Targeting HER family in HER2-positive metastatic breast cancer: Potential biomarkers and novel targeted therapies

Pharmacogenomics

Volumn 16, Issue 3, 2015, Pages 257-271

  De Paula Costa Monteiro, Inês ^a   Madureira, Pedro ^b,c   De Vasconscelos, Alessandro ^d,e   Humberto Pozza, Daniel ^a   De Mello, Ramon Andrade ^a,f,g  

^a University of Porto   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSITY OF PORTO   (Portugal)

^d Sociedade de Oncologia da Bahia   (Brazil)

^e Jorge Valente Hospital   (Brazil)

^f PORTUGUESE ONCOLOGY INSTITUTE   (Portugal)

^g UNIVERSITY OF ALGARVE   (Portugal)

Author keywords

antineoplastic drug resistance; biomarkers; breast cancer; erbB 2 receptor; erbB 3 receptor; molecular targeted therapies; monoclonal antibodies; protein kinase inhibitors

Indexed keywords

AFATINIB; AV 203; BIOLOGICAL MARKER; CAPECITABINE; DOCETAXEL; ENTINOSTAT; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPIDERMAL GROWTH FACTOR RECEPTOR 4; LAPATINIB; LJM 716; MESSENGER RNA; MM 111; MONOCLONAL ANTIBODY; NAVELBINE; NERATINIB; PACLITAXEL; PATRITUMAB; PERTUZUMAB; PHOSPHATIDYLINOSITOL 3 KINASE; PLACEBO; PROTEIN KINASE B; PROTEIN TYROSINE KINASE INHIBITOR; RG 7116; TAXANE DERIVATIVE; TRASTUZUMAB; TRASTUZUMAB EMTANSINE; UNCLASSIFIED DRUG; ERBB2 PROTEIN, HUMAN; ERBB3 PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR; TUMOR MARKER;

ADVANCED CANCER; BRAIN METASTASIS; BREAST CANCER; BREAST METASTASIS; CANCER CHEMOTHERAPY; CANCER PROGNOSIS; CANCER RESISTANCE; CANCER SPECIFIC SURVIVAL; CARDIOTOXICITY; DIMERIZATION; DISEASE FREE SURVIVAL; DRUG TARGETING; HEART DISEASE; HUMAN; MOLECULARLY TARGETED THERAPY; NEGATIVE FEEDBACK; NON SMALL CELL LUNG CANCER; NONHUMAN; ONCOGENE; OVERALL SURVIVAL; PIK3CA GENE; PROGRESSION FREE SURVIVAL; PROTEIN EXPRESSION; PROTO ONCOGENE; REVIEW; SOLID TUMOR; TUMOR GROWTH; UNSPECIFIED SIDE EFFECT; ANTAGONISTS AND INHIBITORS; BREAST NEOPLASMS; DRUG RESISTANCE; FEMALE; GENETICS; METABOLISM; PROCEDURES; SECONDARY; SIGNAL TRANSDUCTION; TRENDS;

BIOMARKERS, TUMOR; BREAST NEOPLASMS; DRUG RESISTANCE, NEOPLASM; FEMALE; GENES, ERBB-2; HUMANS; MOLECULAR TARGETED THERAPY; PROTEIN KINASE INHIBITORS; RECEPTOR, ERBB-2; RECEPTOR, ERBB-3; SIGNAL TRANSDUCTION; TRASTUZUMAB;

EID: 84923643265     PISSN: 14622416     EISSN: 17448042     Source Type: Journal    
DOI: 10.2217/pgs.14.133     Document Type: Review

