Blocking the epithelial-to-mesenchymal transition pathway abrogates resistance to anti-folate chemotherapy in lung cancer

Cell Death and Disease

Volumn 6, Issue 7, 2015, Pages

  Liang, S Q ^a,b   Marti, T M ^a,b   Dorn, P ^a,b   Froment, L ^a,b   Hall, S R R ^a,b   Berezowska, S ^b   Kocher, G ^a,b   Schmid, R A ^a,b   Peng, R W ^a,b  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; ALDEHYDE DEHYDROGENASE; KAEMPFEROL; PEMETREXED; ANTINEOPLASTIC AGENT; FOLIC ACID; FOLIC ACID ANTAGONIST;

ARTICLE; CANCER CELL; CANCER CELL LINE; CANCER RESISTANCE; CANCER STEM CELL; CLONOGENESIS; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME INHIBITION; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; HUMAN TISSUE; NON SMALL CELL LUNG CANCER; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR GENE; CARCINOMA, NON-SMALL-CELL LUNG; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; LUNG NEOPLASMS; METABOLISM; PATHOLOGY; TUMOR CELL LINE; TUMOR RECURRENCE;

ANTINEOPLASTIC AGENTS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; FOLIC ACID; FOLIC ACID ANTAGONISTS; HUMANS; LUNG NEOPLASMS; NEOPLASM RECURRENCE, LOCAL; SIGNAL TRANSDUCTION;

EID: 84989337867     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2015.195     Document Type: Article

