Fisetin inhibits cellular proliferation and induces mitochondria-dependent apoptosis in human gastric cancer cells

Molecular Carcinogenesis

Volumn 56, Issue 2, 2017, Pages 499-514

  Sabarwal, Akash ^a   Agarwal, Rajesh ^b   Singh, Rana P ^a,c  

^a CENTRAL UNIVERSITY OF GUJARAT   (India)

^b UNIVERSITY OF COLORADO   (United States)

^c JAWAHARLAL NEHRU UNIVERSITY   (India)

Author keywords

apoptosis; fisetin; gastric cancer; mitochondrial respiratory chain complex I; ROS

Indexed keywords

ACETYLCYSTEINE; CYCLIN DEPENDENT KINASE; CYCLINE; FISETIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NITRITE; PROTEIN P53; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; ANTINEOPLASTIC AGENT; FLAVONOID;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; APOPTOSIS ASSAY; ARTICLE; CANCER INHIBITION; CELL CYCLE G1 PHASE; CELL GROWTH; CELL MEMBRANE DEPOLARIZATION; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA DAMAGE; DRUG MECHANISM; FLOW CYTOMETRY; GASTRIC CANCER CELL LINE; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RESPIRATORY CHAIN; CELL CYCLE CHECKPOINT; DRUG EFFECTS; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; PATHOLOGY; STOMACH; STOMACH NEOPLASMS; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL PROLIFERATION; FLAVONOIDS; HUMANS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; REACTIVE OXYGEN SPECIES; STOMACH; STOMACH NEOPLASMS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84977525069     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.22512     Document Type: Article

References (47)

