Hispidulin inhibits proliferation and enhances chemosensitivity of gallbladder cancer cells by targeting HIF-1α

Experimental Cell Research

Volumn 332, Issue 2, 2015, Pages 236-246

  Gao, Hui ^a   Xie, Jing ^a   Peng, Jianjun ^b   Han, Yantao ^a   Jiang, Qixiao ^a   Han, Mei ^a   Wang, Chunbo ^a  

^a QINGDAO UNIVERSITY   (China)

^b CHONGQING NORMAL UNIVERSITY   (China)

Author keywords

Chemosensitivity; Gallbladder cancer; HIF 1 ; Hispidulin; P gp

Indexed keywords

CASPASE 3; FLUOROURACIL; GEMCITABINE; HISPIDULIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INITIATION FACTOR 4E BINDING PROTEIN 1; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN; PROTEIN P70; ANTINEOPLASTIC AGENT; DEOXYCYTIDINE; FLAVONE DERIVATIVE; HIF1A PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER INHIBITION; CANCER SIZE; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CELL VIABILITY; CHEMOSENSITIVITY; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; G1 PHASE CELL CYCLE CHECKPOINT; GALLBLADDER CANCER CELL LINE; GALLBLADDER CARCINOMA; HUMAN; HUMAN CELL; MOLECULARLY TARGETED THERAPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; TRANSACTIVATION; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; CELL SURVIVAL; DRUG EFFECTS; DRUG POTENTIATION; DRUG RESISTANCE; DRUG SCREENING; FEMALE; GALLBLADDER NEOPLASMS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NUDE MOUSE; PATHOLOGY; TRANSCRIPTION INITIATION; TUMOR CELL LINE; TUMOR VOLUME;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DEOXYCYTIDINE; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; FEMALE; FLAVONES; FLUOROURACIL; G1 PHASE CELL CYCLE CHECKPOINTS; GALLBLADDER NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MICE, INBRED BALB C; MICE, NUDE; P-GLYCOPROTEIN; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84924351909     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2014.11.021     Document Type: Article

References (41)

