Phosphorylated Insulin-Like Growth Factor 1 Receptor is Implicated in Resistance to the Cytostatic Effect of Gefitinib in Colorectal Cancer Cells

Journal of Gastrointestinal Surgery

Volumn 15, Issue 6, 2011, Pages 942-957

  Yang, Li ^a,b   Li, Jianjun ^a   Ran, Li ^b   Pan, Feng ^a   Zhao, Xiaoxin ^a   Ding, Zhenyu ^a   Chen, Yuying ^a   Peng, Qiuping ^c   Liang, Houjie ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b GUIZHOU MEDICAL UNIVERSITY   (China)

^c The 94th Hospital of PLA   (China)

Author keywords

Colorectal cancer; Epidermal growth factor receptor; Gefitinib; Insulin like growth factor receptor 1 ; Phosphorylation

Indexed keywords

3 BROMO 5 TERT BUTYL 4 HYDROXYBENZYLIDENEMALONONITRILE; AGAMMAGLOBULINAEMIA TYROSINE KINASE; ANTINEOPLASTIC AGENT; EPIDERMAL GROWTH FACTOR RECEPTOR; GEFITINIB; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN TYROSINE KINASE; QUINAZOLINE DERIVATIVE; SCATTER FACTOR RECEPTOR; SOMATOMEDIN C RECEPTOR; TYRPHOSTIN;

APOPTOSIS; ARTICLE; CELL CYCLE; CELL PROLIFERATION; COLORECTAL TUMOR; DRUG EFFECT; DRUG RESISTANCE; HUMAN; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; COLORECTAL NEOPLASMS; DRUG RESISTANCE, NEOPLASM; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-MET; QUINAZOLINES; RECEPTOR CROSS-TALK; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, IGF TYPE 1; SIGNAL TRANSDUCTION; TYRPHOSTINS;

EID: 79955826778     PISSN: 1091255X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11605-011-1504-z     Document Type: Article

References (62)

