Abstract
This systematic review was aimed at identification of cancer stem cells (CSC) molecular markers, which was validated in experiments on transplantation of tumor subpopulations with different phenotypes to immunodeficient animals. After careful examination of available papers, we selected 97 reports, fully consistent with the objectives of the study. The results of their analysis show that markers commonly used for CSC isolation include: CD133, СD44, ALDH, CD34, CD24, and EpCAM. The review also contains description of molecular features of some CSC markers; it also considers modern approaches to cancer treatment by targeting this population and evaluates perspectives of further development of the CSC theory.
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Wright, J., J. Exp. Med., 1910, vol. 12, no. 4, pp. 556–561.
Clarkson, B.D., Natl. Cancer Inst. Monogr., 1969, vol. 30, pp. 81–120.
Pierce, G.B. and Wallace, C., Cancer Res., 1971, vol. 31, pp. 127–134.
Pierce, G.B. and Speers, W.C., Cancer Res., 1988, vol. 48, pp. 1996–2004.
Bonnet, D. and Dick, J.E., Nat. Med., 1997, vol. 3, no. 7, pp. 730–737.
Yoo, Y.D. and Kwon, Y.T., J. Anal. Sci. Technol., 2015, vol. 6, no. 1, p.28.
Li, L. and Neaves, W.B., Cancer Res., 2006, vol. 66, no. 9, pp. 4553–4557.
Li, F., Tiede, B., Massagué, J., and Kang, Y., Cell Res., 2007, vol. 17, no. 1, pp. 3–14.
Vidal, S.J., Rodriguez-Bravo, V., Galsky, M., Cordon-Cardo, C., and Domingo-Domenech, J., Oncogene, 2014, vol. 33, no. 36, pp. 4451–4463.
Guo, Z., Li, L.Q., Jiang, J.H., Ou, C., Zeng, L.X., and Xiang, B.D., World J. Gastroenterol., 2014, vol. 20, no. 8, pp. 2098–2106.
Qu, H., Li, R., Liu, Z., Zhang, J., and Luo, R., Int. J. Clin. Exp. Pathol., 2013, vol. 6, no. 11, pp. 2644–2650.
Wu, Y., Li, Z., Zhang, C., Yu, K., Teng, Z., Zheng, G., Wang, S., Liu, Y., Cui, L., and Yu, X., Int. J. Clin. Exp. Med., 2015, vol. 8, no. 3, pp. 3595–3606.
Nowell, P.C., Science, 1976, vol. 194, no. 4260, pp. 23–28.
Shackleton, M., Quintana, E., Fearon, E.R., and Morrison, S.J., Cell, 2009, vol. 138, no. 5, pp. 822–829.
Ito, R., Takahashi, T., Katano, I., and Ito, M., Cell Mol. Immunol., 2012, vol. 9, no. 3, pp. 208–214.
Trzpis, M., McLaughlin, P.M., de Leij, L.M., and Harmsen, M.C., Am. J. Pathol., 2007, vol. 171, no. 2, pp. 386–395.
Miraglia, S., Godfrey, W., Yin, A.H., Atkins, K., Warnke, R., Holden, J.T., Bray, R.A., Waller, E.K., and Buck, D.W., Blood, 1997, vol. 90, no. 12, pp. 5013–5021.
Fargeas, C.A., Huttner, W.B., and Corbeil, D., Tissue Antigens, 2007, vol. 69, no. 6, pp. 602–606.
Yin, A.H., Miraglia, S., Zanjani, E.D., Almeida-Porada, G., Ogawa, M., Leary, A.G., Olweus, J., Kearney, J., and Buck, D.W., Blood, 1997, vol. 90, no. 12, pp. 5002–5012.
Sugiyama, T., Rodriguez, R.T., McLean, G.W., and Kim, S.K., Proc. Natl. Acad. Sci. USA, 2007, vol. 104, no. 1, pp. 175–180.
Uchida, N., Buck, D.W., He, D., Reitsma, M.J., Masek, M., Phan, T.V., Tsukamoto, A.S., Gage, F.H., and Weissman, I.L., Proc. Natl. Acad. Sci. USA, 2000, vol. 97, no. 26, pp. 14720–14725.
Bertolini, G., Roz, L., Perego, P., Tortoreto, M., Fontanella, E., Gatti, L., Pratesi, G., Fabbri, A., Andriani, F., Tinelli, S., Roz, E., Caserini, R., Lo Vullo, S., Camerini, T., Mariani, L., Delia, D., Calabrò, E., Pastorino, U., and Sozzi, G., Proc. Natl. Acad. Sci. USA, 2009, vol. 106, no. 38, pp. 16281–16286.
