Acquired resistance to EGFR tyrosine kinase inhibitors in cancer cells is mediated by loss of IGF-binding proteins

Journal of Clinical Investigation

Volumn 118, Issue 7, 2008, Pages 2609-2619

  Guix, Marta ^a   Faber, Anthony C ^b   Wang, Shizhen Emily ^c,d   Olivares, Maria Graciela ^a,d   Song, Youngchul ^b   Qu, Sherman ^a   Rinehart, Cammie ^a   Seidel, Brenda ^e   Yee, Douglas ^e   Arteaga, Carlos L ^a,c,f   Engelman, Jeffrey A ^b,g  

^a VANDERBILT UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c Department of Cancer Biology ^*  (United States)

^d VANDERBILT INGRAM CANCER CENTER   (United States)

^e UNIVERSITY OF MINNESOTA   (United States)

^f VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^g Cancer Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; GEFITINIB; INSULIN RECEPTOR SUBSTRATE 1; MITOGEN ACTIVATED PROTEIN KINASE; MK 0646; MONOCLONAL ANTIBODY; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RNA; SOMATOMEDIN BINDING PROTEIN; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN BINDING PROTEIN 4; SOMATOMEDIN C RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CELL GROWTH; CONTROLLED STUDY; DOWN REGULATION; FEMALE; GENE EXPRESSION; GROWTH INHIBITION; HUMAN; HUMAN CELL; LOADING DRUG DOSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; TUMOR CELL; TUMOR RECURRENCE; XENOGRAFT;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL SURVIVAL; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 3; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 4; INSULIN-LIKE GROWTH FACTOR BINDING PROTEINS; INSULIN-LIKE GROWTH FACTOR I; INSULIN-LIKE GROWTH FACTOR II; MICE; MICE, NUDE; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-3; RECEPTOR, IGF TYPE 1; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 46749156706     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JC134588     Document Type: Article

References (49)

