Translational potential of cancer stem cells: A review of the detection of cancer stem cells and their roles in cancer recurrence and cancer treatment

Experimental Cell Research

Volumn 335, Issue 1, 2015, Pages 135-147

  Islam, Farhadul ^a   Gopalan, Vinod ^a   Smith, Robert A ^a,b   Lam, Alfred K Y ^a,c  

^a GRIFFITH UNIVERSITY   (Australia)

^b QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^c GOLD COAST UNIVERSITY HOSPITAL   (Australia)

Author keywords

Cancer stem cell; Metastases; Resistant to therapy; Targeted therapy; Treatment

Indexed keywords

CELL MARKER; TUMOR MARKER;

CANCER DIAGNOSIS; CANCER RECURRENCE; CANCER RESISTANCE; CANCER STEM CELL; CANCER THERAPY; CARCINOGENESIS; CELL ISOLATION; HUMAN; METASTASIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; THERAPY RESISTANCE; CELL SEPARATION; CYTOLOGY; NEOPLASMS; PATHOLOGY; PROCEDURES; TUMOR MICROENVIRONMENT; TUMOR RECURRENCE;

ERINACEIDAE;

CELL SEPARATION; HUMANS; NEOPLASM METASTASIS; NEOPLASM RECURRENCE, LOCAL; NEOPLASMS; NEOPLASTIC STEM CELLS; SIGNAL TRANSDUCTION; TUMOR MARKERS, BIOLOGICAL; TUMOR MICROENVIRONMENT;

EID: 84930760451     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2015.04.018     Document Type: Review

References (208)

