Can we circumvent resistance to ErbB2-targeted agents by targeting novel pathways?

Clinical Breast Cancer

Volumn 8, Issue SUPPL. 3, 2008, Pages

  Pegram, Mark ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Lapatinib; Mammalian target of rapamycin; MUC4; PI3K; PTEN; Trastuzumab

Indexed keywords

3 BROMO 5 TERT BUTYL 4 HYDROXYBENZYLIDENEMALONONITRILE; 4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; ANASTROZOLE; BEVACIZUMAB; CD16 ANTIGEN; CP 751871; CYCLIN DEPENDENT KINASE INHIBITOR 1B; DOXORUBICIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPITOPE; ESTROGEN RECEPTOR; EVEROLIMUS; EXEMESTANE; KI 67 ANTIGEN; LAPATINIB; LETROZOLE; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE; MUCIN 4; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; RAF PROTEIN; RAS PROTEIN; S6 KINASE; TAMOXIFEN; TRASTUZUMAB;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BREAST CANCER; CANCER RESISTANCE; CELL GROWTH; CELL PROLIFERATION; CLINICAL TRIAL; DIARRHEA; DRUG RESEARCH; FATIGUE; GENE MUTATION; HEART LEFT VENTRICLE EJECTION FRACTION; HUMAN; LOADING DRUG DOSE; NAUSEA; NONHUMAN; REVIEW; SIDE EFFECT; SIGNAL TRANSDUCTION; STEREOSPECIFICITY;

EID: 42449124652     PISSN: 15268209     EISSN: None     Source Type: Journal    
DOI: 10.3816/CBC.2008.s.008     Document Type: Article

References (96)

1. Slamon DJ, Clark GM, Wong SG, et al. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/new oncogene. Science 1987; 235:177-82.
2. 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 2001; 344:783-92.
3. Olayioye MA, Neve RM, Lane HA, et al. The ErbB signaling network: receptor heterodimerization in development and cancer. EMBO J 2000; 19:3159-67.
4. Yu X, Sharma KD, Takahashi T, et al. Ligand-independent dimer formation of epidermal growth factor receptor (EGFR) is a step separable from ligand-induced EGFR signaling. Mol Biol Cell 2002; 13:2547-57.
5. Hudis CA. Trastuzumab - mechanism of action and use in clinical practice. N Engl J Med 2007; 357:39-51.
6. Weiner LM, Adams GP. New approaches to antibody therapy. Oncogene 2000; 19:6144-51.
7. Normanno N, Maiello MR, De Luca A. Epidermal growth factor receptor tyrosine kinase inhibitors (EGFR-TKIs): simple drugs with a complex mechanism of action? J Cell Physiol 2003; 194:13-9.
8. Joensuu H, Kellokumpu-Lehtinen P-L, Bono P, et al. Adjuvant docetaxel or vinorelbine with or without trastuzumab for breast cancer. N Engl J Med 2006; 354:809-20.
9. Piccart-Gebhart MJ, Procter M, Leyland-Jones B, et al. Trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer. N Engl J Med 2005; 353:1659-72.
10. Romond EH, Perez EA, Bryant J, et al. Trastuzumab plus adjuvant chemotherapy for operable HER2-positive breast cancer. N Engl J Med 2005; 353:1673-84.
11. Slamon D, Eiermann W, Robert N, et al. BCIRG 006: 2nd interim analysis phase III randomized trial comparing doxorubicin and cyclophosphamide followed by docetaxel (AC→T) with doxorubicin and cyclophosphamide followed by docetaxel and trastuzumab (AC→TH) with docetaxel, carboplatin and trastuzumab (TCH) in Her2neu positive early breast cancer patients. Presented at: 29th Annual San Antonio Breast Cancer Symposium; December 14-17, 2006; San Antonio, TX. Abstract 52.
12. Nahta R, Esteva FJ. Herceptin: mechanisms of action and resistance. Cancer Lett 2006; 232:123-38.
13. Pino V, Ramsauer VP, Salas P, et al. Membrane mucin Muc4 induces density-dependent changes in ERK activation in mammary epithelial and tumor cells: role in reversal of contact inhibition. J Biol Chem 2006; 281:29411-20.
14. Li S, Gerrard ER Jr, Balkovetz DF. Evidence for ERK1/2 phosphorylation controlling contact inhibition of proliferation in Madin-Darby canine kidney epithelial cells. Am J Physiol Cell Physiol 2004; 287:C432-9.
15. Nagy P, Friedländer E, Tanner M, et al. Decreased accessibility and lack of activation of ErbB2 in JIMT-1, a herceptin-resistant, MUC4-expressing breast cancer cell line. Cancer Res 2005; 65:473-82.
