Paclitaxel and the dietary flavonoid fisetin: A synergistic combination that induces mitotic catastrophe and autophagic cell death in A549 non-small cell lung cancer cells

Cancer Cell International

Volumn 16, Issue 1, 2016, Pages

  Klimaszewska Wisniewska, Anna ^a   Halas Wisniewska, Marta ^a   Tadrowski, Tadeusz ^a   Gagat, Maciej ^a   Grzanka, Dariusz ^a   Grzanka, Alina ^a  

^a NICOLAUS COPERNICUS UNIVERSITY   (Poland)

Author keywords

Autophagy; Combination therapy; Fisetin; Lung cancer; Mitotic catastrophe; Paclitaxel

Indexed keywords

ARSENIC TRIOXIDE; CASPASE 3; FISETIN; MESSENGER RNA; METHOTREXATE; MITOXANTRONE; PACLITAXEL; PROTEIN BAX; PROTEIN BCL 2;

A549 CELL LINE; ANTINEOPLASTIC ACTIVITY; ARTICLE; AUTOPHAGY; BAX GENE; BCL 2 GENE; CASPASE 3 GENE; CELL CYCLE PROGRESSION; CELL VACUOLE; CELL VIABILITY; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENTIATION; HUMAN; HUMAN CELL; LC3 II GENE; MITOSIS SPINDLE; NON SMALL CELL LUNG CANCER; TUMOR GENE;

EID: 84957977297     PISSN: None     EISSN: 14752867     Source Type: Journal    
DOI: 10.1186/s12935-016-0288-3     Document Type: Article

References (82)