1. Siegel R., Ma J., Zou Z., Jemal A. Cancer statistics, 2014. CA: Cancer J. Clin. 2014, 64:9-29.
2. Reid K.M., Ramos-De la Medina A., Donohue J.H. Diagnosis and surgical management of gallbladder cancer: a review. J. Gastrointest. Surg.: Off. J. Soc. Surg. Aliment. Tract 2007, 11:671-681.
3. Wang J.W., Peng S.Y., Li J.T., Wang Y., Zhang Z.P., Cheng Y., Cheng D.Q., Weng W.H., Wu X.S., Fei X.Z., Quan Z.W., Li J.Y., Li S.G., Liu Y.B. Identification of metastasis-associated proteins involved in gallbladder carcinoma metastasis by proteomic analysis and functional exploration of chloride intracellular channel 1. Cancer Lett. 2009, 281:71-81.
4. Arany Z., Huang L.E., Eckner R., Bhattacharya S., Jiang C., Goldberg M.A., Bunn H.F., Livingston D.M. An essential role for p300/CBP in the cellular response to hypoxia. Proc. Natl. Acad. Sci. USA 1996, 93:12969-12973.
5. Keith B., Johnson R.S., Simon M.C. HIF1alpha and HIF2alpha: sibling rivalry in hypoxic tumour growth and progression. Nat. Rev. Cancer 2012, 12:9-22.
6. Denko N.C., Fontana L.A., Hudson K.M., Sutphin P.D., Raychaudhuri S., Altman R., Giaccia A.J. Investigating hypoxic tumor physiology through gene expression patterns. Oncogene 2003, 22:5907-5914.
7. Batmunkh E., Shimada M., Morine Y., Imura S., Kanemura H., Arakawa Y., Hanaoka J., Kanamoto M., Sugimoto K., Nishi M. Expression of hypoxia-inducible factor-1 alpha (HIF-1alpha) in patients with the gallbladder carcinoma. Int. J. Clin. Oncol. 2010, 15:59-64.
8. Way T.D., Lee J.C., Kuo D.H., Fan L.L., Huang C.H., Lin H.Y., Shieh P.C., Kuo P.T., Liao C.F., Liu H., Kao J.Y. Inhibition of epidermal growth factor receptor signaling by Saussurea involucrata, a rare traditional Chinese medicinal herb, in human hormone-resistant prostate cancer PC-3 cells. J. Agric. Food Chem. 2010, 58:3356-3365.
9. Yin Y., Gong F.Y., Wu X.X., Sun Y., Li Y.H., Chen T., Xu Q. Anti-inflammatory and immunosuppressive effect of flavones isolated from Artemisia vestita. J. Ethnopharmacol. 2008, 120:1-6.
10. Kavvadias D., Sand P., Youdim K.A., Qaiser M.Z., Rice-Evans C., Baur R., Sigel E., Rausch W.D., Riederer P., Schreier P. The flavone hispidulin, a benzodiazepine receptor ligand with positive allosteric properties, traverses the blood-brain barrier and exhibits anticonvulsive effects. Br. J. Pharmacol. 2004, 142:811-820.
11. Tan R.X., Lu H., Wolfender J.L., Yu T.T., Zheng W.F., Yang L., Gafner S., Hostettmann K. Mono- and sesquiterpenes and antifungal constituents from Artemisia species. Planta Med. 1999, 65:64-67.
12. Nagao T., Abe F., Kinjo J., Okabe H. Antiproliferative constituents in plants 10. Flavones from the leaves of Lantana montevidensis Briq. and consideration of structure-activity relationship. Biol. Pharm. Bull. 2002, 25:875-879.
13. Chen Y.T., Zheng R.L., Jia Z.J., Ju Y. Flavonoids as superoxide scavengers and antioxidants. Free Radic. Biol. Med. 1990, 9:19-21.
14. Bourdillat B., Delautier D., Labat C., Benveniste J., Potier P., Brink C. Mechanism of action of hispidulin, a natural flavone, on human platelets. Prog. Clin. Biol. Res. 1988, 280:211-214.
15. Niu X., Chen J., Wang P., Zhou H., Li S., Zhang M. The effects of hispidulin on bupivacaine-induced neurotoxicity: role of AMPK signaling pathway. Cell Biochem. Biophys. 2014.
16. Zhou R., Wang Z., Ma C. Hispidulin exerts anti-osteoporotic activity in ovariectomized mice via activating AMPK signaling pathway. Cell Biochem Biophys. 2014, 69(2):311-317.
17. Nepal M., Choi H.J., Choi B.Y., Yang M.S., Chae J.I., Li L., Soh Y. Hispidulin attenuates bone resorption and osteoclastogenesis via the RANKL-induced NF-kappaB and NFATc1 pathways. Eur. J. Pharmacol. 2013, 715:96-104.
18. Yang J.M., Hung C.M., Fu C.N., Lee J.C., Huang C.H., Yang M.H., Lin C.L., Kao J.Y., Way T.D. Hispidulin sensitizes human ovarian cancer cells to TRAIL-induced apoptosis by AMPK activation leading to Mcl-1 block in translation. J. Agric. Food Chem. 2010, 58:10020-10026.
19. Lin Y.C., Hung C.M., Tsai J.C., Lee J.C., Chen Y.L., Wei C.W., Kao J.Y., Way T.D. Hispidulin potently inhibits human glioblastoma multiforme cells through activation of AMP-activated protein kinase (AMPK). J. Agric. Food Chem. 2010, 58:9511-9517.
20. He L., Wu Y., Lin L., Wang J., Chen Y., Yi Z., Liu M., Pang X. Hispidulin, a small flavonoid molecule, suppresses the angiogenesis and growth of human pancreatic cancer by targeting vascular endothelial growth factor receptor 2-mediated PI3K/Akt/mTOR signaling pathway. Cancer Sci. 2011, 102:219-225.