O’Brien, C.A., Pollett, A., Gallinger, S., and Dick, J.E., Nature, 2007, vol. 445, no. 7123, pp. 106–110.
Hermann, P.C., Huber, S.L., Herrler, T., Aicher, A., Ellwart, J.W., Guba, M., Bruns, C.J., and Heeschen, C., Cell Stem Cell, 2007, vol. 1, no. 3, pp. 313–323.
Zacchigna, S., Oh, H., Wilsch-Bräuninger, M., Missol-Kolka, E., Jászai, J., Jansen, S., Tanimoto, N., Tonagel, F., Seeliger, M., Huttner, W.B., Corbeil, D., Dewerchin, M., Vinckier, S., Moons, L., and Carmeliet, P., J. Neurosci., 2009, vol. 29, no. 7, pp. 2297–2308.
Corbeil, D., Marzesco, A.M., Wilsch-Bräuninger, M., and Huttner, W.B., FEBS Lett., 2010, vol. 584, no. 9, pp. 1659–1664.
Weigmann, A., Corbeil, D., Hellwig, A., and Huttner, W.B., Proc. Natl. Acad. Sci. USA, 1997, vol. 94, no. 23, pp. 12425–12430.
Marzesco, A.M., Janich, P., Wilsch-Bräuninger, M., Dubreuil, V., Langenfeld, K., Corbeil, D., and Huttner, W.B., J. Cell Sci., 2005, vol. 118, no. 13, pp. 2849–2858.
Dubreuil, V., Marzesco, A.M., Corbeil, D., Huttner, W.B., and Wilsch-Bräuninger, M., J. Cell Biol., 2007, vol. 176, no. 4, pp. 483–495.
Röper, K., Corbeil, D., and Huttner, W.B., Nat. Cell Biol., 2000, vol. 2, no. 9, pp. 582–592.
Taïeb, N., Maresca, M., Guo, X.J., Garmy, N., Fantini, J., and Yahi, N., Cancer Lett., 2009, vol. 278, no. 2, pp. 164–173.
Wang, W., Chen, Y., Deng, J., Zhou, J., Zhou, Y., Wang, S., and Zhou, J., Tumour Biol., 2014, vol. 35, no. 10, pp. 9769–9775.
Wu, H., Qi, X.W., Yan, G.N., Zhang, Q.B., Xu, C., and Bian, X.W., PLoS One, 2014, vol. 9, no. 6, e100168.
Tan, Y., Chen, B., Xu, W., Zhao, W., and Wu, J., Mol. Clin. Oncol., 2014, vol. 2, no. 1, pp. 111–115.
Wu, B., Sun, C., Feng, F., Ge, M., and Xia, L., J. Exp. Clin. Cancer Res., 2015, vol. 34, p.44.
Han, M., Guo, L., Zhang, Y., Huang, B., Chen, A., Chen, W., Liu, X., Sun, S., Wang, K., Liu, A., and Li, X., Mol. Neurobiol., 2016, vol. 53, no. 1, pp. 720–727.
Zhang, W., Chen, H., Lv, S., and Yang, H., Mol. Neurobiol., 2015 [Epub ahead of print].
Wang, K., Xu, J., Zhang, J., and Huang, J., BMC Cancer, 2012, vol. 12, p.573.
Chen, S., Song, X., Chen, Z., Li, X., Li, M., Liu, H., and Li, J., PLoS One, 2013, vol. 8, no. 2, e56380.
Wen, L., Chen, X.Z., Yang, K., Chen, Z.X., Zhang, B., Chen, J.P., Zhou, Z.G., Mo, X.M., and Hu, J.K., PLoS One, 2013, vol. 8, no. 3, e59154.
Li, Y.M., Guo, Y.S., Ma, B., Zang, Y., Wei, T., Liang, G.F., Fan, X., Cui, S.Q., Jiang, J.L., Tang, J., and Chen, Z.N., Oncotarget, 2015.
Zhong, C., Wu, J.D., Fang, M.M., and Pu, L.Y., Tumor Biol., 2015, vol. 36, no. 10, pp. 7623–7630.
Zhou, Q., Chen, A., Song, H., Tao, J., Yang, H., and Zuo, M., Int. J. Clin. Exp. Med., 2015, vol. 8, no. 3, pp. 3080–3088.
