This systematic review aims to analyze molecular markers of cancer stem cells. Only studies that confirmed tumor-initiating capacity of this population by in vivo assay in immunodeficient mice were included. Final sample of papers that fully correspond with initial aim consists of 97 original studies. The results of their analysis reveal that markers commonly used for cancer stem cells deriving were as follows: CD133, СD44, ALDH, CD34, CD24 and EpCAM. The review also contains description of molecular features of some cancer stem cell markers, modern approaches to cancer treatment by targeting this population and brief assessment of cancer stem cell theory development.
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Keywords: cancer stem cell, molecular markers, systemic review
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Kim Y.S., Kaidina A.M., Chiang J.H., Yarygin K.N., Lupatov A.Yu. (2016) Molecular markers of cancer stem cells verified in vivo. Biomeditsinskaya Khimiya, 62(3), 228-238.
Kim Y.S. et al. Molecular markers of cancer stem cells verified in vivo // Biomeditsinskaya Khimiya. - 2016. - V. 62. -N 3. - P. 228-238.
Kim Y.S. et al., "Molecular markers of cancer stem cells verified in vivo." Biomeditsinskaya Khimiya 62.3 (2016): 228-238.
Kim, Y. S., Kaidina, A. M., Chiang, J. H., Yarygin, K. N., Lupatov, A. Yu. (2016). Molecular markers of cancer stem cells verified in vivo. Biomeditsinskaya Khimiya, 62(3), 228-238.
Vidal S.J., Rodriguez-Bravo V., Galsky M., Cordon-Cardo C., Domingo-Domenech J. (2014) Oncogene, 33(36), 4451-4463. CrossRef Scholar google search
Guo Z., Li L.Q., Jiang J.H., Ou C., Zeng L.X., Xiang B.D. (2014) World J. Gastroenterol., 20(8), 2098-2106. CrossRef Scholar google search
Qu H., Li R., Liu Z., Zhang J., Luo R. (2013) Int. J. Clin. Exp. Pathol., 6(11), 2644-2650. Scholar google search
Wu Y., Li Z., Zhang C., Yu K., Teng Z., Zheng G., Wang S., Liu Y., Cui L., Yu X. (2015) Int. J. Clin. Exp. Med., 8(3), 3595-3606. Scholar google search
Sugiyama T., Rodriguez R.T., McLean G.W., Kim S.K. (2007) Proc. Natl. Acad. Sci. USA, 104(1), 175-180. CrossRef Scholar google search
Uchida N., Buck D.W., He D., Reitsma M.J., Masek M., Phan T.V., Tsukamoto A.S., Gage F.H., Weissman I.L. (2000) Proc. Natl. Acad. Sci. USA, 97(26), 14720-14725. CrossRef Scholar google search
Bertolini G., Roz L., Perego P., Tortoreto M., Fontanella E., Gatti L., Pratesi G., Fabbri A., Andriani F., Tinelli S. et al. (2009) Proc. Natl. Acad. Sci. USA, 106(38), 16281-16286. CrossRef Scholar google search
Hermann P.C., Huber S.L., Herrler T., Aicher A., Ellwart J.W., Guba M., Bruns C.J., Heeschen C. (2007) Cell Stem Cell, 1(3), 313-323. CrossRef Scholar google search
Zacchigna S., Oh H., Wilsch-Bräuninger M., Missol-Kolka E., Jászai J., Jansen S., Tanimoto N., Tonagel F., Seeliger M., Huttner W.B. et al. (2009) J. Neurosci., 29(7), 2297-2308. CrossRef Scholar google search
Corbeil D., Marzesco A.M., Wilsch-Bräuninger M., Huttner W.B. (2010) FEBS Lett., 584(9), 1659-1664. CrossRef Scholar google search
Weigmann A., Corbeil D., Hellwig A., Huttner W.B. (1997) Proc. Natl. Acad. Sci. USA, 94(23), 12425-12430. CrossRef Scholar google search
Marzesco A.M., Janich P., Wilsch-Bräuninger M., Dubreuil V., Langenfeld K., Corbeil D., Huttner W.B. (2005) J. Cell Sci., 118(13), 2849-2858. CrossRef Scholar google search
