Luteolin induces G1 arrest in human nasopharyngeal carcinoma cells via the Akt-GSK-3β-Cyclin D1 pathway

Cancer Letters

Volumn 298, Issue 2, 2010, Pages 167-175

  Ong, Chye Sun ^a,b   Zhou, Jing ^b   Ong, Choon Nam ^b   Shen, Han Ming ^b,c  

^a SINGAPORE POLYTECHNIC   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Akt; Cell cycle; Cyclin D; Luteolin; Nasopharyngeal carcinoma

Indexed keywords

CYCLIN D1; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; GLYCOGEN SYNTHASE KINASE 3BETA; LUTEOLIN; PROTEIN KINASE B; RETINOBLASTOMA PROTEIN; THREONINE; TRANSCRIPTION FACTOR E2F1;

APOPTOSIS; ARTICLE; CANCER CELL; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL PROLIFERATION; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; NASOPHARYNX CARCINOMA; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UBIQUITINATION;

APOPTOSIS; CELL CYCLE; CELL LINE, TUMOR; CYCLIN D1; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; E2F1 TRANSCRIPTION FACTOR; FLOW CYTOMETRY; G1 PHASE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOGEN SYNTHASE KINASE 3; HUMANS; IMMUNOBLOTTING; LUTEOLIN; NASOPHARYNGEAL NEOPLASMS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 77957963491     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2010.07.001     Document Type: Article

References (46)

