The favourable effect of catechin in electrochemotherapy in human pancreatic cancer cells

Olga Michel; Dawid Przystupski; Jolanta Saczko; Anna Szewczyk; Natalia Niedzielska; Joanna Rossowska; Julita Kulbacka

doi:10.18388/abp.2018_2602

Olga Michel Wroclaw Medical University
Dawid Przystupski Wroclaw Medical University
Jolanta Saczko Wroclaw Medical University
Anna Szewczyk University of Wroclaw
Natalia Niedzielska Wroclaw University of Science Technology
Joanna Rossowska Institute of Immunology and Experimental Therapy Polish Academy of Sciences
Julita Kulbacka Wroclaw Medical University

DOI: https://doi.org/10.18388/abp.2018_2602

Abstract

Until recently, green tea polyphenols were considered strong antioxidants. However, the latest reports have revealed that bioflavonoids can play a multiple role in anticancer therapy, including the inhibition of cell proliferation and generation of the oxidative stress in a dose-dependent manner. The presented research was designed to examine the potential of the green tea (±)-catechin as a reinforcement of the electrochemotherapy (ECT) with cisplatin in pancreatic cancer in vitro. The study was performed on two cell lines of the pancreatic ductal adenocarcinoma (PDA) – parental EPP85-181P and multidrug-resistant EPP85-181RNOV. Prior to the ECT protocol the cells were preincubated with high or low concentration of catechin for 2 or 24 hours, respectively. We assessed the influence of preincubation on the cisplatin toxicity with and without electroporation (EP), the electrosensitivity of PDA cell lines and the uptake of the daunorubicin and propidium iodide. Additionally, we evaluated the antioxidative properties of catechin by the measurement of the ROS-related fluorescence and the immunoreactivity of the oxidative stress-related enzymes superoxide dismutase (SOD2) and glutathione S-transferase (GST). We found that co-treatment with catechin can firmly enhance the efficacy of electroporation with cisplatin in vitro. More favorable effect was obtained for 2-hour incubation, which indicates the involvement of the transcriptional-independent mechanisms of catechin action. The effect may be partially explained by the increased oxidative stress level, which was higher in multidrug-resistant cells. However, further studies on cisplatin-catechin interplay and the thorough examination of the catechin-cell membrane interaction need to be performed.

Author Biographies

Olga Michel, Wroclaw Medical University

Department of Medical Biochemistry, Wroclaw Medical University, Chałubińskiego 10, 50-368 Wroclaw, Poland

Dawid Przystupski, Wroclaw Medical University

Department of Medical Biochemistry, Wroclaw Medical University, Chałubińskiego 10, 50-368 Wroclaw, Poland

Jolanta Saczko, Wroclaw Medical University

Department of Medical Biochemistry, Wroclaw Medical University, Chałubińskiego 10, 50-368 Wroclaw, Poland

Department of Molecular and Cellular Biology, Wroclaw Medical University, Borowska 211A, 50-556 Wroclaw, Poland

Anna Szewczyk, University of Wroclaw

Department of Animal Developmental Biology, Institute of Experimental Biology, University of Wroclaw, Sienkiewicza 21, 50-335 Wroclaw, Poland

Natalia Niedzielska, Wroclaw University of Science Technology

Department of Biomedical Engineering, Wroclaw University of Science and Technology, Wybrzeże Stanisława Wyspiańskiego 27, 50-370 Wrocław, Poland

Joanna Rossowska, Institute of Immunology and Experimental Therapy Polish Academy of Sciences

Institute of Immunology and Experimental Therapy Polish Academy of Sciences, Rudolfa Weigla 12, 53-114 Wroclaw, Poland

Julita Kulbacka, Wroclaw Medical University

Department of Medical Biochemistry, Wroclaw Medical University, Chałubińskiego 10, 50-368 Wroclaw, Poland

Department of Molecular and Cellular Biology, Wroclaw Medical University, Borowska 211A, 50-556 Wroclaw, Poland

References

Amić D, Davidović-Amić D, Beslo D, Rastija V, Lucić B, Trinajstić N (2007) SAR and QSAR of the antioxidant activity of flavonoids. Curr Med Chem 14: 827–845.