1. Shepherd, F.A., et al. 2005. Erlotinib in previously treated non-small-cell lung cancer. N. Engl J. Med. 353:123-132.
2. Fukuoka, M., et al. 2003. Multi-institutional randomized phase II trial of gefitinib for previously treated patients with advanced non-small-cell lung cancer. J. Clin. Oncol. 21:2237-2246.
3. Kris, M.G., et al. 2003. Efficacy of gefitinib, an inhibitor of the epidermal growth factor receptor tyrosine kinase, in symptomatic patients with non-small cell lung cancer: a randomized trial. JAMA. 290:2149-2158.
4. Perez-Soler, R., et al. 2004. Determinants of tumor response and survival with erlotinib in patients with non-small-cell lung cancer. J. Clin. Oncol. 22:3238-3247.
5. Paez, J.G., et al. 2004. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science. 304:1497-1500.
6. Lynch, T.J., et al. 2004. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N. Engl. J. Med. 350:2129-2139.
7. Pao, W., et al. 2004. 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. U. S. A. 101:13306-13311.
8. Mitsudomi,T., et al. 2005. Mutations of the epidermal growth factor receptor gene predict prolonged survival after gefitinib treatment in patients with non-small-cell lung cancer with postoperative recurrence. J. Clin. Oncol. 23:2513-2520.
9. Han, S.W., et al. 2005. Predictive and prognostic impact of epidermal growth factor receptor mutation in non-small-cell lung cancer patients treated with gefitinib. J. Clin. Oncol. 23:2493-2501.
10. Takano, T., et al. 2005. Epidermal growth factor receptor gene mutations and increased copy numbers predict gefitinib sensitivity in patients with recurrent non-small-cell lung cancer. J. Clin. Oncol 23:6829-6837
11. Cappuzzo, F., et al. 2005. Epidermal growth factor receptor gene and protein and gefitinib sensitivity in non-small-cell lung cancer. J. Natl. Cancer Inst. 97:643-655.
12. Tsao, M.S., et al. 2005. Erlotinib in lung cancer - molecular and clinical predictors of outcome. N. Engl. J. Med. 353:133-144.
13. Engelman, J.A. 2007. The role of phosphoinositide 3-kinase pathway inhibitors in the treatment of lung cancer. Clin. Cancer Res. 13:s4637-s4640.
14. Kobayashi, S., et al. 2005. EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N. Engl. J. Med. 352:786-792.
15. Pao, W., et al. 2005. Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med. 2:e73.
16. Gorre, M.E., Ellwood-Yen, K.,Chiosis, G., Rosen, N., and Sawyers, C.L. 2002. BCR-ABL point mutants isolated from patients with imatinib mesylate-resistant chronic myeloid leukemia remain sensitive to inhibitors of the BCR-ABL chaperone heat shock protein 90. Blood. 100:3041-3044.
17. Antonescu, C.R., et al. 2005. Acquired resistance to imatinib in gastrointestinal stromal tumor occurs through secondary gene mutation. Clin. Cancer Res. 11:4182-4190.
18. Kwak, E.L., et al. 2005. Irreversible inhibitors of the EGF receptor may circumvent acquired resistance to gefitinib. Proc. Natl. Acad. Sci. U. S. A. 102:7665-7670.
19. Kosaka, T., et al. 2006. Analysis of epidermal growth factor receptor gene mutation in patients with non-small cell lung cancer and acquired resistance to gefitinib. Clin. Cancer Res. 12:5764-5769.
20. Balak, M.N., et al. 2006. Novel D761Y and common secondary T790M mutations in epidermal growth factor receptor-mutant lung adenocarcinomas with acquired resistance to kinase inhibitors. Clin. Cancer Res. 12:6494-6501.
21. Engelman, J.A., et al. 2007. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science. 316:1039-1043.
22. Bean, J., et al. 2007. MET amplification occurs with or without T790M mutations in EGFR mutant lung tumors with acquired resistance to gefitinib or erlotinib. Proc. Natl. Acad. Sci. U. S. A. 104:20932-20937.
23. Ogino, A., et al. 2007. Emergence of epidermal growth factor receptor T790M mutation during chronic exposure to gefitinib in a non small cell lung cancer cell line. Cancer Res. 67:7807-7814.
24. Engelman,J.A., et al. 2006. Allelic dilution obscures detection of a biologically significant resistance mutation in EGFR -amplified lung cancer. J. Clin. Invest. 116:2695-2706.
25. Yamasaki, F., et al. 2007. Acquired resistance to erlotinib in A-431 epidermoid cancer cells requires down-regulation of MMAC1/PTEN and up-regulation of phosphorylatedAkt. Cancer Res. 67:5779-5788.
26. Bianco, R., et al. 2003. Loss of PTEN/MMAC1/TEP in EGF receptor-expressing tumor cells counteracts the antitumor action of EGFR tyrosine kinase inhibitors. Oncogene. 22:2812-2822.
