Novel Anti-tumor Strategy for Breast Cancer: Synergistic Role of Oleuropein with Paclitaxel Therapeutic in MCF-7 Cells


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Abstract

Background:The side effects of conventional therapeutics pose a problem for cancer treatment. Recently, combination treatments with natural compounds have attracted attention regarding limiting the side effects of treatment. Oleuropein is a natural polyphenol in olives that has antioxidant and anticancer effects

Objective:This study aimed to investigate the oxidative stress effect of a combination of Paclitaxel, a chemotherapeutic agent, and Oleuropein in the MCF-7 cell line.

Method:The xCELLigence RTCA method was used to determine the cytotoxic effects of Oleuropein and Paclitaxel in the MCF-7 cell line. The Total Oxidant and Total Antioxidant Status were analyzed using a kit. The Oxidative Stress Index was calculated by measuring Total Oxidant and Total Antioxidant states. The levels of superoxide dismutase, reduced glutathione and malondialdehyde, which are oxidative stress markers, were also measured by ELISA assay kit.

Results:As a result of the measurement, IC50 doses of Oleuropein and Paclitaxel were determined as 230 µM and 7.5 µM, respectively. Different percentages of combination ratios were generated from the obtained IC50 values. The effect of oxidative stress was investigated at the combination rates of 10%, 20%, 30%, and 40% which were determined to be synergistic. In terms of the combined use of Oleuropein and Paclitaxel on oxidative stress, antioxidant defense increased, and Oxidative Stress Index levels decreased.

Conclusion:These findings demonstrate that the doses administered to the Oleuropein+Paclitaxel combination group were lower than those administered to groups using one agent alone (e.g. Paclitaxel), the results of which reduce the possibility of administering toxic doses.