16. Moniaux N, Andrianifahanana M, Brand RE, et al. Multiple roles of mucins in pancreatic cancer, a lethal and challenging malignancy. Br J Cancer 2004; 91:1633-8.
17. Carraway KL, Price-Schiavi SA, Komatsu M, et al. Muc4/sialomucin complex in the mammary gland and breast cancer. J Mammary Gland Biol Neoplasia 2001; 6:323-37.
18. Price-Schiavi SA, Jepson S, Li P, et al. Rat Muc4 (sialomucin complex) reduces binding of anti-ErbB2 antibodies to tumor cell surfaces, a potential mechanism for herceptin resistance. Int J Cancer 2002; 99:783-91.
19. Tanner M, Kapanen AI, Junttila T, et al. Characterization of a novel cell line established from a patient with Herceptin-resistant breast cancer. Mol Cancer Ther 2004; 3:1585-92.
20. 2-terminal truncated HER-2 protein but not full-length receptor is associated with nodal metastasis in human breast cancer. Clin Cancer Res 2002; 8:347-53.
21. Anido J, Scaltriti M, Bech Serra JJ, et al. Biosynthesis of tumorigenic HER2 C-terminal fragments by alternative initiation of translation. EMBO J 2006; 25:3234-44.
22. Codony-Servat J, Albaneil J, Lopez-Talavera JC, et al. Cleavage of the HER2 ectodomain is a pervanadate-activable process that is inhibited by the tissue inhibitor of metalloproteases-1 in breast cancer cells. Cancer Res 1999; 59:1196-201.
23. 2-terminally truncated HER-2/neu protein: relationship with shedding of the extracellular domain and with prognostic factors in breast cancer. Cancer Res 1998; 58:5123-9.
24. Burris HA III, Hurwitz HI, Dees EC, et al. Phase I safety, pharmacokinetics, and clinical activity study of lapatinib (GW572016), a reversible dual inhibitor of epidermal growth factor receptor tyrosine kinases, in heavily pretreated patients with metastatic carcinomas. J Clin Oncol 2005; 23:5305-13.
25. Blackwell KL, Kaplan EH, Franco SX, et al. A phase II, open label, multicenter study of GW572016 in patients with trastuzumab-refractory metastatic breast cancer. Proc Am Soc Clin Oncol 2004; 23:196 (Abstract 3006).
26. Burstein H, Storniolo AM, Franco S, et al. A phase II, open label, multicenter study of lapatinib in two cohorts of patients with advanced or metastatic breast cancer who have progressed while receiving trastuzumab-containing regimens. Ann Oncol 2004; 15(suppl 3):27 (Abstract 1040).
27. Geyer CE, Martin A, Newstat B, et al. Lapatinib (L) plus capecitabine (C) in HER2+ advanced breast cancer (ABC): Genomic and updated efficacy data. J Clin Oncol 2007; 25(18 suppl):40s (Abstract 1035).
28. Scaltriti M, Rojo F, Ocaña A, 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 2007; 99:628-38.
29. Paez JG, Jänne PA, Lee JC, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004; 304:1497-500.
30. Kobayashi S, Boggon TJ, Dayaram T, et al. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med 2005; 352:786-92.
31. Lee JW, Soung YH, Seo SH, et al. Somatic mutations of ERBB2 kinase domain in gastric, colorectal, and breast carcinomas. Clin Cancer Res 2006; 12:57-61.
32. Khoury T, Mojica W, Hicks DG, et al. Trastuzumab binding site mutations in HER2 positive invasive breast cancer: a potential predictor of less aggressive disease and trastuzumab resistance. Breast Cancer Res Treat 2006; 100(suppl 1):S31 (Abstract 308).
33. Kip1 via multiple signaling pathways. Cell Cycle 2005; 4:87-95.
34. Kip1 down-regulation is associated with trastuzumab resistance in breast cancer cells. Cancer Res 2004; 64:3981-6.
35. Neve RM, Chin K, Fridlyand J, et al. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 2006; 10:515-27.
36. Pandolfi PP. Breast cancer - loss of PTEN predicts resistance to treatment. N Engl J Med 2004; 351:2337-8.
37. Yakes FM, Chinratanalab W, Ritter CA, et al. Herceptin-induced inhibition of phosphatidylinositol-3 kinase and Akt is required for antibody-mediated effects on p27, cyclin D1, and antitumor action. Cancer Res 2002; 62:4132-41.