1. Venook A. Critical evaluation of current treatments in metastatic colorectal cancer. Oncologist 2005; 10: 250-261.
2. Salomon DS, Brandt R, Ciardiello F, Normanno N. Epidermal growth factor-related peptides and their receptors in human malignancies. Crit Rev Oncol Hematol 1995; 19: 183-232.
3. Nicholson RI, Gee JM, Harper ME. EGFR and cancer prognosis. Eur J Cancer 2001; 37: S9-S15.
4. Mendelsohn J, Baselga J. Status of epidermal growth factor receptor antagonists in the biology and treatment of cancer. J Clin Oncol 2003; 21: 2787-2799.
5. Tabernero J. The role of VEGF and EGFR inhibition: implications for combining anti-VEGF and anti-EGFR agents. Mol Cancer Res 2007; 5: 203-220.
6. Wakeling AE, Guy SP, Woodburn JR, Ashton SE, Curry BJ, Barker AJ, Gibson KH. ZD1839 (Iressa): an orally active inhibitor of epidermal growth factor signaling with potential for cancer therapy. Cancer Res 2002; 62: 5749-5754.
7. Ciardiello F, Caputo R, Bianco R, Damiano V, Pomatico G, De Placido S, Bianco AR, Tortora G. Antitumor effect and potentiation of cytotoxic drugs activity in human cancer cells by ZD-1839 (Iressa), an epidermal growth factor receptor-selective tyrosine kinase inhibitor. Clin Cancer Res 2000; 6: 2053-2063.
8. Sirotnak FM, Zakowski MF, Miller VA, Scher HI, Kris MG. Efficacy of cytotoxic agents against human tumor xenografts is markedly enhanced by coadministration of ZD1839 (Iressa), an inhibitor of EGFR tyrosine kinase. Clin Cancer Res 2000; 6: 4885-4892.
9. Koizumi F, Kanzawa F, Ueda Y, Koh Y, Tsukiyama S, Taguchi F, Tamura T, Saijo N, Nishio K. Synergistic interaction between the EGFR tyrosine kinase inhibitor gefitinib ("Iressa") and the DNA topoisomerase I inhibitor CPT-11 (irinotecan) in human colorectal cancer cells. Int J Cancer 2004; 108: 464-472.
10. Williams KJ, Telfer BA, Stratford IJ, Wedge SR. ZD1839 ('Iressa'), a specific oral epidermal growth factor receptor-tyrosine kinase inhibitor, potentiates radiotherapy in a human colorectal cancer xenograft model. Br J Cancer 2002; 86: 1157-1161.
11. Goss GD, Stewart DJ, Hirte H, Miller W, Major P, Batist G, Mathews S, Douglas L, Lorimer I, Seymour L. Initial results of part 2 of a phase I/II pharmacokinetic, pharmacodynamic and biological activity study of ZD1839 ('Iressa'): NCIC CTG IND. 122. Proc Am Soc Clin Oncol 2002; 21: 16 (Abs 59).
12. Rothenberg ML, LaFleur B, Levy DE, Washington MK, Morgan-Meadows SL, Ramanathan RK, Berlin JD, Benson AB 3rd, Coffey RJ. Randomized phase II trial of the clinical and biological effects of two dose levels of gefitinib in patients with recurrent colorectal adenocarcinoma. J Clin Oncol 2005; 23: 9265-9274.
13. Chau I, Cunningham D, Hickish T, Massey A, Higgins L, Osborne R, Botwood N, Swaisland A. Gefitinib and irinotecan in patients with fluoropyrimidine-refractory, irinotecan-naive advanced colorectal cancer: a phase I-II study. Ann Oncol 2007; 18: 730-737.
14. Jimeno A, Grávalos C, Escudero P, Sevilla I, Vega-Villegas ME, Alonso V, Juez I, García-Carbonero R, Bovio H, Colomer R, Cortés-Funes H. Phase I/II study of gefitinib and capecitabine in patients with colorectal cancer. Clin Transl Oncol 2008; 10: 52-57.
15. Stebbing J, Harrison M, Glynne-Jones R, Bridgewater J, Propper D. A phase II study to determine the ability of gefitinib to reverse fluoropyrimidine resistance in metastatic colorectal cancer (the INFORM study). Br J Cancer 2008; 98: 716-719.
16. Li B, Chang CM, Yuan M, McKenna WG, Shu HK. Resistance to small molecule inhibitors of epidermal growth factor receptor in malignant gliomas. Cancer Res. 2003; 63: 7443-7450.