Appari M, Babu KR, Kaczorowski A, Gross W, Herr I (2014) Sulforaphane, quercetin and catechins complement each other in elimination of advanced pancreatic cancer by miR-let-7 induction and K-ras inhibition. Int J Oncol 45: 1391–1400, doi:10.3892/ijo.2014.2539.

Balentine DA, Wiseman SA, Bouwens LCM (1997a) The chemistry of tea flavonoids. Crit Rev Food Sci Nutr 37: 693–704.

Basu A, Haldar S (2009) Combinatorial effect of epigallocatechin-3-gallate and TRAIL on pancreatic cancer cell death. Int J Oncol 34: 281–286.

Brusselmans K, De Schrijver E, Heyns W, Verhoeven G, Swinnen J V (2003) Epigallocatechin-3-gallate is a potent natural inhibitor of fatty acid synthase in intact cells and selectively induces apoptosis in prostate cancer cells. Int J Cancer 106: 856–862, doi:10.1002/ijc.11317.

Burda S, Oleszek W (2001) Antioxidant and antiradical activities of flavonoids. J Agric Food Chem 49: 2774–2779.

Cao J, Han J, Xiao H, Qiao J, Han M (2016) Effect of tea polyphenol compounds on anticancer drugs in terms of anti-tumor activity, toxicology, and pharmacokinetics. Nutrients 8: doi:10.3390/nu8120762.

Chan MM, Soprano KJ, Weinstein K, Fong D (2006) Epigallocatechin-3-gallate delivers hydrogen peroxide to induce death of ovarian cancer cells and enhances their cisplatin susceptibility. J Cell Physiol 207: 389–396, doi:10.1002/jcp.20569.

Chen C, Wu C, Yang TH, Chang Y, Sheu ML, Liu S (2016) Green tea catechin prevents hypoxia/reperfusion-evoked oxidative stress- regulated autophagy-activated apoptosis and cell death in microglial cells. J Agric Food Chem 64: 4078–4085, doi:10.1021/acs.jafc.6b01513.

Chen S-Z, Zhen Y-S (2013) Molecular targets of tea polyphenols and its roles of anticancer drugs in experimental therapy. Yao Xue Xue Bao 48: 1–7.

Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136: E359–E386, doi:10.1002/ijc.29210.

Forester SC, Lambert JD (2011) The role of antioxidant versus pro-oxidant effects of green tea polyphenols in cancer prevention. Mol Nutr Food Res 55: 844–854, doi:10.1002/mnfr.201000641.

Frandsen SK, Gibot L, Madi M, Gehl J, Rols M-P (2015) Calcium Electroporation: Evidence for Differential Effects in Normal and Malignant Cell Lines, Evaluated in a 3D Spheroid Model. PLoS One 10: e0144028, doi:10.1371/journal.pone.0144028.

Frandsen SK, McNeil AK, Novak I, McNeil PL, Gehl J (2016) Difference in Membrane Repair Capacity Between Cancer Cell Lines and a Normal Cell Line. J Membr Biol 249: 569–576, doi:10.1007/s00232-016-9910-5.

Gehl J (2005) [Investigational treatment of cancer using electrochemotherapy, electrochemoimmunotherapy and electro-gene transfer]. Ugeskr Laeger 167: 3156–3159.

Goess R, Friess H (2018) A look at the progress of treating pancreatic cancer over the past 20 years. Expert Rev Anticancer Ther 18: 1-10, doi:10.1080/14737140.2018.1428093.

Granata V, Fusco R, Piccirillo M, Palaia R, Petrillo A, Lastoria S, Izzo F (2015) Electrochemotherapy in locally advanced pancreatic cancer: Preliminary results. Int. J. Surg. 18: 230-236, doi:10.1016/j.ijsu.2015.04.055.

