Abstract
Toxin–antitoxin systems are genetic modules usually consisting of two genes encoding a stable toxin and labile antidote (antitoxin). These systems are localized on plasmids, phages, and chromosomes and are widespread in bacteria and archaea. The review summarizes recent data regarding the classifications of toxin–antitoxin systems, their mechanisms of action and toxin targets, as well as their functional significance for bacterial cells and possibility of use.
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Ogura, T. and Hiraga, S., Proc. Natl. Acad. Sci. U. S. A., 1983, vol. 80, no. 15, pp. 4784–4788.
Jaffe, A., Ogura, T., and Hiraga, S., J. Bacteriol., 1985, vol. 163, no. 3, pp. 841–849.
Tam, J.E. and Kline, B.C., J. Bacteriol., 1989, vol. 171, no. 5, pp. 2353–2360.
Bernard, P. and Couturier, M., J. Mol. Biol., 1992, vol. 226, no. 3, pp. 735–745.
Gerdes, K., Thisted, T., and Martinussen, J., Mol. Microbiol., 1990, vol. 4, no. 11, pp. 1807–1818.
Faridani, O.R., Nikravesh, A., Pandey, D.P., Gerdes, K., and Good, L., Nucleic Acids Res., 2006, vol. 34, no. 20, pp. 5915–5922.
Unterholzner, S.J., Poppenberger, B., and Rozhon, W., Mob. Genet. Elements, 2013, no. 3, p. e26219. doi 10.4161/mge.26219
Pandey, D.P. and Gerdes, K., Nucleic Acids Res., 2005, vol. 33, no. 3, pp. 966–976.
Fozo, E.M., Makarova, K.S., Shabalina, S.A., Yutin, N., Koonin, E.V., and Storz, G., Nucleic Acids Res., 2010, vol. 38, no. 11, pp. 3743–3759.
Leplae, R., Geeraerts, D., Hallez, R., Guglielmini, J., Dreze, P., and van Meldere., L., Nucleic Acids Res., 2011, vol. 39, no. 13, pp. 5513–5525.
Sberro, H., Leavitt, A., Kiro, R., Koh, E., Peleg, Y., Qimron, U., and Sorek, R., Mol. Cell, 2013, vol. 50, no. 1, pp. 136–148.
Yamaguchi, Y. and Inouye, M., Stress and Environmental Regulation of Gene Expression and Adaptation in Bacteria, de Bruijn, F.J., Ed., Wiley-Blackwell, 2016, vol. 1, pp. 97–107.
Ramage, H.R., Connolly, L.E., and Cox, J.S., PLoS Genetics, 2009, vol. 5, no. 12, p. e1000767. doi 10.1371/journal.pgen.1000767
Sala, A., Bordes, P., and Genevaux, P., Toxins, 2014, vol. 6, no. 3, pp. 1002–1020.
Ramisetty, B.C. and Santhosh, R.S., FEMS Microbiol. Letts., 2016, vol. 363, no. 3.
Goeders, N. and Van Meldere., L., Toxins, 2014, vol. 6, no. 1, pp. 304–324.
Van Mederen de Bas., PLoS Genetics, 2009, vol. 5, no. 3, p. e1000437. doi 10.1371/journal.pgen.1000437
Prozorov, A.A. and Danilenko, V.N., Microbiology (Moscow), 2010, vol. 79, no. 2, pp. 129–140.
Guglielmini, J. and Van Meldere., L., Mob. Genet. Elements, 2011, vol. 1, no. 4, pp. 283–290.
Bukowski, M., Rojowska, A., and Wladyka, B., Acta Biochim. Pol., 2011, vol. 58, no. 1, pp. 1–9.
Demidenok, O.I. and Goncharenko, A.V., Appl. Biochem. Microbiol., 2013, vol. 49, no. 6, pp. 535–541.
Brantl, S. and Jahn, N., FEMS Microbiol. Rev., 2015, vol. 39, no. 3, pp. 413–427.
Chan, W.T., Espinosa, M., and Yeo, C.C., Front. Mol. Biosci., 2016, vol. 3, p. 9. doi 10.3389/fmolb.2016.00009
Sevin, E.W. and Barloy-Hubler, F., Genome Biol., 2007, vol. 8, no. 8, p. 155.
