Resveratrol reduces the hypoxia-induced resistance to doxorubicin in breast cancer cells

Journal of Nutritional Science and Vitaminology

Volumn 60, Issue 2, 2014, Pages 122-128

  Mitani, Takakazu ^a   Ito, Yuta ^a   Harada, Naoki ^a   Nakano, Yoshihisa ^b   Inui, Hiroshi ^a   Ashida, Hitoshi ^c   Yamaji, Ryoichi ^a  

^a Osaka Prefecture University   (Japan)

^b Osaka Women's Junior College   (Japan)

^c KOBE UNIVERSITY   (Japan)

Author keywords

Breast cancer cells; Carbonyl reductase 1; Doxorubicin; Hypoxia inducible factor 1 ; Resveratrol

Indexed keywords

3,5 DIHYDROXY 4 METHOXY TRANS STILBENE; CARBONYL REDUCTASE; CARBONYL REDUCTASE 1; DOXORUBICIN; DOXORUBICINOL; DRUG METABOLITE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; PROTEASOME; PROTEIN; RESVERATROL; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ALCOHOL DEHYDROGENASE; ANTINEOPLASTIC AGENT; BENZYLOXYCARBONYLLEUCYL-LEUCYL-LEUCINE ALDEHYDE; CBR1 PROTEIN, HUMAN; HIF1A PROTEIN, HUMAN; LEUPEPTIN; PLANT EXTRACT; STILBENE DERIVATIVE;

ARTICLE; BREAST CANCER; CELL SURVIVAL; CELL VIABILITY ASSAY; CONTROLLED STUDY; CYTOTOXICITY; DRUG RESISTANCE; FLUOROMETER; GENE SILENCING; HUMAN; HUMAN CELL; HYPOXIA; INTRACELLULAR SIGNALING; LUCIFERASE ASSAY; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; ANOXIA; BREAST NEOPLASMS; DRUG EFFECTS; FEMALE; GENETICS; MCF 7 CELL LINE; METABOLISM; PHYTOTHERAPY;

ALCOHOL OXIDOREDUCTASES; ANOXIA; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; DOXORUBICIN; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LEUPEPTINS; MCF-7 CELLS; PHYTOTHERAPY; PLANT EXTRACTS; RNA, MESSENGER; STILBENES;

EID: 84903598361     PISSN: 03014800     EISSN: 18817742     Source Type: Journal    
DOI: 10.3177/jnsv.60.122     Document Type: Article

References (44)