References (85)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J. Clin. 61(2), 69-90 (2011
2. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 235(4785), 177-182 (1987
3. Ross JS, Fletcher JA. The HER-2/neu oncogene in breast cancer: prognostic factor, predictive factor, and target for therapy. Stem Cells 16(6), 413-428 (1998
4. Perou CM, Sørlie T, Eisen MB et al. Molecular portraits of human breast tumours. Nature 406(6797), 747-752 (2000
5. Baselga J, Tripathy D, Mendelsohn J et al. Phase II study of weekly intravenous recombinant humanized anti-p185HER2 monoclonal antibody in patients with HER2/neu-overexpressing metastatic breast cancer. J. Clin. Oncol. 14(3), 737-744 (1996
6. Rexer BN, Arteaga CL. Intrinsic and acquired resistance to HER2-Targeted therapies in HER2 gene-amplified breast cancer: mechanisms and clinical implications. Crit. Rev. Oncog. 17(1), 1-16 (2012
7. Roskoski Jr R. The ErbB/HER family of protein-Tyrosine kinases and cancer. Pharmacol. Res. 79, 34-74 (2014
8. Yarden Y, Sliwkowski MX. Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2(2), 127-137 (2001
9. Fedi P, Pierce JH, Di Fiore PP, Kraus MH. Efficient coupling with phosphatidylinositol 3-kinase, but not phospholipase C gamma or GTPase-activating protein, distinguishes ErbB-3 signaling from that of other ErbB/ EGFR family members. Mol. Cell. Biol. 14(1), 492-500 (1994
10. Garrett TP, McKern NM, Lou M et al. The crystal structure of a truncated ErbB2 ectodomain reveals an active conformation, poised to interact with other ErbB receptors. Mol. Cell 11(2), 495-505 (2003
11. Ghosh R, Narasanna A, Wang SE et al. Trastuzumab has preferential activity against breast cancers driven by HER2 homodimers. Cancer Res. 71(5), 1871-1882 (2011
12. Graus-Porta D, Beerli RR, Daly JM, Hynes NE. ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J. 16(7), 1647-1655 (1997
13. Shi F, Telesco SE, Liu Y, Radhakrishnan R, Lemmon MA. ErbB3/HER3 intracellular domain is competent to bind ATP and catalyze autophosphorylation. Proc. Natl Acad. Sci. USA 107(17), 7692-7697 (2010
14. 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. 15(10), 2452-2467 (1996
15. Tzahar E, Waterman H, Chen X et al. A hierarchical network of interreceptor interactions determines signal transduction by Neu differentiation factor/neuregulin and epidermal growth factor. Mol. Cell. Biol. 16(10), 5276-5287 (1996
16. Zhang Q, Park E, Kani K, Landgraf R. Functional isolation of activated and unilaterally phosphorylated heterodimers of ERBB2 and ERBB3 as scaffolds in ligand-dependent signaling. Proc. Natl Acad. Sci. USA 109(33), 13237-13242 (2012
17. Bose R, Kavuri SM, Searleman AC et al. Activating HER2 mutations in HER2 gene amplification negative breast cancer. Cancer Discov. 3(2), 224-237 (2013
18. Park K, Han S, Kim H, Kim J, Shin E. HER2 status in pure ductal carcinoma in situ and in the intraductal and invasive components of invasive ductal carcinoma determined by fluorescence in situ hybridization and immunohistochemistry. Histopathology 48(6), 702-707 (2006
19. Chiu CG, Masoudi H, Leung S et al. HER-3 overexpression is prognostic of reduced breast cancer survival: a study of 4046 patients. Ann. Surg. 251(6), 1107-1116 (2010
20. Bae SY, La Choi Y, Kim S et al. HER3 status by immunohistochemistry is correlated with poor prognosis in hormone receptor-negative breast cancer patients. Breast Cancer Res. Treat. 139(3), 741-750 (2013
