Metallothionein and Superoxide Dismutase-Antioxidative Protein Status in Fullerene-Doxorubicin Delivery to MCF-7 Human Breast Cancer Cells

. 2018 Oct 20 ; 19 (10) : . [epub] 20181020

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid30347787

Grantová podpora
ST.D170.18.002 Uniwersytet Medyczny im. Piastów Slaskich we Wroclawiu

Doxorubicin (DOX) is one of the most frequently used anticancer drugs in breast cancer treatment. However, clinical applications of DOX are restricted, largely due to the fact that its action disturbs the pro/antioxidant balance in both cancerous and non-cancerous cells. The aim of this study was to investigate the influence of fullerene (C60) in cell treatment by DOX on the proliferation of human breast cancer cells (MCF-7), concentration of metallothionein (MT) and superoxide dismutase (SOD), and SOD activity in these cells. The use of C60 in complexes with DOX causes a change in the level of cell proliferation of about 5% more than when caused by DOX alone (from 60⁻65% to 70%). The use of C60 as a DOX nanotransporter reduced the MT level increase induced by DOX. C60 alone caused an increase of SOD1 concentration. On the other hand, it led to a decrease of SOD activity. C60 in complex with DOX caused a decrease of the DOX-induced SOD activity level. Exposure of MCF-7 cells to DOX-C60 complexes results in a decrease in viable cells and may become a new therapeutic approach to breast cancer. The effects of C60 in complexes with DOX on MCF-7 cells included a decreased enzymatic (SOD activity) and nonenzymatic (MT) antioxidant status, thus indicating their prooxidant role in MCF-7 cells.

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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. doi: 10.1371/journal.pone.0087371. PubMed DOI PMC

Liou G.-Y., Storz P. Reactive oxygen species in cancer. Free Radic. Res. 2010;44:479–496. doi: 10.3109/10715761003667554. PubMed DOI PMC

Gladyshev V.N. The free radical theory of aging is dead. Long live the damage theory! Antioxid. Redox Signal. 2014;20:727–731. doi: 10.1089/ars.2013.5228. PubMed DOI PMC

Waris G., Ahsan H. Reactive oxygen species: Role in the development of cancer and various chronic conditions. J. Carcinog. 2006;5:14. doi: 10.1186/1477-3163-5-14. PubMed DOI PMC

Kizek R., Adam V., Hrabeta J., Eckschlager T., Smutny S., Burda J.V., Frei E., Stiborova M. Anthracyclines and ellipticines as DNA-damaging anticancer drugs: Recent advances. Pharmacol. Ther. 2012;133:26–39. doi: 10.1016/j.pharmthera.2011.07.006. PubMed DOI

Heger Z., Rodrigo M.A.M., Krizkova S., Ruttkay-Nedecky B., Zalewska M., Del Pozo E.M.P., Pelfrene A., Pourrut B., Stiborova M., Eckschlager T., et al. Metallothionein as a scavenger of free radicals—New cardioprotective therapeutic agent or initiator of tumor chemoresistance? Curr. Drug Targets. 2016;17:1438–1451. doi: 10.2174/1389450116666151001113304. PubMed DOI

Zhu H., Sarkar S., Scott L., Danelisen I., Trush M.A., Jia Z., Li Y.R. Doxorubicin redox biology: Redox cycling, topoisomerase inhibition, and oxidative stress. React. Oxyg. Species. 2016;1:189–198. doi: 10.20455/ros.2016.835. PubMed DOI PMC

Skalickova S., Loffelmann M., Gargulak M., Kepinska M., Docekalova M., Uhlirova D., Stankova M., Fernandez C., Milnerowicz H., Ruttkay-Nedecky B., et al. Zinc-modified nanotransporter of doxorubicin for targeted prostate cancer delivery. Nanomaterials. 2017;7:435. doi: 10.3390/nano7120435. PubMed DOI 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

Singh R., Lillard J.W. Nanoparticle-based targeted drug delivery. Exp. Mol. Pathol. 2009;86:215–223. doi: 10.1016/j.yexmp.2008.12.004. PubMed DOI PMC

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

Chen Z., Ma L., Liu Y., Chen C. Applications of functionalized fullerenes in tumor theranostics. Theranostics. 2012;2:238–250. doi: 10.7150/thno.3509. PubMed DOI PMC

Milnerowicz H., Jabłonowska M., Bizoń A. Change of zinc, copper, and metallothionein concentrations and the copper-zinc superoxide dismutase activity in patients with pancreatitis. Pancreas. 2009;38:681–688. doi: 10.1097/MPA.0b013e3181a53d1. PubMed DOI

