Modulation of induced cytotoxicity of doxorubicin by using apoferritin and liposomal cages

. 2014 Dec 11 ; 15 (12) : 22960-77. [epub] 20141211

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid25514405

Doxorubicin is an effective chemotherapeutic drug, however, its toxicity is a significant limitation in therapy. Encapsulation of doxorubicin inside liposomes or ferritin cages decreases cardiotoxicity while maintaining anticancer potency. We synthesized novel apoferritin- and liposome-encapsulated forms of doxorubicin ("Apodox" and "lip-8-dox") and compared its toxicity with doxorubicin and Myocet on prostate cell lines. Three different prostatic cell lines PNT1A, 22Rv1, and LNCaP were chosen. The toxicity of the modified doxorubicin forms was compared to conventional doxorubicin using the MTT assay, real-time cell impedance-based cell growth method (RTCA), and flow cytometry. The efficiency of doxorubicin entrapment was 56% in apoferritin cages and 42% in the liposome carrier. The accuracy of the RTCA system was verified by flow-cytometric analysis of cell viability. The doxorubicin half maximal inhibition concentrations (IC50) were determined as 170.5, 234.0, and 169.0 nM for PNT1A, 22Rv1, and LNCaP, respectively by RTCA. Lip8-dox is less toxic on the non-tumor cell line PNT1A compared to doxorubicin, while still maintaining the toxicity to tumorous cell lines similar to doxorubicin or epirubicin (IC50 = 2076.7 nM for PNT1A vs. 935.3 and 729.0 nM for 22Rv1 and LNCaP). Apodox IC50 was determined as follows: 603.1, 1344.2, and 931.2 nM for PNT1A, 22Rv1, and LNCaP.

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Blum R.H., Carter S.K. Adriamycin—New anticancer drug with significant clinical activity. Ann. Int. Med. 1974;80:249–259. PubMed

Pommier Y., Leo E., Zhang H.L., Marchand C. DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem. Biol. 2010;17:421–433. doi: 10.1016/j.chembiol.2010.04.012. PubMed DOI PMC

Chatterjee K., Zhang J.Q., Honbo N., Karliner J.S. Doxorubicin cardiomyopathy. Cardiology. 2010;115:155–162. doi: 10.1159/000265166. PubMed DOI PMC

Obryan R.M., Baker L.H., Gottlieb J.E., Rivkin S.E., Balcerzak S.P., Grumet G.N., Salmon S.E., Moon T.E., Hoogstraten B. Dose-response evaluation of adriamycin in human neoplasia. Cancer. 1977;39:1940–1948. doi: 10.1002/1097-0142(197705)39:5<1940::AID-CNCR2820390505>3.0.CO;2-0. PubMed DOI

Minotti G., Menna P., Salvatorelli E., Cairo G., Gianni L. Anthracyclines: Molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol. Rev. 2004;56:185–229. doi: 10.1124/pr.56.2.6. PubMed DOI

Tardi P.G., Boman N.L., Cullis P.R. Liposomal doxorubicin. J. Drug Target. 1996;4:129–140. doi: 10.3109/10611869609015970. PubMed DOI

Rahman A., More N., Schein P.S. Doxorubicin-induced chronic cardiotoxicity and its protection by liposomal administration. Cancer Res. 1982;42:1817–1825. PubMed

Olson F., Mayhew E., Maslow D., Rustum Y., Szoka F. Characterization, toxicity and therapeutic efficacy of adriamycin encapsulated in liposomes. Eur. J. Cancer Clin. Oncol. 1982;18:167–169. doi: 10.1016/0277-5379(82)90060-8. PubMed DOI

Gabizon A., Dagan A., Goren D., Barenholz Y., Fuks Z. Liposomes as invivo carriers of adriamycin-reduced cardiac uptake and preserved anti-tumor activity in mice. Cancer Res. 1982;42:4734–4739. PubMed

Storm G., Roerdink F.H., Steerenberg P.A., Dejong W.H., Crommelin D.J.A. Influence of lipid-composition on the antitumor-activity exerted by doxorubicin-containing liposomes in a rat solid tumor-model. Cancer Res. 1987;47:3366–3372. PubMed

Balazsovits J.A.E., Mayer L.D., Bally M.B., Cullis P.R., McDonell M., Ginsberg R.S., Falk R.E. Analysis of the effect of liposome encapsulation on the vesicant properties, acute and cardiac toxicities, and antitumor efficacy of doxorubicin. Cancer Chemother. Pharmacol. 1989;23:81–86. doi: 10.1007/BF00273522. PubMed DOI

