inhibitor everolimus in combination with trastuzumab and vinorelbine in pre-treated patients with HER2-overexpressing metastatic breast cancer Breast Cancer Res Treat 125 2 2011 447 455
27. F. Andre, M. Campone, and R. O'Regan et al. Phase I study of everolimus plus weekly paclitaxel and trastuzumab in patients with metastatic breast cancer pretreated with trastuzumab J Clin Oncol 28 34 2010 5110 5115
28. E.A. Perez, A.C. Dueck, and A.E. McCullough et al. Impact of PTEN protein expression on benefit from adjuvant trastuzumab in early-stage human epidermal growth factor receptor 2-positive breast cancer in the North Central Cancer Treatment Group N9831 trial J Clin Oncol 31 17 2013 2115 2122
29. E. Yao, W. Zhou, and S.T. Lee-Hoeflich et al. Suppression of HER2/HER3-mediated growth of breast cancer cells with combinations of GDC-0941 PI3K inhibitor, trastuzumab, and pertuzumab Clin Cancer Res 15 12 2009 4147 4156
30. Rodon J, Infante J, Burris H, et al. A dose-escalation study with a special drug delivery system (SDS) of BEZ235, a novel dual PI3K/mTOR inhibitor, in patients with metastatic/advanced solid tumors. In: Proceedings of the 33d annual CTRC-AACR San Antonio Breast Cancer Symposium, San Antonio, Texas, USA; 2010 [abstract P6-15-07].
31. C. Garcia-Garcia, Y.H. Ibrahim, and V. Serra et al. Dual mTORC1/2 and HER2 blockade results in antitumor activity in preclinical models of breast cancer resistant to anti-HER2 therapy Clin Cancer Res 18 9 2012 2603 2612
32. N.A. O'Brien, B.C. Browne, and L. Chow et al. Activated phosphoinositide 3-kinase/AKT signaling confers resistance to trastuzumab but not lapatinib Mol Cancer Ther 9 6 2010 1489 1502
33. W. Xia, I. Husain, and L. Liu et al. Lapatinib antitumor activity is not dependent upon phosphatase and tensin homologue deleted on chromosome 10 in ErbB2-overexpressing breast cancers Cancer Res 67 3 2007 1170 1175
34. A. Chakrabarty, B.N. Rexer, S.E. Wang, R.S. Cook, J.A. Engelman, and C.L. Arteaga H1047R phosphatidylinositol 3-kinase mutant enhances HER2-mediated transformation by heregulin production and activation of HER3 Oncogene 29 37 2010 5193 5203
35. P.J. Eichhorn, M. Gili, and M. Scaltriti et al. Phosphatidylinositol 3-kinase hyperactivation results in lapatinib resistance that is reversed by the mTOR/phosphatidylinositol 3-kinase inhibitor NVP-BEZ235 Cancer Res 68 22 2008 9221 9230
36. G. Zoppoli, E. Moran, and D. Soncini et al. Ras-induced resistance to lapatinib is overcome by MEK inhibition Curr Cancer Drug Targets 10 2 2010 168 175
37. K. Keyomarsi, S.L. Tucker, and T.A. Buchholz et al. Cyclin E and survival in patients with breast cancer N Engl J Med 347 20 2002 1566 1575
38. M. Scaltriti, P.J. Eichhorn, and J. Cortes et al. Cyclin E amplification/overexpression is a mechanism of trastuzumab resistance in HER2+ breast cancer patients Proc Natl Acad Sci USA 108 9 2011 3761 3766
39. T.T. Junttila, R.W. Akita, and K. Parsons et al. Ligand-independent HER2/HER3/PI3K complex is disrupted by trastuzumab and is effectively inhibited by the PI3K inhibitor GDC-0941 Cancer Cell 15 5 2009 429 440
40. R. Dua, J. Zhang, P. Nhonthachit, E. Penuel, C. Petropoulos, and G. Parry EGFR over-expression and activation in high HER2, ER negative breast cancer cell line induces trastuzumab resistance Breast Cancer Res Treat 122 3 2010 685 697
41. C.A. Ritter, M. Perez-Torres, and C. Rinehart et al. Human breast cancer cells selected for resistance to trastuzumab in vivo overexpress epidermal growth factor receptor and ErbB ligands and remain dependent on the ErbB receptor network Clin Cancer Res 13 16 2007 4909 4919
42. M. Gijsen, P. King, and T. Perera et al. HER2 phosphorylation is maintained by a PKB negative feedback loop in response to anti-HER2 herceptin in breast cancer PLoS Biol 8 12 2010 e1000563
43. G. Valabrega, F. Montemurro, and I. Sarotto et al. TGFalpha expression impairs trastuzumab-induced HER2 downregulation Oncogene 24 18 2005 3002 3010
44. J. Rhee, S.W. Han, and Y. Cha et al. High serum TGF-alpha predicts poor response to lapatinib and capecitabine in HER2-positive breast cancer Breast Cancer Res Treat 125 1 2011 107 114
