Trastuzumab (Herceptin®) and breast cancer: Mechanisms of resistance;Trastuzumab (Herceptin®) et cancer du sein: Mécanismes de résistance

Bulletin du Cancer

Volumn 94, Issue 3, 2007, Pages 259-266

  Dieras, Véronique ^a   Vincent Salomon, Anne ^a   Degeorges, Armelle ^a   Beuzeboc, Philippe ^a   Mignot, Laurent ^a   De Cremoux, Patricia ^a  

^a INSTITUT CURIE   (France)

Author keywords

Breast cancer; Resistance; Trastuzumab

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ONCOPROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; SOMATOMEDIN C RECEPTOR; TRASTUZUMAB; ANTINEOPLASTIC AGENT; CYCLIN DEPENDENT KINASE INHIBITOR 1B; MONOCLONAL ANTIBODY; PTEN PROTEIN, HUMAN; SOMATOMEDIN RECEPTOR; TUMOR PROTEIN; UNCLASSIFIED DRUG;

BREAST CANCER; CANCER RELAPSE; CANCER RESISTANCE; CELL CYCLE REGULATION; DRUG MECHANISM; HUMAN; ONCOGENE; PROTEIN EXPRESSION; REVIEW; TREATMENT INDICATION; BREAST TUMOR; DRUG RESISTANCE; FEMALE; GENETICS; METABOLISM; MUTATION; PROTO ONCOGENE; SIGNAL TRANSDUCTION;

ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CYCLIN-DEPENDENT KINASE INHIBITOR P27; DRUG RESISTANCE, NEOPLASM; FEMALE; GENES, ERBB-2; HUMANS; MUTATION; NEOPLASM PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; RECEPTORS, SOMATOMEDIN; SIGNAL TRANSDUCTION;

EID: 33947492723     PISSN: 00074551     EISSN: 17696917     Source Type: Journal    
DOI: 10.1684/bdc.2007.0216     Document Type: Review

References (71)