About the authors

Gamze Yılmaz

Department of Biochemistry, Faculty of Pharmacy, Anadolu University

Email: info@benthamscience.net

Filiz Özdemir

Department of Biochemistry, Faculty of Pharmacy, Anadolu University

Author for correspondence.
Email: info@benthamscience.net

References

  1. Smolarz, B.; Nowak, A.Z.; Romanowicz, H. Breast cancer—epidemiology, classification, pathogenesis and treatment (Review of Literature). Cancers, 2022, 14(10), 2569. doi: 10.3390/cancers14102569 PMID: 35626173
  2. Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin., 2021, 71(3), 209-249. doi: 10.3322/caac.21660 PMID: 33538338
  3. Nguyen, L.H.; Goel, A.; Chung, D.C. Pathways of colorectal carcinogenesis. Gastroenterology, 2020, 158(2), 291-302. doi: 10.1053/j.gastro.2019.08.059 PMID: 31622622
  4. Peters, J.M.; Gonzalez, F.J. The evolution of carcinogenesis. Toxicol. Sci., 2018, 165(2), 272-276. doi: 10.1093/toxsci/kfy184 PMID: 30629266
  5. Agrawal, K.; Asthana, S.; Kumar, D. Role of oxidative stress in metabolic reprogramming of brain cancer. Cancers, 2023, 15(20), 4920. doi: 10.3390/cancers15204920 PMID: 37894287
  6. Liu, L.; Hou, Q.; Chen, B.; Lai, X.; Wang, H.; Liu, H.; Wu, L.; Liu, S.; Luo, K.; Liu, J. Identification of molecular subgroups and establishment of risk model based on the response to oxidative stress to predict overall survival of patients with lung adenocarcinoma. Eur. J. Med. Res., 2023, 28(1), 333. doi: 10.1186/s40001-023-01290-5 PMID: 37689745
  7. Peña-Oyarzun, D.; Bravo-Sagua, R.; Diaz-Vega, A.; Aleman, L.; Chiong, M.; Garcia, L.; Bambs, C.; Troncoso, R.; Cifuentes, M.; Morselli, E.; Ferreccio, C.; Quest, A.F.G.; Criollo, A.; Lavandero, S. Autophagy and oxidative stress in non-communicable diseases: A matter of the inflammatory state? Free Radic. Biol. Med., 2018, 124, 61-78. doi: 10.1016/j.freeradbiomed.2018.05.084 PMID: 29859344
  8. Georgescu, S.R.; Mitran, C.I.; Mitran, M.I.; Caruntu, C.; Sarbu, M.I.; Matei, C.; Nicolae, I.; Tocut, S.M.; Popa, M.I.; Tampa, M. New insights in the pathogenesis of hpv infection and the associated carcinogenic processes: The role of chronic inflammation and oxidative stress. J. Immunol. Res., 2018, 2018, 1-10. doi: 10.1155/2018/5315816 PMID: 30225270
  9. Sosa, V.; Moliné, T.; Somoza, R.; Paciucci, R.; Kondoh, H. LLeonart, M.E. Oxidative stress and cancer: An overview. Ageing Res. Rev., 2013, 12(1), 376-390. doi: 10.1016/j.arr.2012.10.004 PMID: 23123177
  10. Azmanova, M.; Pitto-Barry, A. Oxidative stress in cancer therapy: Friend or enemy? ChemBioChem, 2022, 23(10), e202100641. doi: 10.1002/cbic.202100641 PMID: 35015324
  11. Moo, T.A.; Sanford, R.; Dang, C.; Morrow, M. Overview of breast cancer therapy. PET Clin., 2018, 13(3), 339-354. doi: 10.1016/j.cpet.2018.02.006 PMID: 30100074
  12. Ye, F.; Dewanjee, S.; Li, Y.; Jha, N.K.; Chen, Z-S.; Kumar, A. Advancements in clinical aspects of targeted therapy and immunotherapy in breast cancer. Mol. Cancer, 2023, 22(1), 105. doi: 10.1186/s12943-023-01805-y PMID: 37415164
  13. Pons, D.G.; Nadal-Serrano, M.; Torrens-Mas, M.; Valle, A.; Oliver, J.; Roca, P. UCP2 inhibition sensitizes breast cancer cells to therapeutic agents by increasing oxidative stress. Free Radic. Biol. Med., 2015, 86, 67-77. doi: 10.1016/j.freeradbiomed.2015.04.032 PMID: 25960046