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics 2014. CA Cancer J Clin. 2014;64:9-29.
2. Breathnach OS, Freidlin B, Conley B, Green MR, Johnson DH, Gandara DR, et al. Twenty-two years of phase III trials for patients with advanced non-small-cell lung cancer: sobering results. J Clin Oncol. 2001;19:1734-42.
3. Khan N, Afaq F, Khusro FH, Mustafa Adhami V, Suh Y, Mukhtar H. Dual inhibition of phosphatidylinositol 3-kinase/Akt and mammalian target of rapamycin signaling in human nonsmall cell lung cancer cells by a dietary flavonoid fisetin. Int J Cancer. 2012;130:1695-705.
4. Pan XH, Liu DS, Wang J, Zhang XL, Yan MM, Zhang DH, et al. Peneciraistin C induces caspase-independent autophagic cell death through mitochondrial-derived reactive oxygen species production in lung cancer cells. Cancer Sci. 2013;104:1476-82.
5. Hu L, Liang G, Yuliang W, Bingjing Z, Xiangdong Z, Rufu X. Assessing the effectiveness and safety of liposomal paclitaxel in combination with cisplatin as first-line chemotherapy for patients with advanced NSCLC with regional lymph-node metastasis: study protocol for a randomized controlled trial (PLC-GC trial). Trials. 2013;14:45-51.
6. Socinski MA. Single-agent paclitaxel in the treatment of advanced non-small cell lung cancer. Oncologist. 1999;4:408-16.
7. Chen Z, Zhang X, Li MF, Wang ZQ, Wieand HS, Grandis JR, et al. Simultaneously targeting epidermal growth factor receptor tyrosine kinase and cyclooxygenase-2, an efficient approach to inhibition of squamous cell carcinoma of the head and neck. Clin Cancer Res. 2004;10:5930-9.
8. Lim SJ, Choi MK, Kim MJ, Kim JK. Alpha-Tocopheryl succinate potentiates the paclitaxel-induced apoptosis through enforced caspase 8 activation in human H460 lung cancer cells. Exp Mol Med. 2009;41:737-45.
9. Sak K. Chemotherapy and dietary phytochemical agents. Chemother Res Pract. 2012;2012:282570.
10. Surh YJ. Cancer chemoprevention with dietary phytochemicals. Nat Rev Cancer. 2003;3:768-80.
11. Garg AK, Buchholz TA, Aggarwal BB. Chemosensitization and radiosensitization of tumors by plant polyphenols. Antioxid Redox Signal. 2005;7:1630-47.
12. Kuno T, Tsukamoto T, Hara A, Tanaka T. Cancer chemoprevention through the induction of apoptosis by natural compounds. J Biophys Chem. 2012;3:156-73.
13. Khan N, Afaq F, Syed DN, Mukhtar H. Fisetin, a novel dietary flavonoid, causes apoptosis and cell cycle arrest in human prostate cancer LNCaP cells. Carcinogenesis. 2008;29:1049-56.
14. Haddad AQ, Venkateswaran V, Viswanathan L, Teahan SJ, Fleshner NE, Klotz LH. Novel antiproliferative flavonoids induce cell cycle arrest in human prostate cancer cell lines. Prostate Cancer Prostat Dis. 2006;9:68-76.
15. Syed DN, Adhami VM, Khan MI, Mukhtar H. Inhibition of Akt/mTOR signaling by the dietary flavonoid fisetin. Anticancer Agents Med Chem. 2013;13:995-1001.
16. Touil YS, Fellous A, Scherman D, Chabot GG. Flavonoid-induced morphological modifications of endothelial cells through microtubule stabilization. Nutr Cancer. 2009;61:310-21.
17. Yang PM, Tseng HH, Peng CW, Chen WS, Chiu SJ. Dietary flavonoid fisetin targets caspase-3-deficient human breast cancer MCF-7 cells by induction of caspase-7-associated apoptosis and inhibition of autophagy. Int J Oncol. 2012;40:469-78.
18. Lee WR, Shen SC, Lin HY, Hou WC, Yang LL, Chen YC. Wogonin and fisetin induce apoptosis in human promyeloleukemic cells, accompanied by a decrease of reactive oxygen species, and activation of caspase 3 and Ca2+-dependent endonuclease. Biochem Pharmacol. 2002;63:225-36.
19. Chou TC, Talalay P. Quantitative-analysis of dose-effect relationships-the combined effects of multiple-drugs or enzyme-inhibitors. Adv Enzyme Regul. 1984;22:27-55.