1. Glass AG, Lacey JV Jr, Carreon JD, Hoover RN. 2007. Breast cancer incidence, 1980-2006: combined roles of menopausal hormone therapy, screening mammogra-phy, and estrogen receptor status. J Natl Cancer Inst 99: 1152-1161.
2. Pouysségur J, Dayan F, Mazure NM. 2006. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441: 437-443.
3. Trédan O, Galmarini CM, Patel K, Tannock I F. 2007. Drug resistance and the solid tumor microenvironment. J Natl Cancer Inst 99: 1441-1454.
4. Kaur M, Agarwal C, Agarwal R. 2009. Anticancer and cancer chemopreventive potential of grape seed extract and other grape-based products. J Nutr 139: 1806S-1812S.
5. Li Y, Tollefsbol TO. 2010. Impact on DNA methylation in cancer prevention and therapy by bioactive dietary components. Curr Med Chem 17: 2141-2151.
6. Olaku O, White JD. 2011. Herbal therapy use by cancer patients: a literature review on case reports. Eur J Cancer 47: 508-514.
7. Rimando AM, Kalt W, Magee JB, Dewey J, Ballington JR. 2004. Resveratrol, pterostilbene, and piceatannol in vaccinium berries. J Agric Food Chem 52: 4713-4719.
8. Tsai SH, Lin-Shiau SY, Lin JK. 1999. Suppression of nitric oxide synthase and the down-regulation of the activation of NFkappaB in macrophages by resveratrol. Br J Pharmacol 126: 673-680.
9. Frémont L, Belguendouz L, Delpal S. 1999. Antioxidant activity of resveratrol and alcohol-free wine polyphe-nols related to LDL oxidation and polyunsaturated fatty acids. Life Sci 64: 2511-2521.
10. Leifert WR, Abeywardena MY. 2008. Cardioprotective actions of grape polyphenols. Nutr Res 28: 729-737.
11. Um JH, Park SJ, Kang H, Yang S, Foretz M, McBurney M W, Kim MK, Viollet B, Chung JH. 2010. AMP-activated protein kinase-defcient mice are resistant to the metabolic effects of resveratrol. Diabetes 59: 554-563.
12. Filomeni G, Graziani I, Rotilio G, Ciriolo MR. 2007. trans-Resveratrol induces apoptosis in human breast cancer cells MCF-7 by the activation of MAP kinases pathways. Genes Nutr 2: 295-305.
13. Osman AM, Bayoumi HM, Al-Harthi SE, Damanhouri ZA, Elshal MF. 2012. Modulation of doxorubicin cyto-toxicity by resveratrol in a human breast cancer cell line. Cancer Cell Int 12: 47.
14. Ito Y, Mitani T, Harada N, Isayama A, Tanimori S, Yake-naka S, Nakano Y, Inui H, Yamaji R. 2013. Identifcation of carbonyl reductase 1 as a resveratrol-binding protein by affnity chromatography using 4′-amino-3,5-dihy-droxy-trans-stilbene. J Nutr Sci Vitaminol 59: 358-364.
15. Gonzalez-Covarrubias V, Ghosh D, Lakhman SS, Pen-dyala L, Blanco JG. 2007. A functional genetic polymorphism on human carbonyl reductase 1 (CBR1 V88I) impacts on catalytic activity and NADPH binding affn-ity. Drug Metab Dispos 35: 973-980.
16. Bateman RL, Rauh D, Tavshanjian B, Shokat KM. 2008. Human carbonyl reductase 1 is an S-nitrosoglutathione reductase. J Biol Chem 283: 35756-35762.
17. Bains OS, Karkling MJ, Grigliatti TA, Reid RE, Riggs K W. 2009. Two nonsynonymous single nucleotide polymorphisms of human carbonyl reductase 1 demonstrate reduced in vitro metabolism of daunorubicin and doxo-rubicin. Drug Metab Dispos 37: 1107-1114.
18. Lopez M. 2006. Anthracyclines in the adjuvant treatment of breast carcinoma: thirty years later. Clin Ter 157: 165-177.
19. Varela M, Real MI, Burrel M, Forner A, Sala M, Brunet M, Ayuso C, Castells L, Montañá X, Llovet JM, Bruix J. 2007. Chemoembolization of hepatocellular carcinoma with drug eluting beads: effcacy and doxorubicin phar-macokinetics. J Hepatol 46: 474-481.
20. Kassner N, Huse K, Martin HJ, Gödtel-Armbrust U, Metzger A, Meineke I, Brockmöller J, Klein K, Zanger UM, Maser E, Wojnowski L. 2008. Carbonyl reductase 1 is a predominant doxorubicin reductase in the human liver. Drug Metab Dispos 36: 2113-2120.
21. López de Cerain A, Marín A, Idoate MA, Tuñón MT, Bello J. 1999. Carbonyl reductase and NADPH cytochrome P450 reductase activities in human tumoral versus normal tissues. Eur J Cancer 35: 320-324.
22. Tak E, Lee S, Lee J, Rashid MA, Kim Y W, Park JH, Park WS, Shokat KM, Ha J, Kim SS. 2011. Human carbonyl reductase 1 upregulated by hypoxia renders resistance to apoptosis in hepatocellular carcinoma cells. J Hepatol 54: 328-339.
23. Paul S, Mizuno CS, Lee HJ, Zheng X, Chajkowisk S, Rimoldi JM, Conney A, Suh N, Rimando AM. 2010. In vitro and in vivo studies on stilbene analogs as potential treatment agents for colon cancer. Eur J Med Chem 45: 3702-3708.