  14. Lewis-Wambi, J.S.; Kim, H.R.; Wambi, C.; Patel, R.; Pyle, J.R.; Klein-Szanto, A.J.; Jordan, V.C. Buthionine sulfoximine sensitizes antihormone-resistant human breast cancer cells to estrogen-induced apoptosis. Breast Cancer Res., 2008, 10(6), R104. doi: 10.1186/bcr2208 PMID: 19061505
  15. Wani, M.C.; Taylor, H.L.; Wall, M.E.; Coggon, P.; McPhail, A.T. Plant antitumor agents. VI. Isolation and structure of taxol, a novel antileukemic and antitumor agent from Taxus brevifolia. J. Am. Chem. Soc., 1971, 93(9), 2325-2327. doi: 10.1021/ja00738a045 PMID: 5553076
  16. Foley, E.A.; Kapoor, T.M. Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. Nat. Rev. Mol. Cell Biol., 2013, 14(1), 25-37. doi: 10.1038/nrm3494 PMID: 23258294
  17. Liao, P.C.; Lieu, C.H. Cell cycle specific induction of apoptosis and necrosis by paclitaxel in the leukemic U937 cells. Life Sci., 2005, 76(14), 1623-1639. doi: 10.1016/j.lfs.2004.09.021 PMID: 15680171
  18. Varbiro, G.; Veres, B.; Gallyas, F., Jr; Sumegi, B. Direct effect of Taxol on free radical formation and mitochondrial permeability transition. Free Radic. Biol. Med., 2001, 31(4), 548-558. doi: 10.1016/S0891-5849(01)00616-5 PMID: 11498288
  19. Yamamoto, Y.; Kawano, I.; Iwase, H. Nab-paclitaxel for the treatment of breast cancer: Efficacy, safety, and approval. OncoTargets Ther., 2011, 4, 123-136. doi: 10.2147/OTT.S13836 PMID: 21792318
  20. Vishnu, P.; Roy, V. Safety and efficacy of nab -paclitaxel in the treatment of patients with breast cancer. Breast Cancer, 2011, 5, BCBCR.S5857. doi: 10.4137/BCBCR.S5857 PMID: 21603258
  21. Yue, Q.X.; Liu, X.; Guo, D.A. Microtubule-binding natural products for cancer therapy. Planta Med., 2010, 76(11), 1037-1043. doi: 10.1055/s-0030-1250073 PMID: 20577942
  22. Li, W.B.; Li, Y.; Yu, C.; He, Y.M. Reversal of multidrug resistance by the chinese medicine yiqi jianpi huaji decoction and the mechanism of action in human gastric cancer SGC7901/VCR cells. Evid. Based Complement. Alternat. Med., 2015, 2015, 1-11. doi: 10.1155/2015/390812 PMID: 25705237
  23. Bach-Faig, A.; Berry, E.M.; Lairon, D.; Reguant, J.; Trichopoulou, A.; Dernini, S.; Medina, F.X.; Battino, M.; Belahsen, R.; Miranda, G.; Serra-Majem, L. Mediterranean diet pyramid today. Science and cultural updates. Public Health Nutr., 2011, 14(12A), 2274-2284. doi: 10.1017/S1368980011002515 PMID: 22166184
  24. García-Segovia, P.; Sánchez-Villegas, A.; Doreste, J.; Santana, F.; Serra-Majem, L. Olive oil consumption and risk of breast cancer in the Canary Islands: A population-based case–control study. Public Health Nutr., 2006, 9(1a), 163-167. doi: 10.1079/PHN2005940 PMID: 16512965
  25. La Vecchia, C.; Negri, E.; Franceschi, S.; Decarli, A.; Giacosa, A.; Lipworth, L. Olive oil, other dietary fats, and the risk of breast cancer (Italy). Cancer Causes Control, 1995, 6(6), 545-550. doi: 10.1007/BF00054164 PMID: 8580304
  26. de Lorgeril, M.; Salen, P.; Martin, J.L.; Monjaud, I.; Boucher, P.; Mamelle, N. Mediterranean dietary pattern in a randomized trial: Prolonged survival and possible reduced cancer rate. Arch. Intern. Med., 1998, 158(11), 1181-1187. doi: 10.1001/archinte.158.11.1181 PMID: 9625397
