Purple tea catechins exhibit high antiproliferative activity and synergism with cisplatin against the triple-negative breast cancer cell line 4T1

Authors

  • Joseph Ndacyayisenga 1. Department of Molecular Biology and Biotechnology, Pan African University Institute for Basic Sciences, Technology and Innovation (PAUSTI), Nairobi, Kenya; 2. Department of Biotechnology, Institut d'Enseignement Supérieur de Ruhengeri (INES), Musanze, Rwanda https://orcid.org/0000-0002-2892-6134
  • Esther N. Maina Department of Biochemistry, College of Health Sciences, University of Nairobi, Nairobi, Kenya https://orcid.org/0000-0001-7171-2556
  • Lilian C. Ngeny Centre for Traditional Medicine and Drug Research, Kenya Medical Research Institute (KEMRI), Nairobi, Kenya https://orcid.org/0000-0002-7108-4462
  • Fred Wamunyokoli 1. Department of Molecular Biology and Biotechnology, Pan African University Institute for Basic Sciences, Technology and Innovation (PAUSTI), Nairobi, Kenya; 2. Department of Biochemistry, College of Health Sciences, Jomo Kenyatta University of Agriculture and Technology, Nairobi, Kenya
  • Festus M. Tolo Centre for Traditional Medicine and Drug Research, Kenya Medical Research Institute (KEMRI), Nairobi, Kenya

DOI:

https://doi.org/10.2298/ABS230816039N

Keywords:

tea catechins, tea clone, 4T1 cell line, combination index (CI), Dose Reduction Index (DRI)

Abstract

Paper Description:

  • Tea catechins are reported to have health benefits, that include free radical scavenging and anti-cancer activities. Their content in different tea clones and the effects of their combination with chemotherapy drugs are not well understood.
  • The concentrations of catechins in purple TRFK306 and BB35 tea clones from Rwanda and Kenya were determined, and the antiproliferative activity and synergism of the catechin extracts with cisplatin on the triple-negative breast cancer (TNBC) cell line (4T1) were evaluated.
  • Purple tea catechin extracts showed higher anti-proliferative activity and synergism with cisplatin.
  • Purple tea catechins reduced doses of cisplatin up to 3.7-fold, lowering cisplatin toxicity.

Abstract: The objectives of this study were the selection of the best tea clones with high catechin content among the known tea clones in Rwanda and Kenya, the examination of their antiproliferative effects on the triple-negative breast cancer (TNBC) cell line (4T1), and an evaluation of their combination index with cisplatin. The quantification of catechin contents in 14 different tea clones and 5 different processed teas was performed by high-performance liquid chromatography (HPLC). A comparative study of antiproliferative activities of catechin extracts from purple, TRFK306, and BB35 tea clones on the TNBC cell line (4T1) was undertaken, and their combination index (CI) with cisplatin and the dose reduction index (DRI) were determined. The catechin extract from BB35 had the highest concentration of total catechins (817.81±24.2 mg/g DW). After 72 h, the catechin extracts from TRFK306 showed a high IC50 of 68.68±3.30 µg/mL. The catechin extracts from TRFK306 showed the best synergism with cisplatin (CI=0.59), and they reduced the doses of cisplatin with the highest DRI=3.74493. Catechin extracts from purple tea showed higher antiproliferative activity and synergism with cisplatin against the TNBC cell line.

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References

Wachira F, Kamunya S, Karori S, Chalo R, Maritim T. The Tea Plants: Botanical Aspects. Tea Heal Dis Prev. 2013;(December):3-17. https://doi.org/10.1016/B978-0-12-384937-3.00001-X

Kumar Gupta V. Natural Products: Research Reviews. New Delhi: Daya Publishing House; 2016. p. 21-62.

Cherotich L, Kamunya SM, Alakonya A, Msomba SW, Uwimana MA, Wanyoko JK, Owuor PO. Variation in Catechin Composition of Popularly Cultivated Tea Clones in East Africa (Kenya). Am J Plant Sci. 2013;04(03):628-40. https://doi.org/10.4236/ajps.2013.43081

Samson Kamunya, Simon Ochanda E, Cheramgoi, Richard Chalo KS, Ogise Muku WK and JKB. Tea Growers Guide. Kenya Agric Livest Res Organ. 2019;

Leonida C, Kamunya SM, Alakonya A, Solomon MW, Uwimanna MA, Phillip OO. Characterization of 20 clones of tea (Camellia sinensis (L .) O . Kuntze) using ISSR and SSR markers. Agric Sci Res J. 2013;3:292-302.

