Irreversible pan-ErbB tyrosine kinase inhibitors and breast cancer: Current status and future directions

Cancer Treatment Reviews

Volumn 35, Issue 8, 2009, Pages 685-691

  Ocaña, Alberto ^a,b   Amir, Eitan ^a  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b HOSPITAL GENERAL UNIVERSITARIO DE ALBACETE   (Spain)

Author keywords

Breast cancer; HER2; Irreversible tyrosine kinase inhibitors; Lapatinib; Neratinib; Trastuzumab

Indexed keywords

4 [3 CHLORO 4 (2 PYRIDINYLMETHOXY)ANILINO] 3 CYANO 6 (4 DIMETHYLAMINOCROTONAMIDO) 7 ETHOXYQUINOLINE; ANASTROZOLE; BIBW 2992; CANERTINIB; CAPECITABINE; DOCETAXEL; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; FULVESTRANT; LAPATINIB; LETROZOLE; NAVELBINE; NEU DIFFERENTIATION FACTOR; PACLITAXEL; PELITINIB; PERTUZUMAB; TEMSIROLIMUS; TOVOK; TRASTUZUMAB; UNCLASSIFIED DRUG;

ANOREXIA; BREAST CANCER; CANCER HORMONE THERAPY; CANCER RESISTANCE; CHEMOTHERAPY INDUCED EMESIS; CLINICAL TRIAL; DIARRHEA; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG ERUPTION; DRUG SELECTIVITY; DRUG TOLERABILITY; DRUG TREATMENT FAILURE; DRUG WITHDRAWAL; FATIGUE; GASTROINTESTINAL SYMPTOM; HUMAN; IC 50; MALIGNANT TRANSFORMATION; NAUSEA; NONHUMAN; OVERALL SURVIVAL; PROGRESSION FREE SURVIVAL; RECOMMENDED DRUG DOSE; REVIEW; SOLID TUMOR; STOMATITIS;

AMINOQUINOLINES; ANILINE COMPOUNDS; ANTIBODIES, MONOCLONAL; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; DRUG RESISTANCE, NEOPLASM; FEMALE; FORECASTING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MORPHOLINES; PROGNOSIS; PROTEIN KINASE INHIBITORS; PROTEIN-TYROSINE KINASES; QUINAZOLINES; QUINOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; TUMOR MARKERS, BIOLOGICAL; UP-REGULATION;

EID: 70449722853     PISSN: 03057372     EISSN: 15321967     Source Type: Journal    
DOI: 10.1016/j.ctrv.2009.08.001     Document Type: Review

References (73)

