The Impact of Fullerenes as Doxorubicin Nano-Transporters on Metallothionein and Superoxide Dismutase Status in MCF-10A Cells
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
2019/03/X/NZ7/01704 MINIATURA-3
National Science Center
PubMed
35056998
PubMed Central
PMC8777724
DOI
10.3390/pharmaceutics14010102
PII: pharmaceutics14010102
Knihovny.cz E-zdroje
- Klíčová slova
- doxorubicin, drug delivery system, epithelial cells, fullerenes, metallothionein, superoxide dismutase,
- Publikační typ
- časopisecké články MeSH
This study aimed to synthesise C60-DOX complexes followed by the analysis of their effect on the concentration of metallothionein (MT) as a non-enzymatic antioxidant and on the concentration and activity of superoxide dismutase (SOD) as an antioxidant enzyme in healthy human mammary MCF-10A cells. Dynamic light scattering and electrophoretic light scattering were used to establish the size and zeta potential of the complexes. The MT and SOD concentrations were determined using the ELISA method; SOD activity was determined by tetrazolium salt reduction inhibition. Lower MT concentration following exposure of cells to both DOX and C60 fullerene compared to the control sample was found. However, the concentration of this protein increased as a consequence of the C60-DOX complexes action on MCF-10A cells compared to the control. C60 used alone did not affect the concentration and activity of SOD in MCF-10A cells. Application of free DOX did not activate cellular antioxidant defence in the form of an increase in SOD concentration or its activity. In contrast treatment of cells with the C60-DOX complex resulted in a decrease in SOD1 concentration and a significant increase in SOD activity compared to cells treated with free DOX, C60 and control. Thus, it was found that C60-DOX complexes showed potential for protective effects against DOX-induced toxicity to MCF-10A cells.
BIOCEV 1st Faculty of Medicine Charles University Průmyslová 595 25250 Vestec Czech Republic
CONEM Metallomics Nanomedicine Research Group 116 36 Prague Czech Republic
Zobrazit více v PubMed
McGowan J.V., Chung R., Maulik A., Piotrowska I., Walker J.M., Yellon D.M. Anthracycline Chemotherapy and Cardiotoxicity. Cardiovasc. Drugs Ther. 2017;31:63–75. doi: 10.1007/s10557-016-6711-0. PubMed DOI PMC
Korbut R. Farmakologia. PZWL Wydawnictwo Lekarskie; Warszawa, Poland: 2017. pp. 240–248.
Pilco-Ferreto N., Calaf G.M. Influence of doxorubicin on apoptosis and oxidative stress in breast cancer cell lines. Int. J. Oncol. 2016;49:753–762. doi: 10.3892/ijo.2016.3558. PubMed DOI
International Agency for Research on Cancer. [(accessed on 23 September 2021)]. Available online: https://www.iarc.who.int/
Van der Zanden S.Y., Qiao X., Neefjes J. New insights into the activities and toxicities of the old anticancer drug doxorubicin. FEBS J. 2020;288:6095–6111. doi: 10.1111/febs.15583. PubMed DOI PMC
Tacar O., Sriamornsak P., Dass C.R. Doxorubicin: An update on anticancer molecular action, toxicity and novel drug delivery systems. J. Pharm. Pharmacol. 2013;65:157–170. doi: 10.1111/j.2042-7158.2012.01567.x. PubMed DOI
Kudryavtseva A.V., Krasnov G.S., Dmitriev A., Alekseev B.Y., Kardymon O., Sadritdinova A.F., Fedorova M.S., Pokrovsky A.V., Melnikova N.V., Kaprin A.D., et al. Mitochondrial dysfunction and oxidative stress in aging and cancer. Oncotarget. 2016;7:44879–44905. doi: 10.18632/oncotarget.9821. PubMed DOI PMC
