Caffeic acid stimulates breast cancer death through Reactive oxygen species (ROS) formation, Caspase activation and mitochondrial membrane potential depletion
-
Ali Karami Robati
,
Zahra Shahsavari
,
Mohammad Amin Vaezi
,
Banafsheh Safizadeh
,
Farzad Izak Shirian
,
Masoumeh Tavakoli-Yaraki
Abstract
Objectives: The aim of this study is to evaluate the potential effect of caffeic acid (CAF) on the growth of breast cancer cells, in addition to determining the contributing role of caspases, mitochondria, and oxidative status.
Methods: MCF-7 and MDA-MB-468 breast cancer cells were exposed to varying concentrations of CAF for different periods of time. The potential cytotoxic effect was measured using the MTT assay. The activities of caspase 3 and caspase 8, as well as the cellular level of reactive oxygen species (ROS) and the level of mitochondrial membrane potential (Δψm), were evaluated in different groups of cells.
Results: The findings showed that CAF decreased the percentage of MCF-7 and MDAMB-468 cells in a manner that depended on the dose and duration of exposure. The death of breast cancer cells induced by CAF was associated with an increase in ROS level in both cell lines. The decrease in mitochondrial membrane potential (Δψm) following CAF treatment suggests that mitochondrial dysfunction may be involved in the death of breast cancer cells induced by CAF. Importantly, the activity of caspase 8 increased after treatment, indicating the potential involvement of the extrinsic apoptosis pathway in the
inhibition of breast cancer cell growth by CAF. The dosage of 20μm of CAF following 48 hours of incubation appeared to have the most significant impact on breast cancer cells.
Conclusion: The study highlights the potential pro-apoptotic effect of CAF in both estrogen-positive and estrogen-negative breast cancer cells. This, in conjunction with other evidence, may lead to new insights for more effective therapeutic approaches in breast cancer.
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23. Katsura, C., I. Ogunmwonyi, H.K. Kankam, and S. Saha, Breast cancer: presentation, investigation and management. Br J Hosp Med (Lond), 2022. 83(2): p. 1-7.
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25. Duan, J., Y. Xiaokaiti, S. Fan, Y. Pan, X. Li, and X. Li, Direct interaction between caffeic acid phenethyl ester and human neutrophil elastase inhibits the growth and migration of PANC-1 cells. Oncol Rep, 2017. 37(5): p. 3019-3025.
26. Rosendahl, A.H., C.M. Perks, L. Zeng, A. Markkula, M. Simonsson, C. Rose, et al., Caffeine and Caffeic Acid Inhibit Growth and Modify Estrogen Receptor and Insulin-like Growth Factor I Receptor Levels in Human Breast Cancer. Clin Cancer Res, 2015. 21(8): p. 1877-87.
27. Michaluart, P., J.L. Masferrer, A.M. Carothers, K. Subbaramaiah, B.S. Zweifel, C. Koboldt, et al., Inhibitory effects of caffeic acid phenethyl ester on the activity and expression of cyclooxygenase-2 in human oral epithelial cells and in a rat model of inflammation. Cancer Res, 1999. 59(10): p. 2347-52.
28. Kumar, S., L. Dorstyn, and Y. Lim, The role of caspases as executioners of apoptosis. Biochem Soc Trans, 2022. 50(1): p. 33-45.
29. Kagawa, S., J. Gu, T. Honda, T.J. McDonnell, S.G. Swisher, J.A. Roth, et al., Deficiency of caspase-3 in MCF7 cells blocks Bax-mediated nuclear fragmentation but not cell death. Clin Cancer Res, 2001. 7(5): p. 1474-80.
30. Luo, Z., X. Xu, T. Sho, J. Zhang, W. Xu, J. Yao, et al., ROS-induced autophagy regulates porcine trophectoderm cell apoptosis, proliferation, and differentiation. Am J Physiol Cell Physiol, 2019. 316(2): p. C198-c209.
31. Yuan, L.Q., C. Wang, D.F. Lu, X.D. Zhao, L.H. Tan, and X. Chen, Induction of apoptosis and ferroptosis by a tumor suppressing magnetic field through ROS-mediated DNA damage. Aging (Albany NY), 2020. 12(4): p. 3662-3681.
2. Gonzalez-Angulo, A.M., F. Morales-Vasquez, and G.N. Hortobagyi, Overview of resistance to systemic therapy in patients with breast cancer. Adv Exp Med Biol, 2007. 608: p. 1-22.