Granata V, Fusco R, Setola SV, Piccirillo M, Leongito M, Palaia R, Granata F, Lastoria S, Izzo F, Petrillo A (2017) Early radiological assessment of locally advanced pancreatic cancer treated with electrochemotherapy. World J Gastroenterol 23: 4767, doi: 10.3748/wjg.v23.i26.4767.

Hagen RM, Chedea VS, Mintoff CP, Bowler E, Morse HR, Ladomery MR (2013) Epigallocatechin-3-gallate promotes apoptosis and expression of the caspase 9a splice variant in PC3 prostate cancer cells. Int J Oncol 43: 194-200, doi:10.3892/ijo.2013.1920.

Heim KE, Tagliaferro AR, Bobilya DJ (2002) Flavonoid antioxidants: chemistry, metabolism and structure-activity relationships. J Nutr Biochem 13: 572–584.

Hong J, Lambert JD, Lee SH, Sinko PJ, Yang CS (2003) Involvement of multidrug resistance-associated proteins in regulating cellular levels of (-)-epigallocatechin-3-gallate and its methyl metabolites. Biochem Biophys Res Commun 310: 222–227, doi:10.1016/j.bbrc.2003.09.007.

Hosseinimehr SJ, Rostamnejad M, Ghaffari-rad V (2013) Epicatechin enhances anti-proliferative effect of bleomycin in ovarian cancer cell. Res Mol Med 1: 24–27.

Hussain T, Gupta S, Adhami VM, Mukhtar H (2005) Green tea constituent epigallocatechin-3-gallate selectively inhibits COX-2 without affecting COX-1 expression in human prostate carcinoma cells. Int J Cancer 113: 660–669, doi:10.1002/ijc.20629.

Ilic M, Ilic I (2016) Epidemiology of pancreatic cancer. World J Gastroenterol 22: 9694–9705, doi:10.3748/wjg.v22.i44.9694.

Imai K, Suga K, Nakachi K (1997) Cancer-Preventive Effects of Drinking Green Tea among a Japanese Population. Prev Med (Baltim) 26: 769–775.

Janle EM, Morré DM, Morré DJ, Zhou Q, Zhu Y (2008). Pharmacokinetics of green tea catechins in extract and sustained-release preparations. Journal of dietary supplements, J Diet Suppl 5: 248–263, doi:10.1080/19390210802414279.Pharmacokinetics.

Jiang P, Wu X, Wang X, Huang W, Feng Q (2016) NEAT1 upregulates EGCG-induced CTR1 to enhance cisplatin sensitivity in lung cancer cells. Oncotarget 7: 43337–43351, doi:10.18632/oncotarget.9712.

Jodoin J, Demeule M, Beliveau R (2002) Inhibition of the multidrug resistance P-glycoprotein activity by green tea polyphenols. Biochim Biophys Acta-Molecular Cell Res 1542: 149–159, doi:10.1016/s0167-4889(01)00175-6.

Katiyar SK, Mukhtar H (1997) Tea antioxidants in cancer chemoprevention. J Cell Biochem 67: 59–67, doi:10.1002/(SICI)1097-4644(1997)27+<59::AID-JCB11>3.0.CO;2-G.

Kim H-S, Quon MJ, Kim J (2014) New insights into the mechanisms of polyphenols beyond antioxidant properties; lessons from the green tea polyphenol, epigallocatechin 3-gallate. Redox Biol 2: 187–195, doi:10.1016/j.redox.2013.12.022.

Kitagawa S, Nabekura T, Kamiyama S (2004) Inhibition of P-glycoprotein function by tea catechins in KB-C2 cells. J Pharm Pharmacol 56: 1001–1005, doi:10.1211/0022357044003.

Kommalapati A, Tella SH, Goyal G, Ma WW, Mahipal A (2018) Contemporary Management of Localized Resectable Pancreatic Cancer. Cancers 10: 24, doi:10.3390/cancers10010024.