Rana A, Sharma E, Rawat K, Sharma R, Verma S, Padwad Y, Gulati A. Screening and purification of catechins from underutilized tea plant parts and their bioactivity studies. J Food Sci Technol. 2016;53(11):4023-32. https://doi.org/10.1007/s13197-016-2406-6

Jiang Y, Jiang Z, Ma L, Huang Q. Advances in nanodelivery of green tea catechins to enhance the anticancer activity. Molecules. 2021;26(11): 3301. https://doi.org/10.3390/molecules26113301

UICC. GLOBOCAN 2020: New Global Cancer Data [Internet]. 2020 [cited 2023 Jul 21]. Available from: https://www.uicc.org/news/globocan-2020-new-global-cancer-data

Collignon J, Lousberg L, Schroeder H, Jerusalem G. Triple-negative breast cancer: Treatment challenges and solutions. Breast Cancer Targets Ther. 2016;8:93-107. https://doi.org/10.2147/BCTT.S69488

Mohamad NE, Abu N, Yeap SK, Alitheen NB. Bromelain Enhances the Anti-tumor Effects of Cisplatin on 4T1 Breast Tumor Model In Vivo. Integr Cancer Ther. 2019;18:1534735419880258. https://doi.org/10.1177/1534735419880258

Wang Q, Xu M, Sun Y, Chen J, Chen C, Qian C, Chen Y, Cao L, Xu Q, Du X, Yan W. Recent advances in therapeutic strategies for triple-negative breast cancer. Front Oncol. 2019;15(1):1-30. https://doi.org/10.1186/s13045-022-01341-0

Borah G, Bharali MK. Green tea catechins in combination with irinotecan attenuates tumorigenesis and treatment-associated toxicity in an inflammation-associated colon cancer mice model. J Egypt Natl Canc Inst. 2021;33(1):17. https://doi.org/10.1186/s43046-021-00074-4

Yin S-Y, Wei W-C, Jian F-Y, Yang N-S. Therapeutic Applications of Herbal Medicines for Cancer Patients. Evid Based Complement Alternat Med. 2013;2013:302426. https://doi.org/10.1155/2013/302426

Choung MG, Hwang YS, Lee MS, Lee J, Kang ST, Jun TH. Comparison of extraction and isolation efficiency of catechins and caffeine from green tea leaves using different solvent systems. Int J Food Sci Technol. 2014;49(6):1572-8. https://doi.org/10.1111/ijfs.12454

Theppakorn T, Wongsakul S. Optimization and Validation of the HPLC-Based Method for the Analysis of Gallic acid, Caffeine and 5 Catechins in Green Tea. Naresuan Univ J. 2012;20(2):1-11.

McGaw LJ, Elgorashi EE, Eloff JN. Cytotoxicity of African Medicinal Plants Against Normal Animal and Human Cells. Toxicol Surv African Med Plants. 2014;181-233. https://doi.org/10.1016/B978-0-12-800018-2.00008-X

Pauzi AZM, Yeap SK, Abu N, Lim KL, Omar AR, Aziz SA, Chow ALT, Subramani T, Tan SG, Alitheen NB. Combination of cisplatin and bromelain exerts synergistic cytotoxic effects against breast cancer cell line MDA-MB-231 in vitro. Chinese Med (United Kingdom). 2016;11(1):1-11. https://doi.org/10.1186/s13020-016-0118-5

Reuben Kitimu S, Kirira P, Sokei J, Ochwangi D, Mwitari P, Maina N. Biogenic synthesis of silver nanoparticles using Azadirachta indica methanolic bark extract and their antiproliferative activities against DU-145 human prostate cancer cells. African J Biotechnol. 2022;21(2):64-72.

Chou TC. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev. 2006;58(3):621-81. https://doi.org/10.1124/pr.58.3.10

Chou TC, Martin N. CompuSyn for Drug Combinations and for General Dose-Effect Analysis User's Guide. New Jersey: ComboSyn, Inc. Paramus; 2005.