Yang H., Villani R.M., Wang H., Simpson M.J., Roberts MS., Tang M., Liang X. The role of cellular reactive oxygen species in cancer chemotherapy. J. Exp. Clin. Cancer Res. 2018;37:266. doi: 10.1186/s13046-018-0909-x. PubMed DOI PMC
Borgstahl G.E.O., Oberley-Deegan R.E. Superoxide dismutases (SODs) and SOD mimetics. Antioxidants. 2018;7:156. doi: 10.3390/antiox7110156. PubMed DOI PMC
Weinberg F., Ramnath N., Nagrath D. Reactive oxygen species in the tumor. Cancers. 2019;11:1191. doi: 10.3390/cancers11081191. PubMed DOI PMC
Case A.J. On the origin of superoxide dismutase: An evolutionary perspective of superoxide-mediated redox signaling. Antioxidants. 2017;6:82. doi: 10.3390/antiox6040082. PubMed DOI PMC
Gałecka E., Jacewicz R., Mrowicka M., Gałecki P. Antioxidative enzymes-structure, properties, functions. Pol. Merkur. Lek. 2008;25:266–268. PubMed
Zaręba N., Kepinska M. The Function of Transthyretin Complexes with Metallothionein in Alzheimer’s Disease. Int. J. Mol. Sci. 2020;21:9003. doi: 10.3390/ijms21239003. PubMed DOI PMC
Ostrakhovitch E.A., Olsson P.E., Jiang S., Cherian M.G. Interaction of metallothionein with tumor suppressor p53 protein. FEBS Lett. 2006;580:1235–1238. doi: 10.1016/j.febslet.2006.01.036. PubMed DOI
Shimoda R., Achanzar W.E., Qu W., Nagamine T., Takagi H., Mori M., Waalkes M.P. Metallothionein is a potential negative regulator of apoptosis. Toxicol Sci. 2003;73:294–300. doi: 10.1093/toxsci/kfg095. PubMed DOI
Si M., Lang J. The roles of metallothioneins in carcinogenesis. J. Hematol. Oncol. 2018;11:107. doi: 10.1186/s13045-018-0645-x. PubMed DOI PMC
Lewandowski Ł., Kepinska M., Milnerowicz H. Alterations in Concentration/Activity of Superoxide Dismutases in Context of Obesity and Selected Single Nucleotide Polymorphisms in Genes: SOD1, SOD2, SOD3. Int. J. Mol. Sci. 2020;21:5069. doi: 10.3390/ijms21145069. PubMed DOI PMC
Lewandowski Ł., Kepinska M., Milnerowicz H. Inhibition of copper-zinc superoxide dismutase activity by selected environmental xenobiotics. Environ. Toxicol. Pharmacol. 2018;58:105–113. doi: 10.1016/j.etap.2017.12.022. PubMed DOI
Papa L., Hahn M., Marsh E.L., Evans B.S., Germain D. SOD2 to SOD1 switch in breast cancer. J. Biol. Chem. 2014;289:5412–5416. doi: 10.1074/jbc.C113.526475. PubMed DOI PMC
Papa L., Manfredi G., Germain D. SOD1, an unexpected novel target for cancer therapy. Genes Cancer. 2018;5:15–21. doi: 10.18632/genesandcancer.4. PubMed DOI PMC
Songbo M., Lang H., Xinyong C., Bin X., Ping Z., Liang S. Oxidative stress injury in doxorubicin-induced cardiotoxicity. Toxicol. Lett. 2019;307:41–48. doi: 10.1016/j.toxlet.2019.02.013. PubMed DOI
Gomari H., Moghadam M.F., Soleimani M., Ghavami M., Khodashenas S. Targeted delivery of doxorubicin to HER2 positive tumor models. Int. J. Nanomed. 2019;14:5679–5690. doi: 10.2147/IJN.S210731. PubMed DOI PMC
Rašović I. Water-soluble fullerenes for medical applications. Mater. Sci. Technol. 2016;33:777–794. doi: 10.1080/02670836.2016.1198114. DOI
Goodarzi S., da Ros T., Conde J., Sefat F., Mozafari M. Fullerene: Biomedical engineers get to revisit an old friend. Mater. Today. 2017;20:460–480. doi: 10.1016/j.mattod.2017.03.017. DOI
Castro E., Hernandez Garcia A., Zavala G., Echegoyen L. Fullerenes in Biology and Medicine. J. Mater. Chem. B. 2017;5:6523–6535. doi: 10.1039/C7TB00855D. PubMed DOI PMC
Kerna A., Pruitt K., Flores J., Nwokorie U. The application of fullerene derivatives in medicine and specific endocrinological conditions. EC Endocrinol. Metab. Res. 2020;5:56–66.