Kulbacka J, Daczewska M, Dubińska-Magiera M, Choromańska A, Rembiałkowska N, Surowiak P, Kulbacki M, Kotulska M, Saczko J (2014) Doxorubicin delivery enhanced by electroporation to gastrointestinal adenocarcinoma cells with P-gp overexpression. Bioelectrochemistry 100: 96–104, doi:10.1016/j.bioelechem.2014.03.013.

Lage H, Dietel M (2002) Multiple mechanisms confer different drug-resistant phenotypes in pancreatic carcinoma cells. J Cancer Res Clin Oncol 128: 349–357, doi:10.1007/s00432-002-0349-y.

Lee MJ, Maliakal P, Chen L, Meng X, Bondoc FY, Prabhu S, Lambert G, Mohr S, Yang CS (2002) Pharmacokinetics of tea catechins after ingestion of green tea and (-)-epigallocatechin-3-gallate by humans: Formation of different metabolites and individual variability. Cancer Epidemiol Biomarkers Prev 11: 1025–1032.

Li GX, Chen YK, Hou Z, Xiao H, Jin HY, Lu G, Lee MJ, Liu B, Guan F, Yang ZH, Yu A, Yang CS (2010) Pro-oxidative activities and dose-response relationship of (-)-epigallocatechin-3-gallate in the inhibition of lung cancer cell growth: a comparative study in vivo and in vitro. Carcinogenesis 31: 902–910, doi:10.1093/carcin/bgq039.

Li Y, Zhao S, Zhang W, Zhao P, He B, Wu N, Han P (2011) Epigallocatechin-3-O-gallate (EGCG) attenuates FFAs-induced peripheral insulin resistance through AMPK pathway and insulin signaling pathway in vivo. Diabetes Res Clin Pract 93: 205–214, doi:10.1016/J.DIABRES.2011.03.036.

Long J, Luo G Pei, Xiao Z Wen, Liu Z Qiang, Guo M, Liu L, Liu C, Xu J, Gao Y tang, Zheng Y, Wu C, Ni Q Xing, Li M, Yu X (2014) Cancer statistics: Current diagnosis and treatment of pancreatic cancer in Shanghai, China. Cancer Lett 346: 273–277, doi:10.1016/j.canlet.2014.01.004.

Martin RC, McFarland K, Ellis S, Velanovich V (2013) Irreversible electroporation in locally advanced

pancreatic cancer: Potential improved overall survival. Ann. Surg. Oncol. 20: 443–449.

Mazumder MEH, Beale P, Chan C, Yu JQ, Huq F (2012) Epigallocatechin gallate acts synergistically in combination with cisplatin and designed trans-palladiums in ovarian cancer cells. Anticancer Res 32: 4851–4860.

Meng J, Tong Q, Liu X, Yu Z, Zhang J, Gao B (2017) Epigallocatechin-3-gallate inhibits growth and induces apoptosis in esophageal cancer cells through the demethylation and reactivation of the p16 gene. Oncol Lett 14: 1152–1156, doi:10.3892/ol.2017.6248.

Nakagawa H, Hasumi K, Woo J-T, Nagai K, Wachi M (2004) Generation of hydrogen peroxide primarily contributes to the induction of Fe(II)-dependent apoptosis in Jurkat cells by (-)-epigallocatechin gallate. Carcinogenesis 25: 1567–1574, doi:10.1093/carcin/bgh168.

Neal RE, Rossmeisl JH, Garcia PA, Lanz OI, Henao-Guerrero N, Davalos R V. (2011) Successful Treatment of a Large Soft Tissue Sarcoma With Irreversible Electroporation. J Clin Oncol 29: e372–e377, doi:10.1200/JCO.2010.33.0902.

Patra SK, Rizzi F, Silva A, Rugina DO, Bettuzzi S (2008) Molecular targets of (-)-epigallocatechin-3-gallate (EGCG): specificity and interaction with membrane lipid rafts. J Physiol Pharmacol 59 Suppl 9: 217–235.

