Prolonged pemetrexed pretreatment augments persistence of cisplatin-induced DNA damage and eliminates resistant lung cancer stem-like cells associated with EMT

BMC Cancer

Volumn 16, Issue 1, 2016, Pages

  Tièche, Colin Charles ^a   Peng, Ren Wang ^a   Dorn, Patrick ^a   Froment, Laurène ^a   Schmid, Ralph Alexander ^a   Marti, Thomas Michael ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

Chemotherapy; Cisplatin; EMT; Non small cell lung cancer; Pemetrexed; Resistance; Stem cells

Indexed keywords

CISPLATIN; HISTONE H2AX; PEMETREXED; ANTINEOPLASTIC AGENT;

A549 CELL LINE; APOPTOSIS; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER RESISTANCE; CANCER STEM CELL; CELL CLONE; CELL CYCLE; CELL GROWTH; COLONY FORMATION; CONTROLLED STUDY; DNA DAMAGE; EPITHELIAL MESENCHYMAL TRANSITION; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; NON SMALL CELL LUNG CANCER; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; SENESCENCE; CARCINOMA, NON-SMALL-CELL LUNG; CELL AGING; DRUG EFFECTS; DRUG POTENTIATION; DRUG RESISTANCE; GENETICS; LUNG NEOPLASMS; PATHOLOGY; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; CARCINOMA, NON-SMALL-CELL LUNG; CELL AGING; CELL CYCLE; CELL LINE, TUMOR; CISPLATIN; DNA DAMAGE; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; LUNG NEOPLASMS; NEOPLASTIC STEM CELLS; PEMETREXED;

EID: 84958529809     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/s12885-016-2117-4     Document Type: Article

References (50)

