Evaluation of the effects of the flavonoid apigenin on apoptotic pathway gene expression on the colon cancer cell line (HT29)

Journal of Medicinal Food

Volumn 14, Issue 10, 2011, Pages 1107-1117

  Turktekin, Mehmet ^a,b   Konac, Ece ^a   Onen, H Ilke ^a   Alp, Ebru ^a   Yilmaz, Akin ^a   Menevse, Sevda ^a  

^a GAZI UNIVERSITY   (Turkey)

^b Hemosoft Inc   (Turkey)

Author keywords

5 fluorouracil; apigenin; apoptosis; caspase 3; caspase 8; colon cancer; cyclin D1; HT29 cellline; mammalian target of rapamycin

Indexed keywords

APIGENIN; CASPASE 3; CYCLIN D1; DNA; FLAVONOID; FLUOROURACIL; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; PROTEIN P53;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL STRAIN HT29; COLON ADENOCARCINOMA; COLON CANCER; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFECT; DRUG SCREENING; GENE EXPRESSION; HUMAN; HUMAN CELL; INCUBATION TIME; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANTICARCINOGENIC AGENTS; APIGENIN; APOPTOSIS; CASPASE 3; CASPASE 8; CELL CYCLE CHECKPOINTS; CYCLIN D1; DNA; DNA FRAGMENTATION; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; FLUOROURACIL; GENE EXPRESSION REGULATION, NEOPLASTIC; HT29 CELLS; HUMANS; L-LACTATE DEHYDROGENASE; MICROSCOPY, FLUORESCENCE; RNA, MESSENGER; SIGNAL TRANSDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES;

MAMMALIA;

EID: 80054085637     PISSN: 1096620X     EISSN: 15577600     Source Type: Journal    
DOI: 10.1089/jmf.2010.0208     Document Type: Article

References (64)

