Luteolin Induces Carcinoma Cell Apoptosis through Binding Hsp90 to Suppress Constitutive Activation of STAT3

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Fu, Jin ^a   Chen, Dan ^b   Zhao, Bo ^a   Zhao, Zhihui ^a   Zhou, Jiahong ^a   Xu, Yimiao ^a   Xin, Yinqiang ^a   Liu, Chang ^a   Luo, Lan ^b   Yin, Zhimin ^a  

^a NANJING NORMAL UNIVERSITY   (China)

^b NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GELDANAMYCIN; HEAT SHOCK PROTEIN 90; LUTEOLIN; MYC PROTEIN; PROTEIN KINASE B; STAT3 PROTEIN;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BINDING ASSAY; CANCER CELL DESTRUCTION; CARCINOMA CELL; CELL AGING, CELL DEGENERATION AND CELL SURVIVAL; CELL MEMBRANE BLEBBING; CELL SHRINKAGE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG MECHANISM; DRUG PROTEIN BINDING; EMBRYO; FEMALE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; NUCLEAR CONDENSATION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ANIMALS; APOPTOSIS; CARCINOMA; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; HEK293 CELLS; HELA CELLS; HEP G2 CELLS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LUTEOLIN; MICE; NEOPLASMS; PHOSPHORYLATION; PROTEIN BINDING; PROTEOLYSIS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TYROSINE; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84869003163     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049194     Document Type: Article

References (47)

