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Research Article

Apigenin Enhanced Antitumor Effect of Cisplatin in Lung Cancer via Inhibition of Cancer Stem Cells

, , , , , , , , & show all
Pages 1489-1497 | Received 21 May 2020, Accepted 21 Jul 2020, Published online: 06 Aug 2020

References

  • Chen W, Zheng R, Zeng H, Zhang S. Epidemiology of lung cancer in China. Thorac Cancer. 2015;6(2):209–15. doi:10.1111/1759-7714.12169
  • Herbst RS, Morgensztern D, Boshoff C. The biology and management of non-small cell lung cancer. Nature. 2018;553(7689):446–54. doi:10.1038/nature25183
  • Pignon J-P, Tribodet H, Scagliotti GV, Douillard J-Y, Shepherd FA, Stephens RJ, Dunant A, Torri V, Rosell R, Seymour L, et al. Lung adjuvant cisplatin evaluation: a pooled analysis by the LACE Collaborative Group. J Clin Oncol. 2008;26(21):3552–9. doi:10.1200/JCO.2007.13.9030
  • Koberle B, Tomicic MT, Usanova S, Kaina B. Cisplatin resistance: preclinical findings and clinical implications. Biochim Biophys Acta. 2010;1806(2):172–82. doi:10.1016/j.bbcan.2010.07.004
  • Galluzzi L, Senovilla L, Vitale I, Michels J, Martins I, Kepp O, Castedo M, Kroemer G. Molecular mechanisms of cisplatin resistance. Oncogene. 2012;31(15):1869–83. doi:10.1038/onc.2011.384
  • Ferreira JA, Peixoto A, Neves M, Gaiteiro C, Reis CA, Assaraf YG, Santos LL. Mechanisms of cisplatin resistance and targeting of cancer stem cells: adding glycosylation to the equation. Drug Resist Updates. 2016;24:34–54. doi:10.1016/j.drup.2015.11.003
  • Vinogradov S, Wei X. Cancer stem cells and drug resistance: the potential of nanomedicine. Nanomedicine . 2012;7(4):597–615. doi:10.2217/nnm.12.22
  • Schatton T, Frank NY, Frank MH. Identification and targeting of cancer stem cells. Bioessays. 2009;31(10):1038–49. doi:10.1002/bies.200900058
  • Liu Y-P, Yang C-J, Huang M-S, Yeh C-T, Wu ATH, Lee Y-C, Lai T-C, Lee C-H, Hsiao Y-W, Lu J, et al. Cisplatin selects for multidrug-resistant CD133+ cells in lung adenocarcinoma by activating Notch signaling. Cancer Res. 2013;73(1):406–16. doi:10.1158/0008-5472.CAN-12-1733
  • Ahmed EM, Bandopadhyay G, Coyle B, Grabowska A. A HIF-independent, CD133-mediated mechanism of cisplatin resistance in glioblastoma cells. Cell Oncol (Dordr). 2018;41(3):319–28. doi:10.1007/s13402-018-0374-8
  • Li Y, Yang B, Bai J-Y, Xia S, Mao M, Li X, Li N, Chen L. The roles of synovial hyperplasia, angiogenesis and osteoclastogenesis in the protective effect of apigenin on collagen-induced arthritis. Int Immunopharmacol. 2019;73:362–9. doi:10.1016/j.intimp.2019.05.024
  • Hwang YP, Oh KN, Yun HJ, Jeong HG. The flavonoids apigenin and luteolin suppress ultraviolet A-induced matrix metalloproteinase-1 expression via MAPKs and AP-1-dependent signaling in HaCaT cells. J Dermatol Sci. 2011;61(1):23–31. doi:10.1016/j.jdermsci.2010.10.016
  • Mirzoeva S, Kim ND, Chiu K, Franzen CA, Bergan RC, Pelling JC. Inhibition of HIF-1 alpha and VEGF expression by the chemopreventive bioflavonoid apigenin is accompanied by Akt inhibition in human prostate carcinoma PC3-M cells. Mol Carcinog. 2008;47(9):686–700. doi:10.1002/mc.20421