45. J. Baselga, J. Cortes, and S.B. Kim et al. Pertuzumab plus trastuzumab plus docetaxel for metastatic breast cancer N Engl J Med 366 2 2012 109 119
46. L. Gianni, T. Pienkowski, and Y.H. Im 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 Lancet Oncol 13 1 2012 25 32
47. C.F. McDonagh, A. Huhalov, and B.D. Harms et al. Antitumor activity of a novel bispecific antibody that targets the ErbB2/ErbB3 oncogenic unit and inhibits heregulin-induced activation of ErbB3 Mol Cancer Ther 11 3 2012 582 593
48. Y. Lu, X. Zi, and M. Pollak Molecular mechanisms underlying IGF-I-induced attenuation of the growth-inhibitory activity of trastuzumab (Herceptin) on SKBR3 breast cancer cells Int J Cancer 108 3 2004 334 341
49. Y. Lu, X. Zi, Y. Zhao, D. Mascarenhas, and M. Pollak Insulin-like growth factor-I receptor signaling and resistance to trastuzumab (Herceptin) J Natl Cancer Inst 93 24 2001 1852 1857
50. X. Huang, L. Gao, and S. Wang et al. Heterotrimerization of the growth factor receptors erbB2, erbB3, and insulin-like growth factor-i receptor in breast cancer cells resistant to herceptin Cancer Res 70 3 2010 1204 1214
51. D.L. Rowe, T. Ozbay, L.M. Bender, and R. Nahta Nordihydroguaiaretic acid, a cytotoxic insulin-like growth factor-I receptor/HER2 inhibitor in trastuzumab-resistant breast cancer Mol Cancer Ther 7 7 2008 1900 1908
52. R. Nahta, L.X. Yuan, Y. Du, and F.J. Esteva Lapatinib induces apoptosis in trastuzumab-resistant breast cancer cells: effects on insulin-like growth factor I signaling Mol Cancer Ther 6 2 2007 667 674
53. D.L. Shattuck, J.K. Miller, K.L. Carraway 3rd, and C. Sweeney Met receptor contributes to trastuzumab resistance of Her2-overexpressing breast cancer cells Cancer Res 68 5 2008 1471 1477
54. E. Munzone, G. Curigliano, and A. Rocca et al. Reverting estrogen-receptor-negative phenotype in HER-2-overexpressing advanced breast cancer patients exposed to trastuzumab plus chemotherapy Breast Cancer Res 8 1 2006 R4
55. W. Xia, S. Bacus, and P. Hegde et al. A model of acquired autoresistance to a potent ErbB2 tyrosine kinase inhibitor and a therapeutic strategy to prevent its onset in breast cancer Proc Natl Acad Sci USA 103 20 2006 7795 7800
56. J. Baselga, I. Bradbury, and H. Eidtmann et al. Lapatinib with trastuzumab for HER2-positive early breast cancer (NeoALTTO): a randomised, open-label, multicentre, phase 3 trial Lancet 379 9816 2012 633 640
57. L. Liu, J. Greger, and H. Shi et al. Novel mechanism of lapatinib resistance in HER2-positive breast tumor cells: activation of AXL Cancer Res 69 17 2009 6871 6878
58. J. Huober, P.A. Fasching, and M. Barsoum et al. Higher efficacy of letrozole in combination with trastuzumab compared to letrozole monotherapy as first-line treatment in patients with HER2-positive, hormone-receptor-positive metastatic breast cancer-results of the eLEcTRA trial Breast 21 1 2012 27 33
59. S. Johnston, J. Pippen Jr., and X. Pivot et al. Lapatinib combined with letrozole versus letrozole and placebo as first-line therapy for postmenopausal hormone receptor-positive metastatic breast cancer J Clin Oncol 27 33 2009 5538 5546
60. B. Kaufman, J.R. Mackey, and M.R. Clemens et al. Trastuzumab plus anastrozole versus anastrozole alone for the treatment of postmenopausal women with human epidermal growth factor receptor 2-positive, hormone receptor-positive metastatic breast cancer: results from the randomized phase III TAnDEM study J Clin Oncol 27 33 2009 5529 5537
61. G.E. Konecny, Y.G. Meng, and M. Untch et al. Association between HER-2/neu and vascular endothelial growth factor expression predicts clinical outcome in primary breast cancer patients Clin Cancer Res 10 5 2004 1706 1716
62. Hurvitz SA, Pegram MD, Lin L-S, et al. Final results of a phase II trial evaluating trastuzumab and bevacizumab as first line treatment of HER2-amplified advanced breast cancer. In: 32nd annual San Antonio Breast Cancer Symposium, San Antonio, Texas, USA; December 9-13, 2009 [abstract 6094].