1. Hudis C.A. Trastuzumab - mechanism of action and use in clinical practice. New Engl J Med 357 (2007) 39-51
2. Geyer C.E., Forster J., Lindquist D., et al. Lapatinib plus capecitabine for HER2-positive advanced breast cancer. New Engl J Med 355 (2006) 2733-2743
3. Hanahan D., and Weinberg R.A. The hallmarks of cancer. Cell 100 (2000) 57-70
4. Luo J., Solimini N.L., and Elledge S.J. Principles of cancer therapy: oncogene and non-oncogene addiction. Cell 136 (2009) 823-837
5. Pandiella A., Beguinot L., Vicentini L.M., et al. Transmembrane signalling at the epidermal growth factor receptor. Trends Pharmacol Sci 10 (1989) 411-414
6. Hynes N.E., and Lane H.A. ERBB receptors and cancer: the complexity of targeted inhibitors. Nat Rev Cancer 5 (2005) 341-354
7. Hynes N.E. Stern DF: the biology of ErbB-2/neu/HER2 and its role in cancer. Biochim Biophys Acta 1198 (1994) 165-184
8. Olayioye M.A., Neve R.M., Lane H.A., et al. The ErbB signaling network: receptor heterodimerization in development and cancer. Embo J 19 (2000) 3159-3167
9. Slamon D.J., Godolphin W., Jones L.A., et al. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 244 (1989) 707-712
10. Massagué J., and Pandiella A. Membrane-anchored growth factors. Annu Rev Biochem 62 (1993) 515-541
11. Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 103 (2000) 211-225
12. Cruz J.J., Ocana A., Del Barco E., et al. Targeting receptor tyrosine kinases and their signal transduction routes in head and neck cancer. Ann Oncol 18 (2007) 421-430
13. Graus-Porta D., Beerli R.R., Daly J.M., et al. ErbB-2, the preferred heterodimerization partner of all ErbB receptors, is a mediator of lateral signaling. Embo J 16 (1997) 1647-1655
14. Ocana A., and Pandiella A. Identifying breast cancer druggable oncogenic alterations: lessons learned and future targeted options. Clin Cancer Res 14 (2008) 961-970
15. Slamon D.J., Clark G.M., Wong S.G., et al. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 235 (1987) 177-182
16. Sliwkowski M.X., Lofgren J.A., Lewis G.D., et al. Nonclinical studies addressing the mechanism of action of trastuzumab (Herceptin). Semin Oncol 26 (1999) 60-70
17. Junttila T.T., Akita R.W., Parsons K., 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 (2009) 429-440
18. Xia W., Mullin R.J., Keith B.R., 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 21 (2002) 6255-6263
19. Ocana A., Cruz J.J., and Pandiella A. Trastuzumab and antiestrogen therapy: focus on mechanisms of action and resistance. Am J Clin Oncol 29 (2006) 90-95
20. Nahta R., and Esteva F.J. Trastuzumab: triumphs and tribulations. Oncogene 26 (2007) 3637-3643
21. 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 6 (2004) 117-127
22. Scaltriti M., Rojo F., Ocana 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 99 (2007) 628-638
23. de Alava E., Ocana A., Abad M., et al. Neuregulin expression modulates clinical response to trastuzumab in patients with metastatic breast cancer. J Clin Oncol 25 (2007) 2656-2663
24. Montero J.C., Ocana A., Abad M., et al. Expression of Erk5 in early stage breast cancer and association with disease free survival identifies this kinase as a potential therapeutic target. PLoS ONE 4 (2009) e5565
25. Slamon D.J., Leyland-Jones B., Shak S., et al. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. New Engl J Med 344 (2001) 783-792
26. Romond E.H., Perez E.A., Bryant J., et al. Trastuzumab plus adjuvant chemotherapy for operable HER2-positive breast cancer. New Engl J Med 353 (2005) 1673-1684
27. Piccart-Gebhart M.J., Procter M., Leyland-Jones B., et al. Trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer. New Engl J Med 353 (2005) 1659-1672
28. Joensuu H., Kellokumpu-Lehtinen P.L., Bono P., et al. Adjuvant docetaxel or vinorelbine with or without trastuzumab for breast cancer. New Engl J Med 354 (2006) 809-820
29. Buzdar A.U., Ibrahim N.K., Francis D., 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 23 (2005) 3676-3685