21. Muraoka-Cook RS, Feng S-M, Strunk KE, Earp III HS. ErbB4/HER4: role in mammary gland development, differentiation and growth inhibition. J. Mammary Gland Biol. Neoplasia 13(2), 235-246 (2008
22. Wali VB, Haskins JW, Gilmore-Hebert M, Platt JT, Liu Z, Stern DF. Convergent and divergent cellular responses by ErbB4 isoforms in mammary epithelial cells. Mol. Cancer Res. 12(8), 1-16 (2014
23. Jones FE. HER4 intracellular domain (4ICD) activity in the developing mammary gland and breast cancer. J. Mammary Gland Biol. Neoplasia 13(2), 247-258 (2008
24. Chuu C-P, Chen R-Y, Barkinge JL, Ciaccio MF, Jones RB. Systems-level analysis of ErbB4 signaling in breast cancer: a laboratory to clinical perspective. Mol. Cancer Res. 6(6), 885-891 (2008
25. Stuart AA, Di Fiore P, Kraus MH. Cooperative signaling of ErbB3 and ErbB2 in neoplastic transformation and human mammary carcinomas. Oncogene 10, 1313-1821 (1995
26. Lee-Hoeflich ST, Crocker L, Yao E et al. A central role for HER3 in HER2-amplified breast cancer: implications for targeted therapy. Cancer Res. 68(14), 5878-5887 (2008
27. Holbro T, Beerli RR, Maurer F, Koziczak M, Barbas CF, Hynes NE. The ErbB2/ErbB3 heterodimer functions as an oncogenic unit: ErbB2 requires ErbB3 to drive breast tumor cell proliferation. Proc. Natl Acad. Sci. USA 100(15), 8933-8938 (2003
28. Vaught DB, Stanford JC, Young C et al. HER3 is required for HER2-induced preneoplastic changes to the breast epithelium and tumor formation. Cancer Res. 72(10), 2672-2682 (2012
29. Lahlou H, Müller T, Sanguin-Gendreau V, Birchmeier C, Muller WJ. Uncoupling of PI3K from ErbB3 impairs mammary gland development but does not impact on ErbB2-induced mammary tumorigenesis. Cancer Res. 72(12), 3080-3090 (2012
30. Baselga J, Swain SM. Novel anticancer targets: revisiting ERBB2 and discovering ERBB3. Nat. Rev. Cancer 9(7), 463-475 (2009
31. Nahta R, Yu D, Hung M-C, Hortobagyi GN, Esteva FJ. Mechanisms of disease: understanding resistance to HER2- targeted therapy in human breast cancer. Nat. Clin. Pract. Oncol. 3(5), 269-280 (2006
32. Friedman A, Perrimon N. Genetic screening for signal transduction in the era of network biology. Cell 128(2), 225-231 (2007
33. Sergina NV, Rausch M, Wang D et al. Escape from HER-family tyrosine kinase inhibitor therapy by the kinase-inactive HER3. Nature 445(7126), 437-441 (2007
34. Garrett JT, Olivares MG, Rinehart C et al. Transcriptional and posttranslational up-regulation of HER3 (ErbB3) compensates for inhibition of the HER2 tyrosine kinase. Proc. Natl Acad. Sci. USA 108(12), 5021-5026 (2011
35. Nahta R, Hung M-C, Esteva FJ. The HER-2-Targeting antibodies trastuzumab and pertuzumab synergistically inhibit the survival of breast cancer cells. Cancer Res. 64(7), 2343-2346 (2004
36. Baselga J. Treatment of HER2-overexpressing breast cancer. Ann. Oncol. 21(Suppl. 7), vii36-vii40 (2010
37. Swain SM, Kim S-B, Cortés J et al. Pertuzumab, trastuzumab, and docetaxel for HER2-positive metastatic breast cancer (CLEOPATRA study): overall survival results from a randomised, double-blind, placebo-controlled, Phase 3 study. Lancet Oncol. 14(6), 461-471 (2013
38. Chandarlapaty S, Sawai A, Scaltriti M et al. AKT inhibition relieves feedback suppression of receptor tyrosine kinase expression and activity. Cancer Cell 19(1), 58-71 (2011
