Synergistic inhibitory effects by the combination of gefitinib and genistein on NSCLC with acquired drug-resistance in vitro and in vivo

Molecular Biology Reports

Volumn 39, Issue 4, 2012, Pages 4971-4979

  Zhu, Hang ^a   Cheng, Hua ^b   Ren, Yuan ^c   Liu, Zhan Guo ^d   Zhang, Yi Fang ^a   De Luo, Bing ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

^c GUILIN MEDICAL UNIVERSITY   (China)

^d SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

Acquired drugresistance; Gefitinib; Genistein; Non small cell lung cancer; Synergistic inhibitory effect

Indexed keywords

CASPASE 3; EPIDERMAL GROWTH FACTOR RECEPTOR; GEFITINIB; GENISTEIN; MAMMALIAN TARGET OF RAPAMYCIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN KINASE B; ANTINEOPLASTIC AGENT; PROTEIN KINASE INHIBITOR; QUINAZOLINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL DESTRUCTION; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CANCER RESISTANCE; CELL PROLIFERATION; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENTIATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FEMALE; FLOW CYTOMETRY; GENE MUTATION; HETEROZYGOTE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG NON SMALL CELL CANCER; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; WESTERN BLOTTING; ANIMAL; CELL TRANSFORMATION; DRUG ANTAGONISM; DRUG EFFECT; DRUG RESISTANCE; DRUG SCREENING; GENETICS; IC 50; LUNG TUMOR; METABOLISM; MUTATION; PATHOLOGY; TUMOR CELL LINE;

MUS MUSCULUS;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; BLOTTING, WESTERN; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; GENISTEIN; HUMANS; INHIBITORY CONCENTRATION 50; LUNG NEOPLASMS; MICE; MUTATION; PROTEIN KINASE INHIBITORS; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84863095863     PISSN: 03014851     EISSN: 15734978     Source Type: Journal    
DOI: 10.1007/s11033-011-1293-1     Document Type: Article

References (48)

