188
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Investigation of the combined cytotoxicity induced by sodium butyrate and a flavonoid quercetin treatment on MCF-7 breast cancer cells

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon show all

References

  • Aiello, P., S. Consalvi, G. Poce, A. Raguzzini, E. Toti, M. Palmery, and I. Peluso. 2021. Dietary flavonoids: Nano delivery and nanoparticles for cancer therapy. Semin. Cancer Biol. 69:150–65. doi:10.1016/j.semcancer.2019.08.029.
  • Alam, S., T. Mohammad, R. A. Padder, M. I. Hassan, and M. Husain. 2022. Thymoquinone and quercetin induce enhanced apoptosis in non‐small cell lung cancer in combination through the Bax/Bcl2 cascade. J. Cell. Biochem. 123 (2):259–74. doi:10.1002/jcb.30162.
  • Azamjah, N., Y. Soltan-Zadeh, and F. Zayeri. 2019. Global trend of breast cancer mortality rate: A 25-year study. Asia Pac. J. Cancer Prev 20 (7):2015–20. doi:10.31557/APJCP.2019.20.7.2015.
  • Batiha, G. E., A. M. Beshbishy, M. Ikram, Z. S. Mulla, M. E. A. El-Hack, A. E. Taha, A. M. Algammal, and Y. H. A. Elewa. 2020. The pharmacological activity, biochemical properties, and pharmacokinetics of the major natural polyphenolic flavonoid: Quercetin. Foods 9 (3):374. doi:10.3390/foods9030374.
  • Boly, R., T. Gras, T. Lamkami, P. Guissou, D. Serteyn, R. Kiss, and J. Dubois. 2011. Quercetin inhibits a large panel of kinases implicated in cancer cell biology. Int. J. Oncol. 38 (3):833–42. doi:10.3892/ijo.2010.890.
  • Bouguellid, G., N. Debbache-Benaida, D. Atmani-Kilani, C. Russo, M. Lavorgna, C. Piscitelli, and D. Atmani. 2022. Pistacia lentiscus L. fruits showed promising antimutagenic and antigenotoxic activity using both in-vitro and in-vivo test systems. J. Toxicol. environ. Health A 85 (15):603–21. doi:10.1080/15287394.2022.2057885.
  • Calis, Z., R. Mogulkoc, and A. K. Baltaci. 2020. The roles of flavonols/flavonoids in neurodegeneration and neuroinflammation. Mini. Rev. Med. Chem 20 (15):1475–88. doi:10.2174/1389557519666190617150051.
  • Carullo, G., A. R. Cappello, L. Frattaruolo, M. Badolato, B. Armentano, and F. Aiello. 2017. Quercetin and derivatives: Useful tools in inflammation and pain management. Future Med. Chem 9 (1):79–93. doi:10.4155/fmc-2016-0186.
  • Chen, H. P., Y. T. Zhao, and T. C. Zhao. 2015. Histone deacetylases and mechanisms of regulation of gene expression. Crit. Rev. Oncog. 20 (1–2):35–47. doi:10.1615/CritRevOncog.2015012997.
  • Chien, S. Y., Y. C. Wu, J. G. Chung, J. S. Yang, H. F. Lu, M. F. Tsou, and D. R. Chen. 2009. Quercetin-induced apoptosis acts through mitochondrial-and caspase-3-dependent pathways in human breast cancer MDA-MB-231 cells. Human Exp. Toxicol 28 (8):493–503. doi:10.1177/0960327109107002.
  • Dabeek, W. M., and M. V. Marra. 2019. Dietary quercetin and kaempferol: Bioavailability and potential cardiovascular-related bioactivity in humans. Nutrients 11 (10):2288. doi:10.3390/nu11102288.
  • De Freitas, K. S., I. S. Squarisi, N. O. Acesio, H. D. Nicolella, S. D. Ozelin, M. Reis Santos de Melo, and D. C. Tavares. 2020. Licochalcone A, a licorice flavonoid: Antioxidant, cytotoxic, genotoxic, and chemopreventive potential. J. Toxicol. Environ. Health Part A 83 (21–22):673–86. doi:10.1080/15287394.2020.1813228.
  • Deveci Özkan, A., J. Alimudin, Y. Kilciler, B. Yuksel, O. Aksoy, and Z. Betts. 2022a. In vitro, chemo-protective effect of Eisenia foetida coelomic fluid against histone deacetylase inhibitor-induced oxidative toxicity in breast cancer cells. Int. J. Environ. Health Res 1–10. doi:10.1080/09603123.2022.2120970.