Williams, K., Motiani, K., Giridhar, P.V., and Kasper, S., Exp. Biol. Med. (Maywood), 2013, vol. 238, no. 3, pp. 324–338.
Aruffo, A., Stamenkovic, I., Melnick, M., Underhill, C.B., and Seed, B., Cell, 1990, vol. 61, no. 7, pp. 1303–1313.
Ishii, S., Ford, R., Thomas, P., Nachman, A., Steele, G., Jr., and Jessup, J.M., Surg. Oncol., 1993, vol. 2, no. 4, pp. 255–264.
Jalkanen, S. and Jalkanen, M., J. Cell Biol., 1992, vol. 116, no. 3, pp. 817–825.
Hanley, W.D., Napier, S.L., Burdick, M.M., Schnaar, R.L., Sackstein, R., and Konstantopoulos, K., FASEB J., 2006, vol. 20, no. 2, pp. 337–339.
Tremmel, M., Matzke, A., Albrecht, I., Laib, A.M., Olaku, V., Ballmer-Hofer, K., Christofori, G., Héroult, M., Augustin, H.G., Ponta, H., and Orian-Rousseau, V., Blood, 2009, vol. 114, no. 25, pp. 5236–5244.
Bennett, K.L., Jackson, D.G., Simon, J.C., Tanczos, E., Peach, R., Modrell, B., Stamenkovic, I., Plowman, G., and Aruffo, A., J. Cell Biol., 1995, vol. 128, no. 4, pp. 687–698.
Ponta, H., Sherman, L., and Herrlich, P.A., Nat. Rev. Mol. Cell Biol., 2003, vol. 4, no. 1, pp. 33–45.
Janiszewska, M., De Vito, C., Le Bitoux, M.A., Fusco, C., and Stamenkovic, I., J. Biol. Chem., 2010, vol. 285, no. 40, pp. 30548–30557.
Lee, J.L., Wang, M.J., and Chen, J.Y., J. Cell Biol., 2009, vol. 185, no. 6, pp. 949–957.
Solis, M.A., Chen, Y.H., Wong, T.Y., Bittencourt, V.Z., Lin, Y.C., and Huang, L.L., Biochem. Res. Int., 2012, vol. 2012, 346972.
Shukla, S., Nair, R., Rolle, M.W., Braun, K.R., Chan, C.K., Johnson, P.Y., Wight, T.N., and McDevitt, T.C., J. Histochem. Cytochem., 2010, vol. 58, no. 4, pp. 345–358.
Knudson, W., Bartnik, E., and Knudson, C.B., Proc. Natl. Acad. Sci. USA, 1993, vol. 90, no. 9, pp. 4003–4007.
Sackstein, R., Curr. Opin. Hematol., 2011,vol. 18, no. 4, pp. 239–248.
Zhu, H., Mitsuhashi, N., Klein, A., Barsky, L.W., Weinberg, K., Barr, M.L., Demetriou, A., and Wu, G.D., Stem Cells, 2006, vol. 24, no. 4, pp. 928–935.
Márquez, C., Trigueros, C., Fernández, E., and Toribio, M.L., J. Exp. Med., 1995, vol. 181, no. 2, pp. 475–483.
Ishimoto, T., Nagano, O., Yae, T., Tamada, M., Motohara, T., Oshima, H., Oshima, M., Ikeda, T., Asaba, R., Yagi, H., Masuko, T., Shimizu, T., Ishikawa, T., Kai, K., Takahashi, E., Imamura, Y., Baba, Y., Ohmura, M., Suematsu, M., Baba, H., and Saya, H., Cancer Cell, 2011, vol. 19, no. 3, pp. 387–400.
Su, Y.J., Lai, H.M., Chang, Y.W., Chen, G.Y., and Lee, J.L., EMBO J., 2011, vol. 30, no. 15, pp. 3186–3199.
Singh, A. and Settleman, J., Oncogene, 2010, vol. 29, no. 34, pp. 4741–4751.
Bessède, E., Staedel, C., Acuña Amador, L.A., Nguyen, P.H., Chambonnier, L., Hatakeyama, M., Belleannée, G., Mégraud, F., and Varon, C., Oncogene, 2014, vol. 33, no. 32, pp. 4123–4131.
Jung, T., Castellana, D., Klingbeil, P., Cuesta Hernández, I., Vitacolonna, M., Orlicky, D.J., Roffler, S.R., Brodt, P., and Zöller, M., Neoplasia, 2009, vol. 11, no. 10, pp. 1093–1105.