  27. Nediani, C.; Ruzzolini, J.; Romani, A.; Calorini, L. Oleuropein, a bioactive compound from Olea europaea L., as a potential preventive and therapeutic agent in non-communicable diseases. Antioxidants, 2019, 8(12), 578. doi: 10.3390/antiox8120578 PMID: 31766676
  28. Martínez-González, M.A.; Sayón-Orea, C.; Bullón-Vela, V.; Bes-Rastrollo, M.; Rodríguez-Artalejo, F.; Yusta-Boyo, M.J.; García-Solano, M. Effect of olive oil consumption on cardiovascular disease, cancer, type 2 diabetes, and all-cause mortality: A systematic review and meta-analysis. Clin. Nutr., 2022, 41(12), 2659-2682. doi: 10.1016/j.clnu.2022.10.001 PMID: 36343558
  29. Moral, R.; Escrich, E. Influence of olive oil and its components on breast cancer: Molecular mechanisms. Molecules, 2022, 27(2), 477. doi: 10.3390/molecules27020477 PMID: 35056792
  30. Mitra, S.; Dash, R. Natural products for the management and prevention of breast cancer. Evid. Based Complement. Alternat. Med., 2018, 2018, 1-23. doi: 10.1155/2018/8324696 PMID: 29681985
  31. Sznarkowska, A.; Kostecka, A.; Meller, K.; Bielawski, K.P. Inhibition of cancer antioxidant defense by natural compounds. Oncotarget, 2017, 8(9), 15996-16016. doi: 10.18632/oncotarget.13723 PMID: 27911871
  32. Panieri, E.; Santoro, M.M. ROS homeostasis and metabolism: A dangerous liason in cancer cells. Cell Death Dis., 2016, 7(6), e2253-e2253. doi: 10.1038/cddis.2016.105 PMID: 27277675
  33. Gikas, E.; Bazoti, F.N.; Tsarbopoulos, A. Conformation of oleuropein, the major bioactive compound of Olea europea. J. Mol. Struct. Theochem., 2007, 821(1-3), 125-132. doi: 10.1016/j.theochem.2007.06.033
  34. Servili, M.; Esposto, S.; Fabiani, R.; Urbani, S.; Taticchi, A.; Mariucci, F.; Selvaggini, R.; Montedoro, G.F. Phenolic compounds in olive oil: Antioxidant, health and organoleptic activities according to their chemical structure. Inflammopharmacology, 2009, 17(2), 76-84. doi: 10.1007/s10787-008-8014-y PMID: 19234678
  35. Cicerale, S.; Lucas, L.J.; Keast, R.S.J. Antimicrobial, antioxidant and anti-inflammatory phenolic activities in extra virgin olive oil. Curr. Opin. Biotechnol., 2012, 23(2), 129-135. doi: 10.1016/j.copbio.2011.09.006 PMID: 22000808
  36. Piroddi, M.; Albini, A.; Fabiani, R.; Giovannelli, L.; Luceri, C.; Natella, F.; Rosignoli, P.; Rossi, T.; Taticchi, A.; Servili, M.; Galli, F. Nutrigenomics of extra‐virgin olive oil: A review. Biofactors, 2017, 43(1), 17-41. doi: 10.1002/biof.1318 PMID: 27580701
  37. Delboccio, P.; Dideo, A.; Decurtis, A.; Celli, N.; Iacoviello, L.; Rotilio, D. Liquid chromatography–tandem mass spectrometry analysis of oleuropein and its metabolite hydroxytyrosol in rat plasma and urine after oral administration. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 2003, 785(1), 47-56. doi: 10.1016/S1570-0232(02)00853-X PMID: 12535837
  38. Kimura, Y.; Sumiyoshi, M. Olive leaf extract and its main component oleuropein prevent chronic ultraviolet B radiation-induced skin damage and carcinogenesis in hairless mice. J. Nutr., 2009, 139(11), 2079-2086. doi: 10.3945/jn.109.104992 PMID: 19776181
  39. Chou, T.C.; Talalay, P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv. Enzyme Regul., 1984, 22, 27-55. doi: 10.1016/0065-2571(84)90007-4 PMID: 6382953
  40. Chou, T.C. Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol. Rev., 2006, 58(3), 621-681. doi: 10.1124/pr.58.3.10 PMID: 16968952