Shao, Y., Harrison, E.M., Bi, D., Tai, C., He, X., Ou, H.Y., Rajakumar, K., and Deng, Z., Nucleic Acids Res., 2011, vol. 39 (database issue), pp. D606–D611.
Barbosa, L.C., Garrido, S.S., and Marchetto, R., Comput. Biol. Med., 2015, vol. 58, no. 2, pp. 146–153.
Gerdes, K., Bech, F.W., Jorgensen, S.T., Lobner-Olesen, A., Rasmussen, P.B., Atlung, T., Boe, L., Karlstrom, O., Molin, S., and von Meyenburg, K., EMBO J., 1986, vol. 5, no. 8, pp. 2023–2029.
Fozo, E.M., Hemm, M.R., and Storz, G., Microbiol. Mol. Biol. Rev., 2008, vol. 72, no. 4, pp. 579–589.
Gerdes, K. and Wagner, E.G., Curr. Opin. Microbiol., 2007, vol. 10, no. 2, pp. 117–124.
Kawano, M., Aravind, L., and Storz, G., Mol. Microbiol., 2007, vol. 64, no. 3, pp. 738–754.
Silvaggi, J.M., Perkins, J.B., and Losick, R., J. Bacteriol., 2005, vol. 187, no. 19, pp. 6641–6650.
Darfeuille, F., Unoson, C., Vogel, J., and Wagner, E.G., Mol. Cell, 2007, vol. 26, no. 3, pp. 381–392.
Tian, Q.B., Ohnishi, M., Murata, T., Nakayama, K., Terawaki, Y., and Hayashi, T., Plasmid, 2001, vol. 45, no. 2, pp. 63–74.
Makarova, K.S., Wolf, Y.I., and Koonin, E.V., Biol. Direct, 2009, vol. 4, no. 19, p. 1186.
Marianovsky, I., Aizenman, E., Engelberg-Kulka, H., and Glaser, G., J. Biol. Chem., 2001, vol. 276, no. 8, pp. 5975–5984.
Chan, W.T., Nieto, C., Harikrishna, J.A., Khoo, S.K., Othman, R.Y., Espinosa, M., et al., J. Bacteriol., 2011, vol. 193, no. 18, pp. 4612–4625.
Hayes, F. and Kedzierska, B., Toxins (Basel), 2014, vol. 6, no. 1, pp. 337–358.
Krugel, H., Klimina, K., Mrotzek, G., Tretyakov, A., Schofl, G., Saluz, H.-P., Brantl, S., Poluektova, E., and Danilenko, V., J. Basic Microbiol., 2015, vol. 55, no. 8, pp. 982–991.
Tsuchimoto, S., Nishimura, Y., and Ohtsubo, E., J. Bacteriol., 1992, vol. 174, no. 13, pp. 4205–4211.
Van Meldere., L., Bernard, P., and Couturier, M., Mol. Microbiol., 1994, vol. 11, no. 6, pp. 1151–1157.
Lehnherr, H. and Yarmolinsky, M.B., Proc. Natl. Acad. Sci. U. S. A., 1995, vol. 92, no. 8, pp. 3274–3277.
Santos-Sierra, S., Pardo-Abarrio, C., Giraldo, R., and Diaz-Orejas, R., FEMS Microbiol. Letts., 2002, vol. 206, no. 1, pp. 115–119.
Bernard, P. and Couturier, M., Mol. Gen. Genet., 1991, vol. 226, no. 1, pp. 297–304.
Brown, B.L., Grigoriu, S., Kim, Y., Arruda, J.M., Davenport, A., Wood, T.K., Peti, W., and Page, R., PLoS Pathog., 2009, vol. 5, no. 12, p. e1000706. doi 10.1371/journal.ppat.1000706
Camacho, A.G., Misselwitz, R., Behlke, J., Ayora, S., Welfle, K., Meinhart, A., Lara, B., Saenger, W., Welfle, H., and Alonso, J.C., Biol. Chem., 2002, vol. 383, no. 11, pp. 1701–1713.
Smith, A.S. and Rawlings, D.E., Mol. Microbiol., 1997, vol. 26, no. 5, pp. 961–970.