17. Kassouf W, Dinney CP, Brown G, McConkey DJ, Diehl AJ, Bar-Eli M, Adam L. Uncoupling between epidermal growth factor receptor and downstream signals defines resistance to the antiproliferative effect of gefitinib in bladder cancer cells. Cancer Res 2005; 65: 10524-10535.
18. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW, Harris PL, Haserlat SM, Supko JG, Haluska FG, Louis DN, Christiani DC, Settleman J, Haber DA. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 2004; 350: 2129-2139.
19. Paez JG, Jänne PA, Lee JC, Tracy S, Greulich H, Gabriel S, Herman P, Kaye FJ, Lindeman N, Boggon TJ, Naoki K, Sasaki H, Fujii Y, Eck MJ, Sellers WR, Johnson BE, Meyerson M. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 2004; 304: 1497-1500.
20. Hirsch FR, Varella-Garcia M, Bunn PA Jr, Franklin WA, Dziadziuszko R, Thatcher N, Chang A, Parikh P, Pereira JR, Ciuleanu T, von Pawel J, Watkins C, Flannery A, Ellison G, Donald E, Knight L, Parums D, Botwood N, Holloway B. Molecular predictors of outcome with gefitinib in a phase III placebo-controlled study in advanced non-small-cell lung cancer. J Clin Oncol 2006; 24: 5034-5042.
21. Moroni M, Veronese S, Benvenuti S, Marrapese G, Sartore-Bianchi A, Di Nicolantonio F, Gambacorta M, Siena S, Bardelli A. Gene copy number for epidermal growth factor receptor (EGFR) and clinical response to antiEGFR treatment in colorectal cancer: a cohort study. Lancet Oncol 2005; 6: 279-286.
22. Nagahara H, Mimori K, Ohta M, Utsunomiya T, Inoue H, Barnard GF, Ohira M, Hirakawa K, Mori M. Somatic mutations of epidermal growth factor receptor in colorectal carcinoma. Clin Cancer Res 2005; 11: 1368-1371.
23. Barber TD, Vogelstein B, Kinzler KW, Velculescu VE. Somatic mutations of EGFR in colorectal cancers and glioblastomas. N Engl J Med 2004; 351: 2883.
24. Cappuzzo F, Hirsch FR, Rossi E, Bartolini S, Ceresoli GL, Bemis L, Haney J, Witta S, Danenberg K, Domenichini I, Ludovini V, Magrini E, Gregorc V, Doglioni C, Sidoni A, Tonato M, Franklin WA, Crino L, Bunn PA Jr, Varella-Garcia M. Epidermal growth factor receptor gene and protein and gefitinib sensitivity in non-small-cell lung cancer. J Natl Cancer Inst 2005; 97: 643-655.
25. van Schaeybroeck S, Karaiskou-McCaul A, Kelly D, Longley D, Galligan L, van Cutsem E, Johnston P. Epidermal growth factor receptor activity determines response of colorectal cancer cells to gefitinib alone and in combination with chemotherapy. Clin Cancer Res 2005; 11: 7480-7489.
26. Cunningham MP, Thomas H, Fan Z, Modjtahedi H. Responses of human colorectal tumor cells to treatment with the anti-epidermal growth factor receptor monoclonal antibody ICR62 used alone and in combination with the EGFR tyrosine kinase inhibitor gefitinib. Cancer Res 2006; 66: 7708-7715.
27. Pinter F, Papay J, Almasi A, Sapi Z, Szabo E, Kanya M, Tamasi A, Jori B, Varkondi E, Moldvay J, Szondy K, Keri G, Dominici M, Conte P, Eckhardt S, Kopper L, Schwab R, Petak I. Epidermal growth factor receptor (EGFR) high gene copy number and activating mutations in lung adenocarcinomas are not consistently accompanied by positivity for EGFR protein by standard immunohistochemistry. J Mol Diagn 2008; 10: 160-168.
28. Han SW, Kim TY, Jeon YK, Hwang PG, Im SA, Lee KH, Kim JH, Kim DW, Heo DS, Kim NK, Chung DH, Bang YJ. Optimization of patient selection for gefitinib in non-small cell lung cancer by combined analysis of epidermal growth factor receptor mutation, K-ras mutation, and Akt phosphorylation. Clin Cancer Res 2006; 12: 2538-2544.