Mirkamali E.S., Ahmadi R., Kalateh K., Zarei G. Adsorption of melphalan anticancer drug on the surface of fullerene (C24): A comprehensive DFT study. Nanomed. J. 2019;6:112–119.
Kazemzadeh H., Mozafari M. Fullerene-based delivery systems. Drug Discov. Today. 2019;24:898–905. doi: 10.1016/j.drudis.2019.01.013. PubMed DOI
Misra C., Kumar M., Sharma G., Kumar R., Singh B., Katare O.P., Raza K. Glycinated fullerenes for tamoxifen intracellular delivery with improved anticancer activity and pharmacokinetics. Nanomedicine. 2017;12:1011–1023. doi: 10.2217/nnm-2016-0432. PubMed DOI
Lichota A., Krokosz A. Fullerenols in therapy and diagnosis of cancer. Med. Pr. 2016;67:817–831. doi: 10.13075/mp.5893.00466. PubMed DOI
Kepinska M., Kizek R., Milnerowicz H. Fullerene as a doxorubicin nanotransporter for targeted breast cancer therapy: Capillary electrophoresis analysis. Electrophoresis. 2018;39:2370–2379. doi: 10.1002/elps.201800148. PubMed DOI
Milnerowicz H., Bizoń A. Determination of metallothionein in biological fluids using enzyme-linked immunoassay with commercial antibody. Acta Bioch. Pol. 2010;57:99–104. doi: 10.18388/abp.2010_2379. PubMed DOI
Buzdar A.U. Preoperative chemotherapy treatment of breast cancer-A review. Cancer. 2007;110:2394–2407. doi: 10.1002/cncr.23083. PubMed DOI
Mahalingaiah P.K.S., Singh K.P. Chronic oxidative stress increases growth and tumorigenic potential of MCF-7 breast cancer cells. PLoS ONE. 2014;9:e87371. PubMed PMC
Prylutska S., Grynyuk I., Matyshevska O., Prylutskyy Y., Evstigneev M., Scharff P., Ritter U. C60 Fullerene as Synergistic Agent in Tumor-Inhibitory Doxorubicin Treatment. Drugs R D. 2014;14:333–340. doi: 10.1007/s40268-014-0074-4. PubMed DOI PMC
Prylutskyy Y.I., Evstigneev M.P., Pashkova I.S., Wyrzykowski D. Characterization of C 60 fullerene complexation with antibiotic doxorubicin. Phys. Chem. Chem. Phys. 2014;16:23164–23172. doi: 10.1039/C4CP03367A. PubMed DOI
Brant J. Aggregation and deposition characteristics of fullerene nanoparticles in aqueous systems. J. Nanoparticle Res. 2005;7:545–553. doi: 10.1007/s11051-005-4884-8. DOI
Alargova R.G., Deguchi S., Tsujii K. Stable colloidal dispersions of fullerenes in polar organic solvents. J. Am. Chem. Soc. 2001;123:10460–10467. doi: 10.1021/ja010202a. PubMed DOI
Kumar A., Dixit C.K. Advances in Nanomedicine for the Delivery of Therapeutic Nucleic Acids. Woodhead Publishing; Cambridge, UK: 2017. Methods for Characterization of Nanoparticles.
Joseph E., Singhvi G. Nanomaterials for Drug Delivery and Therapy. William Andrew Publishing; Norwich, NY, USA: 2019. Multifunctional Nanocrystals for Cancer Therapy: A Potential Nanocarrier; pp. 91–116.