1. Alison M.R., Lin W.R., Lim S.M., Nicholson L.J. Cancer stem cells: in the line of fire. Cancer Treat Rev. 2012, 38:589-598.
2. Li C., Heidt D.G., Dalerba P., Burant C.F., Zhang L., Adsay V., Wicha M., Clarke M.F., Simeone D.M. Identification of pancreatic cancer stem cells. Cancer Res. 2007, 67:1030-1037.
3. Zhao C., Chen A., Jamieson C.H., Fereshteh M., Abrahamsson A., Blum J., Kwon H.Y., Kim J., Chute J.P., Rizzieri D., Munchhof M., VanArsdale T., Beachy P.A., Reya T. Hedgehog signalling is essential for maintenance of cancer stem cells in myeloid leukaemia. Nature 2009, 458:776-779.
4. Vermeulen L., de Sousa e Melo F., Richel D.J., Medema J.P. The developing cancer stem-cell model: clinical challenges and opportunities. Lancet Oncol. 2012, 13:e83-e89.
5. Garvalov B.K., Acker T. Cancer stem cells: a new framework for the design of tumor therapies. J. Mol. Med. (Berl) 2011, 89:95-107.
6. Wicha M.S., Liu S., Dontu G. Cancer stem cells: an old idea-a paradigm shift. Cancer Res. 2006, 66:1883-1890.
7. Shackleton M. Normal stem cells and cancer stem cells: similar and different. Semin. Cancer Biol. 2010, 20:85-92.
8. Lou H., Dean M. Targeted therapy for cancer stem cells: the patched pathway and ABC transporters. Oncogene 2007, 26:1357-1360.
9. Mak A.B., Blakely K.M., Williams R.A., Penttilä P.A., Shukalyuk A.I., Osman K.T., Kasimer D., Ketela T., Moffat J. CD133 protein N-glycosylation processing contributes to cell surface recognition of the primitive cell marker AC133 epitope. J. Biol. Chem. 2011, 286:41046-41056.
10. Waldron N.N., Kaufman D.S., Oh S., Inde Z., Hexum M.K., Ohlfest J.R., Vallera D.A. Targeting tumor-initiating cancer cells with dCD133KDEL shows impressive tumor reductions in a xenotransplant model of human head and neck cancer. Mol. Cancer Ther. 2011, 10:1829-1838.
11. Campbell L.L., Polyak K. Breast tumor heterogeneity: cancer stem cells or clonal evolution?. Cell Cycle 2007, 6:2332-2338.
12. Nowell P.C. The clonal evolution of tumor cell populations. Science 1976, 194:23-28.
13. Heppner G.H., Miller F.R. The cellular basis of tumor progression. Int. Rev. Cytol. 1998, 177:1-56.
14. Merlo L.M., Pepper J.W., Reid B.J., Maley C.C. Cancer as an evolutionary and ecological process. Nat. Rev. Cancer 2006, 6:924-935.
15. Crespi B., Summers K. Evolutionary biology of cancer. Trends Ecol. Evol. 2005, 20:545-552.
16. Tysnes B.B., Bjerkvig R. Cancer initiation and progression: involvement of stem cells and the microenvironment. Biochim. Biophys. Acta 2007, 1775:283-297.
17. OConnor M.L., Xiang D., Shigdar S., Macdonald J., Li Y., Wang T., Pu C., Wang Z., Qiao L., Duan W. Cancer stem cells: a contentious hypothesis now moving forward. Cancer Lett. 2014, 344:180-187.
18. Reya T., Morrison S.J., Clarke M.F., Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 2001, 414:105-111.
19. Al-Hajj M., Clarke M.F. Self-renewal and solid tumor stem cells. Oncogene 2004, 23:7274-7282.
20. Islam F., Qiao B., Smith R.A., Gopalan V., Lam A.K. Cancer stem cell: fundamental experimental pathological concepts and updates. Exp. Mol. Pathol. 2015, 98:184-191.
21. Lianidou E.S., Markou A. Circulating tumor cells in breast cancer: detection systems, molecular characterization, and future challenges. Clin. Chem. 2011, 57:1242-1255.
22. Tirino V., Desiderio V., Paino F., De Rosa A., Papaccio F., La Noce M., Laino L., De Francesco F., Papaccio G. Cancer stem cells in solid tumors: an overview and new approaches for their isolation and characterization. FASEB J. 2013, 27:13-24.
23. Milne A.N., Carneiro F., OMorain C., Offerhaus G.J. Nature meets nurture: molecular genetics of gastric cancer. Hum. Genet. 2009, 126:615-628.
24. Podberezin M., Wen J., Chang C.C. Cancer stem cells: a review of potential clinical applications. Arch. Pathol. Lab Med. 2013, 137:1111-1116.
25. Kentrou N.A., Tsagarakis N.J., Tzanetou K., Damala M., Papadimitriou K.A., Skoumi D., Stratigaki A., Anagnostopoulos N.I., Malamou-Lada E., Athanassiadou P., Paterakis G. An improved flow cytometric assay for detection and discrimination between malignant cells and atypical mesothelial cells, in serous cavity effusions. Cytometry B Clin. Cytom. 2011, 80:324-334.
26. Greve B., Beller C., Cassens U., Sibrowski W., Göhde W. The impact of erythrocyte lysing procedures on the recovery of hematopoietic progenitor cells in flow cytometric analysis. Stem Cells 2006, 24:793-799.
27. Stathopoulou A., Gizi A., Perraki M., Apostolaki S., Malamos N., Mavroudis D., Georgoulias V., Lianidou E.S. Real-time quantification of CK-19 mRNA-positive cells in peripheral blood of breast cancer patients using the lightcycler system. Clin. Cancer Res. 2003, 9:5145-5151.
28. Stathopoulou A., Ntoulia M., Perraki M., Apostolaki S., Mavroudis D., Malamos N., Georgoulias V., Lianidou E.S. A highly specific real-time RT-PCR method for the quantitative determination of CK-19 mRNA positive cells in peripheral blood of patients with operable breast cancer. Int. J. Cancer 2006, 119:1654-1659.
29. Obermayr E., Sanchez-Cabo F., Tea M.K., Singer C.F., Krainer M., Fischer M.B., Sehouli J., Reinthaller A., Horvat R., Heinze G., Tong D., Zeillinger R. Assessment of a six gene panel for the molecular detection of circulating tumor cells in the blood of female cancer patients. BMC Cancer 2010, 10:666.
30. Aktas B., Tewes M., Fehm T., Hauch S., Kimmig R., Kasimir-Bauer S. Stem cell and epithelial-mesenchymal transition markers are frequently overexpressed in circulating tumor cells of metastatic breast cancer patients. Breast Cancer Res. 2009, 11:R46.
31. Sieuwerts A.M., Kraan J., Bolt-de Vries J., van der Spoel P., Mostert B., Martens J.W., Gratama J.W., Sleijfer S., Foekens J.A. Molecular characterization of circulating tumor cells in large quantities of contaminating leukocytes by a multiplex real-time PCR. Breast Cancer Res. Treat 2009, 118:455-468.
32. Fulawka L., Donizy P., Halon A. Cancer stem cells - the current status of an old concept: literature review and clinical approaches. Biol. Res. 2014, 47:66.
33. Singh S.K., Clarke I.D., Terasaki M., Bonn V.E., Hawkins C., Squire J., Dirks P.B. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003, 63:5821-5828.