Chen, Y., Fu, Z., Xu, S., Xu, Y., and Xu, P., Biomed. Pharmacother., 2014, vol. 68, no. 6, pp. 693–697.
Wang, W., Dong, L.P., Zhang, N., and Zhao, C.H., Int. J. Clin. Exp. Med., 2014, vol. 7, no. 12, pp. 5059–5066.
Chen, J., Li, T., Liu, Q., Jiao, H., Yang, W., Liu, X., and Huo, Z., PLoS One, 2014, vol. 9, no. 3, e91842.
Luo, Z., Wu, R.R., Lv, L., Li, P., Zhang, L.Y., Hao, Q.L., and Li, W., Int. J. Clin. Exp. Pathol., 2014, vol. 7, no. 7, pp. 3632–3646.
Zhao, S., He, J.L., Qiu, Z.X., Chen, N.Y., Luo, Z., Chen, B.J., and Li, W.M., Asian Pac. J. Cancer Prev., 2014, vol. 15, no. 16, pp. 6761–6766.
Chai, L., Liu, H., Zhang, Z., Wang, F., Wang, Q., Zhou, S., and Wang, S., Tohoku J. Exp. Med., 2014, vol. 232, no. 1, pp. 9–19.
Chen, J., Zhou, J., Lu, J., Xiong, H., Shi, X., and Gong, L., BMC Cancer, 2014, vol. 14, p.15.
Hu, B., Luo, W., Hu, R.T., Zhou, Y., Qin, S.Y., and Jiang, H.X., Medicine (Baltimore), 2015, vol. 94, no. 31, e1238.
Fu, Y., Geng, Y., Yang, N., Zhu, N., Wang, C.Z., Su, X.C., and Zhang, H.B., Clin. Res. Hepatol. Gastroenterol., 2015, vol. 39, no. 6, pp. 736–739.
Li, X., Ma, X., Chen, L., Gu, L., Zhang, Y., Zhang, F., Ouyang, Y., Gao, Y., Huang, Q., and Zhang, X., Sci. Rep., 2015, vol. 5, p. 13157.
Liu, Y., Wu, Y., Gu, S., Sun, Z., Rui, Y., Wang, J., Lu, Y., Li, H., Xu, K., and Sheng, P., Diagn. Pathol., 2014, vol. 9, p.140.
Herlyn, M., Steplewski, Z., Herlyn, D., and Koprowski, H., Proc. Natl. Acad. Sci. USA, 1979, vol. 76, no. 3, pp. 1438–1442.
Schnell, U., Cirulli, V., and Giepmans, B.N., Biochim. Biophys. Acta, 2013, vol. 1828, no. 8, pp. 1989–2001.
Patriarca, C., Macchi, R.M., Marschner, A.K., and Mellstedt, H., Cancer Treat. Rev., 2012, vol. 38, no. 1, pp. 68–75.
Litvinov, S.V., Velders, M.P., Bakker, H.A., Fleuren, G.J., and Warnaar, S.O., J. Cell Biol., 1994, vol. 125, no. 2, pp. 437–446.
Ladwein, M., Pape, U.F., Schmidt, D.S., Schnölzer, M., Fiedler, S., Langbein, L., Franke, W.W., Moldenhauer, G., and Zöller, M., Exp. Cell Res., 2005, vol. 309, no. 2, pp. 345–357.
Litvinov, S.V., Balzar, M., Winter, M.J., Bakker, H.A., Briaire-de Bruijn, I.H., Prins, F., Fleuren, G.J., and Warnaar, S.O., J. Cell Biol., 1997, vol. 139, no. 5, pp. 1337–1348.
Münz, M., Kieu, C., Mack, B., Schmitt, B., Zeidler, R., and Gires, O., Oncogene, 2004, vol. 23, no. 34, pp. 5748–5758.
Maaser, K. and Borlak, J., Br. J. Cancer, 2008, vol. 99, no. 10, pp. 1635–1643.
Chaves-Pérez, A., Mack, B., Maetzel, D., Kremling, H., Eggert, C., Harréus, U., and Gires, O., Oncogene, 2013, vol. 32, no. 5, pp. 641–650.
Maetzel, D., Denzel, S., Mack, B., Canis, M., Went, P., Benk, M., Kieu, C., Papior, P., Baeuerle, P.A., Munz, M., and Gires, O., Nat. Cell Biol., 2009, vol. 11, no. 2, pp. 162–171.