1. 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(12):2893-2917. doi: 10.1002/ijc.25516
2. Gridelli C, Langer C, Maione P, Rossi A, Schild SE (2007) Lung cancer in the elderly. J Clin Oncol 25(14):1898-1907
3. Schiller JH (2001) Current standards of care in small-cell and non-small-cell lung cancer. Oncology 61(Suppl 1):3-13
4. Pavelic K, Banjac Z, Pavelic J, Spaventi S (1993) Evidence for a role of EGF receptor in the progression of human lung carcinoma. Anticancer Res 13(4):1133-1137
5. Cortes-Funes H (2002) New treatment approaches for lung cancer and impact on survival. Semin Oncol 29(3 Suppl 8):26-29
6. Fossella FV, DeVore R, Kerr RN, Crawford J, Natale RR, Dunphy F, Kalman L, Miller V, Lee JS, Moore M, Gandara D, Karp D, Vokes E, Kris M, Kim Y, Gamza F, Hammershaimb L (2000) Randomized phase III trial of docetaxel versus vinorelbine or ifosfamide in patients with advanced non-small-cell lung cancer previously treated with platinum-containing chemotherapy regimens. The TAX 320 Non-Small Cell Lung Cancer Study Group. J Clin Oncol 18(12):2354-2362
7. 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 (2004) Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 350(21):2129-2139
8. Paez JG, Janne 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 (2004) EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science 304(5676):1497-1500
9. Pao W, Miller V, Zakowski M, Doherty J, Politi K, Sarkaria I, Singh B, Heelan R, Rusch V, Fulton L, Mardis E, Kupfer D, Wilson R, Kris M, Varmus H (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 USA 101(36):13306-13311
10. Mok TS, Wu YL, Thongprasert S, Yang CH, Chu DT, Saijo N, Sunpaweravong P, Han B, Margono B, Ichinose Y, Nishiwaki Y, Ohe Y, Yang JJ, Chewaskulyong B, Jiang H, Duffield EL, Watkins CL, Armour AA, Fukuoka M (2009) Gefitinib or carboplatin-paclitaxel in pulmonary adenocarcinoma. N Engl J Med 361(10):947-957
11. Maemondo M, Inoue A, Kobayashi K, Sugawara S, Oizumi S, Isobe H, Gemma A, Harada M, Yoshizawa H, Kinoshita I, Fujita Y, Okinaga S, Hirano H, Yoshimori K, Harada T, Ogura T, Ando M, Miyazawa H, Tanaka T, Saijo Y, Hagiwara K, Morita S, Nukiwa T (2010) Gefitinib or chemotherapy for non-small-cell lung cancer with mutated EGFR. N Engl J Med 362(25):2380-2388. doi:10.1056/NEJMoa0909530
12. Mitsudomi T, Morita S, Yatabe Y, Negoro S, Okamoto I, Tsurutani J, Seto T, Satouchi M, Tada H, Hirashima T, Asami K, Katakami N, Takada M, Yoshioka H, Shibata K, Kudoh S, Shimizu E, Saito H, Toyooka S, Nakagawa K, Fukuoka M (2010) Gefitinib versus cisplatin plus docetaxel in patients with nonsmall-cell lung cancer harbouring mutations of the epidermal growth factor receptor (WJTOG3405): an open label, randomised phase 3 trial. Lancet Oncol 11(2):121-128. doi:10.1016/s1470-2045(09)70364-x
13. Zhou C, Wu YL, Chen G, Feng J, Liu XQ, Wang C, Zhang S, Wang J, Zhou S, Ren S, Lu S, Zhang L, Hu C, Luo Y, Chen L, Ye M, Huang J, Zhi X, Zhang Y, Xiu Q, Ma J, You C (2011) Erlotinib versus chemotherapy as first-line treatment for patients with advanced EGFR mutation-positive non-small-cell lung cancer (OPTIMAL, CTONG-0802): a multicentre, open-label, randomised, phase 3 study. Lancet Oncol 12(8):735-742. doi: 10.1016/s1470-2045(11)70184-x
14. Kobayashi S, Boggon TJ, Dayaram T, Janne PA, Kocher O, Meyerson M, Johnson BE, Eck MJ, Tenen DG, Halmos B (2005) EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med 352(8):786-792
15. Pao W, Miller VA, Politi KA, Riely GJ, Somwar R, Zakowski MF, Kris MG, Varmus H (2005) Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Med 2(3):e73
16. Yun CH, Mengwasser KE, Toms AV, Woo MS, Greulich H, Wong KK, Meyerson M, Eck MJ (2008) The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP. Proc Natl Acad Sci USA 105(6):2070-2075