34. Eramo A., Lotti F., Sette G., Pilozzi E., Biffoni M., Di Virgilio A., Conticello C., Ruco L., Peschle C., De Maria R. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 2007, 15:504-514.
35. Hermann P.C., Huber S.L., Herrler T., Aicher A., Ellwart J.W., Guba M., Bruns C.J., Heeschen C. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 2007, 1:313-323.
36. Collins A.T., Berry P.A., Hyde C., Stower M.J., Maitland N.J. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 2005, 65:10946-10951.
37. Cheung A.M., Wan T.S., Leung J.C., Chan L.Y., Huang H., Kwong Y.L., Liang R., Leung A.Y. Aldehyde dehydrogenase activity in leukemic blasts defines a subgroup of acute myeloid leukemia with adverse prognosis and superior NOD/ SCID engrafting potential. Leukemia 2007, 21:1423-1430.
38. Ginestier C., Hur M.H., Charafe-Jauffret E., Monville F., Dutcher J., Brown M., Jacquemier J., Viens P., Kleer C.G., Liu S., Schott A., Hayes D., Birnbaum D., Wicha M.S., Dontu G. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 2007, 1:555-567.
39. Carpentino J.E., Hynes M.J., Appelman H.D., Zheng T., Steindler D.A., Scott E.W., Huang E.H. Aldehyde dehydrogenase-expressing colon stem cells contribute to tumorigenesis in the transition from colitis to cancer. Cancer Res. 2009, 69:8208-8215.
40. Ma S., Chan K.W., Lee T.K., Tang K.H., Wo J.Y., Zheng B.J., Guan X.Y. Aldehyde dehydrogenase discriminates the CD133 liver cancer stem cell populations. Mol. Cancer Res. 2008, 6:1146-1153.
41. Jiang F., Qiu Q., Khanna A., Todd N.W., Deepak J., Xing L., Wang H., Liu Z., Su Y., Stass S.A., Katz R.L. Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol. Cancer Res. 2009, 7:330-338.
42. Rasheed Z.A., Yang J., Wang Q., Kowalski J., Freed I., Murter C., Hong S.M., Koorstra J.B., Rajeshkumar N.V., He X., Goggins M., Iacobuzio-Donahue C., Berman D.M., Laheru D., Jimeno A., Hidalgo M., Maitra A., Matsui W. Prognostic significance of tumorigenic cells with mesenchymal features in pancreatic adenocarcinoma. J. Natl. Cancer Inst. 2010, 102:340-351.
43. Li R., Wu X., Wei H., Tian S. Characterization of side population cells isolated from the gastric cancer cell line SGC-7901. Oncol. Lett 2013, 5:877-883.
44. Li X.X., Dong Y., Wang W., Wang H.L., Chen Y.Y., Shi G.Y., Yi J., Wang J. Emodin as an effective agent in targeting cancer stem-like side population cells of gallbladder carcinoma. Stem Cells Dev. 2013, 22:554-566.
45. Paget S. The distribution of growth in cancer of the breast. Lancet 1889, 1:571-573.
46. Southam C., Brunschwig A. Quantitative studies of autotransplantation of human cancer. Cancer 1961, 14:461-463.
47. Vermeulen L., Sprick M.R., Kemper K., Stassi G., Medema J.P. Cancer stem cells-old concepts, new insights. Cell Death Differ 2008, 15:947-958.
48. Petersen B.E., Bowen W.C., Patrene K.D., Mars W.M., Sullivan A.K., Murase N., Boggs S.S., Greenberger J.S., Goff J.P. Bone marrow as a potential source of hepatic oval cells. Science 1999, 284:1168-1170.
49. Bjornson C.R., Rietze R.L., Reynolds B.A., Magli M.C., Vescovi A.L. Turning brain into blood: a hematopoietic fate adopted by adult neural stem cells in vivo. Science 1999, 283:534-537.
50. Blau H.M., Brazelton T.R., Weimann J.M. The evolving concept of a stem cell: entity or function?. Cell 2001, 105:829-841.
51. Zipori D. The nature of stem cells: state rather than entity. Nat. Rev. Genet. 2004, 5:873-878.
52. Mocellin S., Keilholz U., Rossi C.R., Nitti D. Circulating tumor cells: the 'leukemic phase' of solid cancers. Trends Mol. Med. 2006, 12:130-139.
53. Chang Y.S., di T.E., McDonald D.M., Jones R., Jain R.K., Munn L.L. Mosaic blood vessels in tumors: frequency of cancer cells in contact with flowing blood. Proc. Natl. Acad. Sci. USA 2000, 97:14608-14613.
54. Malanchi I., Santamaria-Martinez A., Susanto E., Peng H., Lehr H.A., Delaloye J.F., Huelsken J. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 2012, 481:85-89.
55. Brabletz T., Jung A., Spaderna S., Hlubek F., Kirchner T. Opinion: migrating cancer stem cells-an integrated concept of malignant tumour progression. Nat. Rev. Cancer 2005, 5:744-749.
56. Zhang S.S., Han Z.P., Jing Y.Y., Tao S.F., Li T.J., Wang H., Wang Y., Li R., Yang Y., Zhao X., Xu X.D., Yu E.D., Rui Y.C., Liu H.J., Zhang L., Wei L.X. CD133(+)CXCR4(+) colon cancer cells exhibit metastatic potential and predict poor prognosis of patients. BMC Med. 2012, 10:85.
57. Pang R., Law W.L., Chu A.C., Poon J.T., Lam C.S., Chow A.K., Ng L., Cheung L.W., Lan X.R., Lan H.Y., Tan V.P., Yau T.C., Poon R.T., Wong B.C. A subpopulation of CD26+ cancer stem cells with metastatic capacity in human colorectal cancer. Cell Stem Cell 2010, 6:603-615.
58. Dieter S.M., Ball C.R., Hoffmann C.M., Nowrouzi A., Herbst F., Zavidij O., Abel U., Arens A., Weichert W., Brand K., Koch M., Weitz J., Schmidt M., von Kalle C., Glimm H. Distinct types of tumor-initiating cells form human colon cancer tumors and metastases. Cell Stem Cell 2011, 9:357-365.
59. Colak S., Medema J.P. Cancer stem cells--important players in tumor therapy resistance. FEBS J. 2014, 281:4779-4791.
60. Cojoc M., Mäbert K., Muders M.H., Dubrovska A. A role for cancer stem cells in therapy resistance: cellular and molecular mechanisms. Semin. Cancer Biol. 2014, (14):00079. pii: S1044-579X, 0.
61. Ciurea M.E., Georgescu A.M., Purcaru S.O., Artene S.A., Emami G.H., Boldeanu M.V., Tache D.E., Dricu A. Cancer stem cells: biological functions and therapeutically targeting. Int. J. Mol. Sci. 2014, 15:8169-8185.
62. Wang J., Li Z.H., White J., Zhang L.B. Lung cancer stem cells and implications for future therapeutics. Cell Biochem. Biophys. 2014, 69:389-398.
63. Rycaj K., Tang D.G. Cancer stem cells and radioresistance. Int. J. Radiat. Biol. 2014, 90:615-621.
64. Paldino E., Tesori V., Casalbore P., Gasbarrini A., Puglisi M.A. Tumor initiating cells and chemoresistance: which is the best strategy to target colon cancer stem cells?. Biomed. Res. Int. 2014, 2014:859871.
65. Colak S., Zimberlin C.D., Fessler E., Hogdal L., Prasetyanti P.R., Grandela C.M., Letai A., Medema J.P. Decreased mitochondrial priming determines chemoresistance of colon cancer stem cells. Cell Death Differ 2014, 21:1170-1177.