24. Mitani T, Yamaji R, Higashimura Y, Harada N, Nakano Y, Inui H. 2011. Hypoxia enhances transcriptional activity of androgen receptor through hypoxia-inducible factor-1a in a low androgen environment. J Steroid Biochem Mol Biol 123: 58-64.
25. Mathew A, Mathur SK, Morimoto RI. 1998. Heat shock response and protein degradation: regulation of HSF2 by the ubiquitin-proteasome pathway. Mol Cell Biol 18: 5091-5098.
26. Kartner N, Riordan JR, Ling V. 1983. Cell surface P-gly-coprotein associated with multidrug resistance in mammalian cell lines. Science 221: 1285-1288.
27. Gavelová M, Hladíková J, Vildová L, Novotná R, Von-drácek J, Krcmár P, Machala M, Skálová L. 2008. Reduction of doxorubicin and oracin and induction of carbonyl reductase in human breast carcinoma MCF-7 cells. Chem Biol Interact 176: 9-18.
28. Heibein AD, Guo B, Sprowl JA, Maclean DA, Parissenti AM. 2012. Role of aldo-keto reductases and other doxo-rubicin pharmacokinetic genes in doxorubicin resistance, DNA binding, and subcellular localization. BMC Cancer 12: 381.
29. Kassner N, Huse K, Martin HJ, Gödtel-Armbrust U, Metzger A, Meineke I, Brockmöller J, Klein K, Zanger UM, Maser E, Wojnowski L. 2008. Carbonyl reductase 1 is a predominant doxorubicin reductase in the human liver. Drug Metab Dispos 36: 2113-2120.
30. Bains OS, Karkling MJ, Lubieniecka JM, Grigliatti TA, Reid RE, Riggs K W. 2009. Naturally occurring variants of human CBR3 alter anthracycline in vitro metabolism. J Pharmacol Exp Ther 332: 755-763.
31. Martin HJ, Breyer-Pfaff U, Wsol V, Venz S, Block S, Maser E. 2006. Purifcation and characterization of akr1b10 from human liver: role in carbonyl reduction of xenobi-otics. Drug Metab Dispos 34: 464-470.
32. Bains OS, Grigliatti TA, Reid RE, Riggs K W. 2010. Naturally occurring variants of human aldo-keto reductases with reduced in vitro metabolism of daunorubicin and doxorubicin. J Pharmacol Exp Ther 335: 533-545.
33. Penning TM, Burczynski ME, Jez JM, Lin HK, Ma H, Moore M, Ratnam K, Palackal N. 2001. Structure-function aspects and inhibitor design of type 5 17beta-hydroxysteroid dehydrogenase (AKR1C3). Mol Cell Endocrinol 171: 137-149.
34. Du GJ, Song ZH, Lin HH, Han XF, Zhang S, Yang YM. 2008. Luteolin as a glycolysis inhibitor offers superior effcacy and lesser toxicity of doxorubicin in breast cancer cells. Biochem Biophys Res Commun 372: 497-502.
35. Park SW, Cho CS, Jun HO, Ryu NH, Kim JH, Yu YS, Kim JS, Kim JH. 2012. Anti-angiogenic effect of luteolin on retinal neovascularization via blockade of reactive oxygen species production. Invest Ophthalmol Vis Sci 53: 7718-7726.
36. Du G, Lin H, Wang M, Zhang S, Wu X, Lu L, Ji L, Yu L. 2010. Quercetin greatly improved therapeutic index of doxorubicin against 4T1 breast cancer by its opposing effects on HIF-1a in tumor and normal cells. Cancer Che-mother Pharmacol 65: 277-287.
37. Lee DH, Lee YJ. 2008. Quercetin suppresses hypoxia-induced accumulation of hypoxia-inducible factor-1alpha (HIF-1alpha) through inhibiting protein synthesis. J Cell Biochem 105: 546-553.
38. Cao Z, Fang J, Xia C, Shi X, Jiang BH. 2004. trans-3,4,5′-Trihydroxystibene inhibits hypoxia-inducible factor 1alpha and vascular endothelial growth factor expression in human ovarian cancer cells. Clin Cancer Res 10: 5253-5263.
39. Zhang Q, Tang X, Lu QY, Zhang ZF, Brown J, Le AD. 2005. Resveratrol inhibits hypoxia-induced accumulation of hypoxia-inducible factor-1alpha and VEGF expression in human tongue squamous cell carcinoma and hepatoma cells. Mol Cancer Ther 4: 1465-1474.
40. Iguchi K, Toyama T, Ito T, Shakui T, Usui S, Oyama M, Iinuma M, Hirano K. 2012. Antiandrogenic activity of resveratrol analogs in prostate cancer LNCaP cells. J Androl 33: 1208-1215.
41. Lappano R, Rosano C, Madeo A, Albanito L, Plastina P, Gabriele B, Forti L, Stivala LA, Iacopetta D, Dolce V, Andò S, Pezzi V, Maggilini M. 2009. Structure-activity relationships of resveratrol and derivatives in breast cancer cells. Mol Nutr Food Res 53: 845-858.
42. Minotti G, Menna P, Salvatorelli E, Cairo G, Gianni L. 2004. Anthracyclines: molecular advances and phar-macologic developments in antitumor activity and car-diotoxicity. Pharmacol Rev 56: 185-229.
43. Olson LE, Bedja D, Alvey SJ, Cardounel AJ, Gabrielson KL, Reeves RH. 2003. Protection from doxorubicin-induced cardiac toxicity in mice with a null allele of car-bonyl reductase 1. Cancer Res 63: 6602-6606.
44. Gu J, Song ZP, Gui DM, Hu W, Chen YG, Zhang DD. 2012. Resveratrol attenuates doxorubicin-induced car-diomyocyte apoptosis in lymphoma nude mice by heme oxygenase-1 induction. Cardiovasc Toxicol 4: 341-349.