Flavones inhibit the proliferation of human tumor cancer cell lines by inducing apoptosis

Drug and Chemical Toxicology

Volumn 35, Issue 1, 2012, Pages 1-10

  Kilani Jaziri, Soumaya ^a,b   Frachet, Véronique ^c   Bhouri, Wissem ^a,b   Ghedira, Kamel ^a   Chekir Ghedira, Leila ^a,b   Ronot, Xavier ^c  

^a UNIVERSITY OF MONASTIR   (Tunisia)

^b UNIVERSITY OF MONASTIR   (Tunisia)

^c PSL RESEARCH UNIVERSITY   (France)

Author keywords

anticancer action; apigenin; apoptosis; cell cycle; cytotoxicity; Luteolin

Indexed keywords

APIGENIN; LUTEOLIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BLADDER CARCINOMA; CANCER CELL; CANCER INHIBITION; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DNA FRAGMENTATION; DNA STRAND BREAKAGE; DRUG EFFECT; DRUG MECHANISM; DRUG STRUCTURE; ENZYME SYNTHESIS; ERYTHROLEUKEMIA; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IC 50; PROTEIN CLEAVAGE; PROTEIN DEGRADATION;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APIGENIN; APOPTOSIS; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; DNA FRAGMENTATION; DOSE-RESPONSE RELATIONSHIP, DRUG; FLOW CYTOMETRY; HUMANS; K562 CELLS; LEUKEMIA, ERYTHROBLASTIC, ACUTE; LUTEOLIN; TIME FACTORS; URINARY BLADDER NEOPLASMS;

EID: 83255192527     PISSN: 01480545     EISSN: 15256014     Source Type: Journal    
DOI: 10.3109/01480545.2011.564180     Document Type: Article

References (51)