63. H.S. Rugo, A. Jo Chien, and S.X. Franco et al. A phase II study of lapatinib and bevacizumab as treatment for HER2-overexpressing metastatic breast cancer Breast Cancer Res Treat 134 1 2012 13 20
64. J.Y. Pierga, T. Petit, and T. Delozier et al. Neoadjuvant bevacizumab, trastuzumab, and chemotherapy for primary inflammatory HER2-positive breast cancer (BEVERLY-2): an open-label, single-arm phase 2 study Lancet Oncol 13 4 2012 375 384
65. J.S. Ross, E.A. Slodkowska, W.F. Symmans, L. Pusztai, P.M. Ravdin, and G.N. Hortobagyi The HER-2 receptor and breast cancer: ten years of targeted anti-HER-2 therapy and personalized medicine Oncologist 14 4 2009 320 368
66. Huober J, Loibl S, Untch M, et al. New molecular biomarkers for resistance to trastuzumab in primary HER2 positive breast cancer-a translational investigation from the neoadjuvant GeparQuattro study. In: 33rd annual San Antonio Breast Cancer Symposium, San Antonio, Texas, USA; December 9-13, 2010 [PD02-06].
67. E.A. Perez, R.B. Jenkins, and A.C. Dueck et al. C-MYC alterations and association with patient outcome in early-stage HER2-positive breast cancer from the north central cancer treatment group N9831 adjuvant trastuzumab trial J Clin Oncol 29 6 2011 651 659
68. P. Hamberg, M.M. Bos, and H.J. Braun et al. Randomized phase II study comparing efficacy and safety of combination-therapy trastuzumab and docetaxel vs. sequential therapy of trastuzumab followed by docetaxel alone at progression as first-line chemotherapy in patients with HER2+ metastatic breast cancer: HERTAX trial Clin Breast Cancer 11 2 2011 103 113
69. K. Inoue, K. Nakagami, and M. Mizutani et al. Randomized phase III trial of trastuzumab monotherapy followed by trastuzumab plus docetaxel versus trastuzumab plus docetaxel as first-line therapy in patients with HER2-positive metastatic breast cancer: the JO17360 Trial Group Breast Cancer Res Treat 119 1 2010 127 136
70. G. von Minckwitz, A. du Bois, and M. Schmidt et al. Trastuzumab beyond progression in human epidermal growth factor receptor 2-positive advanced breast cancer: a German breast group 26/breast international group 03-05 study J Clin Oncol 27 12 2009 1999 2006
71. C.E. Geyer, J. Forster, and D. Lindquist et al. Lapatinib plus capecitabine for HER2-positive advanced breast cancer N Engl J Med 355 26 2006 2733 2743
72. H.J. Burstein, Y. Sun, and L.Y. Dirix et al. Neratinib, an irreversible ErbB receptor tyrosine kinase inhibitor, in patients with advanced ErbB2-positive breast cancer J Clin Oncol 28 8 2010 1301 1307
73. N.U. Lin, E.P. Winer, and D. Wheatley 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 133 3 2012 1057 1065
74. S. Chandarlapaty, M. Scaltriti, and P. Angelini et al. Inhibitors of HSP90 block p95-HER2 signaling in Trastuzumab-resistant tumors and suppress their growth Oncogene 29 3 2010 325 334
75. C. Ma, X. Niu, J. Luo, Z. Shao, and K. Shen Combined effects of lapatinib and bortezomib in human epidermal receptor 2 (HER2)-overexpressing breast cancer cells and activity of bortezomib against lapatinib-resistant breast cancer cells Cancer Sci 101 10 2010 2220 2226
76. G.E. Konecny, M.D. Pegram, and N. Venkatesan et al. Activity of the dual kinase inhibitor lapatinib (GW572016) against HER-2-overexpressing and trastuzumab-treated breast cancer cells Cancer Res 66 3 2006 1630 1639
77. K.L. Blackwell, H.J. Burstein, and A.M. Storniolo et al. Randomized study of Lapatinib alone or in combination with trastuzumab in women with ErbB2-positive, trastuzumab-refractory metastatic breast cancer J Clin Oncol 28 7 2010 1124 1130
78. G.D. Lewis Phillips, G. Li, and D.L. Dugger et al. Targeting HER2-positive breast cancer with trastuzumab-DM1, an antibody-cytotoxic drug conjugate Cancer Res 68 22 2008 9280 9290
79. T.T. Junttila, G. Li, K. Parsons, G.L. Phillips, and M.X. Sliwkowski Trastuzumab-DM1 (T-DM1) retains all the mechanisms of action of trastuzumab and efficiently inhibits growth of lapatinib insensitive breast cancer Breast Cancer Res Treat 128 2 2011 347 356
80. M. Campone, P. Juin, F. Andre, and T. Bachelot Resistance to HER2 inhibitors: is addition better than substitution? Rationale for the hypothetical concept of drug sedimentation Crit Rev Oncol Hematol 78 3 2011 195 205
81. H.A. Burris, H.S. Rugo, S.J. Vukelja, C.L. Vogel, R.A. Borson, and S. Limentani et al. Phase II study of the antibody drug conjugate trastuzumab-DM1 for the treatment of human epidermal growth factor receptor 2 (HER2)-positive breast cancer after prior HER2-directed therapy J Clin Oncol 29 4 2011 398 405
82. S. Modi, A. Stopeck, H. Linden, D. Solit, S. Chandarlapaty, and N. Rosen et al. HSP90 inhibition is effective in breast cancer: a phase II trial of tanespimycin (17-AAG) plus trastuzumab in patients with HER2-positive metastatic breast cancer progressing on trastuzumab Clin Cancer Res 17 15 2011 5132 5139