Gefitinib (ZD1839) increases the efficacy of cisplatin in ovarian cancer cells

Cancer Biology and Therapy

Volumn 13, Issue 6, 2012, Pages 408-416

  Ohta, Tsuyoshi ^a   Ohmichi, Masahide ^b   Shibuya, Tae ^a   Takahashi, Toshifumi ^a   Tsutsumi, Seiji ^a   Takahashi, Kazuhiro ^a   Kurachi, Hirohisa ^a  

^a YAMAGATA UNIVERSITY   (Japan)

^b OSAKA MEDICAL COLLEGE   (Japan)

Author keywords

Akt; Cisplatin; DNA repair; ERK; Gefitinib; HER2; Ovarian cancer

Indexed keywords

CISPLATIN; EPIDERMAL GROWTH FACTOR RECEPTOR; GEFITINIB; PROTEIN KINASE B;

APOPTOSIS; ARTICLE; CANCER CELL; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENTIATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; OVARY CANCER;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CELL LINE, TUMOR; CISPLATIN; DNA DAMAGE; DNA REPAIR; DNA-ACTIVATED PROTEIN KINASE; DRUG SCREENING ASSAYS, ANTITUMOR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; MICE, NUDE; OVARIAN NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; SIGNAL TRANSDUCTION;

EID: 84860255355     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.19292     Document Type: Article

References (45)