Bordes, P., Cirinesi, A.M., Ummels, R., Sala, A., Sakr, S., Bitter, W., and Genevaux, P., Proc. Natl. Acad. Sci. U. S. A., 2011, vol. 108, no. 20, pp. 8438–8443.
Andrews, E.S.V. and Arcus, V.L., Tuberculosis (Edinburg), 2015, vol. 95, no. 4, pp. 385–394.
Rocker, A. and Meinhart, A., Mol. Microbiol., 2015, vol. 97, no. 3, pp. 589–604.
Polom, D., Boss, L., Wegrzyn, G., Hayes, F., and Kedzierska, B., FEBS J., 2013, vol. 280, no. 22, pp. 5906–5918.
Yang, M., Gao, C., Wang, Y., Zhang, H., and He, Z.-G., PLoS One, 2010, vol. 5, no. 5, p. e10672. doi 0.1371/journal. pone.0010672
Zhu, L., Sharp, J.D., Kobayashi, H., Woychik, N.A., and Inouye, M., J. Biol. Chem., 2010, vol. 285, no. 51, pp. 39732–39738.
Melničáková, J., Bečárová, Z., Makroczyová, J., and Barák, I., Front Microbiol., 2015, vol. 6, p. 808. doi 10.3389/fmicb.2015.00808
Park, S.J., Son, W.S., and Lee, B.-J., Biochim. Biophys. Acta: Proteins. Proteomics, 2013, vol. 1834, no. 6, pp. 1155–1167.
Schmidt, O., Schuenemann, V.J., Hand, N.J., Silhavy, T.J., Martin, J., Lupas, A.N., and Djuranovic, S., J. Mol. Biol., 2007, vol. 372, no. 4, pp. 894–905.
Unterholzner, S.J., Hailer, B., Poppenberger, B., and Rozhon, W., Plasmid, 2013, vol. 70, no. 2, pp. 216–225.
Klimina, K.M., Kjasova, D.Ch., Poluektova, E.U., Leuschner, Y., Krugel, H., Saluz, H.P., and Danilenko, V.N., Anaerobe, 2013, vol. 22, pp. 82–89.
Tsilibaris, V., Maenhaut-Michel, G., Mine, N., and Van Meldere., L., J. Bacteriol., 2007, vol. 189, no. 17, pp. 6101–6108.
Blower, T.R., Short, F.L., Rao, F., Mizuguchi, K., Pei, X.Y., Fineran, P.C., Luisi, B.F., and Salmond, G.P.C., Nucleic Acids Res., 2012, vol. 40, no. 13, pp. 6158–6173.
Chan, W.T., Yeo, C.C., Sadowy, E., and Espinosa, M., Front. Microbiol., 2014, vol. 5, p. 677. doi 10.3389/fmicb.2014.00677
Schuster, C.F. and Bertram, R., Toxins, 2016, vol. 8, no. 5, p. e140. doi 10.3390/toxins8050140
Averina, O., Alekseeva, M., Shkoporov, A., and Danilenko, V., Anaerobe, 2015, vol. 35, pp. 59–67.
Fineran, P.C., Blower, T.R., Foulds, I.J., Humphreys, D.P., Lilley, K.S., and Salmond, G.P., Proc. Natl. Acad. Sci. U. S. A., 2009, vol. 106, no. 3, pp. 894–899.
Blower, T.R., Pei, X.Y., Short, F.L., Fineran, P.C., Humphreys, D.P., Luisi, B.F., and Salmond, G.P., Nat. Struct. Mol. Biol., 2011, vol. 18, no. 2, pp. 185–190.
Samson, J.E., Spinelli, S., Cambillau, C., and Moineau, S., Mol. Microbiol., 2013, vol. 87, no. 4, pp. 756–768.
Masuda, H., Tan, Q., Awano, N., Wu, K.P., and Inouye, M., Mol. Microbiol., 2012, vol. 84, no. 5, pp. 979–989.
Masuda, H., Tan, Q., Awano, N., Yamaguchi, Y., and Inouye, M., FEMS Microbiol. Letts., 2012, vol. 328, no. 2, pp. 174–181.
Wang, X., Lord, D.M., Cheng, H.Y., Osbourne, D.O., Hong, S.H., Sanchez-Torres, V., Quiroga, C., Zheng, K., Herrmann, T., Peti, W., Benedik, M., Rebecca, PageR., and Woo., T., Nat. Chem. Biol., 2012, vol. 8, no. 10, pp. 855–861.
