Drug resistance originating from a TGF-β/FGF-2-driven epithelial-to-mesenchymal transition and its reversion in human lung adenocarcinoma cell lines harboring an EGFR mutation

International Journal of Oncology

Volumn 48, Issue 5, 2016, Pages 1825-1836

  Kurimoto, Ryota ^a   Iwasawa, Shunichiro ^a   Ebata, Takahiro ^a   Ishiwata, Tsukasa ^a   Sekine, Ikuo ^b   Tada, Yuji ^a   Tatsumi, Koichiro ^a   Koide, Shuhei ^a   Iwama, Atsushi ^a   Takiguchi, Yuichi ^a  

^a CHIBA UNIVERSITY   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Chemoresistance; Epidermal growth factor receptor mutation; Epithelial mesenchymal transition; Non small cell lung cancer; PD L1

Indexed keywords

2 (4 AMINO 1 ISOPROPYL 1H PYRAZOLO[3,4 D]PYRIMIDIN 3 YL) 1H INDOL 5 OL; CISPLATIN; DIMETHYL SULFOXIDE; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR 2; GEFITINIB; MAMMALIAN TARGET OF RAPAMYCIN; METFORMIN; MITOGEN ACTIVATED PROTEIN KINASE; PROGRAMMED DEATH 1 LIGAND 1; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; ANTINEOPLASTIC AGENT; CD274 PROTEIN, HUMAN; EGFR PROTEIN, HUMAN; INDOLE DERIVATIVE; PURINE DERIVATIVE; QUINAZOLINE DERIVATIVE;

APOPTOSIS; ARTICLE; CANCER RESISTANCE; CELL MOTILITY; CELL VIABILITY; CHEMOSENSITIVITY; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; FLOW CYTOMETRY; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNE SYSTEM; IMMUNOHISTOCHEMISTRY; LUNG ADENOCARCINOMA; LUNG CANCER CELL LINE; MOLECULAR BIOLOGY; MTT ASSAY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ADENOCARCINOMA; CELL SURVIVAL; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; LUNG TUMOR; METABOLISM; MUTATION; TUMOR CELL LINE;

ADENOCARCINOMA; ANTIGENS, CD274; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CELL SURVIVAL; CISPLATIN; DIMETHYL SULFOXIDE; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INDOLES; LUNG NEOPLASMS; METFORMIN; MUTATION; PURINES; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; TRANSFORMING GROWTH FACTOR BETA;

EID: 84962491772     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2016.3419     Document Type: Article

References (50)