29. Kokubo Y, Gemma A, Noro R, Seike M, Kataoka K, Matsuda K, Okano T, Minegishi Y, Yoshimura A, Shibuya M, Kudoh S. Reduction of PTEN protein and loss of epidermal growth factor receptor gene mutation in lung cancer with natural resistance to gefitinib (IRESSA). Br J Cancer 2005; 92: 1711-1719.
30. Han SW, Hwang PG, Chung DH, Kim DW, Im SA, Kim YT, Kim TY, Heo DS, Bang YJ, Kim NK. Epidermal growth factor receptor (EGFR) downstream molecules as response predictive markers for gefitinib (Iressa, ZD1839) in chemotherapy-resistant non-small cell lung cancer. Int J Cancer 2005; 113: 109-115.
31. Wang SE, Narasanna A, Perez-Torres M, Xiang B, Wu FY, Yang S, Carpenter G, Gazdar AF, Muthuswamy SK, Arteaga CL. 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.
32. Fujimoto N, Wislez M, Zhang J, Iwanaga K, Dackor J, Hanna AE, Kalyankrishna S, Cody DD, Price RE, Sato M, Shay JW, Minna JD, Peyton M, Tang X, Massarelli E, Herbst R, Threadgill DW, Wistuba II, Kurie JM. High expression of ErbB family members and their ligands in lung adenocarcinomas that are sensitive to inhibition of epidermal growth factor receptor. Cancer Res 2005; 65: 11478-11485.
33. Morgillo F, Kim WY, Kim ES, Ciardiello F, Hong WK, Lee HY. Implication of the insulin-like growth factor-IR pathway in the resistance of non-small cell lung cancer cells to treatment with gefitinib. Clin Cancer Res 2007; 13: 2795-2803.
34. Engelman JA, Zejnullahu K, Mitsudomi T, Song Y, Hyland C, Park JO, Lindeman N, Gale CM, Zhao X, Christensen J, Kosaka T, Holmes AJ, Rogers AM, Cappuzzo F, Mok T, Lee C, Johnson BE, Cantley LC, Jänne PA. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 2007; 316: 1039-1043.
35. Di Renzo MF, Olivero M, Giacomini A, Porte H, Chastre E, Mirossay L, Nordlinger B, Bretti S, Bottardi S, Giordano S, Plebani M, Gespach C, Comoglio PM. Overexpression and amplification of the met/HGF receptor gene during the progression of colorectal cancer. Clin Cancer Res 1995; 1: 147-154.
36. Christensen JG, Burrows J, Salgia R. c-Met as a target for human cancer and characterization of inhibitors for therapeutic intervention. Cancer Lett 2005; 225: 1-26.
37. Guo YS, Narayan S, Yallampalli C, Singh P. Characterization of insulinlike growth factor I receptors in human colon cancer. Gastroenterology 1992; 102: 1101-1108.
38. Hakam A, Yeatman TJ, Lu L, Mora L, Marcet G, Nicosia SV, Karl RC, Coppola D. Expression of insulin-like growth factor-1 receptor in human colorectal cancer. Hum Pathol 1999; 30: 1128-1133.
39. Lahm H, Suardet L, Laurent PL, Fischer JR, Ceyhan A, Givel JC, Odartchenko N. Growth regulation and co-stimulation of human colorectal cancer cell lines by insulin-like growth factor I, II and transforming growth factor alpha. Br J Cancer 1992; 65: 341-346.
40. Sekharam M, Zhao H, Sun M, Fang Q, Zhang Q, Yuan Z, Dan HC, Boulware D, Cheng JQ, Coppola D. Insulin-like growth factor 1 receptor enhances invasion and induces resistance to apoptosis of colon cancer cells through the Akt/Bcl-x(L) pathway. Cancer Res 2003; 63: 7708-7716.
41. Párrizas M, Gazit A, Levitzki A, Wertheimer E, LeRoith D. Specific inhibition of insulin-like growth factor-1 and insulin receptor tyrosine kinase activity and biological function by tyrphostins. Endocrinology 1997; 138: 1427-1433.
42. Jones HE, Gee JM, Hutcheson IR, Knowlden JM, Barrow D, Nicholson RI. Growth factor receptor interplay and resistance in cancer. Endocr Relat Cancer 2006; 13 Suppl 1: S45-S51.