Markovski, M. and Wickner, S., Mol. Cell, 2013, vol. 52, no. 5, pp. 611–612.
Wen, Y. and Behiels, E., Pathog. Dis., 2014, vol. 70, no. 3, pp. 240–249.
Unoson, C. and Wagner, E.G.H., Mol. Microbiol., 2008, vol. 70, no. 1, pp. 258–270.
Guo, Y., Quiroga, C., Chen, Q., McAnulty, M.J., Benedik, M.J., Wood, T.K., and Wang, X., Nucleic Acids Res., 2014, vol. 42, no. 10, pp. 6448–6462.
Zhang, Y., Zhang, J., Hoeflich, K.P., Ikura, M., Qing, G., and Inouye, M., Mol. Cell, 2003, vol. 12, no. 4, pp. 913–923.
Vesper, O., Amitai, S., Belitsky, M., Byrgazov, K., Kaberdina, A.C., Engelberg-Kulka, H., and Moll, I., Cell, 2011, vol. 147, no. 1, pp. 147–157.
Schifano, J.M., Edifor, R., Sharp, J.D., Ouyang, M., Konkimalla, A., Husson, R.N., and Woychik, N.A., Proc. Natl. Acad. Sci. U. S. A., 2013, vol. 110, no. 21, pp. 8501–8506.
Munoz-Gomez, A.J., Lemonnier, M., Santos-Sierra, S., Berzal-Herranz, A., and Diaz-Orejas, R., J. Bacteriol., 2005, vol. 187, no. 9, pp. 3151–3157.
Jorgensen, M.G., Pandey, D.P., Jaskolska, M., and Gerdes, K., J. Bacteriol., 2009, vol. 191, no. 4, pp. 1191–1199.
Christensen, S.K. and Gerdes, K., Mol. Microbiol., 2003, vol. 48, no. 5, pp. 1389–1400.
McKenzie, J.L., Robson, J., Berney, M., Smith, T.C., Ruthe, A., Gardner, P.P., Arcus, V.L., and Cook, G.M., J. Bacteriol., 2012, vol. 194, no. 9, pp. 2189–2204.
Winther, K.S. and Gerdes, K., Proc. Natl. Acad. Sci. U. S. A., 2011, vol. 108, no. 18, pp. 7403–7407.
Zhang, Y. and Inouye, M., Mol. Microbiol., 2011, vol. 79, no. 6, pp. 1418–1429.
Germain, E., Castro-Roa, D., Zenkin, N., and Gerdes, K., Mol. Cell, 2013, vol. 52, no. 2, pp. 248–254.
Castro-Roa, D., Garcia-Pino, A., de Gieter, S., van Nulan., N.A., Loris, R., and Zenkin, N., Nat. Chem. Biol., 2013, vol. 9, no. 12, pp. 811–817.
Jiang, Y., Pogliano, J., Helinski, D.R., and Konieczny, I., Mol. Microbiol., 2002, vol. 44, no. 4, pp. 971–979.
Dao-Thi, M.H., Van Melderen, L., De Genst, E., Afif, H., Buts, Ll., Wyns, L., and Loris, R., J. Mol. Biol., 2005, vol. 348, no. 5, pp. 1091–1102.
Mutschler, H., Gebhardt, M., Shoeman, R.L., and Meinhart, A., PLoS Biol., 2011, vol. 9, no. 3, p. e1001033. doi 10.1371/journal.pbio.1001033
Tan, Q., Awano, N., and Inouye, M., Mol. Microbiol., 2011, vol. 79, no. 1, pp. 109–118.
Aakre, C.D., Phung, T.N., Huang, D., and Laub, M.T., Mol. Cell, 2013, vol. 52, no. 5, pp. 617–628.
Zhang, Y., Zhu, L., Zhang, J., and Inouye, M., J. Biol. Chem., 2005, vol. 280, no. 28, pp. 26080–26088.
Yamaguchi, Y., Park, J.H., and Inouye, M., J. Biol. Chem., 2009, vol. 284, no. 42, pp. 28746–28753.
Yamaguchi, Y., Nariya, H., Park, J.H., and Inouye, M., Nat. Commun., 2012, vol. 3.