27. Engelman, J.A., et al. 2005. ErbB-3 mediates phosphoinositide 3-kinase activity in gefitinib-sensitive non-small cell lung cancer cell lines. Proc. Natl. Acad. Sci. U. S. A. 102:3788-3793.
28. Sebolt-Leopold, J.S., et al. 1999. Blockade of the MAP kinase pathway suppresses growth of colon tumors in vivo. Nat. Med. 5:810-816.
29. Knight, Z.A., et al. 2006. A pharmacological map of the P13-K family defines a role for p110alpha in insulin signaling. Cell. 125:733-747.
30. Engelman, J.A., Luo,J., and Cantley, L.C. 2006. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat. Rev. Genet. 7:606-619.
31. Garcia-Echeverria, C, et al. 2004. In vivo antitumor activity of NVP-AEW541-A novel, potent, and selective inhibitor of the IGF-IR kinase. Cancer Cell. 5:231-239.
32. Goetsch, L., et al. 2005. A recombinant humanized anti-insulin-like growth factor receptor type I antibody (h7C10) enhances the antitumor activity of vinorelbine and anti-epidermal growth factor receptor therapy against human cancer xenografts. Int. J. Cancer. 113:316-328.
33. Kurtz, A., Hartl, W., Jelkmann, W., Zapf, J., and Bauer, C. 1985. Activity in fetal bovine serum that stimulates erythroid colony formation in fetal mouse livers is insulinlike growth factor I. J. Clin. Invest. 76:1643-1648.
34. Wakeling, A.E., et al. 2002. ZD1839 (Iressa): an orally active inhibitor of epidermal growth factor signaling with potential for cancer therapy. Cancer Res. 62:5749-5754.
35. She, Q.B., et al. 2005. The BAD protein integrates survival signaling by EGFR/MAPK and P13K/Akt kinase pathways in PTEN-deficient tumor cells. Cancer Cell. 8:287-297.
36. Mellinghoff, I.K., et al. 2005. Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors. N. Engl. J. Med. 353:2012-2024.
37. Berns, K.,et al. 2007. A functional genetic approach identifies the P13K pathway as a major determinant of trastuzumab resistance in breast cancer. Cancer Cell. 12:395-402.
38. Takaoka, M., et al. 2004. Epidermal growth factor receptor regulates aberrant expression of insulinlike growth factor-binding protein 3. Cancer Res. 64:7711-7723.
39. Grimberg, A., and Cohen, P. 2000. Role of insulin-like growth factors and their binding proteins in growth control and carcinogenesis. J. Cell Physiol 183:1-9.
40. Torng, P.L., et al. 2007. Insulin-like growth factor binding protein-3 (IGFBP-3) acts as an invasion-metastasis suppressor in ovarian endometrioid carcinoma. Oncogene. 27:2137-2147.
41. Peng, L., Wang, J., Malloy, P.J., and Feldman, D. 2007. The role of insulin-like growth factor binding protein-3 in the growth inhibitory actions of androgens in LNCaP human prostate cancer cells. Int. J. Cancer. 122:558-566.
42. Takaoka, M., et al. 2007. IGFBP-3 regulates esophageal tumor growth through IGF-dependent and independent mechanisms. Cancer Biol. Ther 6:534-540.
43. Burger, A.M., Leyland-Jones, B., Banerjee, K., Spyropoulos, D.D., and Seth, A.K. 2005. Essential roles of IGFBP-3 and IGFBP-rP1 in breast cancer. Eur J. Cancer. 41:1515-1527.
44. Tolcher, A.W., et al. 2007. A phase I pharmacokinetic and pharmacodynamic study of AMG 479, a fully human monoclonal antibody against insulin-like growth factor type 1 receptor (IGF-1R), in advanced solid tumors. In Journal of Clinical Oncology 2007 ASCO Annual Meeting Proceedings Part I. June 1-5. Chicago, Illinois, USA. 25:3002.
45. Prieur, A., Tirode, F., Cohen, P., and Delattre, O. 2004. EWS/FLI-1 silencing and gene profiling of Ewing cells reveal downstream oncogenic pathways and a crucial role for repression of insulinlike growth factor binding protein 3. Mol. Cell. Biol. 24:7275-7283.
46. Perez-Torres, M., Guix, M., Gonzalez, A., and Arteaga, C.L. 2006. Epidermal growth factor receptor (EGFR) antibody down-regulates mutant receptors and inhibits tumors expressing EGFR mutations. J. Biol. Chem. 281:40183-40192.
47. Hossenlopp, P., Seurin, D., Segovia-Quinson, B., Hardouin, S., and Binoux, M. 1986. Analysis of serum insulin-like growth factor binding proteins using western blotting: use of the method for titration of the binding proteins and competitive binding studies. Anal. Biochem. 154:138-143.
48. McGuire, W.L., Jr., et al. 1992. Regulation of insulinlike growth factor-binding protein (IGFBP) expression by breast cancer cells: use of IGFBP-1 as an inhibitor of insulin-like growth factor action [erratum 1992, 84:1837]. J Natl. Cancer Inst. 84:1336-1341.
49. Debnath, J., Muthuswamy, S.K., and Brugge, J.S. 2003. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods. 30:256-268.