Cherotich L, Kamunya SM, Alakonya A, Msomba SW, Uwimana MA, Wanyoko JK, Owuor PO. Variation in Catechin Composition of Popularly Cultivated Tea Clones in East Africa (Kenya). Am J Plant Sci. 2013;4(3):628-40. https://doi.org/10.4236/ajps.2013.43081

Hu B, Wang L, Zhou B, Zhang X, Sun Y, Ye H, Zhao L, Hu Q, Wang G, Zeng X. Efficient procedure for isolating methylated catechins from green tea and effective simultaneous analysis of ten catechins, three purine alkaloids, and gallic acid in tea by high-performance liquid chromatography with diode array detection. J Chromatogr A. 2009;1216(15):3223-31. https://doi.org/10.1016/j.chroma.2009.02.020

Alkan C, Coe P, Eichler E. Pharmacokinetics of Green Tea Catechins in Extract and Sustained-Release Preparations. Bone. 2011;23(1):1-7.

Nakai Y. Y. Differences in caffein, Flavanols and Amino acids contents in leaves of cultivated species of Camellia. Chem Pharm Bull. 1984;32(2):685-91.

Xiong L, Li J, Li Y, Yuan L, Liu S, Huang J, Liu Z. Dynamic changes in catechin levels and catechin biosynthesis-related gene expression in albino tea plants (Camellia sinensis L.). Plant Physiol Biochem. 2013;71:132-43. https://doi.org/10.1016/j.plaphy.2013.06.019

Shimoda H, Hitoe S, Nakamura S, Matsuda H. Purple tea and its extract suppress diet-induced fat accumulation in mice and human subjects by inhibiting fat absorption and enhancing hepatic carnitine palmitoyltransferase expression. Int J Biomed Sci. 2015;11(2):67-75. https://doi.org/10.59566/IJBS.2015.11067

Abdel-Aal ESM, Rabalski I, Mats L, Rai I. Identification and Quantification of Anthocyanin and Catechin Compounds in Purple Tea Leaves and Flakes. Molecules. 2022;27(19):6676. https://doi.org/10.3390/molecules27196676

Kerio LC, Wachira FN, Wanyoko JK, Rotich MK. Characterization of anthocyanins in Kenyan teas: Extraction and identification. Food Chem. 2012;131(1):31-8. https://doi.org/10.1016/j.foodchem.2011.08.005

Punyasiri PAN, Abeysinghe ISB, Kumar V, Treutter D, Duy D, Gosch C, Martens S, Forkmann G, Fischer TC. Flavonoid biosynthesis in the tea plant Camellia sinensis: Properties of enzymes of the prominent epicatechin and catechin pathways. Arch Biochem Biophys. 2004;431(1):22-30. https://doi.org/10.1016/j.abb.2004.08.003

Karori SM, Wachira FN, Wanyoko JK, Ngure RM. Antioxidant capacity of different types of tea products. African J Biotechnol. 2007;6(19):2287-96. https://doi.org/10.5897/AJB2007.000-2358

Tsai YJ, Chen BH. Preparation of catechin extracts and nanoemulsions from green tea leaf waste and their inhibition effect on prostate cancer cell PC-3. Int J Nanomedicine. 2016;11:1907-26. https://doi.org/10.2147/IJN.S103759

Przystupski D, Michel O, Rossowska J, Kwiatkowski S, Saczko J, Kulbacka J. The modulatory effect of green tea catechin on drug resistance in human ovarian cancer cells. Med Chem Res. 2019;28(5):657-67. https://doi.org/10.1007/s00044-019-02324-6

Bimonte S, Albino V, Piccirillo M, Nasto A, Molino C, Palaia R, Cascella M. Epigallocatechin-3-gallate in the prevention and treatment of hepatocellular carcinoma: Experimental findings and translational perspectives. Drug Des Devel Ther. 2019;13:611-21. https://doi.org/10.2147/DDDT.S180079

Hagen RM, Chedea VS, Mintoff CP, Bowler E, Morse HR, Ladomery MR. Epigallocatechin-3-gallate promotes apoptosis and expression of the caspase 9a splice variant in PC3 prostate cancer cells. Int J Oncol. 2013;43(1):194-200. https://doi.org/10.3892/ijo.2013.1920

Mayr C, Wagner A, Neureiter D, Pichler M, Jakab M, Illig R, Berr F, Kiesslich T. The green tea catechin epigallocatechin gallate induces cell cycle arrest and shows potential synergism with cisplatin in biliary tract cancer cells. BMC Complement Altern Med. 2015;15(1):1-7. https://doi.org/10.1186/s12906-015-0721-5

Keyes K, Cox K, Treadway P, Mann L, Shih C, Faul MM, Teicher BA. An in vitro tumor model: Analysis of angiogenic factor expression after chemotherapy. Cancer Res. 2002;62(19):5597-602.