3. Jafari-Hafshejani, F., K. Shahanipour, M. Kazemipiur, F. Seif, A. Jafari, M.N. Behbahani, et al., Curcumin Attenuates Oxidative Stress-Induced Effects on TGF-β Expression and NF-κB Signaling in Bovine Aortic Endothelial Cells. Acta Biochimica Iranica, 2023. 1(2): p. 90-95.
4. Guarneri, V. and P.F. Conte, The curability of breast cancer and the treatment of advanced disease. Eur J Nucl Med Mol Imaging, 2004. 31 Suppl 1: p. S149-61.
5. Ejlertsen, B., Adjuvant chemotherapy in early breast cancer. Dan Med J, 2016. 63(5).
6. Meshkani, R., H. Saberi, N. MohammadTaghvaei, and M.A. Tabatabaiefar, Estrogen receptor alpha gene polymorphisms are associated with type 2 diabetes and fasting glucose in male subjects. Molecular and cellular biochemistry, 2012. 359: p. 225-233.
7. Yarahmadi, S., Z. Abdolvahabi, Z. Hesari, M. Tavakoli-Yaraki, Z. Yousefi, P. Seiri, et al., Inhibition of sirtuin 1 deacetylase by miR-211-5p provides a mechanism for the induction of cell death in breast cancer cells. Gene, 2019. 711: p. 143939.
8. Jahangard, R.S.S.E., S. Vatannejad, A. Meshkani, R., Autophagy protects peripheral blood mononuclear cells from high glucose-induced inflammation and apoptosis. Acta Biochimica Iranica, 2023. 1(1): p. 40-49.
9. Kashyap, D., V.K. Garg, and N. Goel, Intrinsic and extrinsic pathways of apoptosis: Role in cancer development and prognosis. Adv Protein Chem Struct Biol, 2021. 125: p. 73-120.
10. Gorgani-Firuzjaee, s.M., R. , Resveratrol reduces high glucose-induced de-novo lipogenesis through mTOR mediated induction of autophagy in HepG2 cells. Acta Biochimica Iranica, 2023. 1(1): p. 32-39.
11. Barmoudeh, Z., M.H. Shahraki, H. Pourghadamyari, M.R. Borj, A.H. Doustimotlagh, and K. Abbaszadeh-Goudarzi, C1q tumor necrosis factor related proteins (CTRPs) in patients with cardiovascular diseases. Acta Biochimica Iranica, 2023. 1(1): p. 12-19.
12. Salimi, V., M. Shabani, M. Nourbakhsh, and M. Tavakoli-Yaraki, Involvement of 15-lipoxygenase-1 in the regulation of breast cancer cell death induced by sodium butyrate. Cytotechnology, 2016. 68(6): p. 2519-2528.
13. Ghahremani, H., A. Bahramzadeh, K. Bolandnazar, S. Emamgholipor, H. Hosseini, and R. Meshkani, Resveratrol as a potential protective compound against metabolic inflammation. Acta Biochimica Iranica, 2023. 1(2): p. 50-64.
14. Salimi, V., M. Tavakoli-Yaraki, M. Mahmoodi, S. Shahabi, M.J. Gharagozlou, F. Shokri, et al., The Oncolytic Effect of Respiratory Syncytial Virus (RSV) in Human Skin Cancer Cell Line, A431. Iran Red Crescent Med J, 2013. 15(1): p. 62-7.
15. Rajendra Prasad, N., A. Karthikeyan, S. Karthikeyan, and B.V. Reddy, Inhibitory effect of caffeic acid on cancer cell proliferation by oxidative mechanism in human HT-1080 fibrosarcoma cell line. Mol Cell Biochem, 2011. 349(1-2): p. 11-9.
16. Goodarzi, G., S.S. Tehrani, G. Panahi, A. Bahramzadeh, and R. Meshkani, Combination therapy of metformin and p-coumaric acid mitigates metabolic dysfunction associated with obesity and nonalcoholic fatty liver disease in high-fat diet obese C57BL/6 mice. The Journal of Nutritional Biochemistry, 2023. 118: p. 109369.
17. Arciszewska, Ż., S. Gama, M. Kalinowska, G. Świderski, R. Świsłocka, E. Gołębiewska, et al., Caffeic Acid/Eu(III) Complexes: Solution Equilibrium Studies, Structure Characterization and Biological Activity. Int J Mol Sci, 2022. 23(2).
18. Kinra, M., D. Arora, J. Mudgal, K.S.R. Pai, C. Mallikarjuna Rao, and M. Nampoothiri, Effect of Caffeic Acid on Ischemia-Reperfusion-Induced Acute Renal Failure in Rats. Pharmacology, 2019. 103(5-6): p. 315-319.