38. Nagata Y, Lan K-H, Zhou X, et al. PTEN activation contributes to tumor inhibition by trastuzumab, and loss of PTEN predicts trastuzumab resistance in patients. Cancer Cell 2004; 6:117-27.
39. Campbell RA, Bhat-Nakshatri P, Patel NM, et al. Phosphatidylinositol 3-kinase/AKT-mediated activation of estrogen receptor α: a new model for anti-estrogen resistance. J Biol Chem 2001; 276:9817-24.
40. Cantley LC. The phosphoinositide 3-kinase pathway. Science 2002; 296:1655-7.
41. Nicholson KM, Anderson NG. The protein kinase B/Akt signalling pathway in human malignancy. Cell Signal 2002; 14:381-95.
42. Clark AS, West K, Streicher S, et al. Constitutive and inducible Akt activity promotes resistance to chemotherapy, trastuzumab, or tamoxifen in breast cancer cells. Mol Cancer Ther 2002; 1:707-17.
43. Pérez-Tenorio G, Stål O. Activation of AKT/PKB in breast cancer predicts a worse outcome among endocrine treated patients. Br J Cancer 2002; 86:540-5.
44. Aoki M, Blazek E, Vogt PK. A role of the kinase mTOR in cellular transformation induced by the oncoproteins P3k and Akt. Proc Natl Acad Sci U S A 2001; 98:136-41.
45. Burnett PE, Barrow RK, Cohen NA, et al. RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. Proc Natl Acad Sci U S A 1998; 95:1432-7.
46. Yu K, Toral-Barza L, Discafani C, et al. mTOR, a novel target in breast cancer: the effect of CCI-779, an mTOR inhibitor, in preclinical models of breast cancer. Endocr Relat Cancer 2001; 8:249-58.
47. Beuvink I, Boulay A, Fumagalli S, et al. The mTOR inhibitor RAD001 sensitizes tumor cells to DNA-damaged induced apoptosis through inhibition of p21 translation. Cell 2005; 120:747-59.
48. Macaskill EJ, Bartlett JMS, White S, et al. The mammalian target of rapamycin inhibitor RAD001 (everolimus) in postmenopausal women with early breast cancer: results of a phase II pre-operative trial. Presented at: 29th Annual San Antonio Breast Cancer Conference; December 14-17, 2006; San Antonio, TX. Abstract 6092.
49. Lu C-H, Wyszomierski SL, Tseng LM, et al. Preclinical testing of clinically applicable strategies for overcoming trastuzumab resistance caused by PTEN deficiency. Clin Cancer Res 2007; 13:5883-8.
50. Xia W, Husain I, Liu L, et al. Lapatinib antitumor activity is not dependent upon phosphatase and tensin homologue deleted on chromosome 10 in ErbB2-overexpressing breast cancers. Cancer Res 2007; 67:1170-5.
51. Xia W, Mullin RJ, Keith BR, et al. 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; 21:6255-63.
52. ErbB2) is regulated by heregulin through heterodimer formation with ErbB3 yet remains sensitive to the dual EGFR/ErbB2 kinase inhibitor GW572016. Oncogene 2004; 23:646-53.
53. Graus-Porta D, Beerli RR, Daly JM, et al. ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. EMBO J 1997; 16:1647-55.
54. Nahta R, Yu D, Hung M-C, et al. Mechanisms of disease: understanding resistance to HER2-targeted therapy in human breast cancer. Nat Clin Pract Oncol 2006; 3:269-80.
55. Storniolo AM, Burns HA III, Overmoyer B, et al. A phase I, open-label study of the safety, tolerability and pharmacokinetics of lapatinib (GW572016) in combination with trastuzumab. Breast Cancer Res Treat 2005; 94(suppl 1):S64 (Abstract 1073).
56. ErbB2 over-expressing metastatic breast cancer study using paclitaxel, trastuzumab, and lapatinib. ClinicalTrials.gov [Web site]Available at: http://clinicaltrials.gov/ct2/show/NCT00272987?term= lapatinib+trastuzumab+paclitaxel&rank=2. Accessed: February 25, 2008.
57. ALTTO (Adjuvant Lapatinib and/or Trastuzumab Treatment Optimisation) Study; BIG 2-06/N063D. ClinicalTrials.gov [Web site]. Available at: http://clinicaltrials.gov/ct/show/NCT004901397order=10. Accessed: August 17, 2007.
58. Camirand A, Lu Y, Pollak M. Co-targeting HER2/ErbB2 and insulin-like growth factor-1 receptors causes synergistic inhibition of growth in HER2-overexpressing breast cancer cells. Med Sci Monit 2002; 8:BR521-6.