  • Deveci Ozkan, A., G. G. Eskiler, M. Sarihan, N. Kazan, O. Aksoy, B. Yuksel, and Z. Betts. 2022b. Anticancer properties of Eisenia foetida proteins in prostate cancer cells in vitro. Int. J. Peptide Res. Therap 28 (4):11. doi:10.1007/s10989-022-10428-8.
  • Ezzati, M., B. Yousefi, K. Velaei, and A. Safa. 2020. A review on anti-cancer properties of Quercetin in breast cancer. Life Sci. 248:117463. doi:10.1016/j.lfs.2020.117463.
  • Fidler, M. M., F. Bray, and I. Soerjomataram. 2018. The global cancer burden and human development: A review. Scand J. Public Health 46 (1):27–36. doi:10.1177/1403494817715400.
  • Franzoi, M. A., E. Agostinetto, M. Perachino, L. Del Mastro, E. de Azambuja, I. Vaz-Luis, and A. H. Partridge, M. Lambertini. 2021. Evidence-based approaches for the management of side-effects of adjuvant endocrine therapy in patients with breast cancer. Lancet Oncol. 22 (7):e303–e13. doi:10.1016/S1470-2045(20)30666-5.
  • Freire, J. S., B. C. dos Santos Fernandes, J. A. C. da Silva, J. R. da Silva Araújo, P. M. de Almeida, J. S. da Costa Júnior, F. A. Martins, S. D. L. de Freitas, and F. A. Martins. 2020. Phytochemical and antioxidant characterization, cytogenotoxicity and antigenotoxicity of the fractions of the ethanolic extract of in Poincianella bracteosa (Tul.) L.P. Queiroz. J. Toxicol. Environ. Health Part A 83 (23–24):730–47. doi:10.1080/15287394.2020.1824136.
  • Giuliano, A. E., J. L. Connolly, S. B. Edge, E. A. Mittendorf, H. S. Rugo, L. J. Solin, D. L. Weaver, D. J. Winchester, and G. N. Hortobagyi. 2017. Breast cancer major changes in the American joint committee on cancer eighth edition cancer staging manual. CA. Cancer J. Clin 67 (4):290–303. doi:10.3322/caac.21393.
  • Granato, M., C. Rizzello, M. S. Gilardini Montani, L. Cuomo, M. Vitillo, R. Santarelli, R. Gonnella, G. D’Orazi, A. Faggioni, and M. Cirone. 2017. Quercetin induces apoptosis and autophagy in primary effusion lymphoma cells by inhibiting PI3K/AKT/mTOR and STAT3 signalling pathways. J. Nutr. Biochem. 41:124–36. doi:10.1016/j.jnutbio.2016.12.011.
  • Haro-González, J. N., G. A. Castillo-Herrera, M. Martínez-Velázquez, and H. Espinosa-Andrews. 2021. Clove essential oil (Syzygium aromaticum L. Myrtaceae): Extraction, chemical composition, food applications, and essential bioactivity for human health. Molecules 26 (21):6387. doi:10.3390/molecules26216387.
  • Hashemzaei, M., A. Delarami Far, A. Yari, R. E. Heravi, K. Tabrizian, S. M. Taghdisi, S. E. Sadegh, K. Tsarouhas, D. Kouretas, G. Tzanakakis, et al. 2017. Anti-cancer and apoptosis-inducing effects of quercetin in vitro and in vivo. Oncol. Rep. 38 (2):819–28. doi:10.3892/or.2017.5766.
  • Ho, T. C., A. H. Chan, and A. Ganesan. 2020. Thirty years of HDAC inhibitors: 2020 insight and hindsight. J. Med. Chem. 63 (21):12460–84. doi:10.1021/acs.jmedchem.0c00830.
  • Jia, L., S. Huang, X. Yin, Y. Zan, Y. Gu, and L. Han. 2018. Quercetin suppresses the mobility of breast cancer by suppressing glycolysis through Akt-mTOR pathway-mediated autophagy induction. Life Sci. 208:123–30. doi:10.1016/j.lfs.2018.07.027.
  • Karlsson, H. J., M. Eriksson, E. Perzon, B. Akerman, P. Lincoln, and G. Westman. 2003. Groove-binding unsymmetrical cyanine dyes for staining of DNA: Syntheses and characterization of the DNA-binding. Nucl. Acids Res. 31 (21):6227–34. doi:10.1093/nar/gkg821.
