Relevance of MET activation and genetic alterations of KRAS and E-cadherin for cetuximab sensitivity of gastric cancer cell lines

Journal of Cancer Research and Clinical Oncology

Volumn 138, Issue 5, 2012, Pages 843-858

  Heindl, Stefan ^a   Eggenstein, Evelyn ^a,b   Keller, Simone ^a   Kneissl, Julia ^a   Keller, Gisela ^a   Mutze, Kathrin ^a   Rauser, Sandra ^c   Gasteiger, Georg ^a   Drexler, Ingo ^a,d   Hapfelmeier, Alexander ^a   Höfler, Heinz ^a,c   Luber, Birgit ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Cetuximab; E cadherin; EGFR; Gastric cancer; MET

Indexed keywords

CETUXIMAB; CISPLATIN; FLUOROURACIL; SCATTER FACTOR RECEPTOR; UVOMORULIN; ANTINEOPLASTIC AGENT; CADHERIN; CDH1 PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; KRAS PROTEIN, HUMAN; MET PROTEIN, HUMAN; MONOCLONAL ANTIBODY; ONCOPROTEIN; RAS PROTEIN; TUMOR MARKER;

ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER CELL CULTURE; CELL VIABILITY; CHEMOSENSITIVITY; CONCENTRATION (PARAMETERS); DRUG RESISTANCE; DRUG RESPONSE; DRUG SENSITIVITY; ENZYME ACTIVATION; FLOW CYTOMETRY; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; STOMACH CANCER; TREATMENT RESPONSE; WESTERN BLOTTING; CELL PROLIFERATION; DRUG EFFECTS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; PHOSPHORYLATION; PHYSIOLOGY; STOMACH NEOPLASMS; TUMOR CELL LINE;

ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BLOTTING, WESTERN; CADHERINS; CELL LINE, TUMOR; CELL PROLIFERATION; CISPLATIN; DRUG RESISTANCE, NEOPLASM; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; FLUOROURACIL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MUTATION; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MET; RAS PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; STOMACH NEOPLASMS; TUMOR MARKERS, BIOLOGICAL;

EID: 84863101033     PISSN: 01715216     EISSN: 14321335     Source Type: Journal    
DOI: 10.1007/s00432-011-1128-4     Document Type: Article

References (55)