Mchedlov-Petrossyan N.O., Klochkov V.K., Andrievsky G.V. Colloidal dispersions of fullerene C60 in water: Some properties and regularities of coagulation by electrolytes. J. Chem. Soc. Faraday Trans. 1997;93:4343–4346. doi: 10.1039/a705494g. DOI
Kepinska M., Kizek R., Milnerowicz H. Metallothionein and superoxide dismutase—Antioxidative protein status in fullerene-doxorubicin delivery to MCF-7 human breast cancer cells. Int. J. Mol. Sci. 2018;19:3253. doi: 10.3390/ijms19103253. PubMed DOI PMC
Ilghami R., Barzegari A., Mashayekhi M.R., Letourneur D., Crepin M., Pavon-Djavid G. The conundrum of dietary antioxidants in cancer chemotherapy. Nutr. Rev. 2020;78:65–76. doi: 10.1093/nutrit/nuz027. PubMed DOI
Gajewski E., Gaur S., Akman S.A., Matsumoto L., Balgooy J.N.A., Doroshow J.H. Oxidative DNA Base Damage in MCF-10A Breast Epithelial Cells at Clinically Achievable Concentrations of Doxorubicin. Biochem. Pharmacol. 2007;73:1947. doi: 10.1016/j.bcp.2007.03.022. PubMed DOI PMC
Aminipour Z., Khorshid M., Keshvari H., Bonakdar S., Wagner P., Van der Bruggen B. Passive permeability assay of doxorubicin through model cell membranes under cancerous and normal membrane potential conditions. Eur. J. Pharm. Biopharm. 2020;146:133–142. doi: 10.1016/j.ejpb.2019.10.011. PubMed DOI
Grebinyk A., Prylutska S., Chepurna O., Grebinyk S., Prylutskyy Y., Ritter U., Ohulchanskyy T.Y., Matyshevska O., Dandekar T., Frohme M. Synergy of Chemo- and Photodynamic Therapies with C60 Fullerene-Doxorubicin Nanocomplex. Nanomaterials. 2019;9:1540. doi: 10.3390/nano9111540. PubMed DOI PMC
Jing L., Li L., Zhao J., Sun Z., Peng S. Zinc-induced metallothionein overexpression prevents doxorubicin toxicity in cardiomyocytes by regulating the peroxiredoxins. Xenobiotica. 2016;46:715–725. doi: 10.3109/00498254.2015.1110760. PubMed DOI
Merlos Rodrigo M.A., Jimenez Jimemez A.M., Haddad Y., Bodoor K., Adam P., Krizkova S., Heger Z., Adam V. Metallothionein isoforms as double agents-Their roles in carcinogenesis, cancer progression and chemoresistance. Drug Resist Updat. 2020;52:100691. doi: 10.1016/j.drup.2020.100691. PubMed DOI
Srdjenovic B., Milic-Torres V., Grujic N., Stankov K., Djordjevic A., Vasovic V. Antioxidant properties of fullerenol C60(OH)24 in rat kidneys, testes, and lungs treated with doxorubicin. Toxicol. Mech. Methods. 2010;20:298–305. doi: 10.3109/15376516.2010.485622. PubMed DOI
Yeh Y.C., Lai H.C., Ting C.T., Lee W.L., Wang L.C., Wang K.Y., Lai H.C., Liu T.J. Protection by doxycycline against doxorubicin-induced oxidative stress and apoptosis in mouse testes. Biochem. Pharmacol. 2007;74:969–980. doi: 10.1016/j.bcp.2007.06.031. PubMed DOI
Ali S.S., Hardt J.I., Quick K.L., Sook Kim-Han J., Erlanger B.F., Huang T.T., Epstein C.J., Dugan L.L. A biologically effective fullerene (C 60) derivative with superoxide dismutase mimetic properties. Free Radic. Biol. Med. 2004;37:1191–1202. doi: 10.1016/j.freeradbiomed.2004.07.002. PubMed DOI