  • Khan, H., H. Ullah, M. Aschner, W. S. Cheang, and E. K. Akkol. 2019. Neuroprotective effects of quercetin in Alzheimer’s disease. Biomolecules 10 (1):59. doi:10.3390/biom10010059.
  • Kopustinskiene, D. M., V. Jakstas, A. Savickas, and J. Bernatoniene. 2020. Flavonoids as anticancer agents. Nutrients 12 (2):457. doi:10.3390/nu12020457.
  • Koual, M., C. Tomkiewicz, G. Cano-Sancho, J. P. Antignac, A. S. Bats, and X. Coumoul. 2020. Environmental chemicals, breast cancer progression and drug resistance. Environ. Health 19 (1):117. doi:10.1186/s12940-020-00670-2.
  • Li, Y., S. Li, X. Meng, R. Y. Gan, J. J. Zhang, and H. B. Li. 2017. Dietary natural products for prevention and treatment of breast cancer. Nutrients 9 (7):728. doi:10.3390/nu9070728.
  • Li, L., Y. Sun, J. Liu, X. Wu, L. Chen, L. Ma, and P. Wu. 2015. Histone deacetylase inhibitor sodium butyrate suppresses DNA double strand break repair induced by etoposide more effectively in MCF-7 cells than in HEK293 cells. BMC Biochem. 16 (1):2. doi:10.1186/s12858-014-0030-5.
  • Liu, Y., W. Gong, Z. Y. Yang, X. S. Zhou, C. Gong, T. R. Zhang, X. Wei, D. Ma, F. Ye, and Q. L. Gao. 2017. Quercetin induces protective autophagy and apoptosis through ER stress via the p-STAT3/Bcl-2 axis in ovarian cancer. Apoptosis 22 (4):544–57. doi:10.1007/s10495-016-1334-2.
  • Liu, K., P. C. Liu, R. Liu, and X. Wu. 2015. Dual AO/EB staining to detect apoptosis in osteosarcoma cells compared with flow cytometry. Med. Sci. Monit. Basic Res 21:15–20. doi:10.12659/MSMBR.893327.
  • Li, Y., J. Yao, C. Han, J. Yang, M. T. Chaudhry, S. Wang, H. Liu, and Y. Yin. 2016. Quercetin, inflammation and immunity. Nutrients 8 (3):167. doi:10.3390/nu8030167.
  • Lortet‐Tieulent, J., D. Georges, F. Bray, and S. Vaccarella. 2020. Profiling global cancer incidence and mortality by socioeconomic development. Int. J. Cancer 147 (11):3029–36. doi:10.1002/ijc.33114.
  • Maurya, D., and P. K. Maurya. 2022. Health benefits of quercetin in age-related diseases. Molecules 27 (8):2498. doi:10.3390/molecules27082498.
  • Mirza-Aghazadeh-Attari, M., E. M. Ekrami, S. A. M. Aghdas, A. Mihanfar, S. Hallaj, B. Yousefi, and M. Majidinia. 2020. Targeting PI3K/Akt/mTOR signalling pathway by polyphenols: Implication for cancer therapy. Life Sci. 255:117481. doi:10.1016/j.lfs.2020.117481.
  • Mirza, B., C. R. Croley, M. Ahmad, J. Pumarol, N. Das, G. Sethi, and A. Bishayee. 2021. Mango (Mangifera indica L.): A magnificent plant with cancer preventive and anticancer therapeutic potential. Crit. Rev. Food Sci. Nutr 61 (13):2125–51. doi:10.1080/10408398.2020.1771678.
  • Mushtaq, M., H. V. Gaza, and E. V. Kashuba. 2016. Role of the RB-interacting proteins in stem cell biology. Adv. Cancer Res. 131:133–57.
  • Nourazarian, S. M., A. Nourazarian, M. Majidinia, and E. Roshaniasl. 2016. Effect of root extracts of medicinal herb Glycyrrhiza glabra on HSP90 gene expression and apoptosis in the HT-29 colon cancer cell line. Asian Pac. J. Cancer Prev. 16 (18):8563–66. doi:10.7314/APJCP.2015.16.18.8563.
  • Oboh, G., A. O. Ademosun, and O. B. Ogunsuyi. 2016. Quercetin and its role in chronic diseases. Adv. Exp. Med. Biol. 929:377–87.