30. http://clinicaltrials.gov/ct2/show/NCT00706030 [accessed 25.05.09].
31. Di Leo A., Gomez H.L., Aziz Z., et al. Phase III, double-blind, randomized study comparing lapatinib plus paclitaxel with placebo plus paclitaxel as first-line treatment for metastatic breast cancer. J Clin Oncol 26 (2008) 5544-5552
32. Gelmon K.A., Fumoleau P., Verma S., et al. Results of a phase II trial of trastuzumab (H) and pertuzumab (P) in patients (pts) with HER2-positive metastatic breast cancer (MBC) who had progressed during trastuzumab therapy. J Clin Oncol (2008) 26 [May 20 suppl; abstr 1026]
33. Prat A., and Baselga J. The role of hormonal therapy in the management of hormonal-receptor-positive breast cancer with co-expression of HER2. Nat Clin Pract Oncol 5 (2008) 531-542
34. Mackey JR, Kaufman B, Clemens M, et al. Trastuzumab prolongs progression-free survival in hormone-dependent and HER2-positive metastatic breast cancer. [abstract #a3]. In: Proceedings of the San Antonio Breast Cancer Symposium: 2006 December 14-17; 2006. San Antonio, TX.
35. Johnston S., Pegram M., Press M., et al. Lapatinib combined with letrozole vs. letrozole alone for front line postmenopausal hormone receptor positive (HR plus) metastatic breast cancer (MBC): first results from the EGF30008 Trial. Cancer Res 69 2 (2009) 74S-75S
36. Manning G., Whyte D.B., Martinez R., et al. The protein kinase complement of the human genome. Science 298 (2002) 1912-1934
37. Blume-Jensen P., and Hunter T. Oncogenic kinase signalling. Nature 411 (2001) 355-365
38. Zhang J., Yang P.L., and Gray N.S. Targeting cancer with small molecule kinase inhibitors. Nat Rev Cancer 9 (2009) 28-39
39. Lugo T.G., Pendergast A.M., Muller A.J., et al. Tyrosine kinase activity and transformation potency of bcr-abl oncogene products. Science 247 (1990) 1079-1082
40. Sawyers C.L. Chronic myeloid leukemia. New Engl J Med 340 (1999) 1330-1340
41. Baselga J. Targeting tyrosine kinases in cancer: the second wave. Science 312 (2006) 1175-1178
42. Baselga J., and Arteaga C.L. Critical update and emerging trends in epidermal growth factor receptor targeting in cancer. J Clin Oncol 23 (2005) 2445-2459
43. Paez J.G., Janne P.A., Lee J.C., et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 304 (2004) 1497-1500
44. Sordella R., Bell D.W., Haber D.A., et al. Gefitinib-sensitizing EGFR mutations in lung cancer activate anti-apoptotic pathways. Science 305 (2004) 1163-1177
45. Xia W., Bisi J., Strum J., et al. Regulation of survivin by ErbB2 signaling: therapeutic implications for ErbB2-overexpressing breast cancers. Cancer Res 66 (2006) 1640-1647
46. Shah N.P., Nicoll J.M., Nagar B., et al. Multiple BCR-ABL kinase domain mutations confer polyclonal resistance to the tyrosine kinase inhibitor imatinib (STI571) in chronic phase and blast crisis chronic myeloid leukemia. Cancer Cell 2 (2002) 117-125
47. Pao W., Miller V.A., Politi K.A., et al. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med 2 (2005) e73
48. Ocana A., Serrano R., Calero R., et al. Novel tyrosine kinase inhibitors in the treatment of cancer. Curr Drug Targets 10 6 (2009) 1
49. Sergina N.V., Rausch M., Wang D., et al. Escape from HER-family tyrosine kinase inhibitor therapy by the kinase-inactive HER3. Nature 445 (2007) 437-441
50. Rabindran S.K., Discafani C.M., Rosfjord E.C., et al. Antitumor activity of HKI-272, an orally active, irreversible inhibitor of the HER-2 tyrosine kinase. Cancer Res 64 (2004) 3958-3965
51. Cohen M.S., Zhang C., Shokat K.M., et al. Structural bioinformatics-based design of selective, irreversible kinase inhibitors. Science 308 (2005) 1318-1321
52. Kwak E.L., Sordella R., Bell D.W., et al. Irreversible inhibitors of the EGF receptor may circumvent acquired resistance to gefitinib. Proc Natl Acad Sci USA 102 (2005) 7665-7670
53. Ji H., Li D., Chen L., et al. The impact of human EGFR kinase domain mutations on lung tumorigenesis and in vivo sensitivity to EGFR-targeted therapies. Cancer Cell 9 (2006) 485-495