  41. Erel, O. A new automated colorimetric method for measuring total oxidant status. Clin. Biochem., 2005, 38(12), 1103-1111. doi: 10.1016/j.clinbiochem.2005.08.008 PMID: 16214125
  42. Erel, O. A novel automated direct measurement method for total antioxidant capacity using a new generation, more stable ABTS radical cation. Clin. Biochem., 2004, 37(4), 277-285. doi: 10.1016/j.clinbiochem.2003.11.015 PMID: 15003729
  43. Altmann, K.H.; Gertsch, J. Anticancer drugs from nature—natural products as a unique source of new microtubule-stabilizing agents. Nat. Prod. Rep., 2007, 24(2), 327-357. doi: 10.1039/B515619J PMID: 17390000
  44. Haddad, R.; Alrabadi, N.; Altaani, B.; Li, T. Paclitaxel drug delivery systems: Focus on Nanocrystals’ surface modifications. Polymers, 2022, 14(4), 658. doi: 10.3390/polym14040658 PMID: 35215570
  45. Sparano, J.A.; Wang, M.; Martino, S.; Jones, V.; Perez, E.A.; Saphner, T.; Wolff, A.C.; Sledge, G.W., Jr; Wood, W.C.; Davidson, N.E. Weekly paclitaxel in the adjuvant treatment of breast cancer. N. Engl. J. Med., 2008, 358(16), 1663-1671. doi: 10.1056/NEJMoa0707056 PMID: 18420499
  46. Amjad, M.T.; Chidharla, A.; Kasi, A. Cancer Chemotherapy. In: StatPearls; StatPearls Publishing: Treasure Island, FL, 2022.
  47. Abu Samaan, T.M.; Samec, M.; Liskova, A.; Kubatka, P.; Büsselberg, D. Paclitaxel’s mechanistic and clinical effects on breast cancer. Biomolecules, 2019, 9(12), 789. doi: 10.3390/biom9120789 PMID: 31783552
  48. Fantini, M.; Benvenuto, M.; Masuelli, L.; Frajese, G.; Tresoldi, I.; Modesti, A.; Bei, R. In vitro and in vivo antitumoral effects of combinations of polyphenols, or polyphenols and anticancer drugs: perspectives on cancer treatment. Int. J. Mol. Sci., 2015, 16(12), 9236-9282. doi: 10.3390/ijms16059236 PMID: 25918934
  49. Nurgali, K.; Jagoe, R.T.; Abalo, R. Editorial: Adverse effects of cancer chemotherapy: Anything new to improve tolerance and reduce sequelae? Front. Pharmacol., 2018, 9, 245. doi: 10.3389/fphar.2018.00245 PMID: 29623040
  50. Escrich, E.; Moral, R.; Solanas, M. Olive oil, an essential component of the Mediterranean diet, and breast cancer. Public Health Nutr., 2011, 14(12A), 2323-2332. doi: 10.1017/S1368980011002588 PMID: 22166191
  51. Gorzynik-Debicka, M.; Przychodzen, P.; Cappello, F.; Kuban-Jankowska, A.; Marino, G.A.; Knap, N.; Wozniak, M.; Gorska-Ponikowska, M. Potential health benefits of olive oil and plant polyphenols. Int. J. Mol. Sci., 2018, 19(3), 686. doi: 10.3390/ijms19030686 PMID: 29495598
  52. Nenadis, N.; Papoti, V.T.; Tsimidou, M.Z. Bioactive ingredients in olive leaves. In: Olives and Olive Oil in Health and Disease Prevention; 2nd ed; Preedy, V.R.; Watson, R.R., Eds.; Academic Press: San Diego, 2021; p. 65-78. doi: 10.1016/B978-0-12-819528-4.00056-0
  53. Di Francesco, A.; Falconi, A.; Di Germanio, C.; Micioni Di Bonaventura, M.V.; Costa, A.; Caramuta, S.; Del Carlo, M.; Compagnone, D.; Dainese, E.; Cifani, C.; Maccarrone, M.; D’Addario, C. Extravirgin olive oil up-regulates CB1 tumor suppressor gene in human colon cancer cells and in rat colon via epigenetic mechanisms. J. Nutr. Biochem., 2015, 26(3), 250-258. doi: 10.1016/j.jnutbio.2014.10.013 PMID: 25533906
