Overcoming resistance to tyrosine kinase inhibitors: Lessons learned from cancer cells treated with EGFR antagonists

Cell Cycle

Volumn 8, Issue 1, 2009, Pages 18-22

  Rexer, Brent N ^b   Engelman, Jeffrey A ^b   Arteaga, Carlos L ^a  

^a VANDERBILT INGRAM CANCER CENTER   (United States)

^b NONE

Author keywords

Breast cancer; EGFR; HER2; PI3K; TKI resistance; Tyrosine kinase inhibitors

Indexed keywords

4 [3 CHLORO 4 (2 PYRIDINYLMETHOXY)ANILINO] 3 CYANO 6 (4 DIMETHYLAMINOCROTONAMIDO) 7 ETHOXYQUINOLINE; AEW 541; CETUXIMAB; CL 387785; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; GEFITINIB; IMATINIB; LAPATINIB; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN TYROSINE KINASE INHIBITOR; TRASTUZUMAB; UNCLASSIFIED DRUG; EPIDERMAL GROWTH FACTOR RECEPTOR 2; PROTEIN KINASE INHIBITOR;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BREAST CANCER; CANCER RESISTANCE; CANCER SURVIVAL; CELL VIABILITY; DOWN REGULATION; DRUG INHIBITION; GENE AMPLIFICATION; GENE EXPRESSION PROFILING; HUMAN; LUNG NON SMALL CELL CANCER; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; BIOLOGICAL MODEL; DRUG ANTAGONISM; DRUG EFFECT; DRUG RESISTANCE; ENZYMOLOGY; NEOPLASM; PATHOLOGY;

DRUG RESISTANCE, NEOPLASM; HUMANS; MODELS, BIOLOGICAL; NEOPLASMS; PROTEIN KINASE INHIBITORS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2;

EID: 60749085908     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.8.1.7324     Document Type: Review

References (44)