1. Egan SE, Weinberg RA. The pathway to signal achievement. Nature 1993; 365:781-3; PMID:8413661; http://dx.doi.org/10.1038/365781a0.
2. Verbeek BS, Adriaansen-Slot SS, Vroom TM, Beckers T, Rijksen G. Overexpression of EGFR and c-erbB2 causes enhanced cell migration in human breast cancer cells and NIH3T3 fibroblasts. FEBS Lett 1998; 425:145-50; PMID:9541025; http://dx.doi.org/10.1016/S0014-5793(98)00224-5.
3. Woodburn JR. The epidermal growth factor receptor and its inhibition in cancer therapy. Pharmacol Ther 1999; 82:241-50; PMID:10454201; http://dx.doi.org/10.1016/S0163-7258(98)00045-X.
4. Xia W, Lau YK, Zhang HZ, Xiao FY, Johnston DA, Liu AR, et al. Combination of EGFR, HER-2/neu and HER-3 is a stronger predictor for the outcome of oral squamous cell carcinoma than any individual family members. Clin Cancer Res 1999; 5:4164-74; PMID:10632356.
5. Giaccone G, Herbst RS, Manegold C, Scagliotti G, Rosell R, Miller V, et al. Gefitinib in combination with gemcitabine and cisplatin in advanced non-small-cell lung cancer: a phase III trial-INTACT 1. J Clin Oncol 2004; 22:777-84; PMID:14990632; http://dx.doi.org/10.1200/JCO.2004.08.001.
6. Herbst RS, Giaccone G, Schiller JH, Natale RB, Miller V, Manegold C, et al. Gefitinib in combination with paclitaxel and carboplatin in advanced non-small-cell lung cancer: a phase III trial-INTACT 2. J Clin Oncol 2004; 22:785-94; PMID:14990633; http://dx.doi.org/10.1200/JCO.2004.07.215.
7. Cunningham D, Humblet Y, Siena S, Khayat D, Bleiberg H, Santoro A, et al. Cetuximab monotherapy and cetuximab plus irinotecan in irinotecanrefractory metastatic colorectal cancer. N Engl J Med 2004; 351:337-45; PMID:15269313; http://dx.doi.org/10.1056/NEJMoa033025.
8. Berchuck A, Rodriguez GC, Kamel A, Dodge RK, Soper JT, Clarke-Pearson DL, et al. Epidermal growth factor receptor expression in normal ovarian epithelium and ovarian cancer. I. Correlation of receptor expression with prognostic factors in patients with ovarian cancer. Am J Obstet Gynecol 1991; 164:669-74; PMID:1992720.
9. Morishige K, Kurachi H, Amemiya K, Fujita Y, Yamamoto T, Miyake A, et al. Evidence for the involvement of transforming growth factor receptor autcrine growth mechanism in primary ovarian cancers in vitro. Cancer Res 1991; 51:5322-8; PMID:1717146.
10. Bartlett JM, Langdon SP, Simpson BJ, Stewart M, Katsaros D, Sismondi P, et al. The prognostic value of epidermal growth factor receptor mRNA expression in primary ovarian cancer. Br J Cancer 1996; 73:301-6; PMID:8562334; http://dx.doi.org/10.1038/bjc.1996.53.
11. Morishige K, Kurachi H, Amemiya K, Adachi H, Inoue M, Miyake A, et al. Involvement of transforming growth factor alpha/epidermal growth factor receptor autocrine growth mechanism in an ovarian cancer cell line in vitro. Cancer Res 1991; 51:5951-5; PMID:1718591.
12. Schilder RJ, Sill MW, Chen X, Darcy KM, Decesare SL, Lewandowski G, et al. Phase II study of gefitinib in patients with relapsed or persistent ovarian or primary peritoneal carcinoma and evaluation of epidermal growth factor receptor mutations and immunohistochemical expression: a Gynecologic Oncology Group Study. Clin Cancer Res 2005; 11:5539-48; PMID:16061871; http://dx.doi.org/10.1158/1078-0432.CCR-05-0462.
13. Lacroix L, Pautier P, Duvillard P, Motté N, Saulnier P, Bidart JM, et al. Response of ovarian carcinomas to gefitinib-carboplatin-paclitaxel combination is not associated with EGFR kinase domain somatic mutations. Int J Cancer 2006; 118:1068-9; PMID:16152583; http://dx.doi.org/10.1002/ijc.21460.
14. Hayakawa J, Ohmichi M, Kurachi H, Ikegami H, Kimura A, Matsuoka T, et al. Inhibition of extracellular signal-regulated protein kinase or c-Jun N-terminal protein kinase cascade, differentially activated by cisplatin, sensitizes human ovarian cancer cell line. J Biol Chem 1999; 274:31648-54; PMID:10531373; http://dx.doi.org/10.1074/jbc.274.44.31648.