1. Yarden Y, Sliwkowski MX. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2001 ; 2 : 127-37.
2. Earp HS, Dawson TL, Li X, Yu H. Heterodimerization and functional interaction between EGF receptor family members : a new signaling paradigm with implications for breast cancer research. Breast Cancer Res Treat 1995 ; 35 : 115-32.
3. Olayioye MA, Neve RM, Lane HA, Hynes NE. The ErbB signaling network : receptor heterodimerization in development and cancer. EMBO J 2000 ; 19 : 3159-67.
4. Arteaga CL. Overview of epidermal growth factor receptor biology and its role as a therapeutic target in human neoplasia. Semin Oncol 2002 ; 29(Suppl 14) : 3-9.
5. Menard S, Pupa SM, Campiglio M, Tagliabue E. Biologic and therapeutic role of HER2 in cancer. Oncogene 2003 ; 22 : 6570-8.
6. Vincent-Salomon A, MacGrogan G, Couturier J, Arnould L, Denoux Y, Fiche M, et al. Calibration of immunohistochemistry for assessment of HER2 in breast cancer : results of the French multicentre GEFPICS study. Histopathology 2003 ; 42 : 337-47.
7. Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG, Keith DE, et al. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 1989 ; 244 : 707-12.
8. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL, et al. Human breast cancer : correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987 ; 235 : 177-82.
9. Bange J, Zwick E, Ullrich A. Molecular targets for breast cancer therapy and prevention. Nat Med 2001 ; 7 : 548-52.
10. Cho HS, Mason K, Ramyar KX, Stanley AM, Gabelli SB, Denney DW, et al. Structure of the extracellular region of HER2 alone and in complex with the Herceptin Fab. Nature 2003 ; 421 : 756-60.
11. Baselga J. Clinical trials of Herceptin (R) (trastuzumab). Eur J Cancer 2001 ; 37(Suppl 1) : 18-24.
12. Yu D, Hung MC. Overexpression of ErbB2 in cancer and ErbB2-targeting strategies. Oncogene 2000 ; 19 : 6115-21.
13. Yakes FM, Chinratanalab W, Ritter CA, King W, Seelig S, Arteaga CL. 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.
14. Xu F, Xia W, Luo RZ, Peng H, Zhao S, Dai J, et al. The human ARHI tumor suppressor gene inhibits lactation and growth in transgenic mice. Cancer Res 2000 ; 60 : 4913-20.
15. Molina MA, Codony-Servat J, Albanell J, Rojo F, Arribas J, Baselga J. Trastuzumab (herceptin), a humanized anti-Her2 receptor monoclonal antibody, inhibits basal and activated Her2 ectodomain cleavage in breast cancer cells. Cancer Res 2001 ; 61 : 4744-9.
16. Sliwkowski MX, Lofgren JA, Lewis GD, Hotaling TE, Fendly BM, Fox JA. Nonclinical studies addressing the mechanism of action of trastuzumab (Herceptin). Semin Oncol 1999 ; 26(Suppl 12) : 60-70.
17. Petit AM, Rak J, Hung MC, Rockwell P, Goldstein N, Fendly B, et al. Neutralizing antibodies against epidermal growth factor and ErbB-2/neu receptor tyrosine kinases down-regulate vascular endothelial growth factor production by tumor cells in vitro and in vivo : angiogenic implications for signal transduction therapy of solid tumors. Am J Pathol 1997 ; 151 : 1523-30.
18. Clynes RA, Towers TL, Presta LG, Ravetch JV. Inhibitory Fc receptors modulate in vivo cytoxicity against tumor targets. Nat Med 2000 ; 6 : 443-6.
19. Cobleigh MA, Vogel CL, Tripathy D, Robert NJ, Scholl S, Fehrenbacher L, 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 1999 ; 17 : 2639-48.
20. Spigel DR, Burstein HJ. Trastuzumab regimens for HER2-overexpressing metastatic breast cancer. Clin Breast Cancer 2003 ; 4 : 329-37 ; (discussion 338-9).
21. Vogel CL, Cobleigh MA, Tripathy D, Gutheil JC, Harris LN, Fehrenbacher L, 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 : 719-26.
22. Burstein HJ, Hattis LN, Marcom PK, Lambert-Falls R, Havlin K, Overmoyer B, et al. Trastuzumab and vinorelbine as first-line therapy for HER2-overexpressing metastatic breast cancer : multicenter phase II trial with clinical outcomes, analysis of serum tumor markers as predictive factors, and cardiac surveillance algorithm. J Clin Oncol 2003 ; 21 : 2889-95.
23. Slamon DJ, Leyland-Jones B, Shak S, Fuchs H, Paton V, Bajamonde A, 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.
24. Buzdar AU, Ibrahim NK, Francis D, Booser DJ, Thomas ES, Theriault RL, et al. Significantly higher pathologic complete remission rate after neoadjuvant therapy with trastuzumab, paclitaxel, and epirubicin chemotherapy : results of a randomized trial in human epidermal growth factor receptor 2-positive operable breast cancer. J Clin Oncol 2005 ; 23 : 3656-9.