17. Banerjee S, Li Y, Wang Z, Sarkar FH (2008) Multi-Targeted therapy of cancer by genistein. Cancer Lett 269(2):226-242
18. Sarkar FH, Li Y (2002) Mechanisms of cancer chemoprevention by soy isoflavone genistein. Cancer Metastasis Rev 21(3-4): 265-280
19. Sarkar FH, Li Y (2006) Using chemopreventive agents to enhance the efficacy of cancer therapy. Cancer Res 66(7): 3347-3350
20. Ravindranath MH, Muthugounder S, Presser N, Viswanathan S (2004) Anticancer therapeutic potential of soy isoflavone, genistein. Adv Exp Med Biol 546:121-165
21. El-Rayes BF, Ali S, Ali IF, Philip PA, Abbruzzese J, Sarkar FH (2006) Potentiation of the effect of erlotinib by genistein in pancreatic cancer: the role of Akt and nuclear factor-kappaB. Cancer Res 66(21):10553-10559
22. Gadgeel SM, Ali S, Philip PA, Wozniak A, Sarkar FH (2009) Genistein enhances the effect of epidermal growth factor receptor tyrosine kinase inhibitors and inhibits nuclear factor kappa B in nonsmall cell lung cancer cell lines. Cancer 115(10):2165-2176
23. Ali S, Varghese L, Pereira L, Tulunay-Ugur OE, Kucuk O, Carey TE, Wolf GT, Sarkar FH (2009) Sensitization of squamous cell carcinoma to cisplatin induced killing by natural agents. Cancer Lett 278(2):201-209
24. Jin CY, Park C, Moon SK, Kim GY, Kwon TK, Lee SJ, Kim WJ, Choi YH (2009) Genistein sensitizes human hepatocellular carcinoma cells to TRAIL-mediated apoptosis by enhancing Bid cleavage. Anti-cancer drugs 20(8):713-722
25. Park SJ, Kim MJ, Kim YK, Kim SM, Park JY, Myoung H (2010) Combined cetuximab and genistein treatment shows additive anti-cancer effect on oral squamous cell carcinoma. Cancer Lett 292(1):54-63
26. Cheng H, An S-J, Zhang X-C, Dong S, Zhang Y-F, Chen Z-H, Chen H-J, Guo A-L, Lin Q-x, Wu Y-L (2011) In vitro sequencedependent synergism between paclitaxel and gefitinib in human lung cancer cell lines. Cancer Chemother Pharmacol 67(3):637-646. doi:10.1007/s00280-010-1347-4
27. Chou TC, Talalay P (1984) Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 22:27-55
28. Zhang GC, Lin JY, Wang Z, Zhou Q, Xu CR, Zhu JQ, Wang K, Yang XN, Chen G, Yang JJ, Huang YJ, Liao RQ, Wu YL (2007) Epidermal growth factor receptor double activating mutations involving both exons 19 and 21 exist in Chinese non-small cell lung cancer patients. Clin Oncol (R Coll Radiol) 19(7):499-506
29. Zhu JQ, Zhong WZ, Zhang GC, Li R, Zhang XC, Guo AL, Zhang YF, An SJ, Mok TS, Wu YL (2008) Better survival with EGFR exon 19 than exon 21 mutations in gefitinib-Treated non-small cell lung cancer patients is due to differential inhibition of downstream signals. Cancer Lett 265(2):307-317
30. Sordella R, Bell DW, Haber DA, Settleman J (2004) Gefitinibsensitizing EGFR mutations in lung cancer activate anti-Apoptotic pathways. Science 305(5687):1163-1167
31. Fukuoka M, Wu YL, Thongprasert S, Sunpaweravong P, Leong SS, Sriuranpong V, Chao TY, Nakagawa K, Chu DT, Saijo N, Duffield EL, Rukazenkov Y, Speake G, Jiang H, Armour AA, To KF, Yang JC, Mok TS (2011) Biomarker analyses and final overall survival results from a phase III, randomized, open-label, first-line study of gefitinib versus carboplatin/paclitaxel in clinically selected patients with advanced non-small-cell lung cancer in Asia (IPASS). J Clin Oncol 29(21):2866-2874. doi:10.1200/ jco.2010.33.4235
32. Herbst RS, Prager D, Hermann R, Fehrenbacher L, Johnson BE, Sandler A, Kris MG, Tran HT, Klein P, Li X, Ramies D, Johnson DH, Miller VA (2005) TRIBUTE: a phase III trial of erlotinib hydrochloride (OSI-774) combined with carboplatin and paclitaxel chemotherapy in advanced non-small-cell lung cancer. J Clin Oncol 23(25):5892-5899
33. Giaccone G, Herbst RS, Manegold C, Scagliotti G, Rosell R, Miller V, Natale RB, Schiller JH, Von Pawel J, Pluzanska A, Gatzemeier U, Grous J, Ochs JS, Averbuch SD, Wolf MK, Rennie P, Fandi A, Johnson DH (2004) Gefitinib in combination with gemcitabine and cisplatin in advanced non-small-cell lung cancer: a phase III trial-INTACT 1. J Clin Oncol 22(5):777-784