Ruttkay-Nedecky B., Nejdl L., Gumulec J., Zitka O., Masarik M., Eckschlager T., Stiborova M., Adam V., Kizek R. The role of metallothionein in oxidative stress. Int. J. Mol. Sci. 2013;14:6044–6066. doi: 10.3390/ijms14036044. PubMed DOI PMC

Zalewska M., Trefon J., Milnerowicz H. The role of metallothionein interactions with other proteins. Proteomics. 2014;14:1343–1356. doi: 10.1002/pmic.201300496. PubMed DOI

Bizoń A., Jędryczko K., Milnerowicz H. The role of metallothionein in oncogenesis and cancer treatment. Postepy Hig. Med. Dosw. 2017;71:98–109. doi: 10.5604/01.3001.0010.3794. PubMed DOI

Krizkova S., Kepinska M., Emri G., Eckschlager T., Stiborova M., Pokorna P., Heger Z., Adam V. An insight into the complex roles of metallothioneins in malignant diseases with emphasis on (sub)isoforms/isoforms and epigenetics phenomena. Pharmacol. Ther. 2018;183:90–117. doi: 10.1016/j.pharmthera.2017.10.004. PubMed DOI

Papa L., Manfredi G., Germain D. SOD1, an unexpected novel target for cancer therapy. Genes Cancer. 2014;5:15–21. doi: 10.18632/genesandcancer.4. PubMed DOI PMC

Mason R.P. Redox cycling of radical anion metabolites of toxic chemicals and drugs and the Marcus theory of electron transfer. Environ. Health Perspect. 1990;87:237–243. doi: 10.1289/ehp.9087237. PubMed DOI PMC

Panchuk R.R., Prylutska S.V., Chumakl V.V., Skorokhyd N.R., Lehka L.V., Evstigneev M.P., Prylutskyy Y.I., Berger W., Heffeter P., Scharff P., et al. Application of C60 fullerene-doxorubicin complex for tumor cell treatment in vitro and in vivo. J. Biomed. Nanotechnol. 2015;11:1139–1152. doi: 10.1166/jbn.2015.2058. PubMed DOI

Pelicano H., Lu W., Zhou Y., Zhang W., Chen Z., Hu Y., Huang P. Mitochondrial dysfunction and reactive oxygen species imbalance promote breast cancer cell motility through a CXCL14-mediated mechanism. Cancer Res. 2009;69:2375–2383. doi: 10.1158/0008-5472.CAN-08-3359. PubMed DOI PMC

Hosnedlova B., Kepinska M., Fernandez C., Peng Q., Ruttkay-Nedecky B., Milnerowicz H., Kizek R. Carbon nanomaterials for targeted cancer therapy drugs: A critical review. Chem. Rec. 2018 doi: 10.1002/tcr.201800038. PubMed DOI

Bakry R., Vallant R.M., Najam-ul-Haq M., Rainer M., Szabo Z., Huck C.W., Bonn G.K. Medicinal applications of fullerenes. Int. J. Nanomed. 2007;2:639–649. PubMed PMC

Chistyakov V.A., Smirnova Y.O., Prazdnova E.V., Soldatov A.V. Possible mechanisms of fullerene C60 antioxidant action. BioMed Res. Int. 2013;2013:1–4. doi: 10.1155/2013/821498. PubMed DOI PMC

Gharbi N., Pressac M., Hadchouel M., Szwarc H., Wilson S.R., Moussa F. Fullerene is a powerful antioxidant in vivo with no acute or subacute toxicity. Nano Lett. 2005;5:2578–2585. doi: 10.1021/nl051866b. PubMed DOI

Injac R., Perse M., Boskovic M., Djordjevic-Milic V., Djordjevic A., Hvala A., Cerar A., Strukelj B. Cardioprotective effects of fullerenol C60(OH)24 on a single dose doxorubicin-induced cardiotoxicity in rats with malignant neoplasm. Technol. Cancer Res. Treat. 2008;7:15–25. doi: 10.1177/153303460800700102. PubMed DOI

Montellano A., Da Ros T., Bianco A., Prato M. Fullerene C₆₀ as a multifunctional system for drug and gene delivery. Nanoscale. 2011;3:4035–4041. doi: 10.1039/c1nr10783f. PubMed DOI