1. Adams GP, Weiner LM (2005) Monoclonal antibody therapy of cancer. Nat Biotechnol 23(9):1147-1157. doi:nbt1137[pii]10. 1038/nbt1137 (Pubitemid 41486396)
2. Agarwal S, Zerillo C, Kolmakova J, Christensen JG, Harris LN, Rimm DL, Digiovanna MP, Stern DF (2009) Association of constitutively activated hepatocyte growth factor receptor (Met) with resistance to a dual EGFR/Her2 inhibitor in non-small-cell lung cancer cells. Br J Cancer 100(6):941-949. doi: 6604937[pii]10.1038/sj.bjc.6604937
3. Bachleitner-Hofmann T, Sun MY, Chen CT, Tang L, Song L, Zeng Z, Shah M, Christensen JG, Rosen N, Solit DB, Weiser MR (2008) HER kinase activation confers resistance to MET tyrosine kinase inhibition in MET oncogene-addicted gastric cancer cells. Mol Cancer Ther 7(11):3499-3508. doi:1535-7163.MCT-08-0374 [pii]10.1158/1535-7163.MCT-08-0374
4. Bardelli A, Siena S (2010) Molecular mechanisms of resistance to cetuximab and panitumumab in colorectal cancer. J Clin Oncol 28(7):1254-1261
5. Baselga J, Pfister D, Cooper MR, Cohen R, Burtness B, Bos M, D'Andrea G, Seidman A, Norton L, Gunnett K, Falcey J, Anderson V, Waksal H, Mendelsohn J (2000) Phase I studies of anti-epidermal growth factor receptor chimeric antibody C225 alone and in combination with cisplatin. J Clin Oncol 18(4):904-914 (Pubitemid 30106623)
6. Becker KF, Atkinson MJ, Reich U, Becker I, Nekarda H, Siewert JR, Hofler H (1994) E-cadherin gene mutations provide clues to diffuse type gastric carcinomas. Cancer Res 54(14):3845-3852 (Pubitemid 24241205)
7. Benavente S, Huang S, Armstrong EA, Chi A, Hsu KT, Wheeler DL, Harari PM (2009) Establishment and characterization of a model of acquired resistance to epidermal growth factor receptor targeting agents in human cancer cells. Clin Cancer Res 15(5):1585-1592
8. Bertotti A, Bracco C, Girolami F, Torti D, Gastaldi S, Galimi F, Medico E, Elvin P, Comoglio PM, Trusolino L (2010) Inhibition of Src impairs the growth of met-addicted gastric tumors. Clin Cancer Res 16(15):3933-3943. doi:1078-0432.CCR-10-0106 [pii]10.1158/1078-0432.CCR-10-0106
9. Berx G, Becker KF, Hofler H, van Roy F (1998) Mutations of the human E-cadherin (CDH1) gene. Hum Mutat 12(4):226-237 (Pubitemid 28418891)
10. Black PC, Brown GA, Inamoto T, Shrader M, Arora A, Siefker- Radtke AO, Adam L, Theodorescu D, Wu X, Munsell MF, Bar- Eli M, McConkey DJ, Dinney CP (2008) Sensitivity to epidermal growth factor receptor inhibitor requires E-cadherin expression in urothelial carcinoma cells. Clin Cancer Res 14(5):1478-1486 (Pubitemid 351413932)
11. Boyd MR, Paull KD (1995) Some practical considerations and applications of the national cancer institute in vitro anticancer drug discovery screen. Drug Develop Res 34:91-109
12. Bremm A, Walch A, Fuchs M, Mages J, Duyster J, Keller G, Hermannstadter C, Becker KF, Rauser S, Langer R, von Weyhern CH, Hofler H, Luber B (2008) Enhanced activation of epidermal growth factor receptor caused by tumor-derived E-cadherin mutations. Cancer Res 68(3):707-714. doi: 68/3/707[pii]10.1158/0008- 5472.CAN-07-1588 (Pubitemid 351206746)
13. Cappuzzo F, Varella-Garcia M, Finocchiaro G, Skokan M, Gajapathy S, Carnaghi C, Rimassa L, Rossi E, Ligorio C, Di Tommaso L, Holmes AJ, Toschi L, Tallini G, Destro A, Roncalli M, Santoro A, Janne PA (2008) Primary resistance to cetuximab therapy in EGFR FISH-positive colorectal cancer patients. Br J Cancer 99(1):83-89. doi:6604439[pii]10.1038/sj.bjc.6604439 (Pubitemid 351920237)
14. Chung KY, Shia J, Kemeny NE, Shah M, Schwartz GK, Tse A, Hamilton A, Pan D, Schrag D, Schwartz L, Klimstra DS, Fridman D, Kelsen DP, Saltz LB (2005) Cetuximab shows activity in colorectal cancer patients with tumors that do not express the epidermal growth factor receptor by immunohistochemistry. J Clin Oncol 23(9):1803-1810 (Pubitemid 46211358)
15. Ciardiello F, Tortora G (2008) EGFR antagonists in cancer treatment. N Engl J Med 358(11):1160-1174