Mayer L.D., Bally M.B., Cullis P.R., Wilson S.L., Emerman J.T. Comparison of free and liposome encapsulated doxorubicin tumor drug uptake and antitumor efficacy in the sc115 murine mammary-tumor. Cancer Lett. 1990;53:183–190. doi: 10.1016/0304-3835(90)90212-G. PubMed DOI

Dong H.Q., Dong C.Y., Feng Y., Ren T.B., Zhang Z.H., Li L., Li Y.Y. Engineering of peglayted camptothecin into core-shell nanomicelles for improving solubility, stability and combination delivery. Medchemcomm. 2012;3:1555–1561. doi: 10.1039/c2md20153d. DOI

Rahman A., Husain S.R., Siddiqui J., Verma M., Agresti M., Center M., Safa A.R., Glazer R.I. Liposome-mediated modulation of multidrug resistance in human hl-60 leukemia-cells. J. Natl. Cancer Inst. 1992;84:1909–1915. doi: 10.1093/jnci/84.24.1909. PubMed DOI

Gokhale P.C., Radhakrishnan B., Husain S.R., Abernethy D.R., Sacher R., Dritschilo A., Rahman A. An improved method of encapsulation of doxorubicin in liposomes: Pharmacological, toxicological and therapeutic evaluation. Br. J. Cancer. 1996;74:43–48. doi: 10.1038/bjc.1996.313. PubMed DOI PMC

Oudard S., Thierry A., Jorgensen T.J., Rahman A. Sensitization of multidrug-resistant colon cancer-cells to doxorubicin encapsulated in liposomes. Cancer Chemother. Pharmacol. 1991;28:259–265. PubMed

Thierry A.R., Rahman A., Dritschilo A. A new procedure for the preparation of liposomal doxorubicin: Biological-activity in multidrug-resistant tumor-cells. Cancer Chemother. Pharmacol. 1994;35:84–88. doi: 10.1007/BF00686289. PubMed DOI

Thierry A.R., Vige D., Coughlin S.S., Belli J.A., Dritschilo A., Rahman A. Modulation of doxorubicin resistance in multidrug-resistant cells by liposomes. FASEB J. 1993;7:572–579. PubMed

Mickisch G.H., Rahman A., Pastan I., Gottesman M.M. Increased effectiveness of liposome-encapsulated doxorubicin in multidrug-resistant-transgenic mice compared with free doxorubicin. J. Natl. Cancer Inst. 1992;84:804–805. doi: 10.1093/jnci/84.10.804. PubMed DOI

Yang Z., Wang X.Y., Diao H.J., Zhang J.F., Li H.Y., Sun H.Z., Guo Z.J. Encapsulation of platinum anticancer drugs by apoferritin. Chem. Commun. 2007;33:3453–3455. doi: 10.1039/b705326f. PubMed DOI

Meyer J.S., Sufrin G., Martin S.A. Proliferative activity of benign human-prostate, prostatic adenocarcinoma and seminal-vesicle evaluated by thymidine labeling. J. Urol. 1982;128:1353–1356. PubMed

Simsek E., Kilic M.A. Magic ferritin: A novel chemotherapeutic encapsulation bullet. J. Magn. Magn. Mater. 2005;293:509–513. doi: 10.1016/j.jmmm.2005.01.066. DOI

Tmejova K., Hynek D., Kopel P., Dostalova S., Smerkova K., Stanisavljevic M., Nguyen H.V., Nejdl L., Vaculovicova M., Krizkova S., et al. Electrochemical behaviour of doxorubicin encapsulated in apoferritin. Int. J. Electrochem. Sci. 2013;8:12658–12671.