1. Surh YJ: Cancer chemoprevention with dietary phytochemicals. Nat Rev Cancer 2003;3:768-780.
2. Kim MH: Flavonoids inhibit VEGF/bFGF-induced angiogenesis in vitro by inhibiting the matrix-degrading proteases. J Cell Biochem 2003;89:529-538. (Pubitemid 36648774)
3. Sarkar FH, Li Y: Cell signaling pathways altered by natural chemopreventive agents. Mutat Res 2004;555:53-64. (Pubitemid 39345397)
4. Patel D, Shukla S, Gupta S: Apigenin and cancer chemoprevention: progress, potential and promise. Int J Oncol 2007;30:233-245.
5. Hessenauer A, Montenarh M, Götz C: Inhibition of CK2 activity provokes different responses in hormone-sensitive and hormonerefractory prostate cancer cells. Int J Oncol 2003;22:1263-1270.
6. Way TD, Kao MC, Lin JK: Degradation of HER2/neu by apigenin induces apoptosis through cytochrome c release and caspase-3 activation in HER2/neu-overexpressing breast cancer cells. FEBS Lett 2005;579:1145-1152.
7. Choi EJ, Kim GH: 5-Fluorouracil combined with apigenin enhances anticancer activity through induction of apoptosis in human breast cancer MDA-MB-453 cells. Oncol Rep 2009; 22:1533-1537.
8. Zheng PW, Chiang LC, Lin CC: Apigenin induced apoptosis through p53-dependent pathway in human cervical carcinoma cells. Life Sci 2005;76:1367-1379.
9. Gupta S, Afaq F, Mukhtar H: Selective growth-inhibitory, cellcycle deregulatory and apoptotic response of apigenin in normal versus human prostate carcinoma cells. Biochem Biophys Res Commun 2001;287:914-920. (Pubitemid 32953563)
10. Kaur P, Shukla S, Gupta S: Plant flavonoid apigenin inactivates Akt to trigger apoptosis in human prostate cancer: an in vitro and in vivo study. Carcinogenesis 2008;29:2210-2217.
11. Shukla S, Gupta S: Apigenin suppresses insulin-like growth factor I receptor signaling in human prostate cancer: an in vitro and in vivo study. Mol Carcinog 2009;48:243-252.
12. Caltagirone S, Rossi C, Poggi A, et al.: Flavonoids apigenin and quercetin inhibit melanoma growth and metastatic potential. Int J Cancer 2000;87:595-600. (Pubitemid 30639822)
13. Wang W, VanAlstyne PC, Irons KA, et al.: Individual and interactive effects of apigenin analogs on G2/M cell-cycle arrest in human colon carcinoma cell lines. Nutr Cancer 2004;48:106-114. (Pubitemid 38823552)
14. Karmakar S, Davis KA, Choudhury SR, et al.: Bcl-2 inhibitor and apigenin worked synergistically in human malignant neuroblastoma cell lines and increased apoptosis with activation of extrinsic and intrinsic pathways. Biochem Biophys Res Commun 2009;388:705-710.
15. Zhang Q, Zhao XH, Wang ZJ: Cytotoxicity of flavones and flavonols to a human esophageal squamous cell carcinoma cell line (KYSE-510) by induction of G2/M arrest and apoptosis. Toxicol In Vitro 2009;23:797-807.
16. Melstrom LG, Salabat MR, Ding XZ, et al.: Apigenin inhibits the GLUT-1 glucose transporter and the phosphoinositide 3-kinase/ Akt pathway in human pancreatic cancer cells. Pancreas 2008;37:426-431.
17. Vargo MA, Voss OH, Poustka F, et al.: Apigenin-inducedapoptosisis mediated by the activation of PKCdelta and caspases in leukemia cells. Biochem Pharmacol 2006;72:681-692. (Pubitemid 44233544)
18. Hussain AR, Khan AS, Ahmed SO, et al.: Apigenin induces apoptosis via downregulation of S-phase kinase-associated protein 2-mediated induction of p27Kip1 in primary effusion lymphoma cells. Cell Prolif 2010;43:170-183.
19. Way TD, Kao MC, Lin JK: Apigenin induces apoptosis through proteasomal degradation of HER2/neu in HER2/neuoverexpressing breast cancer cells via the phosphatidylinositol 3-kinase/Akt-dependent pathway. J Biol Chem 2004;279:4479-4489.
20. Shukla S, Gupta S: Molecular mechanisms for apigenin-induced cell-cycle arrest and apoptosis of hormone refractory human prostate carcinoma DU145 cells. Mol Carcinog 2004;39:114-126. (Pubitemid 38167115)
21. Chen D, Daniel KG, Chen MS, et al.: Dietary flavonoids as proteasome inhibitors and apoptosis inducers in human leukemia cells. Biochem Pharmacol 2005;69:1421-1432. (Pubitemid 40602442)
22. Pajak B, Gajkowska B, Orzechowski A: Position of STAT-1 alpha in cycloheximide-dependent apoptosis triggered by TNFalpha in human colorectal COLO 205 cancer cell line: role of polyphenolic compounds. J Physiol Pharmacol 2005;56:119-141. (Pubitemid 43129238)