  • Ozkan, A. D., Z. Betts, B. Yuksel, J. Alimudin, D. Aydin, and E. Guzel. 2023. Assessing in vitro anti-cancer efficacy of sulfonated water-soluble phthalocyanine on breast and prostate cancer cells. J. Porphyrins Phthalocyanines 27 (1n04):493–500. doi:10.1142/S1088424623500256.
  • Ozkan, A., and B. Yuksel. 2022. Poly I: C-Induced TLR3 activation on oxidative stress levels in MCF-7 (hormone-insensitive) and LNCAP (hormone-sensitive) as prostate cancer cells. J. Health Sci. Kocaeli Uni 8 (1):18–24. doi:10.30934/kusbed.915511.
  • Peng, B., C. Guo, H. Guan, S. Liu, and M. Z. Sun. 2014. Annexin A5 as a potential marker in tumours. Clin. Chim. Acta 427:42–48. doi:10.1016/j.cca.2013.09.048.
  • Qi, W., W. Qi, D. Xiong, and M. Long. 2022. Quercetin: Its antioxidant mechanism, antibacterial properties and potential application in prevention and control of toxicpathy. Molecules 27 (19):6545. doi:10.3390/molecules27196545.
  • Rajasekharan, S. K., S. Ramesh, and D. Bakkiyaraj. 2015. Synergy of flavonoids with HDAC inhibitor: New approach to target Candida tropicalis biofilms. J. Chemother 27 (4):246–49. doi:10.1179/1973947814Y.0000000186.
  • Rather, R. A., and M. Bhagat. 2020. Quercetin as an innovative therapeutic tool for cancer chemoprevention: Molecular mechanisms and implications in human health. Cancer. Med 9 (24):9181–92. doi:10.1002/cam4.1411.
  • Ren, M. X., X. H. Deng, F. Ai, G. Y. Yuan, and H. Y. Song. 2015. Effect of quercetin on the proliferation of the human ovarian cancer cell line SKOV-3 in vitro. Ther. Med 10 (2):579–83. doi:10.3892/etm.2015.2536.
  • Reyes-Farias, M., and C. Carrasco-Pozo. 2019. The anti-cancer effect of Quercetin: Molecular implications in cancer metabolism. Int. J. Mol. Sci 20 (13):3177. doi:10.3390/ijms20133177.
  • Salehi, B., L. Machin, L. Monzote, J. Sharifi-Rad, S. M. Ezzat, M. A. Salem, W. C. Cho, N. M. El Mahdy, C. S. Kılıç, and O. Sytar. 2020. Therapeutic potential of quercetin: New insights and perspectives for human health. ACS. Omega 5 (20):11849–72. doi:10.1021/acsomega.0c01818.
  • Salimi, V., Z. Shahsavari, B. Safizadeh, A. Hosseini, N. Khademian, and M. Tavakoli-Yaraki. 2017. Sodium butyrate promotes apoptosis in breast cancer cells through reactive oxygen species (ROS) formation and mitochondrial impairment. Lipids Health Dis. 16 (1):1–11. doi:10.1186/s12944-017-0593-4.
  • Selbach, M. T., A. S. Scotti, C. C. Feistel, C. C. Nicolau, D. Dalberto, N. G. Dos Santos, J. da Silva, A. B. F. Ferraz, I. Grivicich, and G. M. S. de Souza. 2021. Evaluation of the cytotoxic and genotoxic effects of Sida planicaulis Cav extract using human neuroblastoma cell line SH-SY5Y. J. Toxicol. Environ. Health Part A 84 (8):345–55. doi:10.1080/15287394.2020.1871144.
  • Shafabakhsh, R., and Z. Asemi. 2019. Quercetin: A natural compound for ovarian cancer treatment. J. Ovarian. Res 12 (1):55. doi:10.1186/s13048-019-0530-4.
  • Slika, H., H. Mansour, N. Wehbe, S. A. Nasser, R. Iratni, G. Nasrallah, and A. H. Eid. 2022. Therapeutic potential of flavonoids in cancer: ROS-mediated mechanisms. Biomed. Pharmacother. 146:112442. doi:10.1016/j.biopha.2021.112442.
  • Soufi, L., A. Farasat, H. Ahmadpour-Yazdi, L. Zolghadr, and N. Gheibi. 2021. The effects of the esterified Quercetin with omega-3 and omega-6 fatty acids on viability, nanomechanical properties, and BAX/BCL-2 gene expression in MCF-7 cells. Mol. Biol. Rep. 48 (6):5161–69. doi:10.1007/s11033-021-06516-5.