1. Blume-Jensen P, Hunter T. Oncogenic kinase signalling. Nature 2001; 411:355-65.
2. Sergina NV, Moasser MM. The HER family and cancer: emerging molecular mechanisms and therapeutic targets. Trends Mol Med 2007; 13:527-34.
3. Guix M, Faber AC, Wang SE, Olivares MG, Song Y, Qu S, et al. Acquired resistance to EGFR tyrosine kinase inhibitors in cancer cells is mediated by loss of IGF-binding proteins. J Clin Invest 2008; 118:2609-19.
4. 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.
5. Paez JG, Jänne 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.
6. 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 to gefitinib and erlotinib. Proc Natl Acad Sci USA 2004; 101:13306-11.
7. Tsao MS, Sakurada A, Cutz JC, Zhu CQ, Kamel-Reid S, Squire J, et al. Erlotinib in lung cancer - molecular and clinical predictors of outcome. N Engl J Med 2005; 353:133-44.
8. Engelman JA, Zejnullahu K, Mitsudomi T, Song Y, Hyland C, Park JO, et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007; 316:1039-43.
9. Antonescu CR, Besmer P, Guo T, Arkun K, Hom G, Koryotowski B, et al. Acquired resistance to imatinib in gastrointestinal stromal tumor occurs through secondary gene mutation. Clin Cancer Res 2005; 11:4182-90.
10. Gorre ME, Mohammed M, Ellwood K, Hsu N, Paquette R, Rao PN, et al. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 2001; 293:876-80.
11. Shah NP, Sawyers CL. Mechanisms of resistance to STI571 in Philadelphia chromosome-associated leukemias. Oncogene 2003; 22:7389-95.
12. Kobayashi S, Boggon TJ, Dayaram T, Jänne PA, Kocher O, Meyerson M, et al. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med 2005; 352:786-92.
13. Pao W, Miller VA, Politi KA, Riely GJ, Somwar R, Zakowski MF, et al. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med 2005; 2:73.
14. Engelman JA, Mukohara T, Zejnullahu K, Lifshits E, Borrás AM, Gale CM, et al. Allelic dilution obscures detection of a biologically significant resistance mutation in EGFR-amplified lung cancer. J Clin Invest 2006; 116:2695-706.
15. Ogino A, Kitao H, Hirano S, Uchida A, Ishiai M, Kozuki T, et al. Emergence of epidermal growth factor receptor T790M mutation during chronic exposure to gefitinib in a non small cell lung cancer cell line. Cancer Res 2007; 67:7807-14.
16. Yuza Y, Glatt KA, Jiang J, Greulich H, Minami Y, Woo MS, et al. Allele-dependent variation in the relative cellular potency of distinct EGFR inhibitors. Cancer Biol Ther 2007; 6:661-7.
17. Geyer CE, Forster J, Lindquist D, Chan S, Romieu CG, Pienkowski T, et al. Lapatinib plus capecitabine for HER2-positive advanced breast cancer. N Engl J Med 2006; 355:2733-43.
18. Joensuu H, Kellokumpu-Lehtinen PL, Bono P, Alanko T, Kataja V, Asola R, et al. Adjuvant docetaxel or vinorelbine with or without trastuzumab for breast cancer. N Engl J Med 2006; 354:809-20.
19. Piccart-Gebhart MJ, Procter M, Leyland-Jones B, Goldhirsch A, Untch M, Smith I, et al. Trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer. N Engl J Med 2005; 353:1659-72.
20. Romond EH, Perez EA, Bryant J, Suman VJ, Geyer CE, Davidson NE, et al. Trastuzumab plus adjuvant chemotherapy for operable HER2-positive breast cancer. N Engl J Med 2005; 353:1673-84.
21. 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.
22. Valabrega G, Montemurro F, Aglietta M. Trastuzumab: mechanism of action, resistance and future perspectives in HER2-overexpressing breast cancer. Annals of Oncology 2007; 18:977.
23. Engelman JA, Jänne PA, Mermel C, Pearlberg J, Mukohara T, Fleet C, et al. ErbB-3 mediates phosphoinositide 3-kinase activity in gefitinib-sensitive non-small cell lung cancer cell lines. Proc Natl Acad Sci USA 2005; 102:3788-93.
24. Le XF, Lammayot A, Gold D, Lu Y, Mao W, Chang T, et al. Genes affecting the cell cycle, growth, maintenance and drug sensitivity are preferentially regulated by anti-HER2 antibody through phosphatidylinositol 3-kinase-AKT signaling. J Biol Chem 2005; 280:2092-104.
25. 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.
26. Ritter CA, Perez-Torres M, Rinehart C, Guix M, Dugger T, Engelman JA, 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 2007; 13:4909-19.
27. Samuels Y, Ericson K. Oncogenic PI3K and its role in cancer. Curr Opin Oncol2006; 18:77-82.
28. Sansal I, Sellers W. The Biology and Clinical Relevance of the PTEN Tumor Suppressor Pathway. J Clin Oncol 2004; 22:2954.
29. Berns K, Horlings HM, Hennessy BT, Madiredjo M, Hijmans EM, Beelen K, et al. A functional genetic approach identifies the PI3K pathway as a major determinant of trastuzumab resistance in breast cancer. Cancer Cell 2007; 12:395-402.
30. 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.
31. 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.
32. Nahta R, Yu D, Hung MC, Hortobagyi GN, Esteva FJ. Mechanisms of disease: understanding resistance to HER2-targeted therapy in human breast cancer. Nat Clin Pract Oncol 2006; 3:269-80.
33. Nahta R, Yuan LX, Zhang B, Kobayashi R, Esteva FJ. 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.
34. Shattuck DL, Miller JK, Carraway KL, 3rd, Sweeney C. Met receptor contributes to trastuzumab resistance of Her2-overexpressing breast cancer cells. Cancer Res 2008; 68:1471-7.
35. Buttitta F, Barassi F, Fresu G, Felicioni L, Chella A, Paolizzi D, et al. Mutational analysis of the HER2 gene in lung tumors from Caucasian patients: mutations are mainly present in adenocarcinomas with bronchioloalveolar features. Int J Cancer 2006; 119:2586-91.
36. Mounawar M, Mukeria A, Le Calvez F, Hung RJ, Renard H, Cortot A, et al. Patterns of EGFR, HER2, TP53 and KRAS mutations of p14arf expression in non-small cell lung cancers in relation to smoking history. Cancer Res 2007; 67:5667-72.
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. 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.
39. Willmore-Payne C, Holden JA, Layfield LJ. Detection of epidermal growth factor receptor and human epidermal growth factor receptor 2 activating mutations in lung adenocarcinoma by high-resolution melting amplicon analysis: correlation with gene copy number, protein expression and hormone receptor expression. Hum Pathol 2006; 37:755-63.
40. Willmore-Payne C, Holden JA, Layfield LJ. Detection of EGFR- and HER2-activating mutations in squamous cell carcinoma involving the head and neck. Mod Pathol 2006; 19:634-40.
41. Lee JW, Soung YH, Seo SH, Kim SY, Park CH, Wang YP, et al. Somatic mutations of ERBB2 kinase domain in gastric, colorectal and breast carcinomas. Clin Cancer Res 2006; 12:57-61.
42. Wang SE, Narasanna A, Perez-Torres M, Xiang B, Wu FY, Yang S, et al. HER2 kinase domain mutation results in constitutive phosphorylation and activation of HER2 and EGFR and resistance to EGFR tyrosine kinase inhibitors. Cancer Cell 2006; 10:25-38.
43. Xia W, Bacus S, Hegde P, Husain I, Strum J, Liu L, 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 2006; 103:7795-800.
44. Sergina NV, Rausch M, Wang D, Blair J, Hann B, Shokat KM, et al. Escape from HER-family tyrosine kinase inhibitor therapy by the kinase-inactive HER3. Nature 2007; 445:437-41.