Dubreuil V., Marzesco A.M., Corbeil D., Huttner W.B., Wilsch-Bräuninger M. (2007) J. Cell Biol., 176(4), 483-495. CrossRef Scholar google search
Han M., Guo L., Zhang Y., Huang B., Chen A., Chen W., Liu X., Sun S., Wang K., Liu A., Li X. (2016) Mol. Neurobiol., 53(1), 720-727. CrossRef Scholar google search
Zhang W., Chen H., Lv S., Yang H. (2015) Mol. Neurobiol. Epub ahead of print. Scholar google search
Wang K., Xu J., Zhang J., Huang J. (2012) BMC Cancer, 12, 573. Scholar google search
Chen S., Song X., Chen Z., Li X., Li M., Liu H., Li J. (2013) PLoS One, 8(2), e56380. Scholar google search
Wen L., Chen X.Z., Yang K., Chen Z.X., Zhang B., Chen J.P., Zhou Z.G., Mo X.M., Hu J.K. (2013) PLoS One, 8(3), e59154. CrossRef Scholar google search
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., Chen Z.N. (2015) Oncotarget. CrossRef Scholar google search
Hanley W.D., Napier S.L., Burdick M.M., Schnaar R.L., Sackstein R., Konstantopoulos K. (2006) FASEB J., 20 (2), 337-339. Scholar google search
Tremmel M., Matzke A., Albrecht I., Laib A.M., Olaku V., Ballmer-Hofer K., Christofori G., Héroult M., Augustin H.G., Ponta H., Orian-Rousseau V. (2009) Blood, 114(25), 5236-5244. CrossRef Scholar google search
Bennett K.L., Jackson D.G., Simon J.C., Tanczos E., Peach R., Modrell B., Stamenkovic I., Plowman G., Aruffo A. (1995) J. Cell Biol., 128(4), 687-698. CrossRef Scholar google search
Zhu H., Mitsuhashi N., Klein A., Barsky L.W., Weinberg K., Barr M.L., Demetriou A., Wu G.D. (2006) Stem Cells, 24(4), 928-935. CrossRef Scholar google search
Ishimoto T., Nagano O., Yae T., Tamada M., Motohara T., Oshima H., Oshima M., Ikeda T., Asaba R., Yagi H. et al. (2011) Cancer Cell, 19(3), 387-400. CrossRef Scholar google search
Hu B., Luo W., Hu R.T., Zhou Y., Qin S.Y., Jiang H.X. (2015) Medicine (Baltimore), 94(31), e1238. CrossRef Scholar google search
Fu Y., Geng Y., Yang N., Zhu N., Wang C.Z., Su X.C., Zhang H.B. (2015) Clin. Res. Hepatol. Gastroenterol., 39(6), 736-739. CrossRef Scholar google search
Li X., Ma X., Chen L., Gu L., Zhang Y., Zhang F., Ouyang Y., Gao Y., Huang Q., Zhang X. (2015) Sci. Rep., 5, 13157. CrossRef Scholar google search
Liu Y., Wu Y., Gu S., Sun Z., Rui Y., Wang J., Lu Y., Li H., Xu K., Sheng P. (2014) Diagn. Pathol., 9, 140. CrossRef Scholar google search
Herlyn M., Steplewski Z., Herlyn D., Koprowski H. (1979) Proc. Natl. Acad. Sci. USA, 76(3), 1438-1442. CrossRef Scholar google search
Chaves-Pérez A., Mack B., Maetzel D., Kremling H., Eggert C., Harréus U., Gires O. (2013) Oncogene, 32(5), 641-650. CrossRef Scholar google search
Maetzel D., Denzel S., Mack B., Canis M., Went P., Benk M., Kieu C., Papior P., Baeuerle P.A., Munz M., Gires O. (2009) Nat. Cell Biol., 11(2), 162-171. CrossRef Scholar google search
de Boer C.J., van Krieken J.H., Janssen-van Rhijn C.M., Litvinov S.V. (1999) J. Pathol., 188(2), 201-206. CrossRef Scholar google search
Ogura E., Senzaki H., Yoshizawa K., Hioki K., Tsubura A. (1998) Anticancer Res., 18(5B), 3669-3675. Scholar google search
Xie X., Wang C.Y., Cao Y.X., Wang W., Zhuang R., Chen L.H., Dang N.N., Fang L., Jin B.Q. (2005)World J. Gastroenterol., 11(3), 344-347. CrossRef Scholar google search