Yang Y.W. Towards biocompatible nanovalves based on mesoporous silica nanoparticles. Medchemcomm. 2011;2:1033–1049. doi: 10.1039/c1md00158b. DOI

Tseng Y.L., Liu J.J., Hong R.L. Translocation of liposomes into cancer cells by cell-penetrating peptides penetratin and tat: A kinetic and efficacy study. Mol. Pharmacol. 2002;62:864–872. doi: 10.1124/mol.62.4.864. PubMed DOI

Hong R.L., Huang C.J., Tseng Y.L., Pang V.F., Chen S.T., Liu J.J., Chang F.H. Direct comparison of liposomal doxorubicin with or without polyethylene glycol coating in c-26 tumor-bearing mice: Is surface coating with polyethylene glycol beneficial? Clin. Cancer Res. 1999;5:3645–3652. PubMed

Masarik M., Gumulec J., Hlavna M., Sztalmachova M., Babula P., Raudenska M., Pavkova-Goldbergova M., Cernei N., Sochor J., Zitka O., et al. Monitoring of the prostate tumour cells redox state and real-time proliferation by novel biophysical techniques and fluorescent staining. Integr. Biol. 2012;4:672–684. doi: 10.1039/c2ib00157h. PubMed DOI

Komatsu M., Waguri S., Ueno T., Iwata J., Murata S., Tanida I., Ezaki J., Mizushima N., Ohsumi Y., Uchiyama Y., et al. Impairment of starvation-induced and constitutive autophagy in atg7-deficient mice. J. Cell Biol. 2005;169:425–434. doi: 10.1083/jcb.200412022. PubMed DOI PMC

Aitken R.J., Whiting S., de Iuliis G.N., McClymont S., Mitchell L.A., Baker M.A. Electrophilic aldehydes generated by sperm metabolism activate mitochondrial reactive oxygen species generation and apoptosis by targeting succinate dehydrogenase. J. Biol. Chem. 2012;287:33048–33060. doi: 10.1074/jbc.M112.366690. PubMed DOI PMC

He C.C., Klionsky D.J. Regulation mechanisms and signaling pathways of autophagy. Ann. Rev. Genet. 2009;43:67–93. doi: 10.1146/annurev-genet-102808-114910. PubMed DOI PMC

Graeser R., Chung D.E., Esser N., Moor S., Schachtele C., Unger C., Kratz F. Synthesis and biological evaluation of an albumin-binding prodrug of doxorubicin that is cleaved by prostate-specific antigen (PSA) in a PSA-positive orthotopic prostate carcinoma model (LNCaP) Int. J. Cancer. 2008;122:1145–1154. doi: 10.1002/ijc.23050. PubMed DOI

Eom Y.W., Kim M.A., Park S.S., Goo M.J., Kwon H.J., Sohn S., Kim W.H., Yoon G., Choi K.S. Two distinct modes of cell death induced by doxorubicin: Apoptosis and cell death through mitotic catastrophe accompanied by senescence-like phenotype. Oncogene. 2005;24:4765–4777. doi: 10.1038/sj.onc.1208627. PubMed DOI

Maejima Y., Adachi S., Ito H., Hirao K., Isobe M. Induction of premature senescence in cardiomyocytes by doxorubicin as a novel mechanism of myocardial damage. Aging Cell. 2008;7:125–136. doi: 10.1111/j.1474-9726.2007.00358.x. PubMed DOI

Dalby K.N., Tekedereli I., Lopez-Berestein G., Ozpolat B. Targeting the prodeath and prosurvival functions of autophagy as novel therapeutic strategies in cancer. Autophagy. 2010;6:322–329. doi: 10.4161/auto.6.3.11625. PubMed DOI PMC

Skjoth I.H.E., Issinger O.G. Profiling of signaling molecules in four different human prostate carcinoma cell lines before and after induction of apoptosis. Int. J. Oncol. 2006;28:217–229. PubMed

Carruba G., Leake R.E., Rinaldi F., Chalmers D., Comito L., Sorci C., Pavonemacaluso M., Castagnetta L.A.M. Steroid-growth factor interaction in human prostate-cancer. 1. Short-term effects of transforming growth-factors on growth of human prostate-cancer cells. Steroids. 1994;59:412–420. doi: 10.1016/0039-128X(94)90010-8. PubMed DOI

Herman-Antosiewicz A., Xiao H., Lew K.L., Singh S.V. Induction of p21 protein protects against sulforaphane-induced mitotic arrest in lncap human prostate cancer cell line. Mol. Cancer Ther. 2007;6:1673–1681. doi: 10.1158/1535-7163.MCT-06-0807. PubMed DOI

Kominkova M., Guran R., Rodrigo M.A.M., Kopel P., Blazkova I., Chudobova D., Nejdl L., Heger Z., Ruttkay-Nedecky B., Zitka O., et al. Study of functional qualities of different types of tailored liposomes with encapsulated doxorubicin using electrochemical and optical methods. Int. J. Electrochem. Sci. 2014;9:2993–3007.

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