Procházková D, Boušová I, Wilhelmová N (2011) Antioxidant and prooxidant properties of flavonoids. Fitoterapia 82: 513–523, doi:10.1016/J.FITOTE.2011.01.018.

Qanungo S, Das M, Haldar S, Basu A (2005) Epigallocatechin-3-gallate induces mitochondrial membrane depolarization and caspase-dependent apoptosis in pancreatic cancer cells. Carcinogenesis 26: 958–967, doi:10.1093/carcin/bgi040.

Ramadass SK, Anantharaman NV, Subramanian S, Sivasubramanian S, Madhan B (2015) Paclitaxel/Epigallocatechin gallate coloaded liposome: A synergistic delivery to control the invasiveness of MDA-MB-231 breast cancer cells. Colloids Surfaces B Biointerfaces 125: 65–72, doi:10.1016/j.colsurfb.2014.11.005.

Ruarus A, Vroomen L, Puijk R, Scheffer H, Meijerink M (2018) Locally Advanced Pancreatic Cancer: A Review of Local Ablative Therapies. Cancers, 10: 16, doi:10.3390/cancers10010016.

Roy SK, Srivastava RK, Shankar S (2010) Inhibition of PI3K/AKT and MAPK/ERK pathways causes activation of FOXO transcription factor, leading to cell cycle arrest and apoptosis in pancreatic cancer. J Mol Signal 5: 10, doi:10.1186/1750-2187-5-10.

Sang SM, Lambert JD, Ho CT, Yang CS (2011) The chemistry and biotransformation of tea constituents. Pharmacol Res 64: 87–99, doi:10.1016/j.phrs.2011.02.007.

Sarma DN, Barrett ML, Chavez ML, Gardiner P, Ko R, Mahady GB, Marles RJ, Pellicore LS, Giancaspro GI, Low Dog T (2008) Safety of green tea extracts: A systematic review by the US Pharmacopeia. Drug Saf 31: 469–484, doi:10.2165/00002018-200831060-00003.

Schuijer M, Berns EMJJ (2003) TP53 and Ovarian Cancer. Hum Mutat 21: 285–291, doi:10.1002/humu.10181.

Shen G, Xu C, Hu R, Jain MR, Nair S, Lin W, Yang CS, Chan JY, Kong A-NT (2005) Comparison of (−)-Epigallocatechin-3-Gallate Elicited Liver and Small Intestine Gene Expression Profiles Between C57BL/6J Mice and C57BL/6J/Nrf2 (−/−) Mice. Pharm Res 22: 1805–1820, doi:10.1007/s11095-005-7546-8.

Shimizu M, Adachi S, Masuda M, Kozawa O, Moriwaki H (2011) Cancer chemoprevention with green tea catechins by targeting receptor tyrosine kinases. Mol Nutr Food Res 55: 832–843, doi:10.1002/mnfr.201000622.

Shimizu K, Asakawa T, Harada N, Fukumoto D, Tsukada H, Asai T, Yamada S, Kan T, Oku N (2014) Use of positron emission tomography for real-time imaging of biodistribution of green tea catechin. PLoS One 9: doi:10.1371/journal.pone.0085520.

Song Y, Sun H, Zhang A, Yan G, Han Y, Wang X (2014) Plant-derived natural products as leads to anti-cancer drugs. J Med Plant Herb Ther Res 2: 6–15.

Tang H, Zeng L, Wang J, Zhang X, Ruan Q (2017) Reversal of 5-fluorouracil resistance by EGCG is mediate by inactivation of TFAP2A / VEGF signaling pathway and down- regulation of MDR-1 and P-gp expression in gastric cancer. Oncotarget 8: 82842–82853.

Tao L, Park J, Lambert JD (2015) Differential prooxidative effects of the green tea polyphenol , (–) -epigallocatechin-3-gallate , in normal and oral cancer cells are related to differences in sirtuin 3 signaling. Mol Nutr Food Res 59: 203–211, doi:10.1002/mnfr.201400485.