Meng H., Xing G., Sun B., Zhao F., Lei H., Li W., Song Y., Chen Z., Yuan H., Wang X., et al. Potent angiogenesis inhibition by the particulate form of fullerene derivatives. ACS Nano. 2010;4:2773–2783. doi: 10.1021/nn100448z. PubMed DOI

Gewirtz D.A. A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin. Biochem. Pharmacol. 1999;57:727–741. doi: 10.1016/S0006-2952(98)00307-4. PubMed DOI

Wang G.W., Klein J.B., Kang Y.J. Metallothionein inhibits doxorubicin-induced mitochondrial cytochrome c release and caspase-3 activation in cardiomyocytes. J. Pharmacol. Exp. Ther. 2001;298:461–468. PubMed

Wierzowiecka B., Gomulkiewicz A., Cwynar-Zajac L., Olbromski M., Grzegrzolka J., Kobierzycki C., Podhorska-Okolow M., Dziegiel P. Expression of metallothionein and vascular endothelial growth factor isoforms in breast cancer cells. In Vivo. 2016;30:271–278. PubMed

Cherian M.G., Jayasurya A., Bay B.-H. Metallothioneins in human tumors and potential roles in carcinogenesis. Mutat. Res. 2003;533:201–209. doi: 10.1016/j.mrfmmm.2003.07.013. PubMed DOI

Kim H.G., Kim J.Y., Han E.H., Hwang Y.P., Choi J.H., Park B.H., Jeong H.G. Metallothionein-2A overexpression increases the expression of matrix metalloproteinase-9 and invasion of breast cancer cells. FEBS Lett. 2011;585:421–428. doi: 10.1016/j.febslet.2010.12.030. PubMed DOI

Abdel-Mageed A., Agrawal K.C. Antisense down-regulation of metallothionein induces growth arrest and apoptosis in human breast carcinoma cells. Cancer Gene Ther. 1997;4:199–207. PubMed

Jin R., Chow V.T.-K., Tan P.-H., Dheen S.T., Duan W., Bay B.-H. Metallothionein 2A expression is associated with cell proliferation in breast cancer. Carcinogenesis. 2002;23:81–86. doi: 10.1093/carcin/23.1.81. PubMed DOI

Lim D., Jocelyn K.M.-X., Yip G.W.-C., Bay B.-H. Silencing the Metallothionein-2A gene inhibits cell cycle progression from G1- to S-phase involving ATM and cdc25A signaling in breast cancer cells. Cancer Lett. 2009;276:109–117. doi: 10.1016/j.canlet.2008.10.038. PubMed DOI

Lai Y., Lim D., Tan P.-H., Leung T.K.-C., Yip G.W.-C., Bay B.-H. Silencing the metallothionein-2A gene induces entosis in adherent MCF-7 breast cancer cells. Anat. Rec. 2010;293:1685–1691. doi: 10.1002/ar.21215. PubMed DOI

Mehta A., Flora S.J. Possible role of metal redistribution, hepatotoxicity and oxidative stress in chelating agents induced hepatic and renal metallothionein in rats. Food Chem. Toxicol. 2001;39:1029–1038. doi: 10.1016/S0278-6915(01)00046-1. PubMed DOI

Sun X., Zhou Z., Kang Y.J. Attenuation of doxorubicin chronic toxicity in metallothionein-overexpressing transgenic mouse heart. Cancer Res. 2001;61:3382–3387. PubMed

Jacob C., Maret W., Vallee B.L. Control of zinc transfer between thionein, metallothionein, and zinc proteins. Proc. Natl. Acad. Sci. USA. 1998;95:3489–3494. doi: 10.1073/pnas.95.7.3489. PubMed DOI PMC

Yin X., Wu H., Chen Y., Kang Y.J. Induction of antioxidants by adriamycin in mouse heart. Biochem. Pharmacol. 1998;56:87–93. doi: 10.1016/S0006-2952(98)00099-9. PubMed DOI

Doroshow J.H. Role of hydrogen peroxide and hydroxyl radical formation in the killing of Ehrlich tumor cells by anticancer quinones. Proc. Natl. Acad. Sci. USA. 1986;83:4514–4518. doi: 10.1073/pnas.83.12.4514. PubMed DOI PMC

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;52:897–902. PubMed

Doroshow J.H., Akman S., Esworthy S., Chu F.F., Burke T. Doxorubicin resistance conferred by selective enhancement of intracellular glutathione peroxidase or superoxide dismutase content in human MCF-7 breast cancer cells. Free Radic. Res. Commun. 1991;13:779–781. doi: 10.3109/10715769109145859. PubMed DOI