1. Treat J, Scagliotti GV, Peng G, Monberg MJ, Obasaju CK, Socinski MA. Comparison of pemetrexed plus cisplatin with other first-line doublets in advanced non-small cell lung cancer (NSCLC): a combined analysis of three phase 3 trials. Lung Cancer. 2012;76(2):222-7.
2. Besse B, Adjei A, Baas P, Meldgaard P, Nicolson M, Paz-Ares L, et al. 2nd ESMO consensus conference on lung cancer: non-small-cell lung cancer first-line/second and further lines of treatment in advanced disease. Ann Oncol Off Jo Eur Soc Med Oncol / ESMO. 2014;25(8):1475-84.
3. Nowak AK. Chemotherapy for malignant pleural mesothelioma: a review of current management and a look to the future. Ann Cardiothorac Surg. 2012;1(4):508-15.
4. Zeman MK, Cimprich KA. Causes and consequences of replication stress. Nat Cell Biol. 2014;16(1):2-9.
5. Tsaalbi-Shtylik A, Moser J, Mullenders LH, Jansen JG, de Wind N. Persistently stalled replication forks inhibit nucleotide excision repair in trans by sequestering Replication protein A. Nucleic Acids Res. 2014;42(7):4406-13.
6. Harper JW, Elledge SJ. The DNA damage response: ten years after. Mol Cell. 2007;28(5):739-45.
7. Ghosal G, Chen J. DNA damage tolerance: a double-edged sword guarding the genome. Transl Cancer Res. 2013;2(3):107-29.
8. Rodier F, Coppe JP, Patil CK, Hoeijmakers WA, Munoz DP, Raza SR, et al. Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion. Nat Cell Biol. 2009;11(8):973-9.
9. Pattabiraman DR, Weinberg RA. Tackling the cancer stem cells - what challenges do they pose? Nat Rev Drug Discov. 2014;13(7):497-512.
10. Grosse-Wilde A, Fouquier d'Herouel A, McIntosh E, Ertaylan G, Skupin A, Kuestner RE, et al. Stemness of the hybrid epithelial/mesenchymal state in breast cancer and its association with poor survival. PLoS One. 2015;10(5):e0126522.
11. Zhao Z, Cheng X, Wang Y, Han R, Li L, Xiang T, et al. Metformin inhibits the IL-6-induced epithelial-mesenchymal transition and lung adenocarcinoma growth and metastasis. PLoS One. 2014;9(4):e95884.
12. Liang SQ, Marti TM, Dorn P, Froment L, Hall SR, Berezowska S, et al. Blocking the epithelial-to-mesenchymal transition pathway abrogates resistance to anti-folate chemotherapy in lung cancer. Cell Death Dis. 2015;6:e1824.
13. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer. 2002;2(6):442-54.
14. Akunuru S, James Zhai Q, Zheng Y. Non-small cell lung cancer stem/progenitor cells are enriched in multiple distinct phenotypic subpopulations and exhibit plasticity. Cell Death Dis. 2012;3:e352.
15. Gupta PB, Chaffer CL, Weinberg RA. Cancer stem cells: mirage or reality? Nat Med. 2009;15(9):1010-2.
16. Neelsen KJ, Zanini IM, Herrador R, Lopes M. Oncogenes induce genotoxic stress by mitotic processing of unusual replication intermediates. J Cell Biol. 2013;200(6):699-708.
17. Collado M, Serrano M. Senescence in tumours: evidence from mice and humans. Nat Rev Cancer. 2010;10(1):51-7.
18. Hwang ES, Yoon G, Kang HT. A comparative analysis of the cell biology of senescence and aging. Cellular Mol Life sci CMLS. 2009;66(15):2503-24.
19. Xu H, Wang Z, Donaldson JC, Yao H, Zhou S, Kelson AB, et al. Antitumor efficacy and molecular mechanism of TLK58747, a novel DNA-alkylating prodrug. Anticancer Res. 2009;29(10):3845-55.
20. Weeks LD, Zentner GE, Scacheri PC, Gerson SL. Uracil DNA glycosylase (UNG) loss enhances DNA double strand break formation in human cancer cells exposed to pemetrexed. Cell Death Dis. 2014;5:e1045.
21. Marti TM, Hefner E, Feeney L, Natale V, Cleaver JE. H2AX phosphorylation within the G1 phase after UV irradiation depends on nucleotide excision repair and not DNA double-strand breaks. Proc Natl Acad Sci U S A. 2006;103(26):9891-6.
22. Huang X, Halicka HD, Traganos F, Tanaka T, Kurose A, Darzynkiewicz Z. Cytometric assessment of DNA damage in relation to cell cycle phase and apoptosis. Cell Prolif. 2005;38(4):223-43.
23. Knobel PA, Kotov IN, Felley-Bosco E, Stahel RA, Marti TM. Inhibition of REV3 expression induces persistent DNA damage and growth arrest in cancer cells. Neoplasia. 2011;13(10):961-70.
24. 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(5):768-78.
25. Lundholm L, Haag P, Zong D, Juntti T, Mork 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.
26. Kano Y, Akutsu M, Tsunoda S, Izumi T, Kobayashi H, Inoue K, et al. Schedule-dependent interactions between pemetrexed and cisplatin in human carcinoma cell lines in vitro. Oncol Res. 2006;16(2):85-95.
27. Del Bufalo D, Desideri M, De Luca T, Di Martile M, Gabellini C, Monica V, et al. Histone deacetylase inhibition synergistically enhances pemetrexed cytotoxicity through induction of apoptosis and autophagy in non-small cell lung cancer. Mol Cancer. 2014;13:230.