25. Baselga J, Albanell J. Mechanism of action of anti-HER2 monoclonal antibodies. Ann Oncol 2001 ; 12(Suppl 1) : S35-S41.
26. Normanno N, Campiglio M, De LA, Somenzi G, Maiello M, Ciardiello F, et al. Cooperative inhibitory effect of ZD1839 (Iressa) in combination with trastuzumab (Herceptin) on human breast cancer cell growth. Ann Oncol 2002 ; 13 : 65-72.
27. Monnier L, Milano G, Penault-Llorca F, Merlin JL. Bull Cancer 2004 ; 91 : 685-94 ; [Targeting of membrane receptor tyrosine kinases : is there resistance in the HER? ].
28. Nagy P, Friedlander E, Tanner M, Kapanen AI, Carraway KL, Isola J, et al. Decreased accessibiliry and lack of activation of ErbB2 in JIMT-1, a herceptin-resistant, MUC4-expressing breast cancer cell line. Cancer Res 2005 ; 65 : 473-82.
29. Price-Schiavi SA, Jepson S, Li P, Arango M, Rudland PS, Yee L, 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.
30. Russ WP, Engelman DM. The GxxxG motif : a framework for transmembrane helix-helix association. J Mol Biol 2000 ; 296 : 911-9.
31. Fleishman SJ, Schlessinger J, Ben-Tal N. A putative molecular-activation switch in the transmembrane domain of erbB2. Proc Natl Acad Sci USA 2002 ; 99 : 15937-40.
32. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW, et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 2004 ; 350 : 2129-39.
33. Paez JG, Janne PA, Lee JC, Tracy S, Greulich H, Gabriel S, et al. EGFR mutations in lung cancer : correlation with clinical response to gefitinib therapy. Science 2004 ; 304 : 1497-500.
34. Pao W, Miller V, Zakowski M, Doherty J, Politi K, Sarkaria I, et al. EGF receptor gene mutations are common in lung cancers from "never smokers" and are associated with sensitivity of tumors ro gefitinib and erlotinib. Proc Natl Acad Sci USA 2004 ; 101 : 13306-11.
35. Sordella R, Bell DW, Haber DA, Settleman J. Gefitinib-sensitizing EGFR mutations in lung cancer activate anti-apoptotic pathways. Science 2004 ; 305 : 1163-7.
36. Stephens P, Hunter C, Bignell G, Edkins S, Davies H, Teague J, et al. Lung cancer : intragenic ERBB2 kinase mutations in tumours. Nature 2004 ; 431 : 525-6.
37. Shigematsu H, Takahashi T, Nomura M, Majmudar K, Suzuki M, Lee H, et al. Somatic mutations of the HER2 kinase domain in lung adenocarcinomas. Cancer Res 2005 ; 65 : 1642-6.
38. Moulder SL, Yakes FM, Muthuswamy SK, Bianco R, Simpson JF, Arteaga CL. Epidermal growth factor receptor (HER1) tyrosine kinase inhibitor ZD1839 (Iressa) inhibits HER2/neu (erbB2)-overexpressing breast cancer cells in vitro and in vivo. Cancer Res 2001 ; 61 : 8887-95.
39. Konecny G, Slamon DJ. HER2 testing and correlation with efficacy of trastuzumab therapy. Oncology (Huntingt) 2002 ; 16 : 1576-8.
40. Xia W, Mullin RJ, Keith BR, Liu LH, Ma H, Rusnak DW, et al. Antitumor 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.
41. Arteaga CL, O'Neil A, Moulder SL. ECOG1100 : a phase I-II study of combined blockade of the erbB receptor network with trastuzumab and gefitinib (Iressa) in patients (pts) with HER2- overexpressing metastatic breast cancer (met br ca). Breast Cancer Res Treat 2004 ; 88(Suppl 1) : S15 ; (abstract 25).
42. Spector NL, Xia W, Burris 3rd H, Hurwitz H, Dees EC, Dowlati A, et al. Study of the biologic effects of lapatinib, a reversible inhibitor of ErbB1 and ErbB2 tyrosine kinases, on tumor growth and survival pathways in patients with advanced malignancies. J Clin Oncol 2005 ; 23 : 2502-12.
43. Burris 3rd HA, Hurwitz HI, Dees EC, Dowlati A, Blackwell KL, O'Neil B, 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 prerreated patients with metastatic carcinomas. J Clin Oncol 2005 ; 23 : 5305-13.
44. Zhang X, Yee D. Tyrosine kinase signalling in breast cancer : insulin-like growth factors and their receptors in breast cancer. Breast Cancer Res 2000 ; 2 : 170-5.
45. Lu Y, Zi X, Zhao Y, Mascarenhas D, Pollak M. Insulin-like growth factor-I receptor signaling and resistance to trastuzumab (Herceptin). J Natl Cancer Inst 2001 ; 93 : 1852-7.
46. Balana ME, Labriola L, Salatino M, Movsichoff F, Peters G, Charreau EH, et al. Activation of ErbB-2 via a hierarchical interaction between ErbB-2 and type I insulin-like growth factor receptor in mammary tumor cells. Oncogene 2001 ; 20 : 34-47.