1. Ahmad, N., Adhami, V. M., Afaq, F., Feyes, D. K., Mukhtar, H.2001). Resveratrol causes WAF-1/p21-mediated G(1)-phase arrest of cell cycle and induction of apoptosis in human epidermoid carcinoma A431 cells. Clin Cancer Res 7:1466-1473.
2. Birt, D. F., Hendrich, S., Wang, W. (2001). Dietary agents in cancer prevention: flavonoids and isoflavonoids. Pharmacol Ther 90:157-177.
3. Boumendjel, A., Ronot, X., Boutonnat, J.2009). Chalcones derivatives acting as cell cycle blockers: Potential anticancer drugs? Curr Drug Targ 10:363-371.
4. Calcabrini, A., Garcia-Martinez, J. M., Gonzalez, L., Tendero, M. J., Ortuno, M. T., Crateri, P., et al. (2006). Inhibition of proliferation and induction of apoptosis in human breast cancer cells by lauryl gallate. Carcinogenesis 27:1699-1712.
5. Chiang, L. C., Ng, L. T., Lin, I. C., Kuo, P. L., Lin, C.C.2006). Antiproliferative effect of apigenin and its apoptotic induction in human Hep G2 cells. Cancer Lett 237:207-214.
6. Cho, S. G., Choi, E. J.2002). Apoptotic signaling pathways: Caspases and stress-activated protein kinases. J Biochem Mol Biol 35:24-27.
7. Choi, J. A., Kim, J. Y., Lee, J. Y., Kang, C. M., Kwon, H. J., Yoo, Y. D., et al. (2001). Induction of cell cycle arrest and apoptosis in human breast cancer cells by quercetin. Int J Oncol 19:837-844.
8. Csokay, B., Prajda, N., Weber, G., Olah, E.1997). Molecular mechanisms in the antiproliferative action of quercetin. Life Sci 60:2157-2163.
9. Gupta, S., Afaq, F., Mukhtar, H.2002). Involvement of nuclear factor kappa B, Bax, and Bcl-2 in induction of cell cycle arrest and apoptosis by apigenin in human prostate carcinoma cells. Oncogene 21:3727-3738.
10. Harborne, J. B. (Ed.). (1999). The flavonoids-advance in research since 1986. London: Chapman and Hall. Harborne, J. B., Williams, C. A. (2000). Advances in flavonoid research since 1992. Phytochemistry 55:481-504.
11. Horinaka, M., Yoshida, T., Shiraishi, T., Nakata, S., Wakada, M., Nakanishi, R., et al. (2005). Luteolin induces apoptosis via death receptor 5 upregulation in human malignant tumor cells.Oncogene 24:7180-7189.
12. Hsu, Y. L., Kuo, P. L., Liu, C. F., Lin, C.C.2004). Acacetin-induced cell cycle arrest and apoptosis in human non-small cell lung cancer A549 cells. Cancer Lett 212:53-60.
13. Janicke, R. U., Sprengart, M. L., Wati, M. R., Porter, A.G.1998). Caspase-3 is required for alpha-fodrin cleavage but dispensable for cleavage of other death substrates in apoptosis. J Biol Chem 273:9357-9360.
14. Kandaswami, C., Lee, L. T., Lee, P. P., Hwang, J. J., Ke, F. C., Huang, Y. T., Lee, M.T.2005). The antitumor activities of flavonoides. In Vivo 19:895-909.
15. Kaufmann, S. H., Desnoyers, S., Ottaviano, Y., Davidson, N. E., Poirier, G.G.1993). Specific proteolytic cleavage of poly(ADP-ribose) polymerase: An early marker of chemotherapy-induced apoptosis. Cancer Res 53:3976-3985.
16. Klaus, S. O., Herming, W., Wulf, D., Krammer, P. H.1994). Cell nucleus and DNA fragmentation are not required for apoptosis. J Cell Biol 127:15-20.
17. Kuntz, S., Wenzel, U., Daniel, H.1999). Comparative analysis of the effects of flavonoids on proliferation, cytotoxicity, and apoptosis in human colon cancer cell lines. Eur J Nutr 38:133-142.
18. Le Marchand, L. (2002). Cancer preventive effects of flavonoids-a review, Biomed Pharmacother 56:296-301.
19. Lim do, Y., Jeong, Y., Tyner, A. L., Park, J. H.2007). 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 292:G66-G75
20. Luo, X., Budihardjo, I., Zou, H., Slaughter, C., Wang, X. (1998). Bcl-2 interaction protein mediates cytochrome C release from mitochondria in response to activation of cell surface death receptor. Cell 94:481-490.
21. Liu, X., Zou, H., Slaughter, C., Wang, X. (1997). DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89:175-184.
22. Manthey, J. A., Grohmann, K., Guthrie, N. (2001). Biological properties of citrus flavonoids pertaining to cancer and inflammation. Curr Med Chem 8:135-153.
23. Martin, S. J., Green, D.R.1995). Protease activation during apoptosis: death by a thousand cuts? Cell 82:349-352.
24. Mousavi, S. H., Tavakkol-Afshari, J., Brook, A., Jafari-Anarkooli, I.2009). Role of 385 caspases and Bax protein in saffron-induced apoptosis in MCF-7 cells. Food Chem Toxicol 47:1909-1913.
25. Mu, C., Jia, P., Yan, Z., Liu, X., Li, X., Liu, H.2007). Quercetin induces cell cycle G1 arrest through elevating Cdk inhibitors p21 and p27 in human hepatoma cell line (HepG2). Meth Find Exp Clin Pharmacol 29:179-183.