34. Gatzemeier U, Pluzanska A, Szczesna A, Kaukel E, Roubec J, De Rosa F, Milanowski J, Karnicka-Mlodkowski H, Pesek M, Serwatowski P, Ramlau R, Janaskova T, Vansteenkiste J, Strausz J, Manikhas GM, Von Pawel J (2007) Phase III study of erlotinib in combination with cisplatin and gemcitabine in advanced nonsmall-cell lung cancer: the Tarceva lung cancer investigation trial. J Clin Oncol 25(12):1545-1552
35. Herbst RS, Giaccone G, Schiller JH, Natale RB, Miller V, Manegold C, Scagliotti G, Rosell R, Oliff I, Reeves JA, Wolf MK, Krebs AD, Averbuch SD, Ochs JS, Grous J, Fandi A, Johnson DH (2004) Gefitinib in combination with paclitaxel and carboplatin in advanced non-small-cell lung cancer: a phase III trial-INTACT 2. J Clin Oncol 22(5):785-794
36. Li T, Ling YH, Goldman ID, Perez-Soler R (2007) Scheduledependent cytotoxic synergism of pemetrexed and erlotinib in human non-small cell lung cancer cells. Clin Cancer Res 13(11):3413-3422
37. Shiau RJ, Chen KY, Wen YD, Chuang CH, Yeh SL (2010) Genistein and beta-carotene enhance the growth-inhibitory effect of trichostatin A in A549 cells. Eur J Nutr 49(1):19-25. doi: 10.1007/s00394-009-0044-8
38. Fotsis T, Pepper MS, Montesano R, Aktas E, Breit S, Schweigerer L, Rasku S, Wahala K, Adlercreutz H (1998) Phytoestrogens and inhibition of angiogenesis. Bailliere's Clin Endocrinol Metab 12(4):649-666
39. Kennedy SG, Wagner AJ, Conzen SD, Jordan J, Bellacosa A, Tsichlis PN, Hay N (1997) The PI 3-kinase/Akt signaling pathway delivers an anti-Apoptotic signal. Genes Dev 11(6):701-713
40. Franke TF, Hornik CP, Segev L, Shostak GA, Sugimoto C (2003) PI3K/Akt and apoptosis: size matters. Oncogene 22(56): 8983-8998
41. Cardone MH, Roy N, Stennicke HR, Salvesen GS, Franke TF, Stanbridge E, Frisch S, Reed JC (1998) Regulation of cell death protease caspase-9 by phosphorylation. Science 282(5392): 1318-1321
42. Jeong JC, Kim MS, Kim TH, Kim YK (2009) Kaempferol induces cell death through ERK and Akt-dependent down-regulation of XIAP and survivin in human glioma cells. Neurochem Res 34(5):991-1001
43. Dong S, Zhang X, Cheng H, Guo A, Zhu J, Yang S, Wu Y (2010) Effect of everolimus and gefitinib on PI3K/akt/mTOR and raf/ MEK/ERK pathways in NSCLC cells. J Clin Oncol (Meeting Abstracts) 28 (15-suppl):e13654
44. Begum M, Tashiro H, Katabuchi H, Suzuki A, Kurman RJ, Okamura H (2006) Neonatal estrogenic exposure suppresses PTEN-related endometrial carcinogenesis in recombinant mice. Lab Investig 86(3):286-296
45. Anastasius N, Boston S, Lacey M, Storing N, Whitehead SA (2009) Evidence that low-dose, long-Term genistein treatment inhibits oestradiol-stimulated growth in MCF-7 cells by downregulation of the PI3-kinase/Akt signalling pathway. J Steroid Biochem Mol Biol 116(1-2):50-55
46. Ullmann U, Metzner J, Frank T, Cohn W, Riegger C (2005) Safety, tolerability, and pharmacokinetics of single ascending doses of synthetic genistein (Bonistein) in healthy volunteers. Adv Ther 22(1):65-78
47. Li D, Ambrogio L, Shimamura T, Kubo S, Takahashi M, Chirieac LR, Padera RF, Shapiro GI, Baum A, Himmelsbach F, Rettig WJ, Meyerson M, Solca F, Greulich H, Wong aKK (2008) BIBW2992, an irreversible EGFR/HER2 inhibitor highly effective in preclinical lung cancer models. Oncogene 27(34) :4702-4711
48. Engelman JA, Zejnullahu K, Gale CM, Lifshits E, Gonzales AJ, Shimamura T, Zhao F, Vincent PW, Naumov GN, Bradner JE, Althaus IW, Gandhi L, Shapiro GI, Nelson JM, Heymach JV, Meyerson M, Wong KK, Janne PA (2007) PF00299804, an irreversible pan-ERBB inhibitor, is effective in lung cancer models with EGFR and ERBB2 mutations that are resistant to gefitinib. Cancer Res 67(24):11924-11932