21. Yu C.Y., Su K.Y., Lee P.L., Jhan J.Y., Tsao P.H., Chan D.C., Chen Y.L. Potential therapeutic role of hispidulin in gastric cancer through induction of apoptosis via NAG-1 signaling. Evid.-based Complement. Altern. Med.: eCAM 2013, 2013:518301.
22. Gao H., Wang H., Peng J. Hispidulin induces apoptosis through mitochondrial dysfunction and inhibition of P13k/Akt signaling pathway in HepG2 cancer cells. Cell Biochem. Biophys. 2014, 69:27-34.
23. Zhang D.C., Liu J.L., Ding Y.B., Xia J.G., Chen G.Y. Icariin potentiates the antitumor activity of gemcitabine in gallbladder cancer by suppressing NF-kappaB. Acta Pharmacol. Sin. 2013, 34:301-308.
24. Hsu C.C., Wang C.H., Wu L.C., Hsia C.Y., Chi C.W., Yin P.H., Chang C.J., Sung M.T., Wei Y.H., Lu S.H., Lee H.C. Mitochondrial dysfunction represses HIF-1alpha protein synthesis through AMPK activation in human hepatoma HepG2 cells. Biochim. Biophys. Acta 2013, 1830:4743-4751.
25. Wu W.D., Hu Z.M., Shang M.J., Zhao D.J., Zhang C.W., Hong D.F., Huang D.S. Cordycepin down-regulates multiple drug resistant (MDR)/HIF-1alpha through regulating AMPK/mTORC1 signaling in GBC-SD gallbladder cancer cells. Int. J. Mol. Sci. 2014, 15:12778-12790.
26. Wang B.L., Zhai H.Y., Chen B.Y., Zhai S.P., Yang H.Y., Chen X.P., Zhao W.T., Meng L. Clinical relationship between MDR1 gene and gallbladder cancer. Hepatobiliary Pancreat. Dis. Int.: HBPD INT 2004, 3:296-299.
27. Caldow Pilgrim C.H., Groeschl R.T., Quebbeman E.J., Gamblin T.C. Recent advances in systemic therapies and radiotherapy for gallbladder cancer. Surg. Oncol. 2013, 22:61-67.
28. Yao H., Xu W., Shi X., Zhang Z. Dietary flavonoids as cancer prevention agents. J. Environ. Sci. Health Part C, Environ. Carcinog. Ecotoxicol. Rev. 2011, 29:1-31.
29. Li W., Chen Y.Q., Shen Y.B., Shu H.M., Wang X.J., Zhao C.L., Chen C.J. HIF-1alpha knockdown by miRNA decreases survivin expression and inhibits A549 cell growth in vitro and in vivo. Int. J. Mol. Med. 2013, 32:271-280.
30. Melstrom L.G., Salabat M.R., Ding X.Z., Strouch M.J., Grippo P.J., Mirzoeva S., Pelling J.C., Bentrem D.J. Apigenin down-regulates the hypoxia response genes: HIF-1alpha, GLUT-1, and VEGF in human pancreatic cancer cells. J. Surg. Res. 2011, 167:173-181.
31. Zhu Z., Wang Y., Liu Z., Wang F., Zhao Q. Inhibitory effects of epigallocatechin-3-gallate on cell proliferation and the expression of HIF-1alpha and P-gp in the human pancreatic carcinoma cell line PANC-1. Oncol. Rep. 2012, 27:1567-1572.
32. Inoki K., Kim J., Guan K.L. AMPK and mTOR in cellular energy homeostasis and drug targets. Annu. Rev. Pharmacol. Toxicol. 2012, 52:381-400.
33. Inoki K., Zhu T., Guan K.L. TSC2 mediates cellular energy response to control cell growth and survival. Cell 2003, 115:577-590.
34. Gwinn D.M., Shackelford D.B., Egan D.F., Mihaylova M.M., Mery A., Vasquez D.S., Turk B.E., Shaw R.J. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol. Cell 2008, 30:214-226.
35. Ling S., Feng T., Ke Q., Fan N., Li L., Li Z., Dong C., Wang C., Xu F., Li Y., Wang L. Metformin inhibits proliferation and enhances chemosensitivity of intrahepatic cholangiocarcinoma cell lines. Oncol. Rep. 2014, 31:2611-2618.
36. Brown J.M. Exploiting the hypoxic cancer cell: mechanisms and therapeutic strategies. Mol. Med. Today 2000, 6:157-162.
37. Tiwari A.K., Sodani K., Dai C.L., Ashby C.R., Chen Z.S. Revisiting the ABCs of multidrug resistance in cancer chemotherapy. Curr. Pharm. Biotechnol. 2011, 12:570-594.
38. Comerford K.M., Wallace T.J., Karhausen J., Louis N.A., Montalto M.C., Colgan S.P. Hypoxia-inducible factor-1-dependent regulation of the multidrug resistance (MDR1) gene. Cancer Res. 2002, 62:3387-3394.
39. Liu L., Ning X., Sun L., Zhang H., Shi Y., Guo C., Han S., Liu J., Sun S., Han Z., Wu K., Fan D. Hypoxia-inducible factor-1 alpha contributes to hypoxia-induced chemoresistance in gastric cancer. Cancer Sci. 2008, 99:121-128.
40. Nardinocchi L., Puca R., Sacchi A., D'Orazi G. Inhibition of HIF-1alpha activity by homeodomain-interacting protein kinase-2 correlates with sensitization of chemoresistant cells to undergo apoptosis. Mol. Cancer 2009, 8:1.
41. Li J., Shi M., Cao Y., Yuan W., Pang T., Li B., Sun Z., Chen L., Zhao R.C. Knockdown of hypoxia-inducible factor-1alpha in breast carcinoma MCF-7 cells results in reduced tumor growth and increased sensitivity to methotrexate. Biochem. Biophys. Res. Commun. 2006, 342:1341-1351.