43. Doble BW, Woodgett JR. GSK-3: tricks of the trade for a multi-tasking kinase. J Cell Sci 2003; 116: 1175-1186.
44. Jope RS, Johnson GV. The glamour and gloom of glycogen synthase kinase-3. Trends Biochem Sci 2004; 29: 95-102.
45. Eldar-Finkelman H, Seger R, Vandenheede JR, Krebs EG. Inactivation of glycogen synthase kinase-3 by epidermal growth factor is mediated by mitogen-activated protein kinase/p90 ribosomal protein S6 kinase signaling pathway in NIH/3T3 cells. J Biol Chem 1995; 270: 987-990.
46. Rössig L, Badorff C, Holzmann Y, Zeiher AM, Dimmeler S. Glycogen synthase kinase-3 couples AKT-dependent signaling to the regulation of p21Cip1 degradation. J Biol Chem 2002; 277: 9684-9689.
47. Klein PS, Melton DA. A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci USA 1996; 93: 8455-8459.
48. Wang QM, Fiol CJ, DePaoli-Roach AA, Roach PJ. Glycogen synthase kinase-3 beta is a dual specificity kinase differentially regulated by tyrosine and serine/threonine phosphorylation. J Biol Chem 1994; 269: 14566-14574.
49. Massagué J, Czech MP. The subunit structures of two distinct receptors for insulin-like growth factors I and II and their relationship to the insulin receptor. J Biol Chem 1982; 257: 5038-5045.
50. Abbott AM, Bueno R, Pedrini MT, Murray JM, Smith RJ. Insulin-like growth factor I receptor gene structure. J Biol Chem 1992; 267: 10759-10763.
51. Reinmuth N, Liu W, Fan F, Jung YD, Ahmad SA, Stoeltzing O, Bucana CD, Radinsky R, Ellis LM. Blockade of insulin-like growth factor I receptor function inhibits growth and angiogenesis of colon cancer. Clin Cancer Res 2002; 8: 3259-3269.
52. Lehmann M, André F, Bellan C, Remacle-Bonnet M, Garrouste F, Parat F, Lissitsky JC, Marvaldi J, Pommier G. Deficient processing and activity of type I insulin-like growth factor receptor in the furin-deficient LoVo-C5 cells. Endocrinology 1998; 139: 3763-3771.
53. Jones HE, Goddard L, Gee JM, Hiscox S, Rubini M, Barrow D, Knowlden JM, Williams S, Wakeling AE, Nicholson RI. Insulin-like growth factor-I receptor signalling and acquired resistance to gefitinib (ZD1839; Iressa) in human breast and prostate cancer cells. Endocr Relat Cancer 2004; 11: 793-814.
54. Kulik G, Klippel A, Weber MJ. Antiapoptotic signalling by the insulin-like growth factor I receptor, phosphatidylinositol 3-kinase, and Akt. Mol Cell Biol 1997; 17: 1595-1606.
55. 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: 200-207.
56. Ahmad T, Farnie G, Bundred NJ, Anderson NG. The mitogenic action of insulin-like growth factor I in normal human mammary epithelial cells requires the epidermal growth factor receptor tyrosine kinase. J Biol Chem 2004; 279: 1713-1719.
57. Frame S, Cohen P. GSK3 takes centre stage more than 20 years after its discovery. Biochem J 2001; 359: 1-16.
58. Wang Q, Zhou Y, Evers BM. Neurotensin phosphorylates GSK-3alpha/beta through the activation of PKC in human colon cancer cells. Neoplasia 2006; 8: 781-787.
59. Turenne GA, Price BD. Glycogen synthase kinase3 beta phosphorylates serine 33 of p53 and activates p53's transcriptional activity. BMC Cell Biol 2001; 2: 12.
60. Ali A, Hoeflich KP, Woodgett JR. Glycogen synthase kinase-3: properties, functions, and regulation. Chem Rev 2001; 101: 2527-2540.
61. Yamaguchi K, Lee SH, Eling TE, Baek SJ. Identification of nonsteroidal anti-inflammatory drug-activated gene (NAG-1) as a novel downstream target of phosphatidylinositol 3-kinase/AKT/GSK-3beta pathway. J Biol Chem 2004; 279: 49617-49623.
62. Sherr CJ, Roberts JM. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 1999; 13: 1501-1512.