  • Lindenmeyer F, Li H, Menashi S, Soria C, Lu H. Apigenin acts on the tumor cell invasion process and regulates protease production. Nutr Cancer. 2001;39(1):139–47. doi:10.1207/S15327914nc391_19
  • Li Y-W, Xu J, Zhu G-Y, Huang Z-J, Lu Y, Li X-Q, Wang N, Zhang F-X. Apigenin suppresses the stem cell-like properties of triple-negative breast cancer cells by inhibiting YAP/TAZ activity. Cell Death Discov. 2018;4:105. doi:10.1038/s41420-018-0124-8
  • Ketkaew Y, Osathanon T, Pavasant P, Sooampon S. Apigenin inhibited hypoxia induced stem cell marker expression in a head and neck squamous cell carcinoma cell line. Arch Oral Biol. 2017;74:69–74. doi:10.1016/j.archoralbio.2016.11.010
  • Lu H-F, Chie Y-J, Yang M-S, Lu K-W, Fu J-J, Yang J-S, Chen H-Y, Hsia T-C, Ma C-Y, Ip S-W, et al. Apigenin induces apoptosis in human lung cancer H460 cells through caspase- and mitochondria-dependent pathways. Hum Exp Toxicol. 2011;30(8):1053–61. doi:10.1177/0960327110386258
  • Liu R, Ji P, Liu B, Qiao H, Wang X, Zhou L, Deng T, Ba Y. Apigenin enhances the cisplatin cytotoxic effect through p53-modulated apoptosis. Oncol Lett. 2017;13(2):1024–30. doi:10.3892/ol.2016.5495
  • Barr MP, Gray SG, Hoffmann AC, Hilger RA, Thomale J, O'Flaherty JD, Fennell DA, Richard D, O'Leary JJ, O'Byrne KJ, 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. doi:10.1371/journal.pone.0054193
  • Liu B, Yang P, Ye Y, Zhou Y, Li L, Tashiro S-I, Onodera S, Ikejima T. Role of ROS in the protective effect of silibinin on sodium nitroprusside-induced apoptosis in rat pheochromocytoma PC12 cells. Free Radic Res. 2011;45(7):835–47. doi:10.3109/10715762.2011.580343
  • Park EK, Lee JC, Park JW, Bang SY, Yi SA, Kim BK, Park JH, Kwon SH, You JS, Nam SW, et al. Transcriptional repression of cancer stem cell marker CD133 by tumor suppressor p53. Cell Death Dis. 2015;6:e1964. doi:10.1038/cddis.2015.313
  • Schuler M, Green DR. Mechanisms of p53-dependent apoptosis. Biochem Soc Trans. 2001;29(Pt 6):684–8. doi:10.1042/0300-5127:0290684
  • Shukla S, Bhaskaran N, Babcook MA, Fu P, MacLennan GT, Gupta S. Apigenin inhibits prostate cancer progression in TRAMP mice via targeting PI3K/Akt/FoxO pathway. Carcinogenesis. 2014;35(2):452–60. doi:10.1093/carcin/bgt316
  • Masuelli L, Benvenuto M, Mattera R, Di Stefano E, Zago E, Taffera G, Tresoldi I, Giganti MG, Frajese GV, Berardi G, et al. In vitro and in vivo anti-tumoral effects of the flavonoid apigenin in malignant mesothelioma. Front Pharmacol. 2017;8:373 doi:10.3389/fphar.2017.00373
  • Guntur VP, Waldrep JC, Guo JJ, Selting K, Dhand R. Increasing p53 protein sensitizes non-small cell lung cancer to paclitaxel and cisplatin in vitro. Anticancer Res. 2010;30:3557–64.
  • Shang L, Wei M. Inhibition of SMYD2 sensitized cisplatin to resistant cells in NSCLC through activating p53 pathway. Front Oncol. 2019;9:306. doi:10.3389/fonc.2019.00306