Evans DM, Fang J, Silvers T, Delosh R, Laudeman J, Ogle C, Reinhart R, Selby M, Bowles L, Connelly J, Harris E, Krushkal J, Rubinstein L, Doroshow JH, Teicher BA. Exposure time versus cytotoxicity for anticancer agents. Cancer Chemother Pharmacol. 2019;84(2):359-71. https://doi.org/10.1007/s00280-019-03863-w

Indrayanto G, Putra GS, Suhud F. Validation of in-vitro bioassay methods: Application in herbal drug research. In: Al-Majed AA, editor. Profiles of Drug Substances, Excipients and Related Methodology. Elsevier; 2021. p. 273-307. https://doi.org/10.1016/bs.podrm.2020.07.005

Peña-Morán OA, Villarreal ML, Álvarez-Berber L, Meneses-Acosta A, Rodríguez-López V. Cytotoxicity, post-treatment recovery, and selectivity analysis of naturally occurring podophyllotoxins from Bursera fagaroides var. fagaroides on breast cancer cell lines. Molecules. 2016;21(8):1013. https://doi.org/10.3390/molecules21081013

Weerapreeyakul N, Nonpunya A, Barusrux S, Thitimetharoch T, Sripanidkulchai B. Evaluation of the anticancer potential of six herbs against a hepatoma cell line. Chinese Med (United Kingdom). 2012;7:1-7. https://doi.org/10.1186/1749-8546-7-15

Kaigongi MM, Lukhoba CW, Yaouba S, Makunga NP, Githiomi J, Yenesew A. In vitro antimicrobial and antiproliferative activities of the root bark extract and isolated chemical constituents of zanthoxylum paracanthum kokwaro (Rutaceae). Plants. 2020;9(7):920. https://doi.org/10.3390/plants9070920

Koch A, Tamez P, Pezzuto J, Soejarto D. Evaluation of plants used for antimalarial treatment by the Maasai of Kenya. J Ethnopharmacol. 2005;101(1-3):95-9. https://doi.org/10.1016/j.jep.2005.03.011

Kitimu SR, Kirira P, Abdille AA, Sokei J, Ochwang'i D, Mwitari P, Makanya A, Maina N. Anti-Angiogenic and Anti-Metastatic Effects of Biogenic Silver Nanoparticles Synthesized Using <i>Azadirachta indica</i> Adv Biosci Biotechnol. 2022;13(04):188-206. https://doi.org/10.4236/abb.2022.134010

Famuyide IM, Aro AO, Fasina FO, Eloff JN, McGaw LJ. Antibacterial and antibiofilm activity of acetone leaf extracts of nine under-investigated south African Eugenia and Syzygium (Myrtaceae) species and their selectivity indices. BMC Complement Altern Med. 2019;19(1):141. https://doi.org/10.1186/s12906-019-2547-z

Chou JH, Chou TC and TP. Conservation of laboratory animals by improved experimental design, generalized equations and computer analysis. Fed Proc. 1984;43:576.

JH CT and C. Theoretical basis and equations for three dimensional isobolograms for three drug combinations. FASEB J. 1992;6:A1590.

Min K, Kwon TK. Anticancer effects and molecular mechanisms of epigallocatechin-3-gallate. Integr Med Res. 2014;3(1):16-24. https://doi.org/10.1016/j.imr.2013.12.001

Tundo GR, Sbardella D, Ciaccio C, De Pascali S, Campanella V, Cozza P, Tarantino U, Coletta M, Fanizzi FP, Marini S. Effect of cisplatin on proteasome activity. J Inorg Biochem. 2015;153:253-8. https://doi.org/10.1016/j.jinorgbio.2015.08.027

Muir WW. Drug Interactions, Analgesic Protocols and Their Consequences, and Analgesic Drug Antagonism. Handb Vet Pain Manag Third Ed. 2015;335-55. https://doi.org/10.1016/B978-0-323-08935-7.00016-8

Chou J, Chou TC. Computerized simulation of dose reduction index (DRI) in synergistic drug combinations. Pharmacologist. 1988;30:A231.

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Published

2023-12-13

How to Cite

1.
Ndacyayisenga J, Maina EN, Ngeny LC, Wamunyokoli F, Tolo FM. Purple tea catechins exhibit high antiproliferative activity and synergism with cisplatin against the triple-negative breast cancer cell line 4T1. Arch Biol Sci [Internet]. 2023Dec.13 [cited 2024Apr.22];75(4):475-88. Available from: https://serbiosoc.org.rs/arch/index.php/abs/article/view/9000

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