15. Hayakawa J, Ohmichi M, Kurachi H, Kanda Y, Hisamoto K, Nishio Y, et al. Inhibition of BAD phosphorylation either at serine 112 via extracellular signalregulated protein kinase cascade or at serine 136 via Akt cascade sensitizes human ovarian cancer cells to cisplatin. Cancer Res 2000; 60:5988-94; PMID:11085518.
16. Mabuchi S, Ohmichi M, Kimura A, Hisamoto K, Hayakawa J, Nishio Y, et al. Inhibition of phosphorylation of BAD and Raf-1 by Akt sensitizes human ovarian cancer cells to paclitaxel. J Biol Chem 2002; 277:33490-500; PMID:12087097; http://dx.doi.org/10.1074/jbc.M204042200.
17. Janmaat ML, Kruyt FA, Rodriguez JA, Giaccone G. Response to epidermal growth factor receptor inhibitors in non-small cell lung cancer cells: limited antiproliferative effects and absence of apoptosis associated with persistent activity of extracellular signal-regulated kinase or Akt kinase pathways. Clin Cancer Res 2003; 9:2316-26; PMID:12796401.
18. Fujimura M, Hidaka T, Saito S. Selective inhibition of the epidermal growth factor receptor by ZD1839 decreases the growth and invasion of ovarian clear cell adenocarcinoma cells. Clin Cancer Res 2002; 8:2448-54; PMID:12114452.
19. Eastman A. Separation and characterization of products resulting from the reaction of cis-diamminedichloroplatinum (II) with deoxyribonucleosides. Biochemistry 1982; 21:6732-6; PMID:6891601; http://dx.doi.org/10.1021/ bi00269a018.
20. Shen H, Schultz M, Kruh GD, Tew KD. Increased expression of DNA-dependent protein kinase confers resistance to adriamycin. Biochim Biophys Acta 1998; 1381:131-8; PMID:9685611; http://dx.doi.org/10.1016/S0304-4165(98)00020-8.
21. Friedmann B, Caplin M, Hartley JA, Hochhauser D. Modulation of DNA repair in vitro after treatment with chemotherapeutic agents by the epidermal growth factor receptor inhibitor gefitinib (ZD1839). Clin Cancer Res 2004; 10:6476-86; PMID:15475435; http://dx.doi.org/10.1158/1078-0432.CCR-04-0586.
22. Friedmann BJ, Caplin M, Savic B, Shah T, Lord CJ, Ashworth A, et al. Interaction of the epidermal growth factor receptor and the DNA-dependent protein kinase pathway following gefitinib treatment. Mol Cancer Ther 2006; 5:209-18; PMID:16505093; http://dx.doi.org/10.1158/1535-7163.MCT-05-0239.
23. Moasser MM, Basso A, Averbuch SD, Rosen N. The tyrosine kinase inhibitor ZD1839 ("Iressa") inhibits HER2-driven signaling and suppresses the growth of HER2-overexpressing tumor cells. Cancer Res 2001; 61:7184-8; PMID:11585753.
24. Hartley KO, Gell D, Smith GC, Zhang H, Divecha N, Connelly MA, et al. DNA-dependent protein kinase catalytic subunit: a relative of phosphatidylinositol- 3-kinase and the ataxia telangiectasia gene product. Cell 1995; 82:849-56; PMID:7671312; http://dx.doi.org/10.1016/0092-8674(95)90482-4.
25. Benhar M, Engelberg D, Levitzki A. Cisplatin-induced activation of the EGF receptor. Oncogene 2002; 21:8723-31; PMID:12483525; http://dx.doi.org/10. 1038/sj.onc.1205980.
26. Persons DL, Yazlovitskaya EM, Cui W, Pelling JC. Cisplatin-induced activation of mitogen-activated protein kinases in ovarian carcinoma cells: inhibition of extracellular signal-regulated kinase activity increases sensitivity to cisplatin. Clin Cancer Res 1999; 5:1007-14; PMID:10353733.
27. Hu L, Hofmann J, Lu Y, Mills GB, Jaffe RB. Inhibition of phosphatidylinositol-3'-kinase increases efficacy of paclitaxel in in vitro and in vivo ovarian cancer models. Cancer Res 2002; 62:1087-92; PMID:11861387.
28. 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; PMID:15118073; http://dx.doi.org/10.1056/NEJMoa040938.
29. 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; PMID:15118125; http://dx.doi.org/10.1126/ science.1099314.
30. Jennerwein MM, Eastman A. A polymerase chain reaction-based method to detect cisplatin adducts in specific genes. Nucleic Acids Res 1991; 19:6209-14; PMID:1956780; http://dx.doi.org/10.1093/nar/19.22.6209.