  54. Hassan, Z.K.; Elamin, M.H.; Daghestani, M.H.; Omer, S.A.; Al-Olayan, E.M.; Elobeid, M.A.; Virk, P.; Mohammed, O.B. Oleuropein induces anti-metastatic effects in breast cancer. Asian Pac. J. Cancer Prev., 2012, 13(9), 4555-4559. doi: 10.7314/APJCP.2012.13.9.4555 PMID: 23167379
  55. Žukovec Topalović D.; Živković L.; Čabarkapa, A.; Djelić N.; Bajić V.; Dekanski, D.; Spremo-Potparević B. Dry olive leaf extract counteracts L-thyroxine-induced genotoxicity in human peripheral blood leukocytes in vitro. Oxid. Med. Cell. Longev., 2015, 2015, 1-8. doi: 10.1155/2015/762192 PMID: 25789081
  56. Visioli, F.; Galli, C. Biological properties of olive oil phytochemicals. Crit. Rev. Food Sci. Nutr., 2002, 42(3), 209-221. doi: 10.1080/10408690290825529 PMID: 12058980
  57. Cao, S.; Zhu, X.; Du, L. P38 MAP kinase is involved in oleuropein-induced apoptosis in A549 cells by a mitochondrial apoptotic cascade. Biomed. Pharmacother., 2017, 95, 1425-1435. doi: 10.1016/j.biopha.2017.09.072 PMID: 28946190
  58. Elamin, M.H.; Daghestani, M.H.; Omer, S.A.; Elobeid, M.A.; Virk, P.; Al-Olayan, E.M.; Hassan, Z.K.; Mohammed, O.B.; Aboussekhra, A. Olive oil oleuropein has anti-breast cancer properties with higher efficiency on ER-negative cells. Food Chem. Toxicol., 2013, 53, 310-316. doi: 10.1016/j.fct.2012.12.009 PMID: 23261678
  59. Przychodzen, P.; Kuban-Jankowska, A.; Wyszkowska, R.; Barone, G.; Bosco, G.L.; Celso, F.L.; Kamm, A.; Daca, A.; Kostrzewa, T.; Gorska-Ponikowska, M. PTP1B phosphatase as a novel target of oleuropein activity in MCF-7 breast cancer model. Toxicol. In Vitro, 2019, 61, 104624. doi: 10.1016/j.tiv.2019.104624 PMID: 31419504
  60. Sirianni, R.; Chimento, A.; De Luca, A.; Casaburi, I.; Rizza, P.; Onofrio, A.; Iacopetta, D.; Puoci, F.; Andò, S.; Maggiolini, M.; Pezzi, V. Oleuropein and hydroxytyrosol inhibit MCF‐7 breast cancer cell proliferation interfering with ERK1/2 activation. Mol. Nutr. Food Res., 2010, 54(6), 833-840. doi: 10.1002/mnfr.200900111 PMID: 20013881
  61. Han, J.; Talorete, T.P.N.; Yamada, P.; Isoda, H. Anti-proliferative and apoptotic effects of oleuropein and hydroxytyrosol on human breast cancer MCF-7 cells. Cytotechnology, 2009, 59(1), 45-53. doi: 10.1007/s10616-009-9191-2 PMID: 19353300
  62. Sepporta, M.V.; Fuccelli, R.; Rosignoli, P.; Ricci, G.; Servili, M.; Morozzi, G.; Fabiani, R. Oleuropein inhibits tumour growth and metastases dissemination in ovariectomised nude mice with MCF-7 human breast tumour xenografts. J. Funct. Foods, 2014, 8, 269-273. doi: 10.1016/j.jff.2014.03.027
  63. Milanizadeh, S.; Bigdeli, M.R.; Rasoulian, B.; Amani, D. The effects of olive leaf extract on antioxidant enzymes activity and tumor growth in breast cancer. Thrita, 2014, 3(1), e12914. doi: 10.5812/thrita.12914
  64. Choupani, J.; Alivand, M.R.; Derakhshan, M.S.; Zaeifizadeh, M.; S. Khaniani, M. Oleuropein inhibits migration ability through suppression of epithelial-mesenchymal transition and synergistically enhances doxorubicin-mediated apoptosis in MCF-7 cells. J. Cell. Physiol., 2019, 234(6), 9093-9104. doi: 10.1002/jcp.27586 PMID: 30317622
  65. Barbaro, B.; Toietta, G.; Maggio, R.; Arciello, M.; Tarocchi, M.; Galli, A.; Balsano, C. Effects of the olive-derived polyphenol oleuropein on human health. Int. J. Mol. Sci., 2014, 15(10), 18508-18524. doi: 10.3390/ijms151018508 PMID: 25318054