16. Dietel M, Bals U, Schaefer B, Herzig I, Arps H, Zabel M (1993) In vitro prediction of cytostatic drug resistance in primary cell cultures of solid malignant tumours. Eur J Cancer 29A(3): 416-420 (Pubitemid 23025753)
17. Engelman JA, Janne PA (2008) Mechanisms of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small cell lung cancer. Clin Cancer Res 14(10):2895-2899. doi:14/10/2895[pii]10.1158/1078- 0432.CCR-07-2248
18. Engelman JA, Settleman J (2008) Acquired resistance to tyrosine kinase inhibitors during cancer therapy. Curr Opin Genet Dev 18(1):73-79. doi:S0959-437X(08)00008-7[pii]10.1016/j.gde.2008. 01.004 (Pubitemid 351694445)
19. 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, Janne PA (2007) MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 316(5827):1039-1043. doi:1141478[pii]10.1126/ science.1141478 (Pubitemid 46799492)
20. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127:2893-2917. doi:10.1002/ijc.25516
21. Frixen UH, Behrens J, Sachs M, Eberle G, Voss B, Warda A, Lochner D, Birchmeier W (1991) E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J Cell Biol 113(1):173-185 (Pubitemid 21909684)
22. Fuchs BC, Fujii T, Dorfman JD, Goodwin JM, Zhu AX, Lanuti M, Tanabe KK (2008) Epithelial-to-mesenchymal transition and integrin-linked kinase mediate sensitivity to epidermal growth factor receptor inhibition in human hepatoma cells. Cancer Res 68(7):2391-2399 (Pubitemid 351521814)
23. Gamboa-Dominguez A, Dominguez-Fonseca C, Quintanilla-Martinez L, Reyes-Gutierrez E, Green D, Angeles-Angeles A, Busch R, Hermannstadter C, Nahrig J, Becker KF, Becker I, Hofler H, Fend F, Luber B (2004) Epidermal growth factor receptor expression correlates with poor survival in gastric adenocarcinoma from Mexican patients: a multivariate analysis using a standardized immunohistochemical detection system. Mod Pathol 17(5):579-587 (Pubitemid 38868426)
24. Guo A, Villen J, Kornhauser J, Lee KA, Stokes MP, Rikova K, Possemato A, Nardone J, Innocenti G, Wetzel R, Wang Y, MacNeill J, Mitchell J, Gygi SP, Rush J, Polakiewicz RD, Comb MJ (2008) Signaling networks assembled by oncogenic EGFR and c-Met. Proc Natl Acad Sci USA 105(2):692-697. doi: 0707270105[pii]10.1073/ pnas.0707270105 (Pubitemid 351171770)
25. Han SW, Oh DY, Im SA, Park SR, Lee KW, Song HS, Lee NS, Lee KH, Choi IS, Lee MH, Kim MA, Kim WH, Bang YJ, Kim TY (2009) Phase II study and biomarker analysis of cetuximab combined with modified FOLFOX6 in advanced gastric cancer. Br J Cancer 100(2):298-304
26. Hara M, Nakanishi H, Tsujimura K, Matsui M, Yatabe Y, Manabe T, Tatematsu M (2008) Interleukin-2 potentiation of cetuximab antitumor activity for epidermal growth factor receptor-overexpressing gastric cancer xenografts through antibody-dependent cellular cytotoxicity. Cancer Sci 99(7):1471-1478. doi: CAS821[pii]10.1111/j.1349-7006.2008.00821.x (Pubitemid 351761740)
27. Inno A, Salvatore MD, Cenci T, Martini M, Orlandi A, Strippoli A, Ferrara AM, Bagala C, Cassano A, Larocca LM, Barone C (2011) Is there a role for IGF1R and c-MET pathways in resistance to cetuximab in metastatic colorectal cancer? Clin Colorect Cancer. doi:S1533-0028(11)00030-2 [pii] 10.1016/j.clcc.2011.03.028
28. Jhawer M, Goel S, Wilson AJ, Montagna C, Ling YH, Byun DS, Nasser S, Arango D, Shin J, Klampfer L, Augenlicht LH, Soler RP, Mariadason JM (2008) PIK3CA mutation/PTEN expression status predicts response of colon cancer cells to the epidermal growth factor receptor inhibitor cetuximab. Cancer Res 68(6):1953-1961 (Pubitemid 351416582)
29. Keller G, Vogelsang H, Becker I, Plaschke S, Ott K, Suriano G, Mateus AR, Seruca R, Biedermann K, Huntsman D, Doring C, Holinski-Feder E, Neutzling A, Siewert JR, Hofler H (2004) Germline mutations of the E-cadherin(CDH1) and TP53 genes, rather than of RUNX3 and HPP1, contribute to genetic predisposition in German gastric cancer patients. J Med Genet 41(6):e89