1. Prall F: Tumour budding in colorectal carcinoma. Histopathology 50: 151-162, 2007.
2. Thiery JP, Acloque H, Huang RY and Nieto MA: Epithelialmesenchymal transitions in development and disease. Cell 139: 871-890, 2009.
3. Thomson S, Buck E, Petti F, Griffin G, Brown E, Ramnarine N, Iwata KK, Gibson N and Haley JD: Epithelial to mesenchymal transition is a determinant of sensitivity of non-small-cell lung carcinoma cell lines and xenografts to epidermal growth factor receptor inhibition. Cancer Res 65: 9455-9462, 2005.
4. Kurrey NK, Jalgaonkar SP, Joglekar AV, Ghanate AD, Chaskar PD, Doiphode RY and Bapat SA: Snail and slug mediate radioresistance and chemoresistance by antagonizing p53-mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells. Stem Cells 27: 2059-2068, 2009.
5. Lee JK, Joo KM, Lee J, Yoon Y and Nam DH: Targeting the epithelial to mesenchymal transition in glioblastoma: The emerging role of MET signaling. Onco Targets Ther 7: 1933-1944, 2014.
6. Kudo-Saito C, Shirako H, Takeuchi T and Kawakami Y: Cancer metastasis is accelerated through immunosuppression during Snail-induced EMT of cancer cells. Cancer Cell 15: 195-206, 2009.
7. Gavert N and Ben-Ze'ev A: Epithelial-mesenchymal transition and the invasive potential of tumors. Trends Mol Med 14: 199-209, 2008.
8. Grände M, Franzen A, Karlsson JO, Ericson LE, Heldin NE and Nilsson M: Transforming growth factor-beta and epidermal growth factor synergistically stimulate epithelial to mesenchymal transition (EMT) through a MEK-dependent mechanism in primary cultured pig thyrocytes. J Cell Sci 115: 4227-4236, 2002.
9. Derynck R and Zhang YE: Smad-dependent and Smadindependent pathways in TGF-beta family signalling. Nature 425: 577-584, 2003.
10. Shi Y and Massagué J: Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113: 685-700, 2003.
11. Chen XF, Zhang HJ, Wang HB, Zhu J, Zhou WY, Zhang H, Zhao MC, Su JM, Gao W, Zhang L, et al: Transforming growth factor-β1 induces epithelial-to-mesenchymal transition in human lung cancer cells via PI3K/Akt and MEK/Erk1/2 signaling pathways. Mol Biol Rep 39: 3549-3556, 2012.
12. Shirakihara T, Horiguchi K, Miyazawa K, Ehata S, Shibata T, Morita I, Miyazono K and Saitoh M: TGF-β regulates isoform switching of FGF receptors and epithelial-mesenchymal transition. EMBO J 30: 783-795, 2011.
13. Shih JY and Yang PC: The EMT regulator slug and lung carcinogenesis. Carcinogenesis 32: 1299-1304, 2011.
14. Chen H, Zhu G, Li Y, Padia RN, Dong Z, Pan ZK, Liu K and Huang S: Extracellular signal-regulated kinase signaling pathway regulates breast cancer cell migration by maintaining slug expression. Cancer Res 69: 9228-9235, 2009.
15. Lau MT and Leung PC: The PI3K/Akt/mTOR signaling pathway mediates insulin-like growth factor 1-induced E-cadherin downregulation and cell proliferation in ovarian cancer cells. Cancer Lett 326: 191-198, 2012.
16. Lyons JG, Patel V, Roue NC, Fok SY, Soon LL, Halliday GM and Gutkind JS: Snail up-regulates proinflammatory mediators and inhibits differentiation in oral keratinocytes. Cancer Res 68: 4525-4530, 2008.
17. Shintani Y, Okimura A, Sato K, Nakagiri T, Kadota Y, Inoue M, Sawabata N, Minami M, Ikeda N, Kawahara K, et al: Epithelial to mesenchymal transition is a determinant of sensitivity to chemoradiotherapy in non-small cell lung cancer. Ann Thorac Surg 92: 1794-1804, 2011.
18. Marín-Aguilera M, Codony-Servat J, Reig O, Lozano JJ, Fernández PL, Pereira MV, Jiménez N, Donovan M, Puig P, Mengual L, et al: Epithelial-to-mesenchymal transition mediates docetaxel resistance and high risk of relapse in prostate cancer. Mol Cancer Ther 13: 1270-1284, 2014.