26. Nicholson, D. W., Thornberry, N.A.1997). Caspases: killer proteases. Trends Biochem Sci 22:299-306.
27. Parker, B. W., Kaur, G., Nieves-Neira, W., Taimi, M., Kohlhagen, G., Shimizu, T., et al. (1998). Early induction of apoptosis in hematopoetic cell lines after exposure to flavopiridol. Blood 91:458-465.
28. Oberhammer, F., Wilson, J. W., Dive, C., Morris, I. D., Hickman, J. A., Wakeling, A. E., et al. (1993). Apoptotic death in epithelial cells: Cleavage of DNA to 300 and/or 50 kb fragments prior to or in the absence of internucleosomal fragmentation. EMBO J 12:3679-3684.
29. Ramos, S. (2007). Effects of dietary flavonoids on apoptotic pathways related to cancer chemoprevention. J Nutr Biochem 18:427-442.
30. Ren, W., Qiao, Z., Wang, H., Zhu, L., Zhang, L. (2003). Flavonoids: Promising anticancer agents. Med Res Rev 23:519-534
31. Shukla, S., Gupta, S. (2006). Molecular targets for apigenin-induced cell cycle arrest and apoptosis in prostate cancer cell xenograft. Mol Cancer Ther 5:843-852.
32. Shukla, S., Gupta, S. (2007). 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 6:1102-1114.
33. Snyder, R.D.2000). Use of catalytic topoisomerase inhibitors to probe mechanisms of chemical-induced clastogenicity in Chinese hamster V79 cells. Environ Mol Mutagen 35:13-21.
34. Snyder, R. D., Arnone, M.R.2002). Putative identification of functional interactions between DNA intercalating agents and topoisomerase II using the V79 in vitro micronucleus assay. Mutat Res 503:21-35.
35. Snyder, R. D., Gillies, P. J.2002). Evaluation of the clastogenic, DNA intercalative, and topoisomerase II-interactive properties of bioflavonoids in Chinese hamster V79 cells. Environ Mol Mutagen 40:266-276.
36. Steinmetz, K. A., Potter, J.D.1996). Vegetables, fruit, and cancer prevention: A review. J Am Diet Assoc 96:1027-1039.
37. Takagaki, N., Sowa, Y., Oki, T., Nakanishi, R., Yogosawa, S., Sakai,T.2005). Apigenin induces cell cycle arrest and p21/WAF1 expression in a p53-independent pathway. Int J Oncol 26:185-189.
38. Taraphdar, A. K., Roy, M., Bhattacharya, R.K.2001). Natural products as inducers of apoptosis: Implication for cancer therapy and prevention. Curr Sci 80:10-11.
39. Teillet, F., Boumendjel, A., Boutonnat, J., Ronot, X. (2008). Flavonoids as RTK inhibitors and potential anticancer agents [review]. Med Res Rev 28:715-745.
40. Thornberry, N.A.1998). Caspases: key mediators of apoptosis. Chem Biol 5:R97-R103
41. Ujiki, M. B., Ding, X. Z., Salabat, M. R., Bentrem, D. J., Golkar, L.,Milam, B., et al. (2006). Apigenin inhibits pancreatic cancer cell proliferation through G2/M cell cycle arrest. Mol Cancer 5:76-84.
42. Walker, P. R., Leblanc, J., Carson, C., Ribecco, M., Sikorska, M. (1999). Neither caspase 3 nor DNA fragmentation factor is required for high molecular weight DNA degradation in apoptosis. Ann N Y Acad Sci 887:48-59.
43. Wang, C. C., Chen, L. G., Yang, L. L. (2002). Cytotoxic activity of sesquiterpenoids from Atractylodes ovata on leukaemia cell lines. Planta Med 68:204-208.
44. Wang, W., VanAlstyne, P. C., Irons, K. A., Chen, S., Stewart, J. W., Birt, D. F. (2004). Individual and interactive effects of apigenin analogs on G2/M cell-cycle arrest in human colon carcinoma cell lines. Nutr Cancer 48:106-114.
45. Wenzel, U., Kuntz, S., Brendel, M. D., Daniel, H.2000). Dietary flavone is a potent apoptosis inducer in human colon carcinoma cells. Cancer Res 60:3823-3831.
46. Yang, C. S., Landau, J. M., Huang, M. T., Newmark, H.L.2001). Inhibition of carcinogenesis by dietary polyphenolic compounds. Annu Rev Nutr 21:381-406.
47. Zhang, X. D., Franco, A., Myers, K., Gray, C., Nguyen, T., Hersey, P. (1999). Relation of TNF-related apoptosis-inducing ligand (TRAIL) receptor and FLICE-inhibitory protein expression to TRAIL-induced apoptosis of melanoma. Cancer Res 59:2747-2753.
48. Zhang, Q., Zhao, X. H., Wang, Z. J.2009). 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 23:797-807.
49. Zhao-dong, L., Xiao-wen, H., Yu-tian, W., Jing, F. (2009). Apigenin inhibits proliferation of ovarian cancer A2780 cells through Id1. FEBS Lett 583:1999-2003.
50. Zheng, P. W., Chiang, L. C., Lin, C.C.2005). Apigenin induced apoptosis through p53-dependent pathway in human cervical carcinoma cells. Life Sci 76:1367-1379.
51. Zimmermann, K. C., Green, D. R. (2001). How cell die: Apoptosis pathways. J Allergy Clin Immunol 108:s99-s103