66. Ma S., Lee T.K., Zheng B.J., Chan K.W., Guan X.Y. CD133+ HCC cancer stem cells confer chemoresistance by preferential expression of the Akt/PKB survival pathway. Oncogene 2008, 27:1749-1758.
67. 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., Sozzi G. Highly tumorigenic lung cancer CD133+ cells display stem-like features and are spared by cisplatin treatment. Proc. Natl. Acad. Sci. USA 2009, 106:16281-16286.
68. Kim M.P., Fleming J.B., Wang H., Abbruzzese J.L., Choi W., Kopetz S., McConkey D.J., Evans D.B., Gallick G.E. ALDH activity selectively defines an enhanced tumor-initiating cell population relative to CD133 expression in human pancreatic adenocarcinoma. PLoS One 2011, 6:e20636.
69. Ginestier C., Liu S., Diebel M.E., Korkaya H., Luo M., Brown M., Wicinski J., Cabaud O., Charafe-Jauffret E., Birnbaum D., Guan J.L., Dontu G., Wicha M.S. CXCR1 blockade selectively targets human breast cancer stem cells in vitro and in xenografts. J. Clin. Invest. 2010, 120:485-497.
70. OHare T., Corbin A.S., Druker B.J. Targeted CML therapy: controlling drug resistance, seeking cure. Curr. Opin. Genet. Dev. 2006, 16:92-99.
71. Oravecz-Wilson K.I., Philips S.T., Yilmaz O.H., Ames H.M., Li L., Crawford B.D., Gauvin A.M., Lucas P.C., Sitwala K., Downing J.R., Morrison S.J., Ross T.S. Persistence of leukemia-initiating cells in a conditional knockin model of an imatinib-responsive myeloproliferative disorder. Cancer Cell 2009, 16:137-148.
72. Todaro M., Alea M.P., Di Stefano A.B., Cammareri P., Vermeulen L., Iovino F., Tripodo C., Russo A., Gulotta G., Medema J.P., Stassi G. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell 2007, 1:389-402.
73. Dylla S.J., Beviglia L., Park I.K., Chartier C., Raval J., Ngan L., Pickell K., Aguilar J., Lazetic S., Smith-Berdan S., Clarke M.F., Hoey T., Lewicki J., Gurney A.L. Colorectal cancer stem cells are enriched in xenogeneic tumors following chemotherapy. PLoS One 2008, 3:e2428.
74. Ishikawa F., Yoshida S., Saito Y., Hijikata A., Kitamura H., Tanaka S., Nakamura R., Tanaka T., Tomiyama H., Saito N., Fukata M., Miyamoto T., Lyons B., Ohshima K., Uchida N., Taniguchi S., Ohara O., Akashi K., Harada M., Shultz L.D. Chemotherapy-resistant human AML stem cells home to and engraft within the bone-marrow endosteal region. Nat. Biotechnol. 2007, 25:1315-1321.
75. Baumann M., Krause M., Hill R. Exploring the role of cancer stem cells in radioresistance. Nat. Rev. Cancer 2008, 8:545-554.
76. Bao S., Wu Q., McLendon R.E., Hao Y., Shi Q., Hjelmeland A.B., Dewhirst M.W., Bigner D.D., Rich J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444:756-760.
77. Diehn M., Cho R.W., Lobo N.A., Kalisky T., Dorie M.J., Kulp A.N., Qian D., Lam J.S., Ailles L.E., Wong M., Joshua B., Kaplan M.J., Wapnir I., Dirbas F.M., Somlo G., Garberoglio C., Paz B., Shen J., Lau S.K., Quake S.R., Brown J.M., Weissman I.L., Clarke M.F. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009, 458:780-783.
78. Zhou J., Wulfkuhle J., Zhang H., Gu P., Yang Y., Deng J., Margolick J.B., Liotta L.A., Petricoin E., Zhang Y. Activation of the PTEN/mTOR/STAT3 pathway in breast cancer stem-like cells is required for viability and maintenance. Proc. Natl. Acad. Sci. USA 2007, 104:16158-16163.
79. Hardt O., Wild S., Oerlecke I., Hofmann K., Luo S., Wiencek Y., Kantelhardt E., Vess C., Smith G.P., Schroth G.P., Bosio A., Dittmer J. Highly sensitive profiling of CD44+/CD24- breast cancer stem cells by combining global mRNA amplification and next generation sequencing: evidence for a hyperactive PI3K pathway. Cancer Lett. 2012, 325:165-174.
80. Berns K., Horlings H.M., Hennessy B.T., Madiredjo M., Hijmans E.M., Beelen K., Linn S.C., Gonzalez-Angulo A.M., Stemke-Hale K., Hauptmann M., Beijersbergen R.L., Mills G.B., van de Vijver M.J., Bernards R. A functional genetic approach identifies the PI3K pathway as a major determinant of trastuzumab resistance in breast cancer. Cancer Cell 2007, 12:395-402.
81. - stem cell-like breast cancer cells in human tumors. J. Clin. Invest. 2011, 121:2723-2735.
82. Peitzsch C., Kurth I., Kunz-Schughart L., Baumann M., Dubrovska A. Discovery of the cancer stem cell related determinants of radio resistance. Radiother. Oncol. 2013, 108:378-387.
83. Ulasov I.V., Nandi S., Dey M., Sonabend A.M., Lesniak M.S. Inhibition of Sonic hedgehog and Notch pathways enhances sensitivity of CD133(+) glioma stem cells to temozolomide therapy. Mol. Med. 2011, 17:103-112.
84. Liu Y.P., Yang C.J., Huang M.S., Yeh C.T., Wu A.T., Lee Y.C., Lai T.C., Lee C.H., Hsiao Y.W., Lu J., Shen C.N., Lu P.J., Hsiao M. Cisplatin selects for multidrug-resistant CD133+ cells in lung adenocarcinoma by activating Notch signaling. Cancer Res. 2013, 73:406-416.
85. McAuliffe S.M., Morgan S.L., Wyant G.A., Tran L.T., Muto K.W., Chen Y.S., Chin K.T., Partridge J.C., Poole B.B., Cheng K.H., Daggett J., Cullen K., Kantoff E., Hasselbatt K., Berkowitz J., Muto M.G., Berkowitz R.S., Aster J.C., Matulonis U.A., Dinulescu D.M. Targeting Notch, a key pathway for ovarian cancer stem cells, sensitizes tumors to platinum therapy. Proc. Natl. Acad. Sci. USA 2012, 109:E2939-E2948.
86. Mohler J. Requirements for hedgehog, a segmental polarity gene, in patterning larval and adult cuticle of Drosophila. Genetics 1988, 120:1061-1072.
87. Qiang L., Yang Y., Ma Y.J., Chen F.H., Zhang L.B., Liu W., Qi Q., Lu N., Tao L., Wang X.T., You Q.D., Guo Q.L. Isolation and characterization of cancer stem like cells in human glioblastoma cell lines. Cancer Lett. 2009, 279:13-21.
88. Ma X., Chen K., Huang S., Zhang X., Adegboyega P.A., Evers B.M., Zhang H., Xie J. Frequent activation of the hedgehog pathway in advanced gastric adenocarcinomas. Carcinogenesis 2005, 26:1698-1705.
89. Taylor M.D., Liu L., Raffel C., Hui C.C., Mainprize T.G., Zhang X., Agatep R., Chiappa S., Gao L., Lowrance A., Hao A., Goldstein A.M., Stavrou T., Scherer S.W., Dura W.T., Wainwright B., Squire J.A., Rutka J.T., Hogg D. Mutations in SUFU predispose to medulloblastoma. Nat. Genet. 2002, 31:306-310.