39. Chakrabarty A, Sánchez V, Kuba MG, Rinehart C, Arteaga CL. Feedback upregulation of HER3 (ErbB3) expression and activity attenuates antitumor effect of PI3K inhibitors. Proc. Natl Acad. Sci. USA 109(8), 2718-2723 (2012
40. Garrett JT, Sutton CR, Kuba MG, Cook RS, Arteaga CL. Dual blockade of HER2 in HER2-overexpressing tumor cells does not completely eliminate HER3 function. Clin. Cancer Res. 19(3), 610-619 (2013
41. Sauter G, Lee J, Bartlett JM, Slamon DJ, Press MF. Guidelines for human epidermal growth factor receptor 2 testing: biologic and methodologic considerations. J. Clin. Oncol. 27(8), 1323-1333 (2009
42. Higgins MJ, Jelovac D, Barnathan E et al. Detection of tumor PIK3CA status in metastatic breast cancer using peripheral blood. Clin. Cancer Res. 18(12), 3462-3469 (2012
43. Gianni L, Bianchini G, Kiermaier A et al. S5-1: Neoadjuvant pertuzumab (P) and trastuzumab (H): biomarker analyses of a 4-arm randomized Phase II study (NeoSphere) in patients (pts) with HER2-positive breast cancer (BC). Cancer Res. 71(Suppl. 24), S5-S1 (2012
44. Baselga J, Cortés J, Im S et al. Biomarker analyses in CLEOPATRA: a Phase III, placebo-controlled study of pertuzumab in HER2-positive, first-line metastatic breast cancer (MBC). Cancer Res. 72(Suppl. 24), S5-S1 (2012
45. Baselga J, Verma S, Ro J et al. Relationship between tumor biomarkers (BM) and efficacy in EMILIA, a Phase III study of trastuzumab emtansine (T-DM1) in HER2-positive metastatic breast cancer (MBC). Presented at: 104th Annual Meeting of the American Association for Cancer Research. Washington, DC, USA, 6-10 April 2013
46. Lipton A, Goodman L, Leitzel K et al. HER3, p95HER2, and HER2 protein expression levels define multiple subtypes of HER2-positive metastatic breast cancer. Breast Cancer Res. Treat. 141(1), 43-53 (2013
47. Gaykema SB, Brouwers AH, Hovenga S, Lub-de Hooge MN, de Vries EG, Schröder CP. Zirconium-89-Trastuzumab positron emission tomography as a tool to solve a clinical dilemma in a patient with breast cancer. J. Clin. Oncol. 30(6), e74-e75 (2012
48. Perik PJ, Lub-De Hooge MN, Gietema JA et al. Indium-111- labeled trastuzumab scintigraphy in patients with human epidermal growth factor receptor 2-positive metastatic breast cancer. J. Clin. Oncol. 24(15), 2276-2282 (2006
49. Page K, Hava N, Ward B et al. Detection of HER2 amplification in circulating free DNA in patients with breast cancer. Br. J. Cancer 104(8), 1342-1348 (2011
50. Schneeweiss A, Chia S, Hegg R et al. Biomarker (BM) analyses of a Phase II study of neoadjuvant pertuzumab and trastuzumab with and without anthracycline (ATC)- containing chemotherapy for treatment of HER2-positive early breast cancer (BC)(TRYPHAENA). Presented at: ESMO 2012 Vienna. Austria, 28 September-2 October 2012
51. Schoeberl B, Faber AC, Li D et al. An ErbB3 antibody, MM- 121, is active in cancers with ligand-dependent activation. Cancer Res. 70(6), 2485-2494 (2010
52. Meneses-Lorente G, Kolm I, Thomas M et al. 382 Preclinical Pharmacokinetics of GE-huMab-HER3, a Novel Humanized, Glycoengineered Anti-HER3 Antibody Using PHER3/HER3 Ratio as Pharmacodynamics (PD) Marker. Eur. J. Cancer 48, 116-117 (2012
53. Wallweber J, Chenna A, Ravanera R, Huang W, Stathas D, Marshall G. Profiling HER3/ErbB3 activation in formalin-fixed, paraffin-embedded (FFPE) breast tumor samples that express high and low HER2/ErbB2 levels using proximity-based immunoassays. Presented at: 104th Annual Meeting of the American Association for Cancer Research. Washington, DC, USA, 6-10 April 2013