19. Kajiyama H, Shibata K, Terauchi M, Yamashita M, Ino K, Nawa A and Kikkawa F: Chemoresistance to paclitaxel induces epithelial-mesenchymal transition and enhances metastatic potential for epithelial ovarian carcinoma cells. Int J Oncol 31: 277-283, 2007.
20. Yang AD, Fan F, Camp ER, van Buren G, Liu W, Somcio R, Gray MJ, Cheng H, Hoff PM and Ellis LM: Chronic oxaliplatin resistance induces epithelial-to-mesenchymal transition in colorectal cancer cell lines. Clin Cancer Res 12: 4147-4153, 2006.
21. Zhuo W, Wang Y, Zhuo X, Zhang Y, Ao X and Chen Z: Knockdown of Snail, a novel zinc finger transcription factor, via RNA interference increases A549 cell sensitivity to cisplatin via JNK/mitochondrial pathway. Lung Cancer 62: 8-14, 2008.
22. Chang TH, Tsai MF, Su KY, Wu SG, Huang CP, Yu SL, Yu YL, Lan CC, Yang CH, Lin SB, et al: Slug confers resistance to the epidermal growth factor receptor tyrosine kinase inhibitor. Am J Respir Crit Care Med 183: 1071-1079, 2011.
23. Sharma SV, Lee DY, Li B, Quinlan MP, Takahashi F, Maheswaran S, McDermott U, Azizian N, Zou L, Fischbach MA, et al: A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 141: 69-80, 2010.
24. Sato M, Shames DS and Hasegawa Y: Emerging evidence of epithelial-to-mesenchymal transition in lung carcinogenesis. Respirology 17: 1048-1059, 2012.
25. Zhang HJ, Wang HY, Zhang HT, Su JM, Zhu J, Wang HB, Zhou WY, Zhang H, Zhao MC, Zhang L, et al: Transforming growth factor-β1 promotes lung adenocarcinoma invasion and metastasis by epithelial-to-mesenchymal transition. Mol Cell Biochem 355: 309-314, 2011.
26. Lamouille S, Connolly E, Smyth JW, Akhurst RJ and Derynck R: TGF-β-induced activation of mTOR complex 2 drives epithelialmesenchymal transition and cell invasion. J Cell Sci 125: 1259-1273, 2012.
27. Buonato JM and Lazzara MJ: ERK1/2 blockade prevents epithelial-mesenchymal transition in lung cancer cells and promotes their sensitivity to EGFR inhibition. Cancer Res 74: 309-319, 2014.
28. Ishikawa D, Takeuchi S, Nakagawa T, Sano T, Nakade J, Nanjo S, Yamada T, Ebi H, Zhao L, Yasumoto K, et al: mTOR inhibitors control the growth of EGFR mutant lung cancer even after acquiring resistance by HGF. PLoS One 8: e62104, 2013.
29. Li L, Han R, Xiao H, Lin C, Wang Y, Liu H, Li K, Chen H, Sun F, Yang Z, et al: Metformin sensitizes EGFR-TKI-resistant human lung cancer cells in vitro and in vivo through inhibition of IL-6 signaling and EMT reversal. Clin Cancer Res 20: 2714-2726, 2014.
30. Yu HG, Wei W, Xia LH, Han WL, Zhao P, Wu SJ, Li WD and Chen W: FBW7 upregulation enhances cisplatin cytotoxicity in non-small cell lung cancer cells. Asian Pac J Cancer Prev 14: 6321-6326, 2013.
31. Cufí S, Vazquez-Martin A, Oliveras-Ferraros C, Martin-Castillo B, Joven J and Menendez JA: Metformin against TGFβ-induced epithelial-to-mesenchymal transition (EMT): From cancer stem cells to aging-associated fibrosis. Cell Cycle 9: 4461-4468, 2010.
32. Cañadas I, Rojo F, Taus A, Arpí O, Arumí-Uría M, Pijuan L, Menéndez S, Zazo S, Dómine M, Salido M, et al: Targeting epithelial-to-mesenchymal transition with Met inhibitors reverts chemoresistance in small cell lung cancer. Clin Cancer Res 20: 938-950, 2014.
33. Lamouille S and Derynck R: Cell size and invasion in TGF-beta-induced epithelial to mesenchymal transition is regulated by activation of the mTOR pathway. J Cell Biol 178: 437-451, 2007.
34. Maru S, Ishigaki Y, Shinohara N, Takata T, Tomosugi N and Nonomura K: Inhibition of mTORC2 but not mTORC1 up-regulates E-cadherin expression and inhibits cell motility by blocking HIF-2α expression in human renal cell carcinoma. J Urol 189: 1921-1929, 2013.
35. Kim EY, Kim A, Kim SK, Kim HJ, Chang J, Ahn CM and Chang YS: Inhibition of mTORC1 induces loss of E-cadherin through AKT/GSK-3β signaling-mediated upregulation of E-cadherin repressor complexes in non-small cell lung cancer cells. Respir Res 15: 26, 2014.
