Resveratrol inhibits hypoxia-driven ROS-induced invasive and migratory ability of pancreatic cancer cells via suppression of the Hedgehog signaling pathway

Oncology Reports

Volumn 35, Issue 3, 2016, Pages 1718-1726

  Li, Wei ^a   Cao, Lei ^b   Chen, Xin ^a   Lei, Jianjun ^a   Ma, Qingyong ^a  

^a THE FIRST AFFILIATED HOSPITAL OF XI AN JIAOTONG UNIVERSITY   (China)

^b MEDICAL SCHOOL OF XI AN JIAOTONG UNIVERSITY   (China)

Author keywords

Hedgehog signaling; Hypoxia; Invasion; Pancreatic cancer; Reactive oxygen species; Resveratrol

Indexed keywords

ACETYLCYSTEINE; DICHLORODIHYDROFLUORESCEIN DIACETATE; GELATINASE A; HYPOXIA INDUCIBLE FACTOR 1ALPHA; REACTIVE OXYGEN METABOLITE; RESVERATROL; SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI1; UROKINASE; HIF1A PROTEIN, HUMAN; MMP2 PROTEIN, HUMAN; STILBENE DERIVATIVE;

ARTICLE; ASSAY; CANCER GROWTH; CANCER INHIBITION; CELL COUNT; CELL INVASION ASSAY; CELL LEVEL; CELL MIGRATION; CELL MOTILITY; CHEMOPROPHYLAXIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; DRUG EFFECT; GENE EXPRESSION REGULATION; GLI1 GENE; HUMAN; HUMAN CELL; HYPOXIA; IC50; IMMUNOFLUORESCENCE; MMP 2 GENE; PANCREAS CANCER; PANCREATIC CANCER CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SHH GENE; SMO GENE; TUMOR INVASION; UPA GENE; WESTERN BLOTTING; WOUND HEALING ASSAY; BIOSYNTHESIS; CELL HYPOXIA; CELL MOTION; CELL PROLIFERATION; DRUG EFFECTS; EPITHELIAL MESENCHYMAL TRANSITION; GENETICS; METABOLISM; PANCREATIC NEOPLASMS; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

CELL HYPOXIA; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HEDGEHOG PROTEINS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MATRIX METALLOPROTEINASE 2; NEOPLASM INVASIVENESS; PANCREATIC NEOPLASMS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; STILBENES; UROKINASE-TYPE PLASMINOGEN ACTIVATOR;

EID: 84955439963     PISSN: 1021335X     EISSN: 17912431     Source Type: Journal    
DOI: 10.3892/or.2015.4504     Document Type: Article

References (38)