19. Zamani‐Garmsiri, F., S. Emamgholipour, S. Rahmani Fard, G. Ghasempour, R. Jahangard Ahvazi, and R. Meshkani, Polyphenols: potential anti‐inflammatory agents for treatment of metabolic disorders. Phytotherapy Research, 2022. 36(1): p. 415-432.
20. Russo, G.I., D. Campisi, M. Di Mauro, F. Regis, G. Reale, M. Marranzano, et al., Dietary Consumption of Phenolic Acids and Prostate Cancer: A Case-Control Study in Sicily, Southern Italy. Molecules, 2017. 22(12).
21. Min, J., H. Shen, W. Xi, Q. Wang, L. Yin, Y. Zhang, et al., Synergistic Anticancer Activity of Combined Use of Caffeic Acid with Paclitaxel Enhances Apoptosis of Non-Small-Cell Lung Cancer H1299 Cells in Vivo and in Vitro. Cell Physiol Biochem, 2018. 48(4): p. 1433-1442.
22. Pelinson, L.P., C.E. Assmann, T.V. Palma, I.B.M. da Cruz, M.M. Pillat, A. Mânica, et al., Antiproliferative and apoptotic effects of caffeic acid on SK-Mel-28 human melanoma cancer cells. Mol Biol Rep, 2019. 46(2): p. 2085-2092.
23. Katsura, C., I. Ogunmwonyi, H.K. Kankam, and S. Saha, Breast cancer: presentation, investigation and management. Br J Hosp Med (Lond), 2022. 83(2): p. 1-7.
24. Ben-Dror, J., M. Shalamov, and A. Sonnenblick, The History of Early Breast Cancer Treatment. Genes (Basel), 2022. 13(6).
25. Duan, J., Y. Xiaokaiti, S. Fan, Y. Pan, X. Li, and X. Li, Direct interaction between caffeic acid phenethyl ester and human neutrophil elastase inhibits the growth and migration of PANC-1 cells. Oncol Rep, 2017. 37(5): p. 3019-3025.
26. Rosendahl, A.H., C.M. Perks, L. Zeng, A. Markkula, M. Simonsson, C. Rose, et al., Caffeine and Caffeic Acid Inhibit Growth and Modify Estrogen Receptor and Insulin-like Growth Factor I Receptor Levels in Human Breast Cancer. Clin Cancer Res, 2015. 21(8): p. 1877-87.
27. Michaluart, P., J.L. Masferrer, A.M. Carothers, K. Subbaramaiah, B.S. Zweifel, C. Koboldt, et al., Inhibitory effects of caffeic acid phenethyl ester on the activity and expression of cyclooxygenase-2 in human oral epithelial cells and in a rat model of inflammation. Cancer Res, 1999. 59(10): p. 2347-52.
28. Kumar, S., L. Dorstyn, and Y. Lim, The role of caspases as executioners of apoptosis. Biochem Soc Trans, 2022. 50(1): p. 33-45.
29. Kagawa, S., J. Gu, T. Honda, T.J. McDonnell, S.G. Swisher, J.A. Roth, et al., Deficiency of caspase-3 in MCF7 cells blocks Bax-mediated nuclear fragmentation but not cell death. Clin Cancer Res, 2001. 7(5): p. 1474-80.
30. Luo, Z., X. Xu, T. Sho, J. Zhang, W. Xu, J. Yao, et al., ROS-induced autophagy regulates porcine trophectoderm cell apoptosis, proliferation, and differentiation. Am J Physiol Cell Physiol, 2019. 316(2): p. C198-c209.
31. Yuan, L.Q., C. Wang, D.F. Lu, X.D. Zhao, L.H. Tan, and X. Chen, Induction of apoptosis and ferroptosis by a tumor suppressing magnetic field through ROS-mediated DNA damage. Aging (Albany NY), 2020. 12(4): p. 3662-3681.
| Files | ||
| Issue | Vol 1 No 4 (2023) | |
| Section | Original Articles | |
| DOI | https://doi.org/10.18502/abi.v1i4.14719 | |
| Keywords | ||
| Caffeic acid Cytotoxicity Reactive oxygen species Caspase 3 Caspase 8 Mitochondrial Membrane Potential | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Karami Robati A, Shahsavari Z, Vaezi MA, Safizadeh B, Izak Shirian F, Tavakoli-Yaraki M. Caffeic acid stimulates breast cancer death through Reactive oxygen species (ROS) formation, Caspase activation and mitochondrial membrane potential depletion. ABI. 2023;1(4):176-182.