20. Chou TC, Martin N. CompuSyn software for drug combinations and for general dose effect analysis, and user's guide. Paramus: ComboSyn Inc; 2007.
21. Chou TC. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev. 2006;58:621-81.
22. Traganos F, Darzynkiewicz Z. Lysosomal proton pump activity-aupravital cell staining with acridine-orange differentiates leukocyte subpopulations. Methods Cell Biol. 1994;41:185-94.
23. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods. 2001;25:402-8.
24. Shia CS, Tsai SY, Kuo SC, Hou YC, Chao PD. Metabolism and pharmacokinetics of 3,3',4',7-tetrahydroxyflavone (fisetin), 5-hydroxyflavone, and 7-hydroxyflavone and antihemolysis effects of fisetin and its serum metabolites. J Agric Food Chem. 2009;57:83-9.
25. Andre N, Braguer D, Brasseur G, Goncalves A, Lemesle-Meunier D, Guise S, et al. Paclitaxel induces release of cytochrome c from mitochondria isolated from human neuroblastoma cells. Cancer Res. 2000;60:5349-53.
26. Ferlini C, Raspaglio G, Mozzetti S, Distefano M, Filippetti F, Martinelli E, et al. Bcl-2 down-regulation is a novel mechanism of paclitaxel resistance. Mol Pharmacol. 2003;64:51-8.
27. Alexandre J, Batteux F, Nicco C, Chereau C, Laurent A, Guillevin L, et al. Accumulation of hydrogen peroxide is an early and crucial step for paclitaxel-induced cancer cell death both in vitro and in vivo. Int J Cancer. 2006;119:41-8.
28. Odonkor CA, Achilefu S. Differential activity of caspase-3 regulates susceptibility of lung and breast tumor cell lines to Paclitaxel. Open Biochem J. 2008;2:121-8.
29. You J, Li X, de Cui F, Du YZ, Yuan H, Hu FQ. Folate-conjugated polymer micelles for active targeting to cancer cells: preparation, in vitro evaluation of targeting ability and cytotoxicity. Nanotechnology. 2008;19:045102.
30. Zhang D, Qiu L, Jin X, Guo Z, Guo C. Nuclear factor-kappa B inhibition by parthenolide potentiates the efficacy of taxol in non-small cell lung cancer in vitro and in vivo. Mol Cancer Res. 2009;7:1139-49.
31. Korsmeyer SJ, Shutter JR, Veis DJ, Merry DE, Oltvai ZN. Bcl-2/Bax: a rheostat that regulates an anti-oxidant pathway and cell death. Semin Cancer Biol. 1993;4:327-32.
32. Saxena A, Viswanathan S, Moshynska O, Tandon P, Sankaran K, Sheridan DP. Mcl-1 and Bcl-2/Bax ratio are associated with treatment response but not with Rai stage in B-cell chronic lymphocytic leukemia. Am J Hematol. 2004;75:22-33.
33. Blajeski AL, Kottke TJ, Kaufmann SH. A multistep model for paclitaxel-induced apoptosis in human breast cancer cell lines. Exp Cell Res. 2001;270:277-88.
34. Jordan MA, Toso RJ, Thrower D, Wilson L. Mechanism of mitotic block and inhibition of cell-proliferation by taxol at low concentrations. Proc Natl Acad Sci USA. 1993;90:9552-6.
35. Abal M, Andreu JM, Barasoain I. Taxanes: microtubule and centrosome targets, and cell cycle dependent mechanisms of action. Curr Cancer Drug Targets. 2003;3:193-203.
36. Barth S, Glick D, Macleod KF. Autophagy: assays and artifacts. J Pathol. 2010;221:117-24.
37. Tripathi R, Samadder T, Gupta S, Surolia A, Shaha C. Anticancer activity of a combination of cisplatin and fisetin in embryonal carcinoma cells and xenograft tumors. Mol Cancer Ther. 2011;10:255-68.
38. Paglin S, Hollister T, Delohery T, Hackett N, McMahill M, Sphicas E, et al. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res. 2001;61:439-44.
39. Yamamoto A, Tagawa Y, Yoshimori T, Moriyama Y, Masaki R, Tashiro Y. Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct. 1998;23:33-42.
40. Kar R, Singha PK, Venkatachalam MA, Saikumar P. A novel role for MAP1 LC3 in nonautophagic cytoplasmic vacuolation death of cancer cells. Oncogene. 2009;28:2556-68.