90. Dahmane N., Lee J., Robins P., Heller P., Ruiz i Altaba A. Activation of the transcription factor Gli1 and the Sonic hedgehog signalling pathway in skin tumours. Nature 1997, 389:876-881.
91. Ruiz i Altaba A., Sánchez P., Dahmane N. Gli and hedgehog in cancer: tumours, embryos and stem cells. Nat. Rev. Cancer 2002, 2:361-372.
92. Nusse R., Varmus H. Three decades of Wnts: a personal perspective on how a scientific field developed. EMBO J. 2012, 31:2670-2684.
93. Vermeulen L., De Sousa E., Melo F., van der Heijden M., Cameron K., de Jong J.H., Borovski T., Tuynman J.B., Todaro M., Merz C., Rodermond H., Sprick M.R., Kemper K., Richel D.J., Stassi G., Medema J.P. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat. Cell Biol. 2010, 12:468-476.
94. Polakis P. Wnt signaling in cancer. Cold Spring Harb. Perspect Biol. 2012, 4. pii: a008052.
95. Pardal R., Clarke M.F., Morrison S.J. Applying the principles of stem-cell biology to cancer. Nat. Rev. Cancer 2003, 3:895-902.
96. Heidel F.H., Bullinger L., Feng Z., Wang Z., Neff T.A., Stein L., Kalaitzidis D., Lane S.W., Armstrong S.A. Genetic and pharmacologic inhibition of β-catenin targets imatinib-resistant leukemia stem cells in CML. Cell Stem Cell 2012, 10:412-424.
97. Wang Y., Krivtsov A.V., Sinha A.U., North T.E., Goessling W., Feng Z., Zon L.I., Armstrong S.A. The Wnt/beta-catenin pathway is required for the development of leukemia stem cells in AML. Science 2010, 327:1650-1653.
98. Yeung J., Esposito M.T., Gandillet A., Zeisig B.B., Griessinger E., Bonnet D., So C.W. β-Catenin mediates the establishment and drug resistance of MLL leukemic stem cells. Cancer Cell 2010, 18:606-618.
99. Swaminathan S.K., Roger E., Toti U., Niu L., Ohlfest J.R., Panyam J. CD133-targeted paclitaxel delivery inhibits local tumor recurrence in a mouse model of breast cancer. J. Control Release 2013, 171:280-287.
100. Damek-Poprawa M., Volgina A., Korostoff J., Sollecito T.P., Brose M.S., OMalley B.W., Akintoye S.O., DiRienzo J.M. Targeted inhibition of CD133+ cells in oral cancer cell lines. J. Dent. Res. 2011, 90:638-645.
101. Bach P., Abel T., Hoffmann C., Gal Z., Braun G., Voelker I., Ball C.R., Johnston I.C., Lauer U.M., Herold-Mende C., Mühlebach M.D., Glimm H., Buchholz C.J. Specific elimination of CD133+ tumor cells with targeted oncolytic measles virus. Cancer Res. 2013, 73:865-874.
102. Yao H.J., Zhang Y.G., Sun L., Liu Y. The effect of hyaluronic acid functionalized carbon nanotubes loaded with salinomycin on gastric cancer stem cells. Biomaterials 2014, 35:9208-9223.
103. Waldron N.N., Barsky S.H., Dougherty P.R., Vallera D.A. A bispecific EpCAM/CD133-targeted toxin is effective against carcinoma. Target Oncol. 2014, 9:239-249.
104. Song Y., Zhu Z., An Y., Zhang W., Zhang H., Liu D., Yu C., Duan W., Yang C.J. Selection of DNA aptamers against epithelial cell adhesion molecule for cancer cell imaging and circulating tumor cell capture. Anal. Chem. 2013, 85:4141-4149.
105. Mueller M.M., Fusenig N.E. Friends or foes - bipolar effects of the tumour stroma in cancer. Nat. Rev. Cancer 2004, 4:839-849.
106. Hanahan D., Coussens L.M. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 2012, 21:309-322.
107. Ma X., Holt D., Kundu N., Reader J., Goloubeva O., Take Y., Fulton A.M. A prostaglandin E (PGE) receptor EP4 antagonist protects natural killer cells from PGE(2)-mediated immunosuppression and inhibits breast cancer metastasis. Oncoimmunology 2013, 2:e22647.
108. Lin L., Amin R., Gallicano G.I., Glasgow E., Jogunoori W., Jessup J.M., Zasloff M., Marshall J.L., Shetty K., Johnson L., Mishra L., He A.R. The STAT3 inhibitor NSC 74859 is effective in hepatocellular cancers with disrupted TGF-beta signaling. Oncogene 2009, 28:961-972.
109. Gatti M., Pattarozzi A., Bajetto A., Würth R., Daga A., Fiaschi P., Zona G., Florio T., Barbieri F. Inhibition of CXCL12/CXCR4 autocrine/paracrine loop reduces viability of human glioblastoma stem-like cells affecting self-renewal activity. Toxicology 2013, 314:209-220.
110. Warrell R.P., The de H.J., Wang Z.Y., Degos L. Acute promyelocytic leukaemia. N. Engl. J. Med. 1993, 3:177-189.
111. Nowak D., Stewart D., Koeffler H.P. Differentiation therapy of leukemia: 3 decades of development. Blood 2009, 113:3655-3665.
112. You N., Zheng L., Liu W., Zhong X., Wang W., Li J. Proliferation inhibition and differentiation induction of hepatic cancer stem cells by knockdown of BC047440: a potential therapeutic target of stem cell treatment for hepatocellular carcinoma. Oncol. Rep. 2014, 31:1911-1920.
113. Zheng L., Liang P., Li J., Huang X.B., Wang W.W., Wang L., Feng H. Expression of BC047440 protein in hepatocellular carcinoma and its relationship to prognosis. Chin. J. Cancer 2010, 29:931-936.
114. Zieker D., Bühler S., Ustündag Z., Königsrainer I., Manncke S., Bajaeifer K., Vollmer J., Fend F., Northoff H., Königsrainer A., Glatzle J. Induction of tumor stem cell differentiation-novel strategy to overcome therapy resistance in gastric cancer. Langenbecks Arch. Surg. 2013, 398:603-688.
115. Dong Y., Han Q., Zou Y., Deng Z., Lu X., Wang X., Zhang W., Jin H., Su J., Jiang T., Ren H. Long-term exposure to imatinib reduced cancer stem cell ability through induction of cell differentiation via activation of MAPK signaling in glioblastoma cells. Mol. Cell Biochem. 2012, 370:89-102.
116. Wu H., Scher B.M., Chu C.L., Leonard M., Olmedo R., Scher G.S., Stecker S., Scher W., Waxman S. Reduction in lactate accumulation correlates with differentiation-induced terminal cell division of leukemia cells. Differentiation 1991, 48:51-58.
117. Arcangeli A., Carlà M., Del Bene M.R., Becchetti A., Wanke E., Olivotto M. Polar/apolar compounds induce leukemia cell differentiation by modulating cell-surface potential. Proc. Natl. Acad. Sci. USA 1993, 90:5858-5862.
118. Olsson I., Gullberg U., Ivhed I., Nilsson K. Induction of differentiation of the human histiocytic lymphoma cell line U-937 by 1 alpha,25-dihydroxycholecalciferol. Cancer Res. 1983, 43:5862-5867.
119. Munster P.N., Troso-Sandoval T., Rosen N., Rifkind R., Marks P.A., Richon V.M. The histone deacetylase inhibitor suberoylanilide hydroxamic acid induces differentiation of human breast cancer cells. Cancer Res. 2001, 61:8492-8497.