1. Jang HS, Kook SH, Son YO, Kim JG, Jeon YM, et al. (2005) Flavonoids purified from Rhus verniciflua Stokes actively inhibit cell growth and induce apoptosis in human osteosarcoma cells. Biochim Biophys Acta 1726: 309-316.
2. Kook SH, Son YO, Chung SW, Lee SA, Kim JG, et al. (2007) Caspase-independent death of human osteosarcoma cells by flavonoids is driven by p53-mediated mitochondrial stress and nuclear translocation of AIF and endonuclease G. Apoptosis. 12: 1289-1298.
3. Manna SK, Aggarwal RS, Sethi G, Aggarwal BB, Ramesh GT, (2007) Morin (3,5,7,2′,4′-Pentahydroxyflavone) abolishes nuclear factor-kappaB activation induced by various carcinogens and inflammatory stimuli, leading to suppression of nuclear factor-kappaB-regulated gene expression and up-regulation of apoptosis. Clin Cancer Res 13: 2290-2297.
4. Ueda H, Yamazaki C, Yamazaki M, (2002) Luteolin as an anti-inflammatory and anti-allergic constituent of Perilla frutescens. Biol Pharm Bull 25: 1197-1202.
5. Ren W, Qiao Z, Wang H, Zhu L, Zhang L, (2003) Flavonoids: promising anticancer agents. Med Res Rev 23: 519-534.
6. Kim SH, Shin KJ, Kim D, Kim YH, Han MS, et al. (2003) Luteolin inhibits the nuclear factor-kappa B transcriptional activity in Rat-1 fibroblasts. Biochem Pharmacol 66: 955-963.
7. Horinaka M, Yoshida T, Shiraishi T, Nakata S, Wakada M, et al. (2005) The combination of TRAIL and luteolin enhances apoptosis in human cervical cancer HeLa cells. Biochem Biophys Res Commun 333: 833-838.
8. Ju W, Wang X, Shi H, Chen W, Belinsky SA, et al. (2007) A critical role of luteolin-induced reactive oxygen species in blockage of tumor necrosis factor-activated nuclear factor-kappaB pathway and sensitization of apoptosis in lung cancer cells. Mol Pharmacol 71: 1381-1388.
9. Selvendiran K, Koga H, Ueno T, Yoshida T, Maeyama M, et al. (2006) 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 66: 4826-4834.
10. Bromberg J, Darnell JE, (2000) The role of STATs in transcriptional control and their impact on cellular function. Oncogene 19: 2468-2473.
11. Murray PJ, (2007) The JAK-STAT signaling pathway: input and output integration. J Immunol 178: 2623-2629.
12. Bowman T, Garcia R, Turkson J, Jove R, (2000) STATs in oncogenesis. Oncogene 19: 2474-2488.
13. Lin Q, Lai R, Chirieac LR, Li C, Thomazy VA, et al. (2005) Constitutive activation of JAK3/STAT3 in colon carcinoma tumors and cell lines: inhibition of JAK3/STAT3 signaling induces apoptosis and cell cycle arrest of colon carcinoma cells. Am J Pathol 167: 969-980.
14. Shah M, Patel K, Fried VA, Sehgal PB, (2002) Interactions of STAT3 with caveolin-1 and heat shock protein 90 in plasma membrane raft and cytosolic complexes. Preservation of cytokine signaling during fever. J Biol Chem 277: 45662-45669.
15. Sato N, Yamamoto T, Sekine Y, Yumioka T, Junicho A, et al. (2003) Involvement of heat-shock protein 90 in the interleukin-6-mediated signaling pathway through STAT3. Biochem Biophys Res Commun 300: 847-852.
16. Wang C, Chen J, (2003) Phosphorylation and hsp90 binding mediate heat shock stabilization of p53. J Biol Chem 278: 2066-2071.
17. Richter K, Buchner J, (2001) Hsp90: chaperoning signal transduction. J Cell Physiol 188: 281-290.
18. Bagatell R, Whitesell L, (2004) Altered Hsp90 function in cancer: a unique therapeutic opportunity. Mol Cancer Ther 3: 1021-1030.
19. Young JC, Moarefi I, Hartl FU, (2001) Hsp90: a specialized but essential protein-folding tool. J Cell Biol 154: 267-273.
20. Basso AD, Solit DB, Chiosis G, Giri B, Tsichlis P, et al. (2002) Akt forms an intracellular complex with heat shock protein 90 (Hsp90) and Cdc37 and is destabilized by inhibitors of Hsp90 function. J Biol Chem 277: 39858-39866.
21. Zhang H, Burrows F, (2004) Targeting multiple signal transduction pathways through inhibition of Hsp90. J Mol Med (Berl) 82: 488-499.
22. Ge J, Normant E, Porter JR, Ali JA, Dembski MS, et al. (2006) Design, synthesis, and biological evaluation of hydroquinone derivatives of 17-amino-17-demethoxygeldanamycin as potent, water-soluble inhibitors of Hsp90. J Med Chem 49: 4606-4615.
23. Chiosis G, Vilenchik M, Kim J, Solit D, (2004) Hsp90: the vulnerable chaperone. Drug Discov Today 9: 881-888.