Goeders, N., Dreze, P.L., and Van Meldere., L., J. Bacteriol., 2013, vol. 195, no. 11, pp. 2541–2549.
Zhang, Y. and Inouye, M., J. Biol. Chem., 2009, vol. 284, no. 11, pp. 6627–6638.
Goeders, N., Chai, R., Chen, B., Day, D., and Salmond, G., Toxins (Basel), 2016, vol. 8, no. 10, p. e282. doi 10.3390/toxins8100282
Cruz, J.W., Sharp, J.D., Hoffer, E.D., Maehigashi, T., Vvedenskaya, I.O., Konkimalla, A., Husson, R.N., Nickels, B.E., Dunham, C.M., and Woychik, N.A., Nat. Commun., 2015, vol. 6, p. 7480. doi 10.1038/ncomms8480
Winther, K.S., Brodersen, D.E., Brown, A.K., and Gerdes, K., Nat. Commun., 2013, vol. 4, p. 2796. doi 10.1038/ncomms3796
Schifano, J.M., Vvedenskaya, I.O., Knoblauch, J.G., Ouyang, M., Nickels, B.E., and Woychik, N.A., Nat. Commun., 2014, vol. 5, p. 3538. doi 0.1038/ncomms4538
Schifano, J.M., Cruz, J.W., Vvedenskaya, I.O., Edifor, R., Ouyang, M., Husson, R.N., Nickels, B.E., and Woychik, N.A., Nucleic Acids Res., 2016, vol. 44, no. 3, pp. 1256–1270.
Yuan, J., Sterckx, Y., Mitchenall, L.A., Maxwell, A., Loris, R., and Waldor, M.K., J. Biol. Chem., 2010, vol. 285, no. 51, pp. 40397–40408.
Soo, V.W. and Wood, T.K., Sci. Rep., 2013, vol. 3, p. 3186. doi 10.1038/srep03186
Hu, Y., Benedik, M.J., and Wood, T.K., Arch. Microbiol., 2012, vol. 14, no. 3, pp. 669–679.
Lin, C.-Y., Awano, N., Masuda, H., Park, J.-H., and Inouye, M., J. Mol. Microbiol. Biotechnol., 2013, vol. 23, no. 6, pp. 440–447.
Tripathi, A., Dewan, P.C., Barua, B., and Varadarajan, R., Proc. Natl. Acad. Sci. U. S. A., 2012, vol. 109, no. 31, pp. 12497–12502.
Durand, S., Jahn, N., Condon, C., and Brantl, S., RNA Biol., 2012, vol. 9, no. 12, pp. 1491–1497.
Szekeres, S., Dauti, M., Wilde, C., Mazel, D., and Rowe-Magnus, D.A., Mol. Microbiol., 2007, vol. 63, no. 6, pp. 1588–1605.
Wozniak, R.A. and Waldor, M.K., PLoS Genet., 2009, vol. 5, no. 3, p. e1000439. doi 10.1371/journal.pgen.1000439
Koga, M., Otsuka, Y., Lemire, S., and Yonesaki, T., Genetics, 2011, vol. 187, no. 1, pp. 123–130.
Alawneh, A.M., Qi, D., Yonesaki, T., and Otsuka, Y., Mol. Microbiol., 2016, vol. 99, no. 1, pp. 188–198.
de Bast, M.S., Mine, N., and van Meldere., L., J. Bacteriol., 2008, vol. 190, no. 13, pp. 4603–4609.
Keren, I., Shah, D., Spoering, A., Kaldalu, N., and Lewis, K., J. Bacteriol., 2004, vol. 186, no. 24, pp. 8172–8180.
Demidenok, O.I., Kaprelyants, A.S., and Goncharenko, A.V., FEMS Microbiol. Letts., 2014, vol. 352, no. 1, pp. 69–77.
Dorr, T., Vulic, M., and Lewis, K., PLoS Biol., 2010, vol. 8, no. 2, p. e1000317. doi 10.1371/journal.pbio.1000317
Wagner, E.G. and Unoson, C., RNA Biol., 2012, vol. 9, no. 12, pp. 1513–1519.
Maisonneuve, E., Shakespeare, L.J., Jorgensen, M.G., and Gerdes, K., Proc. Natl. Acad. Sci. U. S. A., 2011, vol. 108, no. 32, pp. 13206–13211.