Basak S., Speicher D., Eck S., Wunner W., Maul G., Simmons M.S., Herlyn D. (1998) J. Natl. Cancer Inst., 90(9), 691-697. CrossRef Scholar google search
Sankpal N.V., Willman M.W., Fleming T.P., Mayfield J.D., Gillanders W.E. (2009) Cancer Res., 69(3), 753-757. CrossRef Scholar google search
Ward K., Amaya C., Verma K., Tran D., Diaz D., Torabi A., Bryan B.A. (2015) Mol. Clin. Oncol., 3(1), 31-36. Scholar google search
Spizzo G., Obrist P., Ensinger C., Theurl I., Dünser M., Ramoni A., Gunsilius E., Eibl G., Mikuz G., Gastl G. (2002) Int. J. Cancer, 98(6), 883-888. CrossRef Scholar google search
Varga M., Obrist P., Schneeberger S., Mühlmann G., Felgel-Farnholz C., Fong D., Zitt M., Brunhuber T., Schäfer G., Gastl G., Spizzo G. (2004) Clin. Cancer Res., 10(9), 3131-3136. CrossRef Scholar google search
Brunner A., Schaefer G., Veits L., Brunner B., Prelog M., Ensinger C. (2008) Anticancer Res., 28(1A), 125-128. Scholar google search
Fong D., Steurer M., Obrist P., Barbieri V., Margreiter R., Amberger A., Laimer K., Gastl G., Tzankov A., Spizzo G. (2008) J. Clin. Pathol., 61(1), 31-35. CrossRef Scholar google search
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., Figlin R.A. (2004) Clin. Cancer Res., 10(8), 2659-2669. CrossRef Scholar google search
Ralhan R., Cao J., Lim T., Macmillan C., Freeman J.L., Walfish P.G. (2010) BMC Cancer, 10, 331. CrossRef Scholar google search
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., Fan S.T. (2008) Cancer Cell, 13(2), 153-166. CrossRef Scholar google search
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., Wong A.J. (2014) Cancer Res., 74(4), 1238-1249. CrossRef Scholar google search
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., Frank M.H. (2008) Nature, 451, 345-349. CrossRef Scholar google search
Frank N.Y., Margaryan A., Huang Y., Schatton T., Waaga-Gasser A.M., Gasser M., Sayegh M.H., Sadee W., Frank M.H. (2005) Cancer Res., 65, 4320-4333. CrossRef Scholar google search
Li F., Sethi G. (2010) Biochim. Biophys. Acta, 1805(2), 167-180. Scholar google search
Gupta P.B., Onder T.T., Jiang G., Tao K., Kuperwasser C., Weinberg R.A., Lander E.S. (2009) Cell, 138(4), 645-659. CrossRef Scholar google search
Lombardo Y., Scopelliti A., Cammareri P., Todaro M., Iovino F., Ricci-Vitiani L., Gulotta G., Dieli F., de Maria R., Stassi G. (2011) Gastroenterology, 140(1), 297-309. CrossRef Scholar google search
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., Finocchiaro G. (2006) Cancer Res., 66(21), 10247-10252. CrossRef Scholar google search
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., Li Q. (2012) Cancer Res., 72(7), 1853-1864. CrossRef Scholar google search
Tallerico R., Todaro M., Di Franco S., Maccalli C., Garofalo C., Sottile R., Palmieri C., Tirinato L., Pangigadde P.N., La Rocca R. et al. (2013) J. Immunol., 190(5), 2381-2390. CrossRef Scholar google search
Gammaitoni L., Giraudo L., Leuci V., Todorovic M., Mesiano G., Picciotto F., Pisacane A., Zaccagna A., Volpe M.G., Gallo S. et al. (2013) Clin. Cancer Res., 19(16), 4347-4358. CrossRef Scholar google search
Sangiolo D., Mesiano G., Gammaitoni L., Leuci V., Todorovic M., Giraudo L., Cammarata C., Dell'Aglio C., D'Ambrosio L., Pisacane A. et al. (2014) Cancer Res., 74(1), 119-129. CrossRef Scholar google search