30. Kim JW, Kim HP, Im SA, Kang S, Hur HS, Yoon YK, Oh DY, Kim JH, Lee DS, Kim TY, Bang YJ (2008) The growth inhibitory effect of lapatinib, a dual inhibitor of EGFR and HER2 tyrosine kinase, in gastric cancer cell lines. Cancer Lett 272(2):296-306. doi:S0304-3835(08)00582-X[pii]10.1016/j.canlet.2008.07.018
31. Krumbach R, Schuler J, Hofmann M, Giesemann T, Fiebig HH, Beckers T (2011) Primary resistance to cetuximab in a panel of patient-derived tumour xenograft models: activation of MET as one mechanism for drug resistance. Eur J Cancer 47(8): 1231-1243. doi:S0959-8049(10)01208-6[pii]10.1016/j.ejca.2010. 12.019
32. Liska D, Chen CT, Bachleitner-Hofmann T, Christensen JG, WeiserMR (2011) HGF rescues colorectal cancer cells from EGFR inhibition via MET activation. Clin Cancer Res 17(3):472-482. doi: 1078-0432.CCR-10-0568[pii]10.1158/1078-0432. CCR-10-0568
33. Liu X, Guo WJ, Zhang XW, Cai X, Tian S, Li J (2011) Cetuximab enhances the activities of irinotecan on gastric cancer cell lines through downregulating the EGFR pathway upregulated by irinotecan. Cancer Chemother Pharmacol. doi:10.1007/s00280- 011-1559-2
34. Lordick F, Luber B, Lorenzen S, Hegewisch-Becker S, Folprecht G, Woll E, Decker T, Endlicher E, Rothling N, Schuster T, Keller G, Fend F, Peschel C (2010) Cetuximab plus oxaliplatin/ leucovorin/5-fluorouracil in first-line metastatic gastric cancer: a phase II study of the Arbeitsgemeinschaft Internistische Onkologie (AIO). Br J Cancer 102(3):500-505
35. Luber B, Deplazes J, Keller G, Walch A, Rauser S, Eichmann M, Langer R, Höfler H, Hegewisch-Becker S, Folprecht G, Wöll E, Decker T, Endlicher E, Lorenzen S, Fend F, Peschel C, Lordick F (2011) Biomarker analysis of cetuximab plus oxaliplatin/ leucovorin/5-fluorouracil in first-line metastatic gastric and oesophago-gastric junction cancer: results from a phase II trial of the Arbeitsgemeinschaft Internistische Onkologie (AIO). BMC Cancer, in press
36. Luo FR, Yang Z, Dong H, Camuso A, McGlinchey K, Fager K, Flefleh C, Kan D, Inigo I, Castaneda S, Rose WC, Kramer RA, Wild R, Lee FY (2005) Correlation of pharmacokinetics with the antitumor activity of Cetuximab in nude mice bearing the GEO human colon carcinoma xenograft. Cancer Chemother Pharmacol 56(5):455-464. doi:10.1007/s00280-005-1022-3 (Pubitemid 41549146)
37. Mateus AR, Seruca R, Machado JC, Keller G, Oliveira MJ, Suriano G, Luber B (2007) EGFR regulates RhoA-GTP dependent cell motility in E-cadherin mutant cells. Hum Mol Genet 16(13):1639-1647 (Pubitemid 47050677)
38. McDermott U, Pusapati RV, Christensen JG, Gray NS, Settleman J (2010) Acquired resistance of non-small cell lung cancer cells to MET kinase inhibition is mediated by a switch to epidermal growth factor receptor dependency. Cancer Res 70(4):1625- 1634. doi:0008-5472.CAN-09-3620[pii]10.1158/0008-5472.CAN- 09-3620
39. Moehler M, Mueller A, Trarbach T, Lordick F, Seufferlein T, Kubicka S, Geissler M, Schwarz S, Galle PR, Kanzler S (2010) Cetuximab with irinotecan, folinic acid and 5-fluorouracil as first-line treatment in advanced gastroesophageal cancer: a prospective multi-center biomarker-oriented phase II study. Ann Oncol 22:1358-1366 Epub 2010 Nov 30
40. Nakagawa M, Fukata M, Yamaga M, Itoh N, Kaibuchi K (2001) Recruitment and activation of Rac1 by the formation of E-cadherin-mediated cell-cell adhesion sites. J Cell Sci 114(Pt 10):1829-1838 (Pubitemid 32530038)
41. Nikolova DA, Asangani IA, Nelson LD, Hughes DP, Siwak DR, Mills GB, Harms A, Buchholz E, Pilz LR, Manegold C, Allgayer H (2009) Cetuximab Attenuates Metastasis and u-PAR Expression in Non-Small Cell Lung Cancer: u-PAR and E-Cadherin are Novel Biomarkers of Cetuximab Sensitivity. Cancer Res 69:2461-2470 Epub 2009 Mar 10
42. Oda T, Kanai Y, Oyama T, Yoshiura K, Shimoyama Y, Birchmeier W, Sugimura T, Hirohashi S (1994) E-cadherin gene mutations in human gastric carcinoma cell lines. Proc Natl Acad Sci USA 91(5):1858-1862 (Pubitemid 24080305)