36. Shi XP, Miao S, Wu Y, Zhang W, Zhang XF, Ma HZ, Xin HL, Feng J, Wen AD and Li Y: Resveratrol sensitizes tamoxifen in antiestrogen-resistant breast cancer cells with epithelialmesenchymal transition features. Int J Mol Sci 14: 15655-15668, 2013.
37. Darakhshan S and Ghanbari A: Tranilast enhances the antitumor effects of tamoxifen on human breast cancer cells in vitro. J Biomed Sci 20: 76, 2013.
38. Xu G, Yu H, Shi X, Sun L, Zhou Q, Zheng D, Shi H, Li N, Zhang X and Shao G: Cisplatin sensitivity is enhanced in non-small cell lung cancer cells by regulating epithelial-mesenchymal transition through inhibition of eukaryotic translation initiation factor 5A2. BMC Pulm Med 14: 174, 2014.
39. Kao HF, Chang-Chien PW, Chang WT, Yeh TM and Wang JY: Propolis inhibits TGF-β1-induced epithelial-mesenchymal transition in human alveolar epithelial cells via PPARγ activation. Int Immunopharmacol 15: 565-574, 2013.
40. Yoshida T, Ozawa Y, Kimura T, Sato Y, Kuznetsov G, Xu S, Uesugi M, Agoulnik S, Taylor N, Funahashi Y, et al: Eribulin mesilate suppresses experimental metastasis of breast cancer cells by reversing phenotype from epithelial-mesenchymal transition (EMT) to mesenchymal-epithelial transition (MET) states. Br J Cancer 110: 1497-1505, 2014.
41. Saito RA, Watabe T, Horiguchi K, Kohyama T, Saitoh M, Nagase T and Miyazono K: Thyroid transcription factor-1 inhibits transforming growth factor-beta-mediated epithelial-tomesenchymal transition in lung adenocarcinoma cells. Cancer Res 69: 2783-2791, 2009.
42. Choi T: Dimethyl sulfoxide inhibits spontaneous oocyte fragmentation and delays inactivation of maturation promoting factor (MPF) during the prolonged culture of ovulated murine oocytes in vitro. Cytotechnology 63: 279-284, 2011.
43. Santos NC, Figueira-Coelho J, Martins-Silva J and Saldanha C: Multidisciplinary utilization of dimethyl sulfoxide: Pharmacological, cellular, and molecular aspects. Biochem Pharmacol 65: 1035-1041, 2003.
44. Szmant HH: Physical properties of dimethyl sulfoxide and its function in biological systems. Ann NY Acad Sci 243: 20-23, 1975.
45. Pagan R, Sánchez A, Martin I, Llobera M, Fabregat I and Vilaró S: Effects of growth and differentiation factors on the epithelial-mesenchymal transition in cultured neonatal rat hepatocytes. J Hepatol 31: 895-904, 1999.
46. Pagan R, Martín I, Llobera M and Vilaró S: Epithelialmesenchymal transition of cultured rat neonatal hepatocytes is differentially regulated in response to epidermal growth factor and dimethyl sulfoxide. Hepatology 25: 598-606, 1997.
47. Yu HN, Lee YR, Noh EM, Lee KS, Song EK, Han MK, Lee YC, Yim CY, Park J, Kim BS, et al: Tumor necrosis factor-alpha enhances DMSO-induced differentiation of HL-60 cells through the activation of ERK/MAPK pathway. Int J Hematol 87: 189-194, 2008.
48. Chen L, Gibbons DL, Goswami S, Cortez MA, Ahn YH, Byers LA, Zhang X, Yi X, Dwyer D, Lin W, et al: Metastasis is regulated via microRNA-200/ZEB1 axis control of tumour cell PD-L1 expression and intratumoral immunosuppression. Nat Commun 5: 5241, 2014.
49. Alsuliman A, Colak D, Al-Harazi O, Fitwi H, Tulbah A, Al-Tweigeri T, Al-Alwan M and Ghebeh H: Bidirectional crosstalk between PD-L1 expression and epithelial to mesenchymal transition: Significance in claudin-low breast cancer cells. Mol Cancer 14: 149, 2015.
50. Ota K, Azuma K, Kawahara A, Hattori S, Iwama E, Tanizaki J, Harada T, Matsumoto K, Takayama K, Takamori S, et al: Induction of PD-L1 expression by the EML4-ALK oncoprotein and downstream signaling pathways in non-small cell lung cancer. Clin Cancer Res 21: 4014-4021, 2015.