120. Uchida H., Maruyama T., Nagashima T., Asada H., Yoshimura Y. Histone deacetylase inhibitors induce differentiation of human endometrial adenocarcinoma cells through up-regulation of glycodelin. Endocrinology 2005, 146:5365-5373.
121. Vik-Mo E.O., Nyakas M., Mikkelsen B.V., Moe M.C., Due-Tønnesen P., Suso E.M., Sæbøe-Larssen S., Sandberg C., Brinchmann J.E., Helseth E., Rasmussen A.M., Lote K., Aamdal S., Gaudernack G., Kvalheim G., Langmoen I.A. Therapeutic vaccination against autologous cancer stem cells with mRNA-transfected dendritic cells in patients with glioblastoma. Cancer Immunol. Immunother. 2013, 62:1499-1509.
122. 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., Sangiolo D. Effective activity of cytokine-induced killer cells against autologous metastatic melanoma including cells with stemness features. Clin. Cancer Res. 2013, 19:4347-4358.
123. Nishio N., Fujita M., Tanaka Y., Maki H., Zhang R., Hirosawa T., Demachi-Okamura A., Uemura Y., Taguchi O., Takahashi Y., Kojima S., Kuzushima K. Zoledronate sensitizes neuroblastoma-derived tumor-initiating cells to cytolysis mediated by human γδ T cells. J. Immunother. 2012, 35:598-606.
124. Cervantes F., Pierson B.A., McGlave P.B., Verfaillie C.M., Miller J.S. Autologous activated natural killer cells suppress primitive chronic myelogenous leukemia progenitors in long-term culture. Blood 1996, 87:2476-2485.
125. Xu Q., Liu G., Yuan X., Xu M., Wang H., Ji J., Konda B., Black K.L., Yu J.S. Antigen-specific T-cell response from dendritic cell vaccination using cancer stem-like cell-associated antigens. Stem Cells 2009, 27:1734-1740.
126. Warburg O., Wind F., Negelein E. The metabolism of tumors in the body. J. Gen Physiol. 1927, 8:519-530.
127. Jones R.G., Thompson C.B. Tumor suppressors and cell metabolism: a recipe for cancer growth. Genes Dev. 2009, 23:537-548.
128. Thompson C.B. Rethinking the regulation of cellular metabolism. Cold Spring Harb. Symp. Quant. Biol. 2011, 76:23-29.
129. Daye D., Wellen K.E. Metabolic reprogramming in cancer: unraveling the role of glutamine in tumorigenesis. Semin Cell Dev. Biol. 2012, 23:362-369.
130. Kroemer G., Pouyssegur J. Tumor cell metabolism: cancer[U+05F3]s Achilles[U+05F3] heel. Cancer Cell 2008, 13:472-482.
131. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
132. Akao Y., Noguchi S., Iio A., Kojima K., Takagi T., Naoe T. Dysregulation of microRNA-34a expression causes drug-resistance to 5-FU in human colon cancer DLD-1 cells. Cancer Lett. 2011, 300:197-204.
133. Cassens U., Greve B., Tapernon K., Nave B., Severin E., Sibrowski W., Göhde W. A novel true volumetric method for the determination of residual leucocytes in blood components. Vox Sang 2002, 82:198-206.
134. Panchision D.M., Chen H.L., Pistollato F., Papini D., Ni H.T., Hawley T.S. Optimized flow cytometric analysis of central nervous system tissue reveals novel functional relationships among cells expressing CD133, CD15, and CD24. Stem Cells 2007, 25:1560-1570.
135. Moghbeli M., Moghbeli F., Forghanifard M.M., Abbaszadegan M.R. Cancer stem cell detection and isolation. Med. Oncol. 2014, 31:69.
136. Ablett G.A., Smith P.J., Sheridan J.W., Lihou M.G. Limitations of the agar colony-forming assay for the assessment of paediatric tumours. Br. J. Cancer 1984, 50:541-544.
137. Pastrana E., Silva-Vargas V., Doetsch F. Eyes wide open: a critical review of sphere-formation as an assay for stem cells. Cell Stem Cell 2011, 8:486-498.
138. Yu C., Yao Z., Dai J., Zhang H., Escara-Wilke J., Zhang X., Keller E.T. ALDH activity indicates increased tumorigenic cells, but not cancer stem cells, in prostate cancer cell lines. In Vivo 2011, 25:69-76.
139. Mo S.L., Li J., Loh Y.S., Brown R.D., Smith A.L., Chen Y., Joshua D., Roufogalis B.D., Li G.Q., Fan K., Ng M.C., Sze D.M. Factors influencing the abundance of the side population in a human myeloma cell line. Bone Marrow Res. 2011, 2011:524845.
140. Pece S., Tosoni D., Confalonieri S., Mazzarol G., Vecchi M., Ronzoni S., Bernard L., Viale G., Pelicci P.G., Di Fiore P.P. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 2010, 140:62-73.
141. Slade M.J., Smith B.M., Sinnett H.D., Cross N.C., Coombes R.C. Quantitative polymerase chain reaction for the detection of micrometastases in patients with breast cancer. J. Clin. Oncol. 1999, 17:870-879.
142. Reinholz M.M., Nibbe A., Jonart L.M., Kitzmann K., Suman V.J., Ingle J.N., Houghton R., Zehentner B., Roche P.C., Lingle W.L. Evaluation of a panel of tumor markers for molecular detection of circulating cancer cells in women with suspected breast cancer. Clin. Cancer Res. 2005, 11:3722. 2732.
143. Progatzky F., Dallman M.J., Lo Celso C. From seeing to believing: labelling strategies for in vivo cell-tracking experiments. Interface Focus 2013, 3:20130001.
144. Schadendorf D., Dorn-Beineke A., Borelli S., Riethmuller G., Pantel K. Limitations of the immunocytochemical detection of isolated tumor cells in frozen samples of bone marrow obtained from melanoma patients. Exp. Dermatol. 2003, 12:165-171.
145. Bunea M., Zarnescu O. New current aspects on the immunohistochemical techniques. Roum Biotechnol. Lett. 2001, 6:177-206.
146. Lin H.K., Zheng S., Williams A.J., Balic M., Groshen S., Scher H.I., Fleisher M., Stadler W., Datar R.H., Tai Y.C., Cote R.J. Portable filter-based microdevice for detection and characterization of circulating tumor cells. Clin. Cancer Res. 2010, 16:5011-5018.
147. Zheng S., Lin H.K., Lu B., Williams A., Datar R., Cote R.J., Tai Y.C. 3D microfilter device for viable circulating tumor cell (CTC) enrichment from blood. Biomed. Microdev. 2011, 13:203-213.
148. Nagrath S., Sequist L.V., Maheswaran S., Bell D.W., Irimia D., Ulkus L., Smith M.R., Kwak E.L., Digumarthy S., Muzikansky A., Ryan P., Balis U.J., Tompkins R.G., Haber D.A., Toner M. Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature 2007, 450:1235-1239.
149. Stott S.L., Hsu C.H., Tsukrov D.I., Yu M., Miyamoto D.T., Waltman B.A., Rothenberg S.M., Shah A.M., Smas M.E., Korir G.K., Floyd F.P., Gilman A.J., Lord J.B., Winokur D., Springer S., Irimia D., Nagrath S., Sequist L.V., Lee R.J., Isselbacher K.J., Maheswaran S., Haber D.A., Toner M. Isolation of circulating tumor cells using a microvortex-generating herringbone-chip. Proc. Natl. Acad. Sci. USA 2010, 107:18392-18397.