54. Razumienko EJ, Scollard DA, Reilly RM. Small-animal SPECT/CT of HER2 and HER3 expression in tumor xenografts in athymic mice using trastuzumab Fab-heregulin bispecific radioimmunoconjugates. J. Nucl. Med. 53(12), 1943-1950 (2012
55. Hudis CA. Trastuzumab - mechanism of action and use in clinical practice. N. Engl. J. Med. 357(1), 39-51 (2007
56. Agus DB, Akita RW, Fox WD et al. Targeting ligand-activated ErbB2 signaling inhibits breast and prostate tumor growth. Cancer cell. 2(2), 127-137 (2002
57. Slamon DJ, Leyland-Jones B, Shak S et al. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N. Engl. J. Med. 344(11), 783-792 (2001
58. Cobleigh MA, Vogel CL, Tripathy D et al. Multinational study of the efficacy and safety of humanized anti-HER2 monoclonal antibody in women who have HER2- overexpressing metastatic breast cancer that has progressed after chemotherapy for metastatic disease. J. Clin. Oncol. 17(9), 2639-2639 (1999
59. Cardoso F, Harbeck N, Fallowfield L, Kyriakides S, Senkus E. Locally recurrent or metastatic breast cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 23(Suppl. 7), vii11-vii19 (2012
60. Network NCC: NCCN clinical practice guidelines in oncology: breast cancer 2014, (Version 3.2014). www.nccn.org
61. von Minckwitz G, Du Bois A, Schmidt M 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), 1999-2006 (2009
62. de Azambuja E, Bedard PL, Suter T, Piccart-Gebhart M. Cardiac toxicity with anti-HER-2 therapies-what have we learned so far?. Target Oncol. 4(2), 77-88 (2009
63. Wood ER, Truesdale AT, McDonald OB et al. A unique structure for epidermal growth factor receptor bound to GW572016 (Lapatinib) relationships among protein conformation, inhibitor off-rate, and receptor activity in tumor cells. Cancer Res. 64(18), 6652-6659 (2004
64. O'Donovan N, Byrne AT, O'Connor AE, McGee S, Gallagher WM, Crown J. Synergistic interaction between trastuzumab and EGFR/HER-2 tyrosine kinase inhibitors in HER-2 positive breast cancer cells. Invest. New Drugs 29(5), 752-759 (2011
65. Konecny GE, Pegram MD, Venkatesan N et al. Activity of the dual kinase inhibitor lapatinib (GW572016) against HER-2-overexpressing and trastuzumab-Treated breast cancer cells. Cancer Res. 66(3), 1630-1639 (2006
66. Geyer CE, Forster J, Lindquist D et al. Lapatinib plus capecitabine for HER2-positive advanced breast cancer. N. Engl. J. Med. 355(26), 2733-2743 (2006
67. Baselga J, Cortés J, Kim S-B et al. Pertuzumab plus trastuzumab plus docetaxel for metastatic breast cancer. N. Engl. J. Med. 366(2), 109-119 (2012
68. Verma S, Miles D, Gianni L et al. Trastuzumab emtansine for HER2-positive advanced breast cancer. N. Engl. J. Med. 367(19), 1783-1791 (2012
69. 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. 28(8), 1301-1307 (2010
70. 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. 133(3), 1057-1065 (2012
71. Blackwell KL, Burstein HJ, Storniolo AM et al. Overall survival benefit with lapatinib in combination with trastuzumab for patients with human epidermal growth factor receptor 2-positive metastatic breast cancer: final results from the EGF104900 study. J. Clin. Oncol. 30(21), 2585-2592 (2012