Engelberg-Kulka, H., Hazan, R., and Amitai, S., J. Cell Sci., 2005, vol. 118, no. 19, pp. 4327–4332.
Hazan, R. and Engelberg-Kulka, H., Mol. Genet. Genomics, 2004, vol. 272, no. 2, pp. 227–234.
Sat, B., Hazan, R., Fisher, T., Khaner, H., Glaser, G., and Engelberg-Kulka, H., J. Bacteriol., 2001, vol. 183, no. 6, pp. 2041–2045.
Amitai, S., Yassin, Y., and Engelberg-Kulka, H., J. Bacteriol., 2004, vol. 186, no. 24, pp. 8295–8300.
Kumar, S. and Engelberg-Kulka, H., Curr. Opin. Microbiol., 2014, vol. 21, pp. 22–27.
Amitai, S., Kolodkin-Gal, I., Hananya-Meltabashi, M., Sacher, A., and Engelberg-Kulka, H., PLoS Genet., 2009, vol. 5, no. 3, p. e1000390. doi 10.1371/journal.pgen.1000390
Moll, I. and Engelberg-Kulka, H., Trends Biochem. Sci., 2012, vol. 37, no. 11, pp. 493–498.
Temmel, H., Muller, C., Sauert, M., Vesper, O., Reiss, A., Popow, J., Martinez, J., and Moll, I., Nucleic Acids Res., 2016, pii: gkw1018. doi 10.1093/nar/gkw1018
Sauert, M., Wolfinger, M.T., Vesper, O., Muller, C., Byrgazov, K., and Moll, I., Nucleic Acids Res., 2016, vol. 44, no. 14, pp. 6660–6675.
Wang, X. and Wood, T.K., Appl. Environ. Microbiol., 2011, vol. 77, no. 16, pp. 5577–5583.
Wang, X., Lord, D.M., Hong, S.H., Peti, W., Benedik, M.J., Page, R., Benedik, M.J., Page, R., and Wood, T.K., Environ. Microbiol., 2013, vol. 15, no. 6, pp. 1734–1744.
Theunissen, S., De Smet, L., Dansercoer, A., Motte, B., Coenye, T., Van Beeumen, J.J., Devreese, B., Savvides, S.N., and Vergauwen, B., Res. Microbiol., 2010, vol. 161, no. 2, pp. 144–152.
Georgiades, K. and Raoult, D., PLoS One, 2011, vol. 6, no. 3, p. e17962. doi 10.1371/journal.pone.0017962
Moritz, E.M. and Hergenrother, P.J., Proc. Natl. Acad. Sci. U. S. A., 2007, vol. 104, no. 1, pp. 311–316.
Sadeghifard, N., Soheili, S., Sekawi, Z., and Ghafourian, S., GMS Hyg. Infect. Control., 2014, vol. 9, no. 1, Doc05. doi 10.3205/dgkh000225
Ren, D., Walker, A.N., and Daines, D., BMC Microbiol., 2012, vol. 12, p. 263. doi 10.1186/1471-2180-12-263
Sayeed, S., Reaves, L., Radnedge, L., and Austin, S., J. Bacteriol., 2000, vol. 182, no. 9, pp. 2416–2421.
Hurley, J.M. and Woychik, N., J. Biol. Chem., 2009, vol. 284, no. 28, pp. 18605–18613.
Mutschler, H. and Meinhart, A.E., J. Mol. Med. (Berl.), 2011, vol. 89, no. 12, pp. 1183–1194.
Zhu, L., Inoue, K., Yoshizumi, S., Kobayashi, H., Zhang, Y., Ouyang, M., Kato, F., Sugai, M., and Inouye, M., J. Bacteriol., 2009, vol. 191, no. 10, pp. 3248–3255.
Muthuramalingam, M., White, J.C., and Bourne, C.R., Toxins (Basel), 2016, vol. 8, no. 7, p. e214. doi 10.3390/toxins8070214
Daimon, Y., Narita, S.-I., and Akiyama, Y., J. Bacteriol., 2015, vol. 197, no. 14, pp. 2316–2324.