24. Janin YL, (2005) Heat shock protein 90 inhibitors. A text book example of medicinal chemistry? J Med Chem 48: 7503-7512.
25. Fujiwara H, Yamakuni T, Ueno M, Ishizuka M, Shinkawa T, et al. (2004) IC101 induces apoptosis by Akt dephosphorylation via an inhibition of heat shock protein 90-ATP binding activity accompanied by preventing the interaction with Akt in L1210 cells. J Pharmacol Exp Ther 310: 1288-1295.
26. Goetz MP, Toft DO, Ames MM, Erlichman C, (2003) The Hsp90 chaperone complex as a novel target for cancer therapy. Ann Oncol 14: 1169-1176.
27. Mandler R, Wu C, Sausville EA, Roettinger AJ, Newman DJ, et al. (2000) Immunoconjugates of geldanamycin and anti-HER2 monoclonal antibodies: antiproliferative activity on human breast carcinoma cell lines. J Natl Cancer Inst 92: 1573-1581.
28. Wang X, Ju W, Renouard J, Aden J, Belinsky SA, et al. (2006) 17-allylamino-17-demethoxygeldanamycin synergistically potentiates tumor necrosis factor-induced lung cancer cell death by blocking the nuclear factor-kappaB pathway. Cancer Res 66: 1089-1095.
29. Turkson J, Jove R, (2000) STAT proteins: novel molecular targets for cancer drug discovery. Oncogene 19: 6613-6626.
30. Shuai K, (2000) Modulation of STAT signaling by STAT-interacting proteins. Oncogene 19: 2638-2644.
31. Matsuo M, Sasaki N, Saga K, Kaneko T, (2005) Cytotoxicity of flavonoids toward cultured normal human cells. Biol Pharm Bull 28: 253-259.
32. Lassus P, Opitz-Araya X, Lazebnik Y, (2002) Requirement for caspase-2 in stress-induced apoptosis before mitochondrial permeabilization. Science 297: 1352-1354.
33. Hanahan D, Weinberg RA, (2000) The hallmarks of cancer. Cell 100: 57-70.
34. Kamal A, Thao L, Sensintaffar J, Zhang L, Boehm MF, et al. (2003) A high-affinity conformation of Hsp90 confers tumour selectivity on Hsp90 inhibitors. Nature 425: 407-410.
35. Prodromou C, Pearl LH, (2003) Structure and functional relationships of Hsp90. Curr Cancer Drug Targets 3: 301-323.
36. Roe SM, Prodromou C, O'Brien R, Ladbury JE, Piper PW, et al. (1999) Structural basis for inhibition of the Hsp90 molecular chaperone by the antitumor antibiotics radicicol and geldanamycin. J Med Chem 42: 260-266.
37. Stebbins CE, Russo AA, Schneider C, Rosen N, Hartl FU, et al. (1997) Crystal structure of an Hsp90-geldanamycin complex: targeting of a protein chaperone by an antitumor agent. Cell 89: 239-250.
38. Calvin Yu-Chian Chen G-WC, Winston Yu-Chen Chen, (2008) Molecular Simulation of HER2/neu Degradation by Inhibiting HSP90. Journal of the Chinese Chemical Society 55: 297-302.
39. Schulte TW, Neckers LM, (1998) The benzoquinone ansamycin 17-allylamino-17-demethoxygeldanamycin binds to HSP90 and shares important biologic activities with geldanamycin. Cancer Chemother Pharmacol 42: 273-279.
40. Miyagi Y, Om AS, Chee KM, Bennink MR, (2000) Inhibition of azoxymethane-induced colon cancer by orange juice. Nutr Cancer 36: 224-229.
41. Ferry DR, Smith A, Malkhandi J, Fyfe DW, deTakats PG, et al. (1996) Phase I clinical trial of the flavonoid quercetin: pharmacokinetics and evidence for in vivo tyrosine kinase inhibition. Clin Cancer Res 2: 659-668.
42. Horinaka M, Yoshida T, Shiraishi T, Nakata S, Wakada M, et al. (2005) Luteolin induces apoptosis via death receptor 5 upregulation in human malignant tumor cells. Oncogene 24: 7180-7189.
43. Ong CS, Zhou J, Ong CN, Shen HM, (2010) Luteolin induces G1 arrest in human nasopharyngeal carcinoma cells via the Akt-GSK-3beta-Cyclin D1 pathway. Cancer Lett 298: 167-175.
44. Zhao Y, Yang G, Ren D, Zhang X, Yin Q, et al. (2011) Luteolin suppresses growth and migration of human lung cancer cells. Mol Biol Rep 38: 1115-1119.
45. Cheng JQ, Jiang X, Fraser M, Li M, Dan HC, et al. (2002) Role of X-linked inhibitor of apoptosis protein in chemoresistance in ovarian cancer: possible involvement of the phosphoinositide-3 kinase/Akt pathway. Drug Resist Updat 5: 131-146.
46. Asselin E, Mills GB, Tsang BK, (2001) XIAP regulates Akt activity and caspase-3-dependent cleavage during cisplatin-induced apoptosis in human ovarian epithelial cancer cells. Cancer Res 61: 1862-1868.
47. Dan HC, Sun M, Kaneko S, Feldman RI, Nicosia SV, et al. (2004) Akt phosphorylation and stabilization of X-linked inhibitor of apoptosis protein (XIAP). J Biol Chem 279: 5405-5412.