150. Ponta H., Sherman L., Herrlich P.A. CD44: from adhesion molecules to signalling regulators. Nat. Rev. Mol. Cell Biol. 2003, 4:33-45.
151. Takaishi S., Okumura T., Tu S., Wang S.S., Shibata W., Vigneshwaran R., Gordon S.A., Shimada Y., Wang T.C. Identification of gastric cancer stem cells using the cell surface marker CD44. Stem Cells 2009, 27:1006-1020.
152. Prince M.E., Sivanandan R., Kaczorowski A., Wolf G.T., Kaplan M.J., Dalerba P., Weissman I.L., Clarke M.F., Ailles L.E. Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc. Natl. Acad. Sci. USA 2007, 104:973-978.
153. 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. Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell 2008, 13:153-166.
154. Rege T.A., Hagood J.S. Thy-1, a versatile modulator of signaling affecting cellular adhesion, proliferation, survival, and cytokine/growth factor responses. Biochim. Biophys. Acta 2006, 1763:991-999.
155. Kroczek R.A., Gunter K.C., Germain R.N., Shevach E.M. Thy-1 functions as a signal transduction molecule in T lymphocytes and transfected B lymphocytes. Nature 1986, 322:181-184.
156. He J., Liu Y., Zhu T., Zhu J., Dimeco F., Vescovi A.L., Heth J.A., Muraszko K.M., Fan X., Lubman D.M. CD90 is identified as a candidate marker for cancer stem cells in primary high-grade gliomas using tissue microarrays. Mol. Cell Proteomics 2012, 11(M111):010744.
157. Yang Z.F., Ngai P., Ho D.W., Yu W.C., Ng M.N., Lau C.K., Li M.L., Tam K.H., Lam C.T., Poon R.T., Fan S.T. Identification of local and circulating cancer stem cells in human liver cancer. Hepatology 2008, 47:919-928.
158. Kristiansen G., Sammar M., Altevogt P. Tumour biological aspects of CD24, a mucin-like adhesion molecule. J. Mol. Histol. 2004, 35:255-262.
159. Zhang C., Li C., He F., Cai Y., Yang H. Identification of CD44+CD24+ gastric cancer stem cells. J. Cancer Res. Clin. Oncol. 2011, 137:1679-1686.
160. Gulino A., Ferretti E., De Smaele E. Hedgehog signalling in colon cancer and stem cells. EMBO Mol. Med. 2009, 1:300-302.
161. Medema J.P. Cancer stem cells: the challenges ahead. Nat. Cell Biol. 2013, 15:338-344.
162. Ferrero E., Malavasi F. The metamorphosis of a molecule: from soluble enzyme to the leukocyte receptor CD38. J. Leukoc. Biol. 1999, 65:151-161.
163. Hoogland A.M., Verhoef E.I., Roobol M.J., Schröder F.H., Wildhagen M.F., van der Kwast T.H., Jenster G., van Leenders G.J. Validation of stem cell markers in clinical prostate cancer: α6-integrin is predictive for non-aggressive disease. Prostate 2014, 74:488-496.
164. Chen K.G., Szakács G., Annereau J.P., Rouzaud F., Liang X.J., Valencia J.C., Nagineni C.N., Hooks J.J., Hearing V.J., Gottesman M.M. Principal expression of two mRNA isoforms (ABCB 5alpha and ABCB 5beta) of the ATP-binding cassette transporter gene ABCB 5 in melanoma cells and melanocytes. Pigment Cell Res. 2005, 18:102-112.
165. Wilson B.J., Saab K.R., Ma J., Schatton T., Pütz P., Zhan Q., Murphy G.F., Gasser M., Waaga-Gasser A.M., Frank N.Y., Frank M.H. ABCB5 maintains melanoma-initiating cells through a proinflammatory cytokine signaling circuit. Cancer Res. 2014, 74:4196-4207.
166. Morimoto C., Schlossman S.F. The structure and function of CD26 in the T-cell immune response. Immunol. Rev. 1998, 161:55-70.
167. Herrmann H., Sadovnik I., Cerny-Reiterer S., Rülicke T., Stefanzl G., Willmann M., Hoermann G., Bilban M., Blatt K., Herndlhofer S., Mayerhofer M., Streubel B., Sperr W.R., Holyoake T.L., Mannhalter C., Valent P. Dipeptidylpeptidase IV (CD26) defines leukemic stem cells (LSC) in chronic myeloid leukemia. Blood 2014, 123:3951-3962.
168. Vassilopoulos A., Chisholm C., Lahusen T., Zheng H., Deng C.X. A critical role of CD29 and CD49f in mediating metastasis for cancer-initiating cells isolated from a Brca1-associated mouse model of breast cancer. Oncogene 2014, 33:5477-5482.
169. Rutella S., Bonanno G., Procoli A., Mariotti A., Corallo M., Prisco M.G., Eramo A., Napoletano C., Gallo D., Perillo A., Nuti M., Pierelli L., Testa U., Scambia G., Ferrandina G. Cells with characteristics of cancer stem/progenitor cells express the CD133 antigen in human endometrial tumors. Clin. Cancer Res. 2009, 15:4299-4311.
170. Ma S., Chan K.W., Hu L., Lee T.K., Wo J.Y., Ng I.O., Zheng B.J., Guan X.Y. Identification and characterization of tumorigenic liver cancer stem/progenitor cells. Gastroenterology 2007, 132:2542-2556.
171. 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., Sozzi G. Highly tumorigenic lung cancer CD133+ cells display stem-like features and are spared by cisplatin treatment. Proc. Natl. Acad. Sci. USA 2009, 106:16281-16286.
172. Ferrandina G., Bonanno G., Pierelli L., Perillo A., Procoli A., Mariotti A., Corallo M., Martinelli E., Rutella S., Paglia A., Zannoni G., Mancuso S., Scambia G. Expression of CD133-1 and CD133-2 in ovarian cancer. Int. J. Gynecol. Cancer 2008, 18:506-514.
173. Tachezy M., Zander H., Wolters-Eisfeld G., Müller J., Wicklein D., Gebauer F., Izbicki J.R., Bockhorn M. Activated leukocyte cell adhesion molecule (CD166): an inert cancer stem cell marker for non-small cell lungcancer?. Stem Cells 2014, 32:1429-1436.
174. Walker F., Zhang H.H., Odorizzi A., Burgess A.W. LGR5 is a negative regulator of tumourigenicity, antagonizes Wnt signalling and regulates cell adhesion in colorectal cancer cell lines. PLoS ONE 2011, 6:e22733.
175. Kerr M.A., Stocks S.C. The role of CD15-(Le(X))-related carbohydrates in neutrophil adhesion. Histochem. J. 1992, 24:811-826.
176. Kleeberger W., Bova G.S., Nielsen M.E., Herawi M., Chuang A.Y., Epstein J.I., Berman D.M. Roles for the stem cell-associated intermediate filament nestin in prostate cancer migration and metastasis. Cancer Res. 2007, 67:9199-9206.
177. Wickström M., Larsson R., Nygren P., Gullbo J. Aminopeptidase N (CD13) as a target for cancer chemotherapy. Cancer Sci. 2011, 102:501-508.
178. Fang D., Nguyen T.K., Leishear K., Finko R., Kulp A.N., Hotz S., Van Belle P.A., Xu X., Elder D.E., Herlyn M. A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res. 2005, 65:9328-9337.
