Abstract
Bacterial ribonuclease binase is a potential anticancer agent. In the present study, we have determined the toxic effect of binase towards cell lines of T-cell acute lymphoblastic leukemia Jurkat and CEMss. We have shown that binase induces apoptosis in these cells. At the same time, binase does not cause toxic effects in leukocytes of healthy donors, which suggests that binase activity towards leukemic cells is selective. We have found that the treatment of cancer cells with binase leads to a reduction in reactive oxygen species and transcription factor NFκB levels, and demonstrated that these effects are a common feature of the action of RNases on cancer cells.
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References
Roti G., Stegmaier K. 2014. New approaches to target T-ALL. Front. Oncol. 4, 170.
Aifantis I., Raetz E., Buonamici S. 2008. Molecular pathogenesis of T-cell leukaemia and lymphoma. Nat. Rev. Immunol. 8, 380–390.
Fang E.F., Ng T.B. 2011. Ribonucleases of different origins with a wide spectrum of medicinal applications. Biochim. Biophys. Acta. 1815, 65–74.
Mironova N.L., Petrushanko I.Y., Patutina O.A., Sen’kova A.V., Simonenko O.V., Mitkevich V.A., Markov O.V., Zenkova M.A., Makarov A.A. 2013. Ribonuclease binase inhibits primary tumor growth and metastases via apoptosis induction in tumor cells. Cell Cycle. 12, 2120–2131.
Mitkevich V.A., Makarov A.A., Ilinskaya O.N. 2014. Cett targets of antitumor ribonucleases. Mol. Biol. (Moscow). 48 (2), 181–188.
Ulyanova V., Vershinina V., Ilinskaya O. 2011. Barnase and binase: Twins with different fates. FEBS J. 278, 3633–3643.
Mitkevich V.A., Ilinskaya O.N., Makarov A.A. 2015. Antitumor RNases: Killer’s secrets. Cell Cycle. 14, 931–932.
Mitkevich V.A., Burnysheva K.M., Il’inskaia O.N., Pace C.N., Makarov A.A. 2014. Cytotoxicity of RNase Sa to the acute myeloid leukemia Kasumi-1 cells depends on the net charge. Oncoscience. 1, 738–744.
Edelweiss E., Balandin T.G., Ivanova J.L., Lutsenko G.V., Leonova O.G., Popenko V.I., Sapozhnikov A.M., Deyev S.M. 2008. Barnase as a new therapeutic agent triggering apoptosis in human cancer cells. PLoS ONE. 3, e2434.
Ilinskaya O.N., Zelenikhin P.V., Petrushanko I.Y., Mitkevich V.A., Prassolov V.S., Makarov A.A. 2007. Binase induces apoptosis of transformed myeloid cells and does not induce T-cell immune response. Biochem. Biophys. Res. Commun. 361, 1000–1005.
Schulga A., Kurbanov F., Kirpichnikov M., Protasevich I., Lobachev V., Ranjbar B., Chekhov V., Polyakov K., Engelborghs Y., Makarov A. 1998. Comparative study of binase and barnase: Experience in chimeric ribonucleases. Protein Eng. 11, 775–782.
Tsai S.Y., Ardelt B., Hsieh T.C., Darzynkiewicz Z., Shogen K., Wu J.M. 2004. Treatment of Jurkat acute T-lymphocytic leukemia cells by onconase (Ranpirnase) is accompanied by an altered nucleocytoplasmic distribution and reduced expression of transcription factor NF-kappaB. Int. J. Oncol. 25, 1745–1752.
Ardelt W., Ardelt B., Darzynkiewicz Z. 2009. Ribonucleases as potential modalities in anticancer therapy. Eur. J. Pharmacol. 625, 181–189.
Libonati M., Gotte G., Vottariello F. 2008. A novel biological actions acquired by ribonuclease through oligomerization. Curr. Pharm. Biotechnol. 9, 200–209.
Makarov A.A., Kolchinsky A., Ilinskaya O.N. 2008. Binase and other microbial RNases as potential anticancer agents. BioEssays. 30, 781–790.
Castro J., Ribó M., Benito A., Vilanova M. 2013. Minireview: Nucleus-targeted ribonucleases as antitumor drugs. Curr. Med. Chem. 20, 1225–1231.
Sevcik J., Urbanikova L., Leland P.A., Raines R.T. 2002. X-ray structure of two crystalline forms of a streptomycete ribonuclease with cytotoxic activity. J. Biol. Chem. 277, 47325–47330.
Mitkevich V.A., Petrushanko I.Y., Spirin P.V., Fedorova T.V., Kretova O.V., Tchurikov N.A., Prassolov V.S., Ilinskaya O.N., Makarov A.A. 2011. Sensitivity of acute myeloid leukemia Kasumi-1 cells to binase toxic action depends on the expression of KIT and AML1-ETO oncogenes. Cell Cycle. 10, 4090–4097.
Garipov A.R., Nesmelov A.A., Cabrera-Fuentes H.A., Ilinskaya O.N. 2014. Bacillus intermedius ribonuclease (BINASE) induces apoptosis in human ovarian cancer cells. Toxicon. 92, 54–59.
Sen’kova A.V., Mironova N.L., Patutina O.A., Mitkevich V.A., Markov O.V., Petrushanko I.Y., Burnysheva K.M., Zenkova M.A., Makarov A.A. 2014. Ribonuclease binase decreases destructive changes of the liver and restores its regeneration potential in mouse lung carcinoma model. Biochimie. 101, 256–259.
Mitkevich V.A., Kretova O.V., Petrushanko I.Y., Burnysheva K.M., Sosin D.V., Simonenko O.V., Ilinskaya O.N., Tchurikov N.A., Makarov A.A. 2013. Ribonuclease binase apoptotic signature in leukemic Kasumi-1 cells. Biochimie. 95, 1344–1349.
Ita M., Halicka H.D., Tanaka T., Kurose A., Ardelt B., Shogen K., Darzynkiewicz Z. 2008. Remarkable enhancement of cytotoxicity of onconase and cepharanthine when used in combination on various tumor cell lines. Cancer Biol. Ther. 7, 1104–1108.
Goparaju C.M., Blasberg J.D., Volinia S., Palatini J., Ivanov S., Donington J.S., Croce C., Carbone M., Yang H., Pass H.I. 2011. Onconase mediated NF-kβ downregulation in malignant pleural mesothelioma. Oncogene. 30, 2767–2777.
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Original Russian Text © K.M. Burnysheva, I.Yu. Petrushanko, P.V. Spirin, V.S. Prassolov, A.A. Makarov, V.A. Mitkevich, 2016, published in Molekulyarnaya Biologiya, 2016, Vol. 50, No. 2, pp. 347–352.
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Burnysheva, K.M., Petrushanko, I.Y., Spirin, P.V. et al. Ribonuclease binase induces death in T-cell acute lymphoblastic leukemia cells by apoptosis. Mol Biol 50, 302–306 (2016). https://doi.org/10.1134/S0026893316020035
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DOI: https://doi.org/10.1134/S0026893316020035