41. Kanzawa T, Germano IM, Komata T, Ito H, Kondo Y, Kondo S. Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ. 2004;11:448-57.
42. Jäger S, Bucci C, Tanida I, Ueno T, Kominami E, Saftig P, et al. Role for Rab7 in maturation of late autophagic vacuoles. J Cell Sci. 2004;117:4837-48.
43. Wirawan E, Vanden Berghe T, Lippens S, Agostinis P, Vandenabeele P. Autophagy: for better or for worse. Cell Res. 2012;22:43-61.
44. Eskelinen EL. The dual role of autophagy in cancer. Curr Opin Pharmacol. 2011;11:294-300.
45. Xi G, Hu X, Wu B, Jiang H, Young CY, Pang Y, et al. Autophagy inhibition promotes paclitaxel-induced apoptosis in cancer cells. Cancer Lett. 2011;307:141-8.
46. Chou TC. Preclinical versus clinical drug combination studies. Leuk Lymphoma. 2008;49:2059-80.
47. Smith MA, Houghton P. A proposal regarding reporting of in vitro testing results. Clin Cancer Res. 2013;19:2828-33.
48. Ehninger G, Proksch B, Heinzel G, Woodward DL. Clinical-pharmacology of mitoxantrone. Cancer Treat Rep. 1986;70:1373-8.
49. Jonnalagadda M, Brown CE, Chang WC, Ostberg JR, Forman SJ, Jensen MC. Efficient selection of genetically modified human T cells using methotrexate-resistant human dihydrofolate reductase. Gene Ther. 2013;20:853-60.
50. Shen ZX, Chen GQ, Ni JH, Li XS, Xiong SM, Qiu QY, et al. Use of arsenic trioxide (As2O3) in the treatment of acute promyelocytic leukemia (APL): II. Clinical efficacy and pharmacokinetics in relapsed patients. Blood. 1997;89:3354-60.
51. Liao YC, Shih YW, Chao CH, Lee XY, Chiang TA. Involvement of the ERK signaling pathway in fisetin reduces invasion and migration in the human lung cancer cell line A549. J Agric Food Chem. 2009;57:8933-41.
52. Sung B, Pandey MK, Aggarwal BB. Fisetin, an inhibitor of cyclin-dependent kinase 6, down-regulates nuclear factor-kappa B-regulated cell proliferation, antiapoptotic and metastatic gene products through the suppression of TAK-1 and receptor-interacting protein-regulated I kappa B alpha kinase activation. Mol Pharmacol. 2007;71:1703-14.
53. Touil YS, Seguin J, Scherman D, Chabot GG. Improved antiangiogenic and antitumour activity of the combination of the natural flavonoid fisetin and cyclophosphamide in Lewis lung carcinoma-bearing mice. Cancer Chemother Pharmacol. 2011;68:445-55.
54. Karna P, Zughaier S, Pannu V, Simmons R, Narayan S, Aneja R. Induction of reactive oxygen species-mediated autophagy by a novel microtubule-modulating agent. J Biol Chem. 2010;285:18737-48.
55. Demidenko ZN, Kalurupalle S, Hanko C, Lim CU, Broude E, Blagosklonny MV. Mechanism of G1-like arrest by low concentrations of paclitaxel: next cell cycle p53-dependent arrest with sub G1 DNA content mediated by prolonged mitosis. Oncogene. 2008;27:4402-10.
56. Karna P, Rida PC, Pannu V, Gupta KK, Dalton WB, Joshi H, et al. A novel microtubule-modulating noscapinoid triggers apoptosis by inducing spindle multipolarity via centrosome amplification and declustering. Cell Death Differ. 2011;18:632-44.
57. Ikui AE, Yang CP, Matsumoto T, Horwitz SB. Low concentrations of taxol cause mitotic delay followed by premature dissociation of p55CDC from mad2 and BubR1 and abrogation of the spindle checkpoint, leading to aneuploidy. Cell Cycle. 2005;4:1385-8.
58. Zhu J, Beattie EC, Yang Y, Wang HJ, Seo JY, Yang LX. Centrosome impairments and consequent cytokinesis defects are possible mechanisms of taxane drugs. Anticancer Res. 2005;25:1919-25.
59. Chen JG, Horwitz SB. Differential mitotic responses to microtubule-stabilizing and -destabilizing drugs. Cancer Res. 2002;62:1935-8.
60. Morse DL, Gray H, Payne CM, Gillies RJ. Docetaxel induces cell death through mitotic catastrophe in human breast cancer cells. Mol Cancer Ther. 2005;4:1495-504.