54. Ji H., Zhao X., Yuza Y., et al. Epidermal growth factor receptor variant III mutations in lung tumorigenesis and sensitivity to tyrosine kinase inhibitors. Proc Natl Acad Sci USA 103 (2006) 7817-7822
55. Wong K.K., Fracasso P.M., Bukowski R.M., et al. A phase I study with neratinib (HKI-272), an irreversible pan ErbB receptor tyrosine kinase inhibitor, in patients with solid tumors. Clin Cancer Res 15 (2009) 2552-2558
56. Burstein H.J., Sun Y., Tan A.R., et al. Neratinib (HKI-272), an irreversible pan ErbB receptor tyrosine kinase inhibitor: phase 2 results in patients with advanced HER2+ breast cancer. Cancer Res 69 Suppl. 2 (2009) 73s [abstract 37]
57. Eskens F.A., Mom C.H., Planting A.S., et al. A phase I dose escalation study of BIBW 2992, an irreversible dual inhibitor of epidermal growth factor receptor 1 (EGFR) and 2 (HER2) tyrosine kinase in a 2-week on, 2-week off schedule in patients with advanced solid tumours. Brit J Cancer 98 (2008) 80-85
58. Agus D, Terlizzi E, Stopfer P, et al. A phase I dose escalation study of BIBW 2992, an irreversible dual EGFR/HER2 receptor tyrosine kinase inhibitor, in a continuous schedule in patients with advanced solid tumours. J Clin Oncol 2006;24:49s (suppl; abstract 2074).
59. Hickish T, Wheatley D, Lin N, et al. Use of BIBW 2992, a novel irreversible EGFR/HER2 tyrosine kinase inhibitor (TKI), to treat patients with HER2-positive metastatic breast cancer after failure of treatment with trastuzumab. J Clin Oncol 2009;27:15s (suppl; abstr 1023).
60. Erlichman C., Hidalgo M., Boni J.P., et al. Phase I study of EKB-569, an irreversible inhibitor of the epidermal growth factor receptor, in patients with advanced solid tumors. J Clin Oncol 24 (2006) 2252-2260
61. Nemunaitis J., Eiseman I., Cunningham C., et al. Phase 1 clinical and pharmacokinetics evaluation of oral CI-1033 in patients with refractory cancer. Clin Cancer Res 11 (2005) 3846-3853
62. Rixe O, Franco SX, Yardley DA, et al. A randomized, phase II, dose-finding study of the pan-ErbB receptor tyrosine-kinase inhibitor CI-1033 in patients with pretreated metastatic breast cancer. Cancer Chemother Pharmacol 2009.
63. Ritter C.A., Perez-Torres M., Rinehart C., 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 (2007) 4909-4919
64. Eichhorn P.J., Gili M., Scaltriti M., 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 (2008) 9221-9230
65. Kaufman B., Mackey J., Clemens M., et al. Trastuzumab plus anastrozole prolongs progression-free survival in postmenopausal women with HER2-positive, hormonedependent metastatic breast cancer (MBC). Ann Oncol 17 Suppl. 17 (2006) LBA2 [abstract]
66. Johnston S., Pegram M., Press M., et al. Lapatinib combined with letrozole vs. letrozole alone for front line postmenopausal hormone receptor positive (HR+) metastatic breast cancer (MBC): first results from the EGF30008 Trial. Cancer Res 69 2 (2009) 74S-75S
67. Montero J.C., Rodriguez-Barrueco R., Ocana A., et al. Neuregulins and cancer. Clin Cancer Res 14 (2008) 3237-3241
68. Paik S., Kim C., and Wolmark N. HER2 status and benefit from adjuvant trastuzumab in breast cancer. New Engl J Med 358 (2008) 1409-1411
69. Vogel C.L., Cobleigh M.A., Tripathy D., et al. Efficacy and safety of trastuzumab as a single agent in first-line treatment of HER2-overexpressing metastatic breast cancer. J Clin Oncol 20 (2002) 719-726
70. Marty M., Cognetti F., Maraninchi D., 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 (2005) 4265-4274
71. Marcom P.K., Isaacs C., Harris L., et al. The combination of letrozole and trastuzumab as first or second-line biological therapy produces durable responses in a subset of HER2 positive and ER positive advanced breast cancers. Breast Cancer Res Treat 102 (2007) 43-49
72. 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 (2009) 1999-2006
73. Cameron .D., Casey M., Press M., 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 (2008) 533-543