59. Lu Y, Zi X, Zhao Y, et al. Insulin-like growth factor-I receptor signaling and resistance to trastuzumab (Herceptin). J Natl Cancer Inst 2001; 93:1852-7.
60. Harris LN, You F, Schnitt SJ, et al. Predictors of resistance to preoperative trastuzumab and vinorelbine for HER2-positive early breast cancer. Clin Cancer Res 2007; 13:1198-207.
61. Chakravarti A, Loeffler JS, Dyson NJ. Insulin-like growth factor receptor I mediates resistance to anti-epidermal growth factor receptor therapy in primary human glioblastoma cells through continued activation of phosphoinositide 3-kinase signaling. Cancer Res 2002; 62:200-7.
62. Jones HE, Goddard L, Gee JMW, et al. Insulin-like growth factor-1 receptor signalling and acquired resistance to gefitinib (ZD1839; Iressa) in human breast and prostate cancer cells. Endocr Relat Cancer 2004; 11:793-814.
63. Wan X, Harkavy B, Shen N, et al. Rapamycin induces feedback activation of Akt signaling through an IGF-1R-dependent mechanism. Oncogene 2007; 26:1932-40.
64. Nahta R, Yuan LXH, Zhang B, et al. Insulin-like growth factor-I receptor/human epidermal growth factor receptor 2 heterodimerization contributes to trastuzumab resistance of breast cancer cells. Cancer Res 2005; 65:11118-28.
65. Karp DD, Paz-Ares LG, Blakely LJ, et al. Efficacy of the anti-insulin like growth factor I receptor (IGF-IR) antibody CP-751871 in combination with paclitaxel and carboplatin as first-line treatment for advanced non-small cell lung cancer (NSCLC). J Clin Oncol 2007; 25(18 suppl):386s (Abstract 7506).
66. Study Of CP-751,871 in combination with exemestane in postmenopausal women with hormone receptor positive advanced breast cancer. ClinicalTrials.gov [Web site]. Available at: http://clinicaltrials.gov/ct/show/NCT00372996?order=3. Accessed: September 13, 2007.
67. Schiff R, Massarweh SA, Shou J, et al. Cross-talk between estrogen receptor and growth factor pathways as a molecular target for overcoming endocrine resistance. Clin Cancer Res 2004; 10:331S-6S.
68. Cato AC, Nestl A, Mink S. Rapid actions of steroid receptors in cellular signaling pathways. Sci STKE 2002; 2002:RE9.
69. Lösel RM, Falkenstein E, Feuring M, et al. Nongenomic steroid action: controversies, questions, and answers. Physiol Rev 2003; 83:965-1016.
70. Chung Y-L, Sheu M-L, Yang S-C, et al. Resistance to tamoxifen-induced apoptosis is associated with direct interaction between Her2/neu and cell membrane estrogen receptor in breast cancer. Int J Cancer 2002; 97:306-12.
71. Figtree GA, McDonald D, Watkins H, et al. Truncated estrogen receptor α 46-kDa isoform in human endothelial cells: relationship to acute activation of nitric oxide synthase. Circulation 2003; 107:120-6.
72. Li L, Haynes MP, Bender JR. Plasma membrane localization and function of the estrogen receptor α variant (ER46) in human endothelial cells. Proc Natl Acad Sci U S A 2003; 100:4807-12.
73. Osborne CK, Coronado-Heinsohn EB, Hilsenbeck SG, et al. Comparison of the effects of a pure steroidal antiestrogen with those of tamoxifen in a model of human breast cancer. J Natl Cancer Inst 1995; 87:746-50.
74. Wong C-W, McNally C, Nickbarg E, et al. Estrogen receptor-interacting protein that modulates its nongenomic activity-crosstalk with Src/Erk phosphorylation cascade. Proc Natl Acad Sci U S A 2002; 99:14783-8.
75. Nicholson RI, McClelland RA, Robertson JFR, et al. Involvement of steroid hormone and growth factor cross-talk in endocrine response in breast cancer. Endocr Relat Cancer 1999; 6:373-87.
76. Osborne CK, Bardou V, Hopp TA, et al. Role of the estrogen receptor coactivator AIB1 (SRC-3) and HER-2/neu in tamoxifen resistance in breast cancer. J Natl Cancer Inst 2003; 95:353-61.
77. Shou J, Massarweh S, Osborne CK, et al. Mechanisms of tamoxifen resistance: increased estrogen receptor-HER2/neu cross-talk in ER/HER2-positive breast cancer. J Natl Cancer Inst 2004; 96:926-35.