61. Vakifahmetoglu H, Olsson M, Zhivotovsky B. Death through a tragedy: mitotic catastrophe. Cell Death Differ. 2008;15:1153-62.
62. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV, et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ. 2012;19:107-20.
63. Portugal J, Mansilla S, Bataller M. Mechanisms of drug-induced mitotic catastrophe in cancer cells. Curr Pharm Des. 2010;16:69-78.
64. Jordan MA, Wilson L. Microtubules as a target for anticancer drugs. Nat Rev Cancer. 2004;4:253-65.
65. Diaz-Martinez LA, Karamysheva ZN, Warrington R, Li B, Wei S, Xie XJ, et al. Genome-wide siRNA screen reveals coupling between mitotic apoptosis and adaptation. EMBO J. 2014;33:1960-76.
66. Castedo M, Perfettini JL, Roumie T, Andreau K, Medema R, Kroemer G. Cell death by mitotic catastrophe: a molecular definition. Oncogene. 2004;23:2825-37.
67. Vogel C, Kienitz A, Hofmann I, Muller R, Bastians H. Crosstalk of the mitotic spindle assembly checkpoint with p53 to prevent polyploidy. Oncogene. 2004;23:6845-53.
68. Salmela AL, Pouwels J, Varis A, Kukkonen AM, Toivonen P, Halonen PK, et al. Dietary flavonoid fisetin induces a forced exit from mitosis by targeting the mitotic spindle checkpoint. Carcinogenesis. 2009;30:1032-40.
69. Kuwahara Y, Oikawa T, Ochiai Y, Roudkenar MH, Fukumoto M, Shimura T, et al. Enhancement of autophagy is a potential modality for tumors refractory to radiotherapy. Cell Death Dis. 2011;2:177.
70. Reyjal J, Cormier K, Turcotte S. Autophagy and cell death to target cancer cells: exploiting synthetic lethality as cancer therapies. Adv Exp Med Biol. 2014;772:167-88.
71. Sui X, Chen R, Wang Z, Huang Z, Kong N, Zhang M, et al. Autophagy and chemotherapy resistance: a promising therapeutic target for cancer treatment. Cell Death Dis. 2013;4:838.
72. Janji B, Viry E, Baginska J, Van Moer K, Berchem G. Role of autophagy in cancer and tumor progression. In: Bailly Y, editor. Autophagy-a double-edged sword-cell survival or death. Croatia: InTech; 2013. p. 141-161.
73. Zhang Q, Si S, Schoen S, Chen J, Jin XB, Wu G. Suppression of autophagy enhances preferential toxicity of paclitaxel to folliculin-deficient renal cancer cells. J Exp Clin Cancer Res. 2013;32:99.
74. Suh Y, Afaq F, Khan N, Johnson JJ, Khusro FH, Mukhtar H. Fisetin induces autophagic cell death through suppression of mTOR signaling pathway in prostate cancer cells. Carcinogenesis. 2010;31:1424-33.
75. Gewirtz DA. An autophagic switch in the response of tumor cells to radiation and chemotherapy. Biochem Pharmacol. 2014;90:208-11.
76. Shen HM, Codogno P. Autophagic cell death Loch Ness monster or endangered species? Autophagy. 2011;7:457-65.
77. Wilson EN, Bristol ML, Di X, Maltese WA, Koterba K, Beckman MJ, et al. A switch between cytoprotective and cytotoxic autophagy in the radiosensitization of breast tumor cells by chloroquine and vitamin D. Horm Cancer. 2011;2:272-85.
78. Sharma K, Goehe RW, Di X, Hicks MA, Torti SV, Torti FM, et al. A novel cytostatic form of autophagy in sensitization of non-small cell lung cancer cells to radiation by vitamin D and the vitamin D analog, EB 1089. Autophagy. 2014;10:2346-61.
79. Kumar S, Kumar A, Pathania AS, Guru SK, Jada S, Sharma PR, et al. Tiron and trolox potentiate the autophagic cell death induced by magnolol analog Ery5 by activation of Bax in HL-60 cells. Apoptosis. 2013;18:605-17.
80. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol. 2007;8:741-52.
81. Gozuacik D, Kimchi A. Autophagy as a cell death and tumor suppressor mechanism. Oncogene. 2004;23:2891-906.
82. Liu WT, Huang CY, Lu IC, Gean PW. Inhibition of glioma growth by minocycline is mediated through endoplasmic reticulum stress-induced apoptosis and autophagic cell death. Neuro Oncol. 2013;15:1127-41.