31. Hoeijmakers JH. Genome maintenance mechanisms for preventing cancer. Nature 2001; 411:366-74; PMID:11357144; http://dx.doi.org/10.1038/35077232.
32. Ciardiello F, Caputo R, Bianco R, Damiano V, Pomatico G, De Placido S, et al. 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; 6:2053-63; PMID:10815932.
33. Smith JA, Gaikwad A, Yu J, Wolf JK, Brown J, Ramondetta LM, et al. In vitro evaluation of the effects of gefitinib on the modulation of cytotoxic activity of selected anticancer agents in a part of human ovarian cancer cell lines. Cancer Chemother Pharmacol 2008; 62:51-8; PMID:17849119; http://dx.doi.org/10.1007/s00280-007-0572-y.
34. Duton CJ. New options for the treatment of advanced ovarian cancer. Semin Oncol 1997; 24:5-11.
35. Blackledge G, Lawton F, Redman C, Kelly K. Response of patients in phase II studies of chemotherapy in ovarian cancer: implications for patient treatment and the design of phase II trials. Br J Cancer 1989; 59:650-3; PMID:2713253; http://dx.doi.org/10.1038/bjc.1989.132.
36. Ciardiello F, Caputo R, Troiani T, Borriello G, Kandimalla ER, Agrawal S, et al. Antisense oligonucleotides targeting the epidermal growth factor receptor inhibit proliferation, induce apoptosis and cooperate with cytotoxic drugs in human cancer cell lines. Int J Cancer 2001; 93:172-8; PMID:11410862; http://dx.doi.org/10.1002/ijc.1335.
37. Hirata A, Hosoi F, Miyagawa M, Ueda S, Naito S, Fujii T, et al. HER2 overexpression increases sensitivity to gefitinib, an epidermal growth factor receptor tyrosine kinase inhibitor, through inhibition of HER2/HER3 heterodimer formation in lung cancer cells. Cancer Res 2005; 65:4253-60; PMID:15899817; http://dx.doi. org/10.1158/0008-5472.CAN-04-2748.
38. 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; PMID:15731348; http://dx.doi.org/10.1073/pnas.0409773102.
39. Judde JG, Rebucci M, Vogt N, de Cremoux P, Livartowski A, Chapelier A, et al. Gefitinib and chemotherapy combination studies in five novel human non small cell lung cancer xenografts. Evidence linking EGFR signaling to gefitinib antitumor response. Int J Cancer 2007; 120:1579-90; PMID:17205515; http://dx.doi.org/10.1002/ijc.22364.
40. Nozawa S, Tsukazaki K, Sakayori M, Jeng CH, Iizuka R. Establishment of a human ovarian clear cell carcinoma cell line (RMG-1) and its single cell cloning - with secial reference to the stem cell of the tumor. Hum Cell 1998; 1:426-35.
41. Hamilton TC, Winker MA, Louie KG, Batist G, Behrens BC, Tsuruo T, et al. Augmentation of adriamycin, melphalan and cisplatin cytotoxicity in drugresistant and -sensitive human ovarian carcinoma cell lines by buthionine sulfoximine mediated glutathione depletion. Biochem Pharmacol 1985; 34:2583-6; PMID:4040369; http://dx.doi.org/10.1016/0006-2952(85)90551-9.
42. Mabuchi S, Ohmichi M, Nishio Y, Hayasaka T, Kimura A, Ohta T, et al. Inhibition of NFkappaB increases the efficacy of cisplatin in in vitro and in vivo ovarian cancer models. J Biol Chem 2004; 279:23477-85; PMID:15026414; http://dx.doi.org/10.1074/jbc.M313709200.
43. Ohta T, Ohmichi M, Hayasaka T, Mabuchi S, Saitoh M, Kawagoe J, et al. Inhibition of phosphatidylinositol-3-kinase increases efficacy of cisplatin in in vivo ovarian cancer model. Endcrinology 2006; 147:1761-9; http://dx.doi.org/10.1210/en.2005-1450.
44. Potapova O, Haghighi A, Bost F, Liu C, Birrer MJ, Gjerset R, et al. The Jun kinase/stress-activated protein kinase pathway functions to regulate DNA repair and inhibition of the pathway sensitizes tumor cells to cisplatin. J Biol Chem 1997; 272:14041-4; PMID:9162025; http://dx.doi.org/10.1074/jbc.272.22. 14041.
45. Hayakawa J, Depatie C, Ohmichi M, Mercola D. The activation of c-Jun NH2-terminal kinase (JNK) by DNA-damaging agents serves to promote drug resistance via activating transcription factor 2 (ATF2)-dependent enhanced DNA repair. J Biol Chem 2003; 278:20582-92; PMID:12663670; http://dx.doi.org/10. 1074/jbc.M210992200.