References (50)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011; 61: 69-90.
2. Siegel R, DeSantis C, Virgo K, Stein K, Mariotto A, Smith T et al. Cancer treatment and survivorship statistics, 2012. CA Cancer J Clin 2012; 62: 220-241.
3. Holohan C, Van Schaeybroeck S, Longley DB, Johnston PG. Cancer drug resistance: An evolving paradigm. Nat Rev Cancer 2013; 13: 714-726.
4. Valent P, Bonnet D, De Maria R, Lapidot T, Copland M, Melo JV et al. Cancer stem cell definitions and terminology: The devil is in the details. Nat Rev Cancer 2012; 12: 767-775.
5. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005; 5: 275-284.
6. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997; 3: 730-737.
7. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100: 3983-3988.
8. Driessens G, Beck B, Caauwe A, Simons BD, Blanpain C. Defining the mode of tumour growth by clonal analysis. Nature 2012; 488: 527-530.
9. Schepers AG, Snippert HJ, Stange DE, van den Born M, van Es JH, van de Wetering M et al. Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adenomas. Science 2012; 337: 730-735.
10. Chen J, Li Y, Yu TS, McKay RM, Burns DK, Kernie SG et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 2012; 488: 522-526.
11. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444: 756-760.
12. Seguin L, Kato S, Franovic A, Camargo MF, Lesperance J, Elliott KC et al. An integrin β3-KRAS-RalB complex drives tumour stemness and resistance to EGFR inhibition. Nat Cell Biol 2014; 16: 457-468.
13. Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, Di Virgilio A et al. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 2008; 15: 504-514.
14. Bertolini G, Roz L, Perego P, Tortoreto M, Fontanella E, Gatti L et al. Highly tumorigenic lung cancer CD133+ cells display stem-like features and are spared by cisplatin treatment. Proc Natl Acad Sci USA 2009; 106: 16281-16286.
15. Jung MJ, Rho JK, Kim YM, Jung JE, Jin YB, Ko YG et al. Upregulation of CXCR4 is functionally crucial for maintenance of stemness in drug-resistant non-small cell lung cancer cells. Oncogene 2013; 32: 209-221.
16. Zhang WC, Shyh-Chang N, Yang H, Rai A, Umashankar S, Ma S et al. Glycine decarboxylase activity drives non-small cell lung cancer tumor-initiating cells and tumorigenesis. Cell 2012; 148: 259-272.
17. Zheng Y, de la Cruz CC, Sayles LC, Alleyne-Chin C, Vaka D, Knaak TD et al. A rare population of CD24(+)ITGB4(+)Notch(hi) cells drives tumor propagation in NSCLC and requires Notch3 for self-renewal. Cancer Cell 2013; 24: 59-74.
18. Bartucci M, Svensson S, Romania P, Dattilo R, Patrizii M, Signore M et al. Therapeutic targeting of Chk1 in NSCLC stem cells during chemotherapy. Cell Death Differ 2012; 19: 768-778.
19. Liu YP, Yang CJ, Huang MS, Yeh CT, Wu AT, Lee YC et al. Cisplatin selects for multidrugresistant CD133+ cells in lung adenocarcinoma by activating Notch signaling. Cancer Res 2013; 73: 406-416.
20. Lundholm L, Hååg P, Zong D, Juntti T, Mörk B, Lewensohn R et al. Resistance to DNA-damaging treatment in non-small cell lung cancer tumor-initiating cells involves reduced DNA-PK/ATM activation and diminished cell cycle arrest. Cell Death Dis 2013; 4: E478.
21. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139: 871-890.
22. Scheel C, Eaton EN, Li SH, Chaffer CL, Reinhardt F, Kah KJ C et al. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell 2011; 145: 926-940.
23. Tam WL, Weinberg RA. The epigenetics of epithelial-mesenchymal plasticity in cancer. Nat Med 2013; 19: 1438-1449.
24. Mani SA, GuoW, Liao MJ, Eaton EN, Ayyanan A, Zhou AY et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008; 133: 704-715.
25. Pattabiraman DR, Weinberg RA. Tackling the cancer stem cells-what challenges do they pose? Nat Rev Drug Discov 2014; 13: 497-512.
26. Thomson S, Buck E, Petti F, Griffin G, Brown E, Ramnarine N et al. 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 2005; 65: 9455-9462.
27. Yang AD, Fan F, Camp ER, van Buren G, Liu W, Somcio R et al. Chronic oxaliplatin resistance induces epithelial-To-mesenchymal transition in colorectal cancer cell lines. Clin Cancer Res 2006; 12: 4147-4153.
28. Kurrey NK, Jalgaonkar SP, Joglekar AV, Ghanate AD, Chaskar PD, Doiphode RY et al. Snail and slug mediate radioresistance and chemoresistance by antagonizing p53-mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells. Stem Cells 2009; 27: 2059-2068.
29. Gonen N, Assaraf YG. Antifolates in cancer therapy: Structure, activity and mechanisms of drug resistance. Drug Resist Updat 2012; 15: 183-210.
30. Nguyen TT, Tran E, Ong CK, Lee SK, Do PT, Huynh TT et al. Kaempferol-induced growth inhibition and apoptosis in A549 lung cancer cells is mediated by activation of MEK-MAPK. J Cell Physiol 2003; 197: 110-121.
31. Sharma V, Joseph C, Ghosh S, Agarwal A, Mishra MK, Sen E. Kaempferol induces apoptosis in glioblastoma cells through oxidative stress. Mol Cancer Ther 2007; 6: 2544-2553.
32. Siegelin MD, Reuss DE, Habel A, Herold-Mende C, von Deimling A. The flavonoid kaempferol sensitizes human glioma cells to TRAIL-mediated apoptosis by proteasomal degradation of survivin. Mol Cancer Ther 2008; 7: 3566-3574.
33. Shoemaker RH. The NCI60 human tumour cell line anticancer drug screen. Nat Rev 2006; 6: 813-823.
34. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007; 1: 555-567.
35. Sullivan JP, Spinola M, Dodge M, Raso MG, Behrens C, Gao B et al. Aldehyde dehydrogenase activity selects for lung adenocarcinoma stem cells dependent on notch signaling. Cancer Res 2010; 70: 9937-9948.
36. Shao C, Sullivan JP, Girard L, Augustyn A, Yenerall P, Rodriguez-Canales J et al. Essential role of aldehyde dehydrogenase 1A3 for the maintenance of non-small cell lung cancer stem cells is associated with the STAT3 pathway. Clin Cancer Res 2014; 20: 4154-4166.
37. Gyorffy B, Surowiak P, Budczies J, Lanczky A. Online survival analysis software to assess the prognostic value of biomarkers using transcriptomic data in non-small-cell lung cancer. PLoS One 2013; 8: E82241.
38. Tan TZ, Miow QH, Miki Y, Noda T, Mori S, Huang RY et al. Epithelial-mesenchymal transition spectrum quantification and its efficacy in deciphering survival and drug responses of cancer patients. EMBO Mol Med 2014; 6: 1279-1293.
39. Gong JH, Cho IH, Shin D, Han SY, Park SH, Kang YH. Inhibition of airway epithelial-Tomesenchymal transition and fibrosis by kaempferol in endotoxin-induced epithelial cells and ovalbumin-sensitized mice. Lab Invest 2014; 94: 297-308.
40. Nasarre P, Gemmill RM, Potiron VA, Roche J, Lu X, Barsn AE et al. Neuropilin-2 Is upregulated in lung cancer cells during TGF-β1-induced epithelial-mesenchymal transition. Cancer Res 2013; 73: 7111-7121.
41. Buqué A, Aresti U, Calvo B, Sh Muhialdin J, Muñoz A, Carrera S et al. Thymidylate synthase expression determines pemetrexed targets and resistance development in tumour cells. PLoS One 2013; 8: E63338.
42. Canino C, Mori F, Cambria A, Diamantini A, Germoni S, Alessandrini G et al. SASP mediates chemoresistance and tumor-initiating-Activity of mesothelioma cells. Oncogene 2012; 31: 3148-3163.
43. Cortes-Dericks L, Carboni GL, Schmid RA, Karoubi G. Putative cancer stem cells in malignant pleural mesothelioma show resistance to cisplatin and pemetrexed. Int J Oncol 2010; 37: 437-444.
44. Nijveldt RJ, van Nood E, van Hoorn DE, Boelens PG, van Norren K, van Leeuwen PA. Flavonoids: A review of probable mechanisms of action and potential applications. Am J Clin Nutr 2001; 74: 418-425.
45. Deryugina EI, Quigley JP. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev 2006; 25: 9-34.
46. Lin CW, Shen SC, Chien CC, Yang LY, Shia LT, Chen YC. 12-O-Tetradecanoylphorbol-13-Acetate-induced invasion/migration of glioblastoma cells through activating PKCalpha/ERK/ NF-kappaB-dependent MMP-9 expression. J Cell Physiol 2010; 225: 472-481.
47. Lin CW, Chen PN, Chen MK, Yang WE, Tang CH, Yang SF et al. Kaempferol reduces matrix metalloproteinase-2 expression by down-regulating ERK1/2 and the activator protein-1 signaling pathways in oral cancer cells. PLoS One 2013; 8: E80883.
48. Hardie WD, Hagood JS, Dave V, Perl AK, Whitsett JA, Korfhagen TR et al. Signaling pathways in the epithelial origins of pulmonary fibrosis. Cell Cycle 2010; 9: 2769-2776.
49. Franken NA, Rodermond HM, Stap J, Haveman J, van Bree C. Clonogenic assay of cells in vitro. Nat Protoc 2006; 1: 2315-2319.
50. Liang CC, Park AY, Guan JL. In vitro scratch assay: A convenient and inexpensive method for analysis of cell migration in vitro. Nat Protoc 2007; 2: 329-333.