1. Ross J.A., Kasum C.M. Dietary flavonoids: bioavailability, metabolic effects, and safety. Annu. Rev. Nutr. 2002, 22:19-34.
2. Middleton E., Kandaswami C., Theoharides T.C. The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease, and cancer. Pharmacol. Rev. 2000, 52:673-751.
3. Lopez-Lazaro M. Flavonoids as anticancer agents: structure-activity relationship study. Curr. Med. Chem. Anticancer Agents 2002, 2:691-714.
4. Li Y., Fang H., Xu W. Recent advance in the research of flavonoids as anticancer agents. Mini Rev. Med. Chem. 2007, 7:663-678.
5. Ramos S. Effects of dietary flavonoids on apoptotic pathways related to cancer chemoprevention. J. Nutr. Biochem. 2007, 18:427-442.
6. Kale A., Gawande S., Kotwal S. Cancer phytotherapeutics: role for flavonoids at the cellular level. Phytother. Res. 2008, 22:567-577.
7. Singh R.P., Agarwal R. Natural flavonoids targeting deregulated cell cycle progression in cancer cells. Curr. Drug Targets 2006, 7:345-354.
8. Obaya A.J., Sedivy J.M. Regulation of cyclin-Cdk activity in mammalian cells. Cell Mol. Life Sci. 2002, 59:126-142.
9. Giacinti C., Giordano A. RB and cell cycle progression. Oncogene 2006, 25:5220-5227.
10. Genovese C., Trani D., Caputi M., Claudio P.P. Cell cycle control and beyond: emerging roles for the retinoblastoma gene family. Oncogene 2006, 25:5201-5209.
11. Malumbres M., Barbacid M. Cell cycle, CDKs and cancer: a changing paradigm. Nat. Rev. Cancer 2009, 9:153-166.
12. Blain S.W. Switching cyclin D-Cdk4 kinase activity on and off. Cell Cycle 2008, 7:892-898.
13. Liang J., Slingerland J.M. Multiple roles of the PI3K/PKB (Akt) pathway in cell cycle progression. Cell Cycle 2003, 2:339-345.
14. Blume-Jensen P., Hunter T. Oncogenic kinase signalling. Nature 2001, 411:355-365.
15. Diehl J.A., Cheng M., Roussel M.F., Sherr C.J. Glycogen synthase kinase-3β regulates cyclin D1 proteolysis and subcellular localization. Genes Dev. 1998, 12:3499-3511.
16. Diehl J.A., Zindy F., Sherr C.J. Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitin-proteasome pathway. Genes Dev. 1997, 11:957-972.
17. Lopez-Lazaro M. Distribution and biological activities of the flavonoid luteolin. Mini Rev. Med. Chem. 2009, 9:31-59.
18. Seelinger G., Merfort I., Wolfle U., Schempp C.M. Anti-carcinogenic effects of the flavonoid luteolin. Molecules 2008, 13:2628-2651.
19. Lin Y., Shi R., Wang X., Shen H.M. Luteolin, a flavonoid with potential for cancer prevention and therapy. Curr. Cancer Drug Targets 2008, 8:634-646.
20. Seelinger G., Merfort I., Schempp C.M. Anti-oxidant, anti-inflammatory and anti-allergic activities of luteolin. Planta Med. 2008, 74:1667-1677.
21. Cheng A.C., Huang T.C., Lai C.S., Pan M.H. Induction of apoptosis by luteolin through cleavage of Bcl-2 family in human leukemia HL-60 cells. Eur. J. Pharmacol. 2005, 509:1-10.
22. Fang J., Zhou Q., Shi X.L., Jiang B.H. Luteolin inhibits insulin-like growth factor 1 receptor signaling in prostate cancer cells. Carcinogenesis 2007, 28:713-723.
23. Lee H.J., Wang C.J., Kuo H.C., Chou F.P., Jean L.F., Tseng T.H. Induction apoptosis of luteolin in human hepatoma HepG2 cells involving mitochondria translocation of Bax/Bak and activation of JNK. Toxicol. Appl. Pharmacol. 2005, 203:124-131.
24. Selvendiran K., Koga H., Ueno T., Yoshida T., Maeyama M., Torimura T., Yano H., Kojiro M., Sata M. Luteolin promotes degradation in signal transducer and activator of transcription 3 in human hepatoma cells: an implication for the antitumor potential of flavonoids. Cancer Res. 2006, 66:4826-4834.
25. Xavier C.P., Lima C.F., Preto A., Seruca R., Fernandes-Ferreira M., Pereira-Wilson C. Luteolin, quercetin and ursolic acid are potent inhibitors of proliferation and inducers of apoptosis in both KRAS and BRAF mutated human colorectal cancer cells. Cancer Lett. 2009, 281:162-170.
26. Horinaka M., Yoshida T., Shiraishi T., Nakata S., Wakada M., Nakanishi R., Nishino H., Matsui H., Sakai T. Luteolin induces apoptosis via death receptor 5 upregulation in human malignant tumor cells. Oncogene 2005, 24:7180-7189.
27. Shi R.X., Ong C.N., Shen H.M. Protein kinase C inhibition and x-linked inhibitor of apoptosis protein degradation contribute to the sensitization effect of luteolin on tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis in cancer cells. Cancer Res. 2005, 65:7815-7823.
28. Shi R.X., Ong C.N., Shen H.M. Luteolin sensitizes tumor necrosis factor-α-induced apoptosis in human tumor cells. Oncogene 2004, 23:7712-7721.
29. 2-terminal kinase-mediated p53 phosphorylation and stabilization. Mol. Cancer Ther. 2007, 6:1338-1347.
30. Wu B., Zhang Q., Shen W., Zhu J. Anti-proliferative and chemosensitizing effects of luteolin on human gastric cancer AGS cell line. Mol. Cell Biochem. 2008, 313:125-132.
31. Horinaka M., Yoshida T., Shiraishi T., Nakata S., Wakada M., Nakanishi R., Nishino H., Sakai T. The combination of TRAIL and luteolin enhances apoptosis in human cervical cancer HeLa cells. Biochem. Biophys. Res. Commun. 2005, 333:833-838.
32. Qi Y., Tu Y., Yang D., Chen Q., Xiao J., Chen Y., Fu J., Xiao X., Zhou Z. Cyclin A but not cyclin D1 is essential for c-myc-modulated cell-cycle progression. J. Cell Physiol. 2007, 210:63-71.
33. Casagrande F., Darbon J.M. Effects of structurally related flavonoids on cell cycle progression of human melanoma cells: regulation of cyclin-dependent kinases CDK2 and CDK1. Biochem. Pharmacol. 2001, 61:1205-1215.
34. Lim do Y., Jeong Y., Tyner A.L., Park J.H. 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-G75.
35. Gladden A.B., Diehl J.A. Location, location, location: the role of cyclin D1 nuclear localization in cancer. J. Cell Biochem. 2005, 96:906-913.
36. Tashiro E., Tsuchiya A., Imoto M. Functions of cyclin D1 as an oncogene and regulation of cyclin D1 expression. Cancer Sci. 2007, 98:629-635.
37. Kim J.K., Diehl J.A. Nuclear cyclin D1: an oncogenic driver in human cancer. J. Cell Physiol. 2009, 220:292-296.
38. Altomare D.A., Testa J.R. Perturbations of the AKT signaling pathway in human cancer. Oncogene 2005, 24:7455-7464.
39. Tokunaga E., Oki E., Egashira A., Sadanaga N., Morita M., Kakeji Y., Maehara Y. Deregulation of the Akt pathway in human cancer. Curr. Cancer Drug Targets 2008, 8:27-36.
40. Diehl J.A. Cycling to cancer with cyclin D1. Cancer Biol. Ther. 2002, 1:226-231.
41. Lee W.J., Wu L.F., Chen W.K., Wang C.J., Tseng T.H. Inhibitory effect of luteolin on hepatocyte growth factor/scatter factor-induced HepG2 cell invasion involving both MAPK/ERKs and PI3K-Akt pathways. Chem. Biol. Interact. 2006, 160:123-133.
42. Bagli E., Stefaniotou M., Morbidelli L., Ziche M., Psillas K., Murphy C., Fotsis T. Luteolin inhibits vascular endothelial growth factor-induced angiogenesis; inhibition of endothelial cell survival and proliferation by targeting phosphatidylinositol 3'-kinase activity. Cancer Res. 2004, 64:7936-7946.
43. Yu M.C. Nasopharyngeal carcinoma: epidemiology and dietary factors. IARC Sci. Publ. 1991, 39-47.
44. Hanley A.J., Choi B.C., Holowaty E.J. Cancer mortality among Chinese migrants: a review. Int. J. Epidemiol. 1995, 24:255-265.
45. Chan A.T., Teo P.M., Johnson P.J. Nasopharyngeal cancer. Cancer Treat. Res. 2003, 114:275-293.
46. Chou J., Lin Y.C., Kim J., You L., Xu Z., He B., Jablons D.M. Nasopharyngeal carcinoma - review of the molecular mechanisms of tumorigenesis. Head Neck 2008, 30:946-963.