1. Siegel RL, Miller KD and Jemal A: Cancer statistics, 2015. CA Cancer J Clin 65: 5-29, 2015.
2. V incent A, Herman J, Schulick R, Hruban RH and Goggins M: Pancreatic cancer. Lancet 378: 607-620, 2011.
3. Castellanos EH, Cardin DB and Berlin JD: Treatment of earlystage pancreatic cancer. Oncology 25: 182-189, 2011.
4. Semenza GL: Hypoxia-inducible factors: Mediators of cancer progression and targets for cancer therapy. Trends Pharmacol Sci 33: 207-214, 2012.
5. Hoffmann AC, Mori R, Vallbohmer D, Brabender J, Klein E, Drebber U, Baldus SE, Cooc J, Azuma M, Metzger R, et al: High expression of HIF1 is a predictor of clinical outcome in patients with pancreatic ductal adenocarcinomas and correlated to PDGFA, VEGF, and bFGF. Neoplasia 10: 674-679, 2008.
6. Zhao T, Gao S, Wang X, Liu J, Duan Y, Yuan Z, Sheng J, Li S, Wang F, Yu M, et al: Hypoxia-inducible factor-1 regulates chemotactic migration of pancreatic ductal adenocarcinoma cells through directly transactivating the CX3CR1 gene. PLoS One 7: e43399, 2012.
7. Pouyssegur J, Dayan F and Mazure NM: Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441: 437-443, 2006.
8. Wu H, Liang X, Fang Y, Qin X, Zhang Y and Liu J: Resveratrol inhibits hypoxia-induced metastasis potential enhancement by restricting hypoxia-induced factor-1 alpha expression in colon carcinoma cells. Biomed Pharmacother 62: 613-621, 2008.
9. Matsuo Y, Ding Q, Desaki R, Maemura K, Mataki Y, Shinchi H, Natsugoe S and Takao S: Hypoxia inducible factor-1 alpha plays a pivotal role in hepatic metastasis of pancreatic cancer: An immunohistochemical study. J Hepatobiliary Pancreat Sci 21: 105-112, 2014.
10. Zhao X, Gao S, Ren H, Sun W, Zhang H, Sun J, Yang S and Hao J: Hypoxia-inducible factor-1 promotes pancreatic ductal adenocarcinoma invasion and metastasis by activating transcription of the actin-bundling protein fascin. Cancer Res 74: 2455-2464, 2014.
11. Lei J, Ma J, Ma Q, Li X, Liu H, Xu Q, Duan W, Sun Q, Xu J, Wu Z, et al: Hedgehog signaling regulates hypoxia induced epithelial to mesenchymal transition and invasion in pancreatic cancer cells via a ligand-independent manner. Mol Cancer 12: 66, 2013.
12. McMahon AP, Ingham PW and Tabin CJ: Developmental roles and clinical significance of hedgehog signaling. Curr Top Dev Biol 53: 1-114, 2003.
13. Nguyen NT, Lin DP, Yen SY, Tseng JK, Chuang JF, Chen BY, Lin TA, Chang HH and Ju JC: Sonic hedgehog promotes porcine oocyte maturation and early embryo development. Reprod Fertil Dev 21: 805-815, 2009.
14. Olive KP, Jacobetz MA, Davidson CJ, Gopinathan A, McIntyre D, Honess D, Madhu B, Goldgraben MA, Caldwell ME, Allard D, et al: Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 324: 1457-1461, 2009.
15. Li W, Cao L, Han L, Xu Q and Ma Q: Superoxide dismutase promotes the epithelial-mesenchymal transition of pancreatic cancer cells via activation of the H2O2/ERK/NF-B axis. Int J Oncol 46: 2613-2620, 2015.
16. Li W, Ma Q, Li J, Guo K, Liu H, Han L and Ma G: Hyperglycemia enhances the invasive and migratory activity of pancreatic cancer cells via hydrogen peroxide. Oncol Rep 25: 1279-1287, 2011.
17. Lei J, Huo X, Duan W, Xu Q, Li R, Ma J, Li X, Han L, Li W, Sun H, et al: Mangostin inhibits hypoxia-driven ROS-induced PSC activation and pancreatic cancer cell invasion. Cancer Lett 347: 129-138, 2014.
18. Chen BY, Kuo CH, Liu YC, Ye LY, Chen JH and Shieh CJ: Ultrasonic-assisted extraction of the botanical dietary supplement resveratrol and other constituents of Polygonum cuspidatum. J Nat Prod 75: 1810-1813, 2012.
19. Albani D, Polito L, Signorini A and Forloni G: Neuroprotective properties of resveratrol in different neurodegenerative disorders. Biofactors 36: 370-376, 2010.