Schnell, U., Kuipers, J., and Giepmans, B.N., Biosci. Rep., 2013, vol. 33, no. 2, e00030.
Tarmann, T., Dohr, G., Schiechl, H., Barth, S., and Hartmann, M., Acta Anat. (Basel), 1990, vol. 137, no. 2, pp. 141–145.
Schiechl, H. and Dohr, G., Histochemistry, 1987, vol. 87, no. 5, pp. 491–498.
de Boer, C.J., van Krieken, J.H., Janssen-van Rhijn, C.M., and Litvinov, S.V., J. Pathol., 1999, vol. 188, no. 2, pp. 201–206.
Ogura, E., Senzaki, H., Yoshizawa, K., Hioki, K., and Tsubura, A., Anticancer Res., 1998, vol. 18, no. 5B, pp. 3669–3675.
Xie, X., Wang, C.Y., Cao, Y.X., Wang, W., Zhuang, R., Chen, L.H., Dang, N.N., Fang, L., and Jin, B.Q., World J. Gastroenterol., 2005, vol. 11, no. 3, pp. 344–347.
Basak, S., Speicher, D., Eck, S., Wunner, W., Maul, G., Simmons, M.S., and Herlyn, D., J. Natl. Cancer Inst., 1998, vol. 90, no. 9, pp. 691–697.
Sankpal, N.V., Willman, M.W., Fleming, T.P., Mayfield, J.D., and Gillanders, W.E., Cancer Res., 2009, vol. 69, no. 3, pp. 753–757.
Ward, K., Amaya, C., Verma, K., Tran, D., Diaz, D., Torabi, A., and Bryan, B.A., Mol. Clin. Oncol., 2015, vol. 3, no. 1, pp. 31–36.
Spizzo, G., Obrist, P., Ensinger, C., Theurl, I., Dünser, M., Ramoni, A., Gunsilius, E., Eibl, G., Mikuz, G., and Gastl, G., Int. J. Cancer, 2002, vol. 98, no. 6, pp. 883–888.
Varga, M., Obrist, P., Schneeberger, S., Mühlmann, G., Felgel-Farnholz, C., Fong, D., Zitt, M., Brunhuber, T., Schäfer, G., Gastl, G., and Spizzo, G., Clin. Cancer Res., 2004, vol. 10, no. 9, pp. 3131–3136.
Brunner, A., Schaefer, G., Veits, L., Brunner, B., Prelog, M., Ensinger, C., Anticancer Res., 2008, vol. 28, no. 1A, pp. 125–128.
Fong, D., Steurer, M., Obrist, P., Barbieri, V., Margreiter, R., Amberger, A., Laimer, K., Gastl, G., Tzankov, A., and Spizzo, G., J. Clin. Pathol., 2008, vol. 61, no. 1, pp. 31–35.
Seligson, D.B., Pantuck, A.J., Liu, X., Huang, Y., Horvath, S., Bui, M.H., Han, K.R., Correa, A.J., Eeva, M., Tze, S., Belldegrun, A.S., and Figlin, R.A., Clin. Cancer Res., 2004, vol. 10, no. 8, pp. 2659–2669.
Ralhan, R., Cao, J., Lim, T., Macmillan, C., Freeman, J.L., and Walfish, P.G., BMC Cancer, 2010, vol. 10, p.331.
Jin, L., Hope, K.J., Zhai, Q., Smadja-Joffe, F., and Dick, J.E., Nat. Med., 2006, vol. 12, pp. 1167–1174.
Yang, Z.F., Ho, D.W., Ng, M.N., Lau, C.K., Yu, W.C., Ngai, P., Chu, P.W., Lam, C.T., Poon, R.T., and Fan, S.T., Cancer Cell, 2008, vol. 13, no. 2, pp. 153–166.
Deonarain, M.P., Kousparou, C.A., and Epenetos, A.A., MAbs, 2009, vol. 1, no. 1, pp. 12–25.
Emlet, D.R., Gupta, P., Holgado-Madruga, M., Del Vecchio, C.A., Mitra, S.S., Han, S.Y., Li, G., Jensen, K.C., Vogel, H., Xu, L.W., Skirboll, S.S., and Wong, A.J., Cancer Res., 2014, vol. 74, no. 4, pp. 1238–1249.