23. Das A, Banik NL, Ray SK: Mechanism of apoptosis with the involvement of calpain and caspase cascades in human malignant neuroblastoma SH-SY5Y cells exposed to flavonoids. Int J Cancer 2006;119:2575-2585. (Pubitemid 44691310)
24. Choi EJ, Kim GH: Apigenin causes G(2)/M arrest associated with the modulation of p21(Cip1) and Cdc2 and activates p53- dependent apoptosis pathway in human breast cancer SK-BR-3 cells. J Nutr Biochem 2009;20:285-290.
25. Kiechle FL, Zhang X: Apoptosis: biochemical aspects and clinical implications. Clin Chim Acta 2002;326:27-45. (Pubitemid 35341162)
26. Guertin DA, Sabatini DM: Defining the role of mTOR in cancer. Cancer Cell 2007;12:9-22. (Pubitemid 47001784)
27. Zhang YJ, Dai Q, Sun DF, et al.: mTOR signaling pathway is a target for the treatment of colorectal cancer. Ann Surg Oncol 2009;16:2617-2628.
28. Palozza P, Bellovino D, Simone R, et al.: Effect of beta-carotenerich tomato lycopene beta-cyclase (tlcy-b) on cell growth inhibition in HT-29 colon adenocarcinoma cells. Br J Nutr 2009;102:207-214.
29. Stahtea XN, Roussidis AE, Kanakis I, et al.: Imatinib inhibits colorectal cancer cell growth and suppresses stromal-induced growth stimulation, MT1-MMP expression and pro-MMP2 activation. Int J Cancer 2007;121:2808-2814. (Pubitemid 350136431)
30. Grivicich I, Regner A, Zanoni C, et al.: Hsp70 response to 5-fluorouracil treatment in human colon cancer cell lines. Int J Colorectal Dis 2007;22:1201-1208. (Pubitemid 47304789)
31. Gong JP, Traganos F, Darzynkiewicz Z: A selective procedure for DNA extraction from apoptotic cells applicable for gel electrophoresis and flow cytometry. Anal Biochem 1994;218:314-319. (Pubitemid 24141629)
32. Pfaffl MW, Horgan GW, Dempfle L: Relative expression software tool (REST) for group wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002;30:e36.
33. Kim DH, Lee JT, Lee IK, Ha JH: Comparative anticancer effects of flavonoids and diazepam in cultured cancer cells. Biol Pharm Bull 2008;31:255-259.
34. Lordan S, O'Neill C, O'Brien NM: Effects of apigenin, lycopene and astaxanthin on 7 beta-hydroxycholesterol-induced apoptosis and Akt phosphorylation in U937 cells. Br J Nutr 2008;100:287-296.
35. Szliszka E, Czuba ZP, Jernas K, Król W: Dietary flavonoids sensitize HeLa cells to tumor necrosis factor-related apoptosisinducing ligand (TRAIL). Int J Mol Sci 2008;9:56-64. (Pubitemid 351263331)
36. Tsuji PA, Walle T: Cytotoxic effects of the dietary flavones chrysin and apigenin in a normal trout liver cell line. Chem Biol Interact 2008;171:37-44. (Pubitemid 350191840)
37. Zhang Q, Zhao XH, Wang ZJ: Flavones and flavonols exert cytotoxic effects on a human oesophageal adenocarcinoma cell line (OE33) by causing G2/M arrest and inducing apoptosis. Food Chem Toxicol 2008;46:2042-2053.
38. Li XL, Wang CZ, Sun S, et al.: American ginseng berry enhances chemopreventive effect of 5-FU on human colorectal cancer cells. Oncol Rep 2009;22:943-952.
39. Bourikas LA, Kolios G, Valatas V, et al.: Ciprofloxacin decreases survival in HT-29 cells via the induction of TGF-beta1 secretion and enhances the anti-proliferative effect of 5-fluorouracil. Br J Pharmacol 2009;157:362-370.
40. Flis S, Sp1wiński J: Inhibitory effects of 5-fluorouracil and oxaliplatin on human colorectal cancer cell survival are synergistically enhanced by sulindac sulfide. Anticancer Res 2009;29:435-441.
41. Bernhaus A, Fritzer-Szekeres M, Grusch M, et al.: Digalloylresveratrol,a new phenolic acid derivative induces apoptosis and cell cycle arrest in human HT-29 colon cancer cells. Cancer Lett 2009;274:299-304.
42. Patel BB, Sengupta R, Qazi S, et al.: Curcumin enhances the effects of 5-fluorouracil and oxaliplatin in mediating growth inhibition of colon cancer cells by modulating EGFR and IGF-1R. Int J Cancer 2008;122:267-273. (Pubitemid 350234711)
43. Chuang CM, Monie A, Wu A, Hung CF: Combination of apigenin treatment with therapeutic HPV DNA vaccination generates enhanced therapeutic antitumor effects. J Biomed Sci 2009;16:49.
44. Strouch MJ, Milam BM, Melstrom LG, et al.: The flavonoid apigenin potentiates the growth inhibitory effects of gemcitabine and abrogates gemcitabine resistance in human pancreatic cancer cells. Pancreas 2009;38:409-415.