43. Oliveira C, Seruca R, Caldas C (2003) Genetic screening for hereditary diffuse gastric cancer. Expert Rev Mol Diagn 3(2):201-215 (Pubitemid 36313752)
44. Paull KD, Shoemaker RH, Hodes L, Monks A, Scudiero DA, Rubinstein L, Plowman J, Boyd MR (1989) Display and analysis of patterns of differential activity of drugs against human tumor cell lines: development of mean graph and COMPARE algorithm. J Natl Cancer Inst 81(14):1088-1092 (Pubitemid 19175145)
45. Pinto C, Di Fabio F, Siena S, Cascinu S, Rojas Llimpe FL, Ceccarelli C, Mutri V, Giannetta L, Giaquinta S, Funaioli C, Berardi R, Longobardi C, Piana E, Martoni AA (2007) Phase II study of cetuximab in combination with FOLFIRI in patients with untreated advanced gastric or gastroesophageal junction adenocarcinoma (FOLCETUX study). Ann Oncol 18(3):510-517 (Pubitemid 46359631)
46. Pinto C, Di Fabio F, Barone C, Siena S, Falcone A, Cascinu S, Rojas Llimpe FL, Stella G, Schinzari G, Artale S, Mutri V, Giaquinta S, Giannetta L, Bardelli A, Martoni AA (2009) Phase II study of cetuximab in combination with cisplatin and docetaxel in patients with untreated advanced gastric or gastro-oesophageal junction adenocarcinoma (DOCETUX study). Br J Cancer 101(8):1261-1268
47. Qian X, Karpova T, Sheppard AM, McNally J, Lowy DR (2004) E-cadherin-mediated adhesion inhibits ligand-dependent activation of diverse receptor tyrosine kinases. EMBO J 23(8):1739-1748 (Pubitemid 38649637)
48. Robert F, Ezekiel MP, Spencer SA, Meredith RF, Bonner JA, Khazaeli MB, Saleh MN, Carey D, LoBuglio AF, Wheeler RH, Cooper MR, Waksal HW (2001) Phase I study of anti-epidermal growth factor receptor antibody cetuximab in combination with radiation therapy in patients with advanced head and neck cancer. J Clin Oncol 19(13):3234-3243 (Pubitemid 32591441)
49. Rocher-Ros V, Marco S, Mao JH, Gines S, Metzger D, Chambon P, Balmain A, Saura CA (2010) Presenilin modulates EGFR signaling and cell transformation by regulating the ubiquitin ligase Fbw7. Oncogene 29(20):2950-2961. doi:onc201057[pii] 10.1038/onc.2010.57
50. Smolen GA, Muir B, Mohapatra G, Barmettler A, Kim WJ, Rivera MN, Haserlat SM, Okimoto RA, Kwak E, Dahiya S, Garber JE, Bell DW, Sgroi DC, Chin L, Deng CX, Haber DA (2006) Frequent met oncogene amplification in a Brca1/Trp53 mouse model of mammary tumorigenesis. Cancer Res 66(7):3452- 3455. doi:66/7/3452[pii]10.1158/0008-5472.CAN-05-4181
51. Stommel JM, Kimmelman AC, Ying H, Nabioullin R, Ponugoti AH, Wiedemeyer R, Stegh AH, Bradner JE, Ligon KL, Brennan C, Chin L, DePinho RA (2007) Coactivation of receptor tyrosine kinases affects the response of tumor cells to targeted therapies. Science 318(5848):287-290. doi:1142946[pii]10.1126/science. 1142946
52. Wagner AD, Grothe W, Haerting J, Kleber G, Grothey A, Fleig WE (2006) Chemotherapy in advanced gastric cancer: a systematic review and meta-analysis based on aggregate data. J Clin Oncol 24(18):2903-2909. doi:24/18/2903[pii]10. 1200/JCO.2005.05.0245 (Pubitemid 46630593)
53. Wild R, Fager K, Flefleh C, Kan D, Inigo I, Castaneda S, Luo FR, Camuso A, McGlinchey K, Rose WC (2006) Cetuximab preclinical antitumor activity (monotherapy and combination based) is not predicted by relative total or activated epidermal growth factor receptor tumor expression levels. Mol Cancer Ther 5(1):104-113. doi:5/1/104[pii]10.1158/1535-7163.MCT-05-0259
54. Witta SE, Gemmill RM, Hirsch FR, Coldren CD, Hedman K, Ravdel L, Helfrich B, Dziadziuszko R, Chan DC, Sugita M, Chan Z, Baron A, Franklin W, Drabkin HA, Girard L, Gazdar AF, Minna JD, Bunn PA Jr (2006) Restoring E-cadherin expression increases sensitivity to epidermal growth factor receptor inhibitors in lung cancer cell lines. Cancer Res 66(2):944-950 (Pubitemid 43165962)
55. Witta SE, Dziadziuszko R, Yoshida K, Hedman K, Varella-Garcia M, Bunn PA Jr, Hirsch FR (2009) ErbB-3 expression is associated with E-cadherin and their coexpression restores response to gefitinib in non-small-cell lung cancer (NSCLC). Ann Oncol 20:689-695 Epub 2009 Jan 15