20. Fulda S: Resveratrol and derivatives for the prevention and treatment of cancer. Drug Discov Today 15: 757-765, 2010.
21. Jha RK, Ma Q, Sha H and Palikhe M: Emerging role of resveratrol in the treatment of severe acute pancreatitis. Front Biosci 2: 168-175, 2010.
22. Li W, Ma J, Ma Q, Li B, Han L, Liu J, Xu Q, Duan W, Yu S, Wang F, et al: Resveratrol inhibits the epithelial-mesenchymal transition of pancreatic cancer cells via suppression of the PI-3K/Akt/NF-B pathway. Curr Med Chem 20: 4185-4194, 2013.
23. Qin Y, Ma Z, Dang X, Li W and Ma Q: Effect of resveratrol on proliferation and apoptosis of human pancreatic cancer MIA PaCa-2 cells may involve inhibition of the Hedgehog signaling pathway. Mol Med Rep 10: 2563-2567, 2014.
24. Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2-CT method. Methods 25: 402-408, 2001.
25. Semenza GL: Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3: 721-732, 2003.
26. Spivak-Kroizman TR, Hostetter G, Posner R, Aziz M, Hu C, Demeure MJ, Von Hoff D, Hingorani SR, Palculict TB, Izzo J, et al: Hypoxia triggers hedgehog-mediated tumor-stromal interactions in pancreatic cancer. Cancer Res 73: 3235-3247, 2013.
27. Luoto KR, Kumareswaran R and Bristow RG: Tumor hypoxia as a driving force in genetic instability. Genome Integr 4: 5, 2013.
28. Ye LY, Zhang Q, Bai XL, Pankaj P, Hu QD and Liang TB: Hypoxia-inducible factor 1 expression and its clinical significance in pancreatic cancer: A meta-analysis. Pancreatology 14: 391-397, 2014.
29. Bijlsma MF, Groot AP, Oduro JP, Franken RJ, Schoenmakers SH, Peppelenbosch MP and Spek CA: Hypoxia induces a hedgehog response mediated by HIF-1alpha. J Cell Mol Med 13: 2053.2060, 2009.
30. Nishikawa M, Hashida M and Takakura Y: Catalase delivery for inhibiting ROS-mediated tissue injury and tumor metastasis. Adv Drug Deliv Rev 61: 319-326, 2009.
31. Xu Q, Zong L, Chen X, Jiang Z, Nan L, Li J, Duan W, Lei J, Zhang L, Ma J, et al: Resveratrol in the treatment of pancreatic cancer. Ann NY Acad Sci 1348: 10-19, 2015.
32. Mitani T, Harada N, Tanimori S, Nakano Y, Inui H and Yamaji R: Resveratrol inhibits hypoxia-inducible factor-1α-mediated androgen receptor signaling and represses tumor progression in castration-resistant prostate cancer. J Nutr Sci Vitaminol 60: 276-282, 2014.
33. Mitani T, Ito Y, Harada N, Nakano Y, Inui H, Ashida H and Yamaji R: Resveratrol reduces the hypoxia-induced resistance to doxorubicin in breast cancer cells. J Nutr Sci Vitaminol 60: 122-128, 2014.
34. Ji Q, Liu X, Fu X, Zhang L, Sui H, Zhou L, Sun J, Cai J, Qin J, Ren J, et al: Resveratrol inhibits invasion and metastasis of colorectal cancer cells via MALAT1 mediated Wnt/β-catenin signal pathway. PLoS One 8: e78700, 2013.
35. Sun L, Li H, Chen J, Dehennaut V, Zhao Y, Yang Y, Iwasaki Y, Kahn-Perles B, Leprince D, Chen Q, et al: A SUMOylationdependent pathway regulates SIRT1 transcription and lung cancer metastasis. J Natl Cancer Inst 105: 887-898, 2013.
36. Zhang Q, Tang X, Lu QY, Zhang ZF, Brown J and Le AD: Resveratrol inhibits hypoxia-induced accumulation of hypoxiainducible factor-1alpha and VEGF expression in human tongue squamous cell carcinoma and hepatoma cells. Mol Cancer Ther 4: 1465-1474, 2005.
37. Gao Q, Yuan Y, Gan HZ and Peng Q: Resveratrol inhibits the hedgehog signaling pathway and epithelial-mesenchymal transition and suppresses gastric cancer invasion and metastasis. Oncol Lett 9: 2381-2387, 2015.
38. Su YC, Li SC, Wu YC, Wang LM, Chao KS and Liao HF: Resveratrol downregulates interleukin-6-stimulated sonic hedgehog signaling in human acute myeloid leukemia. Evid Based Complement Alternat Med 2013: 547430, 2013.