1. Ferlay J, Soerjomataram I, Dikshit R, et al. Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 2015; 136:E359–E386.
2. Bertuccio P, Chatenoud L, Levi F, et al. Recent patterns in gastric cancer: A global overview. Int J Cancer 2009; 125:666–673.
3. Delaunoit T. Latest developments and emerging treatment options in the management of stomach cancer. Cancer Manag Res 2011; 3:257–266.
4. Tyagi A, Agarwal C, Harrison G, Glode LM, Agarwal R. Silibinin causes cell cycle arrest and apoptosis in human bladder transitional cell carcinoma cells by regulating CDKI-CDK-cyclin cascade, and caspase 3 and PARP cleavages. Carcinogenesis 2004; 25:1711–1720.
5. Singh RP, Dhanalakshmi S, Agarwal C, Agarwal R. Silibinin strongly inhibits growth and survival of human endothelial cells via cell cycle arrest and downregulation of survivin, Akt and NF-kappaB: Implications for angioprevention and antiangiogenic therapy. Oncogene 2005; 24:1188–1202.
6. Xiao D, Powolny AA, Singh SV. Benzyl isothiocyanate targets mitochondrial respiratory chain to trigger reactive oxygen species-dependent apoptosis in human breast cancer cells. J Biol Chem 2008; 283:30151–30163.
7. Cao J, Jia L, Zhou HM, Liu Y, Zhong LF. Mitochondrial and nuclear DNA damage induced by curcumin in human hepatoma G2 cells. Toxicol Sci 2006; 91:476–483.
8. Sakao K, Singh SV. D,L-sulforaphane-induced apoptosis in human breast cancer cells is regulated by the adapter protein p66Shc. J Cell Biochem 2012; 113:599–610.
9. Alexandre J, Batteux F, Nicco C, 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; 119:41–48.
10. Bickers DR, Athar M. Oxidative stress in the pathogenesis of skin disease. J Invest Dermatol 2006; 126:2565–2575.
11. Tsugane S, Sasazuki S. Diet and the risk of gastric cancer: Review of epidemiological evidence. Gastric Cancer 2007; 10:75–83.
12. Cohen JH, Kristal AR, Stanford JL. Fruit and vegetable intakes and prostate cancer risk. J Natl Cancer Inst 2000; 92:61–68.
13. Li Y, Fang H, Xu W. Recent advance in the research of flavonoids as anticancer agents. Mini Rev Med Chem 2007; 7:663–678.
14. Kimira M, Arai Y, Shimoi K, Watanabe S. Japanese intake of flavonoids and isoflavonoids from foods. J Epidemiol 1998; 8:168–175.
15. Woo HD, Lee J, Choi IJ, et al. Dietary flavonoids and gastric cancer risk in a Korean population. Nutrients 2014; 6:4961–4973.
16. Middleton E, Jr., Kandaswami C, Theoharides TC. The effects of plant flavonoids on mammalian cells: Implications for inflammation, heart disease, and cancer. Pharmacol Rev 2000; 52:673–751.
17. Beecher GR. Overview of dietary flavonoids: Nomenclature, occurrence and intake. J Nutr 2003; 133:3248S–3254S.
18. Guajardo-Flores D, Serna-Saldivar SO, Gutierrez-Uribe JA. Evaluation of the antioxidant and antiproliferative activities of extracted saponins and flavonols from germinated black beans (Phaseolus vulgaris L.). Food Chem 2013; 141:1497–1503.
19. Sahu BD, Kalvala AK, Koneru M, et al. Ameliorative effect of fisetin on cisplatin-induced nephrotoxicity in rats via modulation of NF-kappaB activation and antioxidant defence. PLoS ONE 2014; 9:e105070.
20. 2 /M arrest and apoptosis of human epidermoid carcinoma A431 cells: Role of mitochondrial membrane potential disruption and consequent caspases activation. Exp Dermatol 2013; 22:470–475.
21. Lu X, Jung J, Cho HJ, et al. Fisetin inhibits the activities of cyclin-dependent kinases leading to cell cycle arrest in HT-29 human colon cancer cells. J Nutr 2005; 135:2884–2890.
22. Ravichandran N, Suresh G, Ramesh B, Manikandan R, Choi YW, Vijaiyan Siva G. Fisetin modulates mitochondrial enzymes and apoptotic signals in benzo(a)pyrene-induced lung cancer. Mol Cell Biochem 2014; 390:225–234.
23. Li J, Cheng Y, Qu W, et al. Fisetin, a dietary flavonoid, induces cell cycle arrest and apoptosis through activation of p53 and inhibition of NF-kappa B pathways in bladder cancer cells. Basic Clin Pharmacol Toxicol 2011; 108:84–93.
24. 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; 29:1049–1056.
25. Bhat TA, Nambiar D, Pal A, Agarwal R, Singh RP. Fisetin inhibits various attributes of angiogenesis in vitro and in vivo-implications for angioprevention. Carcinogenesis 2012; 33:385–393.
26. Mateen S, Tyagi A, Agarwal C, Singh RP, Agarwal R. Silibinin inhibits human nonsmall cell lung cancer cell growth through cell-cycle arrest by modulating expression and function of key cell-cycle regulators. Mol Carcinog 2010; 49:247–258.
27. Yim D, Singh RP, Agarwal C, Lee S, Chi H, Agarwal R. A novel anticancer agent, decursin, induces G1 arrest and apoptosis in human prostate carcinoma cells. Cancer Res 2005; 65:1035–1044.
28. Varghese L, Agarwal C, Tyagi A, Singh RP, Agarwal R. Silibinin efficacy against human hepatocellular carcinoma. Clin Cancer Res 2005; 11:8441–8448.
29. Tice RR, Agurell E, Anderson D, et al. Single cell gel/comet assay: Guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 2000; 35:206–221.
30. Roy S, Kaur M, Agarwal C, Tecklenburg M, Sclafani RA, Agarwal R. P21 and p27 induction by silibinin is essential for its cell cycle arrest effect in prostate carcinoma cells. Mol Cancer Ther. 2007; 6:2696–2707.
31. Singh T, Sharma SD, Katiyar SK. Grape proanthocyanidins induce apoptosis by loss of mitochondrial membrane potential of human non-small cell lung cancer cells in vitro and in vivo. PLoS ONE 2011; 6:e27444.
32. De Paepe B, Smet J, Vanlander A, et al. Fluorescence imaging of mitochondria in cultured skin fibroblasts: A useful method for the detection of oxidative phosphorylation defects. Pediatr Res 2012; 72:232–240.
33. Kuo LJ, Yang LX. Gamma-H2AX—A novel biomarker for DNA double-strand breaks. In Vivo (Athens, Greece) 2008; 22:305–309.
34. Ambrosini G, Adida C, Altieri DC. A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nat Med 1997; 3:917–921.
35. Tsuburaya A, Noguchi Y, Yoshikawa T, et al. An anti-apoptosis gene, survivin and telomerase expression in gastric cancer. Hepatogastroenterology 2002; 49:1150–1152.
36. Smith ML, Seo YR. P53 regulation of DNA excision repair pathways. Mutagenesis 2002; 17:149–156.
37. Dewaele M, Maes H, Agostinis P. ROS-mediated mechanisms of autophagy stimulation and their relevance in cancer therapy. Autophagy 2010; 6:838–854.
38. Sesti F, Tsitsilonis OE, Kotsinas A, Trougakos IP. Oxidative stress-mediated biomolecular damage and inflammation in tumorigenesis. In Vivo (Athens, Greece) 2012; 26:395–402.
39. Ricci JE, Waterhouse N, Green DR. Mitochondrial functions during cell death, a complex (I-V) dilemma. Cell Death Differ 2003; 10:488–492.
40. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 2009; 417:1–13.
41. Starkov AA. The role of mitochondria in reactive oxygen species metabolism and signaling. Ann NY Acad Sci 2008; 1147:37–52.
42. Abbas T, Dutta A. P21 in cancer: Intricate networks and multiple activities. Nat Rev Cancer 2009; 9:400–414.
43. Ekholm SV, Reed SI. Regulation of G(1) cyclin-dependent kinases in the mammalian cell cycle. Curr Opin Cell Biol 2000; 12:676–684.
44. Shi Y. A structural view of mitochondria-mediated apoptosis. Nat Struct Biol 2001; 8:394–401.
45. Jang KY, Jeong SJ, Kim SH, et al. Activation of reactive oxygen species/AMP activated protein kinase signaling mediates fisetin-induced apoptosis in multiple myeloma U266 cells. Cancer Lett 2012; 319:197–202.
46. Maurya BK, Trigun SK. Fisetin modulates antioxidant enzymes and inflammatory factors to inhibit aflatoxin-B1 induced hepatocellular carcinoma in rats. Oxid Med Cell Longevity 2016; 2016:1–9.
47. Kang KA, Piao MJ, Kim KC, et al. Fisetin attenuates hydrogen peroxide-induced cell damage by scavenging reactive oxygen species and activating protective functions of cellular glutathione system. In Vitro Cell Dev Biol Anim 2014; 50:66–74.