45. Lim do Y, Jeong Y, Tyner AL, Park JH: Induction of cell cycle arrest and apoptosis in HT-29 human colon cancer cells by the dietary compound luteolin. Am J Physiol Gastrointest Liver Physiol 2007;292:G66-75. (Pubitemid 46090252)
46. Morley KL, Ferguson PJ, Koropatnick J: Tangeretin and nobiletin induce G1 cell cycle arrest but not apoptosis in human breast and colon cancer cells. Cancer Lett 2007;251:168-178. (Pubitemid 46589774)
47. Wenzel U, Nickel A, Daniel H: Melatonin potentiates flavone-induced apoptosis in human colon cancer cells by increasing the level of glycolytic end products. Int J Cancer 2005;116:236-242. (Pubitemid 40967260)
48. Chen YC, Shen SC, Chow JM, Ko CH, Tseng SW: Flavone inhibition of tumor growth via apoptosis in vitro and in vivo. Int J Oncol 2004;25:661-670.
49. Farah M, Parhar K, Moussavi M, Eivemark S, Salh B: 5,6- Dichloro-ribifuranosylbenzimidazole- and apigenin-induced sensitization of colon cancer cells to TNF-alpha-mediated apoptosis. Am J Physiol Gastrointest Liver Physiol 2003;285:G919-928.
50. Chung CS, Jiang Y, Cheng D, Birt DF: Impact of adenomatous polyposis coli (APC) tumor supressor gene in human colon cancer cell lines on cell cycle arrest by apigenin. Mol Carcinog 2007;46:773-782. (Pubitemid 47438728)
51. Al-Fayez M, Cai H, Tunstall R, Steward WP, Gescher AJ: Differential modulation of cyclooxygenase-mediated prostaglandin production by the putative cancer chemopreventive flavonoids tricin, apigenin and quercetin. Cancer Chemother Pharmacol 2006;58:816-825. (Pubitemid 44351263)
52. Izeradjene K, Douglas L, Delaney A, Houghton JA: Casein kinase II (CK2) enhances death-inducing signaling complex (DISC) activity in TRAIL-induced apoptosis in human colon carcinoma cell lines. Oncogene 2005;24:2050-2058. (Pubitemid 40516198)
53. Takagaki N, Sowa Y, Oki T, et al.: Apigenin induces cell cycle arrest and p21/WAF1 expression in a p53-independent pathway. Int J Oncol 2005;26:185-189.
54. Wang W, Heideman L, Chung CS, et al.: Cell-cycle arrest at G2/ M and growth inhibition by apigenin in human colon carcinoma cell lines. Mol Carcinog 2000;28:102-110. (Pubitemid 30432478)
55. Kuntz S, Wenzel U, Daniel H: Comparative analysis of the effects of flavonoids on proliferation, cytotoxicity, and apoptosis in human colon cancer cell lines. Eur J Nutr 1999;38:133-142. (Pubitemid 29352529)
56. Lee WR, Shen SC, Lin HY, et al.: Wogonin and fisetin induce apoptosis in human promyeloleukemic cells, accompanied by a decrease of reactive oxygen species, and activation of caspase 3 and Ca(2 + )-dependent endonuclease. Biochem Pharmacol 2002;63:225-236.
57. Choi EJ, Kim GH: Apigenin induces apoptosis through a mitochondria/ caspase-pathway in human breast cancer MDA-MB- 453 cells. J Clin Biochem Nutr 2009;44:260-265.
58. Torkin R, Lavoie JF, Kaplan DR, Yeger H: Induction of caspasedependent, p53-mediated apoptosis by apigenin in human neuroblastoma. Mol Cancer Ther 2005;4:1-11. (Pubitemid 40268061)
59. Monasterio A, Urdaci MC, Pinchuk IV, López-Moratalla N, Martínez-Irujo JJ: Flavonoids induce apoptosis in human leukemia U937 cells through caspase- and caspase-calpain-dependent pathways. Nutr Cancer 2004;50:90-100. (Pubitemid 39587610)
60. Shukla S, Gupta S: Apigenin-induced cell cycle arrest is mediated by modulation of MAPK, PI3K-Akt, and loss of cyclin D1 associated retinoblastoma dephosphorylation in human prostate cancer cells. Cell Cycle 2007;6:1102-1114. (Pubitemid 46708584)
61. Lepley DM, Pelling JC: Induction of p21/WAF1 and G1 cellcycle arrest by the chemopreventive agent apigenin. Mol Carcinog 1997;19:74-82. (Pubitemid 27296738)
62. Gupta S, Afaq F, Mukhtar H: Involvement of nuclear factorkappa B, Bax and Bcl-2 in induction of cell cycle arrest and apoptosis by apigenin in human prostate carcinoma cells. Oncogene 2002;21:3727-3738. (Pubitemid 34620536)
63. Eddy SF, Guo S, Demicco EG, et al.: Inducible IkappaB kinase/ IkappaB kinase epsilon expression is induced by CK2 and promotes aberrant nuclear factor-kappaB activation in breast cancer cells. Cancer Res 2005;65:11375-11383. (Pubitemid 41823949)
64. Yin F, Giuliano AE, Law RE, Van Herle AJ: Apigenin inhibits growth and induces G2/M arrest by modulating cyclin-CDK regulators and ERK MAP kinase activation in breast carcinoma cells. Anticancer Res 2001;21:413-420. (Pubitemid 32267675)