Wessner, F., Lacoux, C., Goeders, N. Fouquier d'Héroue., A., Matos, R., Serror, P., Van Melderen, L., and Repoila, F., RNA Biol., 2015, vol. 12, no. 10, pp. 1099–108.
Kasari, V., Mets, T., Tenson, T., and Kaldalu, N., BMC Microbiol., 2013, vol. 13, p. 45. doi 10.1186/1471-2180–13-45
Williams, J.J. and Hergenrother, P.J., Trends Microbiol., 2012, vol. 20, no. 6, pp. 291–298.
Chan, W.T., Balsa, D., and Espinosa, M., FEMS Microbiol. Rev., 2015, vol. 39, no. 4, pp. 522–540.
Agarwal, S., Mishra, N.K., Bhatnagar, S., and Bhatnagar, R., J. Biol. Chem., 2010, vol. 285, no. 10, pp. 7254–7270.
Lee, I.G., Lee, S.J., Chae, S., Lee, K.Y., Kim, J.H., and Lee, B.J., Nucleic Acids Res., 2015, vol. 43, no. 15, pp. 7624–7637.
Shimazu, T., Mirochnitchenko, O., Phadtare, S., and Inouye, M., J. Mol. Microb. Biotech., vol. 24, no. 4, pp. 228–233.
Preston, M.A., Pimentel, B., Bermejo-Rodriguez, C., Dionne, I., Turnbull, A., and de la Cueva-Mende., G., ACS Synth. Biol., 2016, vol. 5, no. 7, pp. 540–546.
Chono, H., Matsumoto, K., Tsuda, H., Saito, N., Lee, K., Kim, S., Shibata, H., Ageyama, N., Terao, K., Yasutomi, Y., Mineno, J., Kim, S., Inouye, M., and Kato, I., Hum. Gene Ther., 2011, vol. 22, no. 1, pp. 35–43.
Shapira, A., Shapira, S., Gal-Tanamy, M., Zemel, R., Tur-Kaspa, R., and Benhar, I., PLoS One, 2012, vol. 7, no. 2, p. e32320. doi 10.1371/journal.pone.0032320
Trovatti, E., Cotrim, C.A., Garrido, S.S., Barros, R.S., and Marchetto, R., Bioorg. Med. Chem. Lett., 2008, vol. 18, no. 23, pp. 6161–6164.
Bernard, P., Gabant, P., Bahassi, E.M., and Couturier, M., Gene, 1994, vol. 148, no. 1, pp. 71–74.
Wright, O., Delmans, M., Stan, G.-B., and Ellis, T., Gene Guard: ACS Synth. Biol., 2015, vol. 4, no. 3, pp. 307–316.
Averina, O.V., Alekseeva, M.G., Abilev, S.K., Il’in, V.K., and Danilenko, V.N., Genetika, 2013, vol. 49, no. 3, pp. 315–327.
Fiedoruk, K., Daniluk, T., Swiecicka, I., Sciepuk, M., and Leszczynska, K., Microbiology, 2015, vol. 161, no. 1, pp. 158–167.
RF Patent no. 2526576, 2011.
Poluektova, E.U., Yunes, R.A., Epiphanova, M.V., Orlova, V.S., and Danilenko, V.N., Arch. Microbiol., 2017. doi 10.1007/s00203-017-1346-5
RF Patent no. 2527069, 2011.
RF Patent no. 2547598156, 2013.
Zaychikova, M.V., Zakharevich, N.V., Sagaidak, M.O., Bogolubova, N.A., Smirnova, T.G., Andreevskaya, S.N., Larionova, E.E., Alekseeva, M.G., Chernousova, L.N., and Danilenko, V.N., PLoS One, 2015, vol. 10, no. 12, p. e0143682. doi 10.1371/journal. pone.0143682
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Original Russian Text © K.M. Klimina, E.U. Poluektova, V.N. Danilenko, 2017, published in Prikladnaya Biokhimiya i Mikrobiologiya, 2017, Vol. 53, No. 5, pp. 449–461.
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Klimina, K.M., Poluektova, E.U. & Danilenko, V.N. Bacterial toxin–antitoxin systems: Properties, functional significance, and possibility of use (Review). Appl Biochem Microbiol 53, 494–505 (2017). https://doi.org/10.1134/S0003683817050076
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DOI: https://doi.org/10.1134/S0003683817050076