  66. El-azem, N.; Pulido-Moran, M.; Ramirez-Tortosa, C.L.; Quiles, J.L.; Cara, F.E.; Sanchez-Rovira, P.; Granados-Principal, S.; Ramirez-Tortosa, M.C. Modulation by hydroxytyrosol of oxidative stress and antitumor activities of paclitaxel in breast cancer. Eur. J. Nutr., 2019, 58(3), 1203-1211. doi: 10.1007/s00394-018-1638-9 PMID: 29468462
  67. Arı M.; Karul, A.; Sakarya, S. Investigation of antiproliferative, apoptotic and antioxidant effects of oleuropein and vitamin D on breast cancer cell lines (MCF-7). Proceedings, 2018, 2, 1534. doi: 10.3390/proceedings2251534
  68. Milanizadeh, S.; Reza, B.M. Pro-apoptotic and anti-angiogenesis effects of olive leaf extract on spontaneous mouse mammary tumor model by balancing vascular endothelial growth factor and endostatin levels. Nutr. Cancer, 2019, 71(8), 1374-1381. doi: 10.1080/01635581.2019.1609054 PMID: 31074644
  69. Dalton, T.P.; Chen, Y.; Schneider, S.N.; Nebert, D.W.; Shertzer, H.G. Genetically altered mice to evaluate glutathione homeostasis in health and disease. Free Radic. Biol. Med., 2004, 37(10), 1511-1526. doi: 10.1016/j.freeradbiomed.2004.06.040 PMID: 15477003
  70. Estrela, J.M.; Ortega, A.; Obrador, E. Glutathione in cancer biology and therapy. Crit. Rev. Clin. Lab. Sci., 2006, 43(2), 143-181. doi: 10.1080/10408360500523878 PMID: 16517421
  71. Franco, R.; Cidlowski, J.A. Apoptosis and glutathione: Beyond an antioxidant. Cell Death Differ., 2009, 16(10), 1303-1314. doi: 10.1038/cdd.2009.107 PMID: 19662025
  72. Ortega, A.L.; Mena, S.; Estrela, J.M. Glutathione in cancer cell death. Cancers, 2011, 3(1), 1285-1310. doi: 10.3390/cancers3011285 PMID: 24212662
  73. Cui, X.Y.; Park, S.H.; Park, W.H. Anti-cancer effects of auranofin in human lung cancer cells by increasing intracellular ROS levels and depleting GSH levels. Molecules, 2022, 27(16), 5207. doi: 10.3390/molecules27165207 PMID: 36014444
  74. You, B.R.; Kim, S.Z.; Kim, S.H.; Park, W.H. Gallic acid-induced lung cancer cell death is accompanied by ROS increase and glutathione depletion. Mol. Cell. Biochem., 2011, 357(1-2), 295-303. doi: 10.1007/s11010-011-0900-8 PMID: 21625953
  75. Niki, E. Do antioxidants impair signaling by reactive oxygen species and lipid oxidation products? FEBS Lett., 2012, 586(21), 3767-3770. doi: 10.1016/j.febslet.2012.09.025 PMID: 23022561
  76. Celep, A.G.S.; Yilmaz, S.; Coruh, N. Antioxidant capacity and cytotoxicity of Aesculus hippocastanum on breast cancer MCF-7 cells. Yao Wu Shi Pin Fen Xi, 2012, 20. doi: 10.6227/jfda.2012200318
  77. Timur, M.; Akbas, S.H.; Ozben, T. The effect of Topotecan on oxidative stress in MCF-7 human breast cancer cell line. Acta Biochim. Pol., 2005, 52(4), 897-902. doi: 10.18388/abp.2005_3404 PMID: 16273129
  78. Wang, C.; Yu, J.; Wang, H.; Zhang, J.; Wu, N. Lipid peroxidation and altered anti-oxidant status in breast adenocarcinoma patients. Drug Res., 2014, 64(12), 690-692. doi: 10.1055/s-0034-1372580 PMID: 25050522
  79. de Oliveira, S.T.; Bessani, M.P.; Scandolara, T.B.; Silva, J.C.; Kawassaki, A.C.B.; Fagotti, P.A.F.; Maito, V.T.; de Souza, J.A.; Rech, D.; Panis, C. Systemic lipid peroxidation profile from patients with breast cancer changes according to the lymph nodal metastasis status. Oncoscience, 2022, 9, 1-10. doi: 10.18632/oncoscience.550 PMID: 35233438

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