  • Ouyang DY, Wang YY, Zheng YT. Activation of c-Jun N-terminal kinases by ribotoxic stresses. Cell Mol Immunol. 2005;2(6):419–25.
  • Dhanasekaran DN, Reddy EP. JNK signaling in apoptosis. Oncogene. 2008;27(48):6245–51. doi:10.1038/onc.2008.301
  • Chen M, Wang X, Zha D, Cai F, Zhang W, He Y, Huang Q, Zhuang H, Hua Z-C. Apigenin potentiates TRAIL therapy of non-small cell lung cancer via upregulating DR4/DR5 expression in a p53-dependent manner. Sci Rep. 2016;6(1):35468. doi:10.1038/srep35468
  • Kroemer G, Levine B. Autophagic cell death: the story of a misnomer. Nat Rev Mol Cell Biol. 2008;9(12):1004–10. doi:10.1038/nrm2529
  • Cao X, Liu B, Cao W, Zhang W, Zhang F, Zhao H, Meng R, Zhang L, Niu R, Hao X, et al. Autophagy inhibition enhances apigenin-induced apoptosis in human breast cancer cells. Chin J Cancer Res. 2013;25(2):212–22. doi:10.3978/j.issn.1000-9604.2013.04.01
  • Hao C, Liu G, Tian G. Autophagy inhibition of cancer stem cells promotes the efficacy of cisplatin against non-small cell lung carcinoma. Ther Adv Respir Dis. 2019;13:1753466619866097. doi:10.1177/1753466619866097
  • Jerry DJ, Tao L, Yan H. Regulation of cancer stem cells by p53. Breast Cancer Res. 2008;10(4):304. doi:10.1186/bcr2133
  • Deshmukh A, Deshpande K, Arfuso F, Newsholme P, Dharmarajan A. Cancer stem cell metabolism: a potential target for cancer therapy. Mol Cancer. 2016;15(1):69. doi:10.1186/s12943-016-0555-x
  • Phi LTH, Sari IN, Yang Y-G, Lee S-H, Jun N, Kim KS, Lee YK, Kwon HY. Cancer stem cells (CSCs) in drug resistance and their therapeutic implications in cancer treatment. Stem Cells Int. 2018;2018:5416923. doi:10.1155/2018/5416923
  • Riley T, Sontag E, Chen P, Levine A. Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol. 2008;9(5):402–12. doi:10.1038/nrm2395
  • Godar S, Ince TA, Bell GW, Feldser D, Donaher JL, Bergh J, Liu A, Miu K, Watnick RS, Reinhardt F, et al. Growth-inhibitory and tumor-suppressive functions of p53 depend on its repression of CD44 expression. Cell. 2008;134(1):62–73. doi:10.1016/j.cell.2008.06.006
  • Wang Z, Oron E, Nelson B, Razis S, Ivanova N. Distinct lineage specification roles for NANOG, OCT4, and SOX2 in human embryonic stem cells. Cell Stem Cell. 2012;10(4):440–54. doi:10.1016/j.stem.2012.02.016
  • Liu A, Yu X, Liu S. Pluripotency transcription factors and cancer stem cells: small genes make a big difference. Chin J Cancer. 2013;32(9):483–7. doi:10.5732/cjc.012.10282
  • Song W-S, Yang Y-P, Huang C-S, Lu K-H, Liu W-H, Wu W-W, Lee Y-Y, Lo W-L, Lee S-D, Chen Y-W, et al. Sox2, a stemness gene, regulates tumor-initiating and drug-resistant properties in CD133-positive glioblastoma stem cells. J Chin Med Assoc. 2016;79(10):538–45. doi:10.1016/j.jcma.2016.03.010
  • Chen B, Zhu Z, Li L, Ye W, Zeng J, Gao J, Wang S, Zhang L, Huang Z. Effect of overexpression of Oct4 and Sox2 genes on the biological and oncological characteristics of gastric cancer cells. Onco Targets Ther. 2019;12:4667–82. doi:10.2147/OTT.S209734

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