Ravid A., Rocker D., Machlenkin A., Rotem C., Hochman A., Kessler-Icekson G., Liberman U.A., Koren R. 1,25-Dihydroxyvitamin D3 enhances the susceptibility of breast cancer cells to doxorubicin-induced oxidative damage. Cancer Res. 1999;59:862–867. PubMed

Awasthi K.K., John P.J., Awasthi A., Awasthi K. Multi walled carbon nano tubes induced hepatotoxicity in Swiss albino mice. Micron. 2013;44:359–364. doi: 10.1016/j.micron.2012.08.008. PubMed DOI

Prylutska S.V., Grynyuk I.I., Matyshevska O.P., Prylutskyy Y.I., Ritter U., Scharff P. Anti-oxidant properties of C60 fullerenes in vitro. Fuller. Nanotub. Car. Nanostr. 2008;16:698–705. doi: 10.1080/15363830802317148. DOI

Kaliszewski M., Kennedy A.K., Blaes S.L., Shaffer R.S., Knott A.B., Song W., Hauser H.A., Bossy B., Huang T.-T., Bossy-Wetzel E. SOD1 Lysine 123 acetylation in the adult central nervous system. Front. Cell. Neurosci. 2016;10 doi: 10.3389/fncel.2016.00287. PubMed DOI PMC

Hitchler M.J., Domann F.E. Regulation of CuZnSOD and its redox signaling potential: Implications for amyotrophic lateral sclerosis. Antioxid. Redox Signal. 2014;20:1590–1598. doi: 10.1089/ars.2013.5385. PubMed DOI PMC

Carroll M.C., Girouard J.B., Ulloa J.L., Subramaniam J.R., Wong P.C., Valentine J.S., Culotta V.C. Mechanisms for activating Cu- and Zn-containing superoxide dismutase in the absence of the CCS Cu chaperone. Proc. Natl. Acad. Sci. USA. 2004;101:5964–5969. doi: 10.1073/pnas.0308298101. PubMed DOI PMC

Culotta V.C., Yang M., O’Halloran T.V. Activation of superoxide dismutases: Putting the metal to the pedal. Biochim. Biophys. Acta Mol. Cell Res. 2006;1763:747–758. doi: 10.1016/j.bbamcr.2006.05.003. PubMed DOI PMC

Vonk W.I.M., Wijmenga C., Berger R., van de Sluis B., Klomp L.W.J. Cu,Zn Superoxide dismutase maturation and activity are regulated by COMMD1. J. Biol. Chem. 2010;285:28991–29000. doi: 10.1074/jbc.M110.101477. PubMed DOI PMC

Innocenti A., Durdagi S., Doostdar N., Strom T.A., Barron A.R., Supuran C.T. Nanoscale enzyme inhibitors: Fullerenes inhibit carbonic anhydrase by occluding the active site entrance. Bioorg. Med. Chem. 2010;18:2822–2828. doi: 10.1016/j.bmc.2010.03.026. PubMed DOI

Vapa I., Torres V.M., Djordjevic A., Vasovic V., Srdjenovic B., Simic V.D., Popovic J.K. Effect of fullerenol C60(OH)24 on lipid peroxidation of kidneys, testes and lungs in rats treated with doxorubicine. Eur. J. Drug Metab. Pharmacokinet. 2012;37:301. doi: 10.1007/s13318-012-0092-y. PubMed DOI

Rao A.K., Ziegler Y.S., McLeod I.X., Yates J.R., Nardulli A.M. Effects of Cu/Zn superoxide dismutase on estrogen responsiveness and oxidative stress in human breast cancer cells. Mol. Endocrinol. 2008;22:1113–1124. doi: 10.1210/me.2007-0381. PubMed DOI PMC

Glasauer A., Sena L.A., Diebold L.P., Mazar A.P., Chandel N.S. Targeting SOD1 reduces experimental non–small-cell lung cancer. J. Clin. Investig. 2014;124:117–128. doi: 10.1172/JCI71714. PubMed DOI PMC

Milnerowicz H., Bizoń A. Determination of metallothionein in biological fluids using enzyme-linked immunoassay with commercial antibody. Acta Biochim. Pol. 2010;57:99–104. PubMed

Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976;72:248–254. doi: 10.1016/0003-2697(76)90527-3. PubMed DOI

Misra H.P., Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J. Biol. Chem. 1972;247:3170–3175. PubMed

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