28. Morgillo F, Martinelli E, Troiani T, Laus G, Pepe S, Gridelli C, et al. Sequence-dependent, synergistic antiproliferative and proapoptotic effects of the combination of cytotoxic drugs and enzastaurin, a protein kinase Cbeta inhibitor, in non-small cell lung cancer cells. Mol Cancer Ther. 2008;7(6):1698-707.
29. Castro MA, Schwartsmann G, Moreira JC. Intercellular contact-dependent survival of human A549, NCI-H596 and NCI-H520 non-small cell lung carcinoma cell lines. Braz J Med Biol Res. 2001;34(8):1007-13.
30. Dimanche-Boitrel MT, Micheau O, Hammann A, Haugg M, Eymin B, Chauffert B, et al. Contribution of the cyclin-dependent kinase inhibitor p27KIP1 to the confluence-dependent resistance of HT29 human colon carcinoma cells. Int J Cancer. 1998;77(5):796-802.
31. Zhang Y, Tao L, Fan L, Peng Y, Yang K, Zhao Y, et al. Different gap junction-propagated effects on cisplatin transfer result in opposite responses to cisplatin in normal cells versus tumor cells. Sci Rep. 2015;5:12563.
32. 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(26):3148-63.
33. Yang TY, Chang GC, Chen KC, Hung HW, Hsu KH, Wu CH, et al. Pemetrexed induces both intrinsic and extrinsic apoptosis through ataxia telangiectasia mutated/p53-dependent and -independent signaling pathways. Mol Carcinog. 2013;52(3):183-94.
34. Shah MA, Schwartz GK. Cell cycle-mediated drug resistance: an emerging concept in cancer therapy. Clin Cancer Res Off J Am Assoc Cancer Res. 2001;7(8):2168-81.
35. Yang TY, Chang GC, Chen KC, Hung HW, Hsu KH, Sheu GT, et al. Sustained activation of ERK and Cdk2/cyclin-A signaling pathway by pemetrexed leading to S-phase arrest and apoptosis in human non-small cell lung cancer A549 cells. Eur J Pharmacol. 2011;663(1-3):17-26.
36. Donaldson KL, Goolsby GL, Wahl AF. Cytotoxicity of the anticancer agents cisplatin and taxol during cell proliferation and the cell cycle. Int J Cancer. 1994;57(6):847-55.
37. Choma D, Daures JP, Quantin X, Pujol JL. Aneuploidy and prognosis of non-small-cell lung cancer: a meta-analysis of published data. Br J Cancer. 2001;85(1):14-22.
38. Takeshita M, Koga T, Takayama K, Ijichi K, Yano T, Maehara Y, et al. Aurora-B overexpression is correlated with aneuploidy and poor prognosis in non-small cell lung cancer. Lung Cancer. 2013;80(1):85-90.
39. Lin ZP, Lee Y, Lin F, Belcourt MF, Li P, Cory JG, et al. Reduced level of ribonucleotide reductase R2 subunits increases dependence on homologous recombination repair of cisplatin-induced DNA damage. Mol Pharmacol. 2011;80(6):1000-12.
40. Kunz C, Focke F, Saito Y, Schuermann D, Lettieri T, Selfridge J, et al. Base excision by thymine DNA glycosylase mediates DNA-directed cytotoxicity of 5-fluorouracil. PLoS Biol. 2009;7(4):e91.
41. Olive PL, Banath JP. Kinetics of H2AX phosphorylation after exposure to cisplatin. Cytometry B Clin Cytom. 2009;76(2):79-90.
42. Zakaria N, Yusoff NM, Zakaria Z, Lim MN, Baharuddin PJ, Fakiruddin KS, et al. Human non-small cell lung cancer expresses putative cancer stem cell markers and exhibits the transcriptomic profile of multipotent cells. BMC Cancer. 2015;15:84.
43. Barr MP, Gray SG, Hoffmann AC, Hilger RA, Thomale J, O'Flaherty JD, et al. Generation and characterisation of cisplatin-resistant non-small cell lung cancer cell lines displaying a stem-like signature. PLoS One. 2013;8(1):e54193.
44. Sampson VB, David JM, Puig I, Patil PU, de Herreros AG, Thomas GV, et al. Wilms' tumor protein induces an epithelial-mesenchymal hybrid differentiation state in clear cell renal cell carcinoma. PLoS One. 2014;9(7):e102041.
45. Brabletz T. To differentiate or not--routes towards metastasis. Nat Rev Cancer. 2012;12(6):425-36.
46. Schliekelman MJ, Taguchi A, Zhu J, Dai X, Rodriguez J, Celiktas M, et al. Molecular portraits of epithelial, mesenchymal, and hybrid States in lung adenocarcinoma and their relevance to survival. Cancer Res. 2015;75(9):1789-800.
47. Lu M, Jolly MK, Levine H, Onuchic JN, Ben-Jacob E. MicroRNA-based regulation of epithelial-hybrid-mesenchymal fate determination. Proc Natl Acad Sci U S A. 2013;110(45):18144-9.
48. Li XJ, Ren ZJ, Tang JH. MicroRNA-34a: a potential therapeutic target in human cancer. Cell Death Dis. 2014;5:e1327.
49. Chen Z, Fillmore CM, Hammerman PS, Kim CF, Wong KK. Non-small-cell lung cancers: a heterogeneous set of diseases. Nat Rev Cancer. 2014;14(8):535-46.
50. Chattopadhyay S, Moran RG, Goldman ID. Pemetrexed: biochemical and cellular pharmacology, mechanisms, and clinical applications. Mol Cancer Ther. 2007;6(2):404-17.