Taubert D, Breitenbach T, Lazar A, Censarek P, Harlfinger S, Berkels R, Klaus W, Roesen R (2003) Reaction rate constants of superoxide scavenging by plant antioxidants. Free Radic Biol Med 35: 1599–1607, doi:10.1016/J.FREERADBIOMED.2003.09.005.

Ueda J, Saito N, Shimazu Y, Ozawa T (1996) A Comparison of Scavenging Abilities of Antioxidants against Hydroxyl Radicals. Arch Biochem Biophys 333: 377–384, doi:10.1006/ABBI.1996.0404.

Vroomen L, Petre EN, Cornelis FH, Solomon SB, Srimathveeravalli G (2017) Irreversible electroporation and thermal ablation of tumors in the liver, lung, kidney and bone: What are the differences? Diagn. Interv. Imaging 98: 609–617, doi:10.1016/j.diii.2017.07.007.

Wang X, Jiang P, Wang P, Yang CS, Wang X, Feng Q (2015) EGCG Enhances Cisplatin Sensitivity by Regulating Expression of the Copper and Cisplatin Influx Transporter CTR1 in Ovary Cancer. PLoS One 10: e0125402, doi:10.1371/journal.pone.0125402.

Wong MCS, Jiang JY, Liang M, Fang Y, Yeung MS, Sung JJY (2017) Global temporal patterns of pancreatic cancer and association with socioeconomic development. Sci Rep 7: 3165, doi:10.1038/s41598-017-02997-2.

Wu L, Zhang QL, Zhang XY, Lv C, Li J, Yuan Y, Yin FX (2012) Pharmacokinetics and blood-brain barrier penetration of (+)-Catechin and (-)-Epicatechin in rats by microdialysis sampling coupled to high-performance liquid chromatography with chemiluminescence detection. J Agric Food Chem 60: 9377–9383, doi:10.1021/jf301787f.

Yamamoto T, Lewis J, Wataha J, Dickinson D, Singh B, Bollag WB, Ueta E, Osaki T, Athar M, Schuster G, Hsu S (2004) Roles of catalase and hydrogen peroxide in green tea polyphenol-induced chemopreventive effects. J Pharmacol Exp Ther 308: 317–323, doi:10.1124/jpet.103.058891.

Yong Feng W (2006) Metabolism of Green Tea Catechins: An Overview. Curr Drug Metab 7: 755–809, doi:10.2174/138920006778520552.

Yuan C-H, Horng C-T, Lee C-F, Chiang N-N, Tsai F-J, Lu C-C, Chiang J-H, Hsu Y-M, Yang J-S, Chen F-A (2017) Epigallocatechin gallate sensitizes cisplatin-resistant oral cancer CAR cell apoptosis and autophagy through stimulating AKT/STAT3 pathway and suppressing multidrug resistance 1 signaling. Environ Toxicol 32: 845–855, doi:10.1002/tox.22284.

Zhang N, Zhang H, Xia L, Zheng Y, Yu Y, Zhu Y, Chen G, Di W (2009) NSC606985 induces apoptosis, exerts synergistic effects with cisplatin, and inhibits hypoxia-stabilized HIF-1 a protein in human ovarian cancer cells. Cancer Lett 278: 139–144, doi:10.1016/j.canlet.2008.12.025.

Zhang Q, Zeng L, Chen Y, Lian G, Qian C, Chen S, Li J, Huang K (2016) Pancreatic Cancer Epidemiology , Detection , and Management. Gastroenterology research and practice 2016, doi:10.1155/2016/8962321.

Zhang Y, Wang X, Han L, Zhou Y, Sun S (2015) Green tea polyphenol EGCG reverse cisplatin resistance of A549/DDP cell line through candidate genes demethylation. Biomed Pharmacother 69: 285–290, doi:10.1016/j.biopha.2014.12.016.

Zhu A, Wang X, Guo Z (2001) Study of tea polyphenol as a reversal agent for carcinoma cell lines ’ multidrug resistance (study of TP as a MDR reversal agent). Nucl Med Biol 28: 735–740.