47. Reiss K, Valentinis B, Tu X, Xu SQ, Baserga R. Molecular markers of IGF-I-mediated mitogenesis. Exp Cell Res 1998 ; 242 : 361-72.
48. Lu Y, Zi X, Pollak M. Molecular mechanisms underlying IGF-I-induced attenuation of the growth-inhibitory acrivity of trastuzumab (Herceptin) on SKBR3 breast cancer cells. Int J Cancer 2004 ; 108 : 334-41.
49. Albanell J, Baselga J. Unraveling resistance to trastuzumab (Herceptin) : insulin-like growth factor-I receptor, a new suspect. J Natl Cancer Inst 2001 ; 93 : 1830-2.
50. Datta SR, Brunet A, Greenberg ME. Cellular survival : a play in three Akts. Genes Dev 1999 ; 13 : 2905-27.
51. del Peso L, Gonzalez-Garcia M, Page C, Herrera R, Nunez G. Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 1997 ; 278 : 687-9.
52. Cardone MH, Roy N, Stennicke HR, Salvesen GS, Franke TF, Stanbridge E, et al. Regulation of cell death protease caspase-9 by phosphorylation. Science 1998 ; 282 : 1318-21.
53. Kang SS, Kwon T, Kwon DY, Do SI. Akt protein kinase enhances human telomerase activity through phosphorylation of telomerase reverse Transcriptase subunit. J Biol Chem 1999 ; 274 : 13085-90.
54. Clark AS, West K, Streicher S, Dennis PA. Constitutive and inducible Akt activity promotes resistance to chemotherapy, trastuzumab, or tamoxifen in breast cancer cells. Mol Cancer Ther 2002 ; 1 : 707-17.
55. Shin I, Yakes FM, Rojo F, Shin NY, Bakin AV, Baselga J, et al. PKB/Akt mediates cell-cycle progression by phosphorylation of p27 (Kip1) at threonine 157 and modulation of its cellular localization. Nat Med 2002 ; 8 : 1145-52.
56. Kute T, Lack CM, Willingham M, Bishwokama B, Williams H, Barrett K, et al. Development of Herceptin resistance in breast cancer cells. Cytometry A 2004 ; 57 : 86-93.
57. Liang J, Zubovitz J, Petrocelli T, Kotchetkov R, Connor MK, Han K, et al. PKB/Akt phosphorylates p27, impairs nuclear import of p27 and opposes p27-mediated G1 arrest. Nat Med 2002 ; 8 : 1153-60.
58. Penuel E, Schaefer G, Akita RW, Sliwkowski MX. Structural requirements for ErbB2 transactivation. Semin Oncol 2001 ; 28(6 Suppl 18) : 36-42.
59. Nahta R, Takahashi T, Ueno NT, Hung MC, Esteva FJ. P27 (kip1) down-regulation is associated with trastuzumab resistance in breast cancer cells. Cancer Res 2004 ; 64 : 3981-6.
60. Pagano M, Tam SW, Theodoras AM, Beer-Romero P, Del Sal G, Chau V, et al. Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science 1995 ; 269 : 682-5.
61. Cantley LC. The phosphoinositide 3-kinase pathway. Science 2002 ; 296 : 1655-7.
62. Sansal I, Sellers WR. The biology and clinical relevance of the PTEN tumor suppressor pathway. J Clin Oncol 2004 ; 22 : 2954-63.
63. Nagata Y, Lan KH, Zhou X, Tan M, Esteva FJ, Sahin AA, 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.
64. Di Cristofano A, Pandolfi PP. The multiple roles of PTEN in tumor suppression. Cell 2000 ; 100 : 387-90.
65. Feilotter HE, Coulon V, McVeigh JL, Boag AH, Dorion-Bonnet F, Duboue B, et al. Analysis of the 10q23 chromosomal region and the PTEN gene in human sporadic breast carcinoma. Br J Cancer 1999 ; 79 : 718-23.
66. Whang YE, Wu X, Suzuki H, Reiter RE, Tran C, Vessella RL, et al. Inactivation of the tumor suppressor PTEN/MMAC1 in advanced human prostate cancer through loss of expression. Proc Natl Acad Sci USA 1998 ; 95 : 5246-50.
67. Parsons R, Simpson L. PTEN and cancer. Methods Mol Biol 2003 ; 222 : 147-66.
68. Lu Y, Lin YZ, LaPushin R, Cuevas B, Fang X, Yu SX, et al. The PTEN/MMAC1/TEP tumor suppressor gene decreases cell growth and induces apoptosis and anoikis in breast cancer cells. Oncogene 1999 ; 18 : 7034-45.
69. Trotman LC, Niki M, Dotan ZA, Koutcher JA, Di Cristofano A, Xiao A, et al. Pten dose dictates cancer progression in the prostate. PLoS Biol 2005 ; 1 : E59.
70. Buzdar AU, Hunt KK, Smith T, Francis D, Ewer M, Booser D, et al. Significantly higher pathological complete remission (PCR) rate following neoadjuvant therapy with trastuzumab (H), paclitaxel (P), and anthracycline-containing chemotherapy (CT) : Initial results of a randomized trial in operable breast cancer (BC) with HER/2 positive disease. J Clin Oncol 2004 ; 22(Suppl.) : 14S.
71. Gennari R, Menard S, Fagnoni F, Ponchio L, Scelsi M, Tagliabue E, et al. Pilot study of the mechanism of action of preoperative trastuzumab in patients with primary operable breast tumors overexpressing HER2. Clin Cancer Res 2004 ; 10 : 5650-5.