78. Arpino G, Weiss H, Wakeling AE, et al. Complete disappearance of ER+/HER2+ breast cancer xenografts with the combination of gefitinib, trastuzumab, and pertuzumab to block HER2 crosstalk with ER and restore tamoxifen inhibition. Breast Cancer Res Treat 2004; 88(suppl 1):S15 (Abstract 23).
79. Rimawi MF, Weiss HL, Arpino G, et al. Potent inhibition of EGFR(ErbB1)/HER2(ErbB2) pathway plus estrogen deprivation is a superior therapeutic combination in ER positive HER2-neu over-expressing breast tumor xenografts. Breast Cancer Res Treat 2006; 100(suppl 1): (Abstract 302).
80. Xia W, Bacus S, Hegde P, 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 U S A 2006; 103:7795-800.
81. Mackey JR, Kaufman B, Clemens M, et al. Trastuzumab prolongs progression-free survival in hormone-dependent and HER2-positive metastatic breast cancer. Breast Cancer Res Treat 2006; 100(suppl 1):S5 (Abstract 3).
82. Chu I, Blackwell K, Chen S, et al. The dual ErbB1/ErbB2 inhibitor, lapatinib (GW572016), cooperates with tamoxifen to inhibit both cell proliferation- and estrogen-dependent gene expression in antiestrogen-resistant breast cancer. Cancer Res 2005; 65:18-25.
83. Gasparini G, Toi M, Gion M, et al. Prognostic significance of vascular endothelial growth factor protein in node-negative breast carcinoma. J Natl Cancer Inst 1997; 89:139-47.
84. Relf M, LeJeune S, Scott PAE, et al. Expression of the angiogenic factors vascular endothelial cell growth factor, acidic and basic fibroblast growth factor, tumor growth factor β-1, platelet-derived endothelial cell growth factor, placenta growth factor, and pleiotrophin in human primary breast cancer and its relation to angiogenesis. Cancer Res 1997; 57:963-9.
85. Sjögren S, Inganäs M, Lindgren A, et al. Prognostic and predictive value of c-erbB-2 overexpression in primary breast cancer, alone and in combination with other prognostic markers. J Clin Oncol 1998; 16:462-9.
86. Konecny GE, Meng YG, Untch M, et al. Association between HER-2 neu and vascular endothelial growth factor expression predicts clinical outcome in primary breast cancer patients. Clin Cancer Res 2004; 10:1706-16.
87. du Manoir JM, Francia G, Man S, et al. Strategies for delaying or treating in vivo acquired resistance to trastuzumab in human breast cancer xenografts. Clin Cancer Res 2006; 12:904-16.
88. Pegram MD, Yeon C, Ku NC, et al. Phase I combined biological therapy of breast cancer using two humanized monoclonal antibodies directed against HER2 proto-oncogene and vascular endothelial growth factor (VEGF). Breast Cancer Res Treat 2004; 88(suppl 1):S124 (Abstract 3039).
89. Pegram M, Chan D, Dichmann RA, et al. Phase II combined biological therapy targeting the HER2 proto-oncogene and the vascular endothelial growth factor using trastuzumab (T) and bevacizumab (B) as first line treatment of HER2-amplified breast cancer. Breast Cancer Res Treat 2006; 100(suppl 1):S28 (Abstract 301).
90. Dejonge M, Savage S, Verweij JA, et al. A phase I, open-label study of the safety and pharmacokinetics (PK) of pazopanib (P) and lapatinib (L) administered concurrently. J Clin Oncol 2006; 24(18 suppl):142s (Abstract 3088).
91. Clynes RA, Towers TL, Presta LG, et al. Inhibitory Fc receptors modulate in vivo cytoxicity against tumor targets. Nat Med 2000; 6:443-6.
92. Musolino A, Naldi N, Bortesi B, et al. Immunoglobulin G fragment C receptor polymorphisms and response to trastuzumab-based treatment in patients with HER-2/neu-positive metastatic breast cancer. Breast Cancer Res Treat 2006; 100(suppl 1): (Abstract 3137).
93. Varchetta S, Gibelli N, Oliviero B, et al. Elements related to heterogeneity of antibody-dependent cell cytotoxicity in patients under trastuzumab therapy for primary operable breast cancer overexpressing Her2. Cancer Res 2007; 67:11991-9.
94. Lazar GA, Dang W, Karki S, et al. Engineered antibody Fc variants with enhanced effector function. Proc Natl Acad Sci U S A 2006; 103:4005-10.
95. Miller KD. The role of ErbB inhibitors in trastuzumab resistance. Oncologist 2004; 9(suppl 3):16-9.
96. Nahta R, Esteva FJ. HER2 therapy: molecular mechanisms of trastuzumab resistance. Breast Cancer Res 2006; 8:215.