Schatton, T., Murphy, G.F., Frank, N.Y., Yamaura, K., Waaga-Gasser, A.M., Gasser, M., Zhan, Q., Jordan, S., Duncan, L.M., Weishaupt, C., Fuhlbrigge, R.C., Kupper, T.S., Sayegh, M.H., and Frank, M.H., Nature, 2008, vol. 451, pp. 345–349.
Frank, N.Y., Margaryan, A., Huang, Y., Schatton, T., Waaga-Gasser, A.M., Gasser, M., Sayegh, M.H., Sadee, W., and Frank, M.H., Cancer Res., 2005, vol. 65, pp. 4320–4333.
Li, F. and Sethi, G., Biochim. Biophys. Acta, 2010, vol. 1805, no. 2, pp. 167–180.
Gupta, P.B., Onder, T.T., Jiang, G., Tao, K., Kuperwasser, C., Weinberg, R.A., and Lander, E.S., Cell, 2009, vol. 138, no. 4, pp. 645–659.
Lombardo, Y., Scopelliti, A., Cammareri, P., Todaro, M., Iovino, F., Ricci-Vitiani, L., Gulotta, G., Dieli, F., de Maria, R., and Stassi, G., Gastroenterology, 2011, vol. 140, no. 1, pp. 297–309.
van Es, J.H. and Clevers, H., Trends Mol. Med., 2005, vol. 11, pp. 496–502.
Pellegatta, S., Poliani, P.L., Corno, D., Menghi, F., Ghielmetti, F., Suarez-Merino, B., Caldera, V., Nava, S., Ravanini, M., Facchetti, F., Bruzzone, M.G., and Finocchiaro, G., Cancer Res., 2006, vol. 66, no. 21, pp. 10247–10252.
Ning, N., Pan, Q., Zheng, F., Teitz-Tennenbaum, S., Egenti, M., Yet, J., Li, M., Ginestier, C., Wicha, M.S., Moyer, J.S., Prince, M.E., Xu, Y., Zhang, X.L., Huang, S., Chang, A.E., and Li, Q., Cancer Res., 2012, vol. 72, no. 7, pp. 1853–1864.
Tallerico, R., Todaro, M., Di Franco, S., Maccalli, C., Garofalo, C., Sottile, R., Palmieri, C., Tirinato, L., Pangigadde, P.N., La Rocca, R., Mandelboim, O., Stassi, G., Di Fabrizio, E., Parmiani, G., Moretta, A., Dieli, F., Kärre, K., and Carbone, E., J. Immunol., 2013, vol. 190, no. 5, pp. 2381–2390.
Schmidt-Wolf, I.G., Lefterova, P., Mehta, B.A., Fernandez, L.P., Huhn, D., Blume, K.G., Weissman, I.L., and Negrin, R.S., Exp. Hematol., 1993, vol. 21, no. 13, pp. 1673–1679.
Gammaitoni, L., Giraudo, L., Leuci, V., Todorovic, M., Mesiano, G., Picciotto, F., Pisacane, A., Zaccagna, A., Volpe, M.G., Gallo, S., Caravelli, D., Giacone, E., Venesio, T., Balsamo, A., Pignochino, Y., Grignani, G., Carnevale-Schianca, F., Aglietta, M., and Sangiolo, D., Clin. Cancer Res., 2013, vol. 19, no. 16, pp. 4347–4358.
Sangiolo, D., Mesiano, G., Gammaitoni, L., Leuci, V., Todorovic, M., Giraudo, L., Cammarata, C., Dell’Aglio, C., D’Ambrosio, L., Pisacane, A., Sarotto, I., Miano, S., Ferrero, I., Carnevale-Schianca, F., Pignochino, Y., Sassi, F., Bertotti, A., Piacibello, W., Fagioli, F., Aglietta, M., and Grignani, G., Cancer Res., 2014, vol. 74, no. 1, pp. 119–129.
Dick, J.E., Blood, 2008, vol. 112, no. 13, pp. 4793–4807.
Clevers, H., Nat. Med., 2011, vol. 17, no. 3, pp. 313–319.
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Original Russian Text © Y.S. Kim, A.M. Kaidina, J.-H. Chiang, K.N. Yarygin, A.Yu. Lupatov, 2017, published in Biomeditsinskaya Khimiya.
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Kim, Y.S., Kaidina, A.M., Chiang, JH. et al. Cancer stem cell molecular markers verified in vivo. Biochem. Moscow Suppl. Ser. B 11, 43–54 (2017). https://doi.org/10.1134/S1990750817010036
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DOI: https://doi.org/10.1134/S1990750817010036