179. Kuijpers T.W., Bende R.J., Baars P.A., Grummels A., Derks I.A., Dolman K.M., Beaumont T., Tedder T.F., van Noesel C.J., Eldering E., van Lier R.A. CD20 deficiency in humans results in impaired T cell-independent antibody responses. J. Clin. Invest. 2010, 120:214-222.
180. Murillo-Sauca O., Chung M.K., Shin J.H., Karamboulas C., Kwok S., Jung Y.H., Oakley R., Tysome J.R., Farnebo L.O., Kaplan M.J., Sirjani D., Divi V., Holsinger F.C., Tomeh C., Nichols A., Le Q.T., Colevas A.D., Kong C.S., Uppaluri R., Lewis J.S., Ailles L.E., Sunwoo J.B. CD271 is a functional and targetable marker of tumor-initiating cells in head and neck squamous cell carcinoma. Oncotarget 2014, 5:6854-6866.
181. Furge K.A., Zhang Y.W., Vande Woude G.F. Met receptor tyrosine kinase: enhanced signaling through adapter proteins. Oncogene 2000, 19(49):5582-5589.
182. Branford W.W., Yost H.J. Nodal signaling: crypticLefty mechanism of antagonism decoded. Curr biol 2004, 14:R341-R343.
183. Boado R.J., Li J.Y., Nagaya M., Zhang C., Pardridge W.M. Selective expression of the large neutral amino acid transporter at the blood-brain barrier. Proc. Natl. Acad. Sci. USA 1999, 96:12079-12084.
184. Tokar E.J., Diwan B.A., Waalkes M.P. Arsenic exposure transforms human epithelial stem/progenitor cells into a cancer stem-like phenotype. Environ. Health Perspect. 2010, 118:108-115.
185. Mulvihill M.S., Kratz J.R., Pham P. The role of stem cells in airway repair: implications for the origins of lung cancer. Chin. J. Cancer 2013, 32:71-74.
186. Di Como C.J., Urist M.J., Babayan I., Drobnjak M., Hedvat C.V., Teruya-Feldstein J., Pohar K., Hoos A., Cordon-Cardo C. p63 Expression Profiles in Human Normal and Tumor Tissues. Clin. Cancer Res. 2002, 8:494-501.
187. Shi G., Jin Y. Role of Oct4 in maintaining and regaining stem cell pluripotency. Stem Cell Res. Ther. 2010, 1:39.
188. Cao L., Zhou Y., Zhai B., Liao J., Xu W., Zhang R., Li J., Zhang Y., Chen L., Qian H., Wu M., Yin Z. Sphere-forming cell subpopulations with cancer stem cell properties in human hepatoma cell lines. BMC Gastroenterol. 2011, 11:71.
189. Abu-Remaileh M., Gerson A., Farago M., Nathan G., Alkalay I., Zins Rousso S., Gur M., Fainsod A., Bergman Y. Oct-3/4 regulates stem cell identity and cell fate decisions by modulating Wnt/β-catenin signalling. EMBO J. 2010, 29:3236-3248.
190. Maetzel D., Denzel S., Mack B., Canis M., Went P., Benk M., Kieu C., Papior P., Baeuerle P.A., Munz M., Gires O. Nuclear signalling by tumour-associated antigen EpCAM. Nat. Cell Biol. 2009, 11:162-171.
191. Miettinen M., Lasota J. KIT (CD117): a review on expression in normal and neoplastic tissues, and mutations and their clinicopathologic correlation. Appl. Immunohistochem. Mol. Morphol. 2005, 13:205-220.
192. Civin C.I., Strauss L.C., Brovall C., Fackler M.J., Schwartz J.F., Shaper J.H. Antigenic analysis of hematopoiesis. III. A hematopoietic progenitor cell surface antigen defined by a monoclonal antibody raised against KG-1a cells. J. Immunol. 1984, 133:157-165.
193. Andrews R.G., Singer J.W., Bernstein I.D. Precursors of colony-forming cells in humans can be distinguished from colony-forming cells by expression of the CD33 and CD34 antigens and light scatter properties. J. Exp. Med. 1989, 169:1721-1731.
194. Lin G., Finger E., Gutierrez-Ramos J.C. Expression of CD34 in endothelial cells, hematopoietic progenitors and nervous cells in fetal and adult mouse tissues. Eur. J. Immunol. 1995, 25:1508-1516.
195. Chua C., Zaiden N., Chong K.H., See S.J., Wong M.C., Ang B.T., Tang C. Characterization of a side population of astrocytoma cells in response to temozolomide. J. Neurosurg. 2008, 109:856-866.
196. Haraguchi N., Utsunomiya T., Inoue H., Tanaka F., Mimori K., Barnard G.F., Mori M. Characterization of a side population of cancer cells from human gastrointestinal system. Stem Cells 2006, 24:506-513.
197. Bleau A.M., Hambardzumyan D., Ozawa T., Fomchenko E.I., Huse J.T., Brennan C.W., Holland E.C. PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell 2009, 4:226-235.
198. Chiba T., Kita K., Zheng Y.W., Yokosuka O., Saisho H., Iwama A., Nakauchi H., Taniguchi H. Side population purified from hepatocellular carcinoma cells harbors cancer stem cell-like properties. Hepatology 2006, 44:240-251.
199. Ho M.M., Ng A.V., Lam S., Hung J.Y. Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res. 2007, 67:4827-4833.
200. Qiao B., Gopalan V., Chen Z., Smith R.A., Tao Q., Lam A.K. Epithelial-mesenchymal transition and mesenchymal-epithelial transition are essential for the acquisition of stem cell properties in hTERT-immortalised oral epithelial cells. Biol. Cell 2012, 104:476-489.
201. Qiao B., Chen Z., Hu F., Tao Q., Lam A.K. BMI-1 activation is crucial in hTERT-induced epithelial-mesenchymal transition of oral epithelial cells. Exp. Mol. Pathol. 2013, 95:57-61.
202. Keitel U., Scheel C., Dobbelstein M. Overcoming EMT-driven therapeutic resistance by BH3 mimetics. Oncoscience 2014, 1:706-708.
203. Forbes S.A., Bindal N., Bamford S., Cole C., Kok C.Y., Beare D., Jia M., Shepherd R., Leung K., Menzies A., Teague J.W., Campbell P.J., Stratton M.R., Futreal P.A. COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res. 2011, 39:D945-D950.
204. Shakhova O., Leung C., Marino S. Bmi1 in development and tumorigenesis of the central nervous system. J. Mol. Med. (Berl) 2005, 83:596-600.
205. Kim R.J., Nam J.S. OCT4 expression enhances features of cancer stem cells in a mouse model of breast cancer. Lab Anim. Res. 2011, 27:147-152.
206. Maugeri-Saccà M., Bartucci M., De Maria R. DNA damage repair pathways in cancer stem cells. Mol. Cancer Ther. 2012, 11:1627-1636.
207. Yang F., Nam S., Brown C.E., Zhao R., Starr R., Ma Y., Xie J., Horne D.A., Malkas L.H., Jove R., Hickey R.J. A novel berbamine derivative inhibits cell viability and induces apoptosis in cancer stem-like cells of human glioblastoma, via up-regulation of miRNA-4284 and JNK/AP-1 signaling. PLoS One 2014, 9:e94443.
208. Kumar D., Shankar S., Srivastava R.K. Rottlerin-induced autophagy leads to the apoptosis in breast cancer stem cells: molecular mechanisms. Mol. Cancer 2013, 12:171.