  • Sung, H., J. Ferlay, R. L. Siegel, M. Laversanne, I. Soerjomataram, A. Jemal, and F. Bray. 2021. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA. Cancer. J. Clin. 71 (3):209–49. doi:10.3322/caac.21660.
  • Suraweera, A., K. J. O’Byrne, and D. J. Richard. 2018. Combination therapy with histone deacetylase inhibitors (HDACi) for the treatment of cancer: Achieving the full therapeutic potential of HDACi. Front. Oncol 8:92. doi:10.3389/fonc.2018.00092.
  • Tang, S. M., X. T. Deng, J. Zhou, Q. P. Li, X. X. Ge, and L. Miao. 2020. Pharmacological basis and new insights of quercetin action in respect to its anti-cancer effects. Biomed. Pharmacother. 121:109604. doi:10.1016/j.biopha.2019.109604.
  • Taylor, M. A., F. Khathayer, and S. K. Ray. 2019. Quercetin and sodium butyrate synergistically increase apoptosis in rat C6 and human T98G glioblastoma cells through inhibition of autophagy. Neurochem. Res. 44 (7):1715–25. doi:10.1007/s11064-019-02802-8.
  • Teekaraman, D., S. P. Elayapillai, M. P. Viswanathan, and A. Jagadeesan. 2019. Quercetin inhibits human metastatic ovarian cancer cell growth and modulates components of the intrinsic apoptotic pathway in the PA-1 cell line. Chem. Biol. Interact. 300:91–100. doi:10.1016/j.cbi.2019.01.008.
  • Tu, S. H., L. C. Chen, and Y. S. Ho. 2017. An apple a day to prevent cancer formation: Reducing cancer risk with flavonoids. J. Food Drug Anal. 25 (1):119–24. doi:10.1016/j.jfda.2016.10.016.
  • Ullah, A., S. Munir, S. L. Badshah, N. Khan, L. Ghani, B. G. Poulson, A.-H. Emwas, and M. Jaremko. 2020. Important flavonoids and their role as a therapeutic agent. Molecules 25 (22):5243. doi:10.3390/molecules25225243.
  • Vafadar, A., Z. Shabaninejad, A. Movahedpour, F. Fallahi, M. Taghavipour, Y. Ghasemi, and H. Mirzaei. 2020. Quercetin and cancer: New insights into its therapeutic effects on ovarian cancer cells. Cell Biosci. 10 (1):1–17. doi:10.1186/s13578-020-00397-0.
  • Vargas, J. E., E. C. Filippi-Chiela, T. Suhre, F. C. Kipper, D. Bonatto, and G. Lenz. 2014. Inhibition of HDAC increases the senescence induced by natural polyphenols in glioma cells. Biochem. Cell Biol 92 (4):297–304. doi:10.1139/bcb-2014-0022.
  • Wang, K., R. Liu, J. Li, J. Mao, Y. Lei, J. Wu, J. Zeng, T. Zhang, H. Wu, L. Chen, et al. 2011. Quercetin induces protective autophagy in gastric cancer cells: Involvement of Akt-mTOR- and hypoxia-induced factor 1α-mediated signaling. Autophagy 7 (9):966–78. doi:10.4161/auto.7.9.15863.
  • Wilkinson, L., and T. Gathani. 2022. Understanding breast cancer as a global health concern. Br. J. Radiol 95 (1130):20211033. doi:10.1259/bjr.20211033.
  • Xu, D., M. J. Hu, Y. Q. Wang, and Y. L. Cui. 2019. Antioxidant activities of quercetin and its complexes for medicinal application. Molecules 24 (6):1123. doi:10.3390/molecules24061123.
  • Yarahmadi, A., F. Khademi, Z. Mostafavi-Pour, and F. Zal. 2018. In-vitro analysis of glucose and quercetin effects on m-TOR and Nrf-2 expression in HepG2 cell line (Diabetes and cancer Connection). Nutr. Cancer 70 (5):770–75. doi:10.1080/01635581.2018.1470654.
  • Yuksel, B., and A. D. Ozkan. 2021. The role of citrus nobiletin on oxidative stress levels and superoxide dismutase activities in metastatic castration-resistant prostate cancer. Commagene J. Biol 5:84–89. doi:10.31594/commagene.895415.
  • Yuksel, B., A. D. Ozkan, D. Aydın, and Z. Betts. 2022. Evaluation of sodium butyrate’s antioxidative and genotoxic effects on breast cancer cells. Saudi J. Biol. Sci. 29 (3):1394–401. doi:10.1016/j.sjbs.2021.12.061.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.