72. Dieras V, Harbeck N, Albain K et al. A Phase Ib/II trial of trastuzumab-DM1 (T-DM1) with pertuzumab for patients with HER2-positive, locally advanced or metastatic breast cancer: interim efficacy and safety results. Presented at: Thirty-Third Annual CTRC-AACR San Antonio Breast Cancer Symposium . San Antonio, TX, USA, 8-12 December 2010
73. Swaby R, Blackwell K, Jiang Z et al. Neratinib in combination with trastuzumab for the treatment of advanced breast cancer: a Phase I/II study. J. Clin. Oncol. 27(15S), 1004 (2009
74. LoRusso P, Jänne PA, Oliveira M et al. Phase I study of U3-1287, a fully human anti-HER3 monoclonal antibody, in patients with advanced solid tumors. Clin. Cancer Res. 19(11), 3078-3087 (2013
75. Tyler SM, Vincent S, Fleet C et al. AV-203, a fully humanized ERBB3 inhibitory antibody, reverses ERBB3- induced resistance to targeted therapies. Presented at: 104th Annual Meeting of the American Association for Cancer Research. Washington, DC, USA, 6-10 April 2013
76. Garner AP, Bialucha CU, Sprague ER et al. An antibody that locks HER3 in the inactive conformation inhibits tumor growth driven by HER2 or Neuregulin. Cancer Res. 73(19), 6024-6035 (2013
77. Mirschberger C, Schiller CB, Schräml M et al. RG7116, a therapeutic antibody that binds the inactive HER3 receptor and is optimized for immune effector activation. Cancer Res. 73(16), 5183-5194 (2013
78. Meulendijks D, Lolkema MPJK, Voest EE et al. A first-in-human trial of RG7116, a glycoengineered monoclonal antibody targeting HER3, in patients with advanced/ metastatic tumors of epithelial cell origin expressing HER3 protein. Presented at: 104th Annual Meeting of the American Association for Cancer Research. Washington, DC, USA, 6-10 April 2013
79. Robinson MK, Hodge KM, Horak E et al. Targeting ErbB2 and ErbB3 with a bispecific single-chain Fv enhances targeting selectivity and induces a therapeutic effect in vitro. Br. J. Cancer. 99(9), 1415-1425 (2008
80. McDonagh CF, Huhalov A, Harms BD et al. Antitumor activity of a novel bispecific antibody that targets the ErbB2/ErbB3 oncogenic unit and inhibits heregulin-induced activation of ErbB3. Mol. Cell. Biol. 11(3), 582-593 (2012
81. Beeram M, Denlinger C, Tolcher A et al. MM-111 - a novel bispecific antibody targeting HER-2/HER-3 Z heterodimer: safety and tolerability in a first-in human Phase I/II study in patients with refractory HER2-positive (HER-2+) cancers Presented at: Thirty-Third Annual CTRC-AACR San Antonio Breast Cancer Symposium . San Antonio, TX, USA, 8-12 December 2010
82. Wang S, Huang J, Lyu H et al. Functional cooperation of miR-125a, miR-125b, and miR-205 in entinostat-induced downregulation of erbB2/erbB3 and apoptosis in breast cancer cells. Cell Death Dis. 4(3), e556 (2013
83. Huang X, Gao L, Wang S, Lee C-K, Ordentlich P, Liu B. HDAC inhibitor SNDX-275 induces apoptosis in erbB2- overexpressing breast cancer cells via down-regulation of erbB3 expression. Cancer Res. 69(21), 8403-8411 (2009
84. Huang X, Wang S, Lee C-K, Yang X, Liu B. HDAC inhibitor SNDX-275 enhances efficacy of trastuzumab in erbB2- overexpressing breast cancer cells and exhibits potential to overcome trastuzumab resistance. Cancer Lett. 307(1), 72-79 (2011
85. Kummar S, Gutierrez M, Gardner ER et al. Phase I trial of MS-275, a histone deacetylase inhibitor, administered weekly in refractory solid tumors and lymphoid malignancies. Clin. Cancer Res. 13(18), 5411-5417 (2007