Current concepts of how to eliminate cancer stem cells

Role of Cancer Stem Cells in Cancer Biology and Therapy

Volumn , Issue , 2016, Pages 167-198

  Campos Sanchez, Elena ^a   Romero Camarero, Isabel ^b   Sanchez Garcia, Isidro ^b   Cobaleda, Cesar ^a  

^a CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^b UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84880933902     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (148)

1. Abollo-Jimenez, F., R. Jimenez, and C. Cobaleda. 2010. Physiological cellular reprogramming and cancer. Semin Cancer Biol 20: 98-106.
2. Anderson, K., C. Lutz, F.W. van Delft, C.M. Bateman, Y. Guo, S.M. Colman, H. Kempski, A.V. Moorman, I. Titley, J. Swansbury, L. Kearney, T. Enver, and M. Greaves. 2011. Genetic variegation of clonal architecture and propagating cells in leukaemia. Nature 469: 356-361.
3. Angers, S., and R.T. Moon. 2009. Proximal events in Wnt signal transduction. Nat Rev Mol Cell Biol 10: 468-477.
4. Barker, N. 2008. The canonical Wnt/beta-catenin signalling pathway. Methods Mol Biol 468: 5-15.
5. Barker, N., and H. Clevers. 2006. Mining the Wnt pathway for cancer therapeutics. Nat Rev Drug Discov 5: 997-1014.
6. Barnett, B.E., M.L. Ciocca, R. Goenka, L.G. Barnett, J. Wu, T.M. Laufer, J.K. Burkhardt, M.P. Cancro, and S.L. Reiner. 2012. Asymmetric B Cell Division in the Germinal Center Reaction. Science 335: 342-344.
7. Baumann, M., M. Krause, and R. Hill. 2008. Exploring the role of cancer stem cells in radioresistance. Nat Rev Cancer 8: 545-554.
8. Beck, B., G. Driessens, S. Goossens, K.K. Youssef, A. Kuchnio, A. Caauwe, P.A. Sotiropoulou, S. Loges, G. Lapouge, A. Candi, G. Mascre, B. Drogat, S. Dekoninck, J.J. Haigh, P. Carmeliet, and C. Blanpain. 2011. A vascular niche and a VEGF-Nrp1 loop regulate the initiation and stemness of skin tumours. Nature 478: 399-403.
9. Ben-Porath, I., M.W. Thomson, V.J. Carey, R. Ge, G. W. Bell, A. Regev, and R.A. Weinberg. 2008. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 40: 499-507.
10. Bertucci, F., N. Cervera, and D. Birnbaum. 2007. A gene signature in breast cancer. N Engl J Med 356: 1887-8; author reply 1887-1888.
11. Bonnet, D., and J.E. Dick. 1997. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3: 730-737.
12. Brennan, S.K., Q. Wang, R. Tressler, C. Harley, N. Go, E. Bassett, C.A. Huff, R.J. Jones, and W. Matsui. 2010. Telomerase inhibition targets clonogenic multiple myeloma cells through telomere length-dependent and independent mechanisms. PLoS One 5.
13. Castellanos, A., C. Vicente-Duenas, E. Campos-Sanchez, J.J. Cruz, F.J. Garcia-Criado, M.B. Garcia-Cenador, P.A. Lazo, J. Perez-Losada, and I. Sanchez-Garcia. 2010. Cancer as a reprogramming-like disease: implications in tumor development and treatment. Semin Cancer Biol 20: 93-97.
14. Clevers, H. 2011. The cancer stem cell: premises, promises and challenges. Nat Med 17: 313-319.
15. Cobaleda, C., and I. Sanchez-Garcia. 2009. B-cell acute lymphoblastic leukaemia: towards understanding its cellular origin. Bioessays 31: 600-609.
16. Corbin, A.S., A. Agarwal, M. Loriaux, J. Cortes, M.W. Deininger, and B.J. Druker. 2011. Human chronic myeloid leukemia stem cells are insensitive to imatinib despite inhibition of BCR-ABL activity. J Clin Invest 121: 396-409.
17. Chabner, B.A., and T.G. Roberts, Jr. 2005. Timeline: Chemotherapy and the war on cancer. Nat Rev Cancer 5: 65-72.
18. Chalhoub, N., and S.J. Baker. 2009. PTEN and the PI3-kinase pathway in cancer. Annu Rev Pathol 4: 127-150.
19. Cheli, Y., S. Giuliano, T. Botton, S. Rocchi, V. Hofman, P. Hofman, P. Bahadoran, C. Bertolotto, and R. Ballotti. 2011. Mitf is the key molecular switch between mouse or human melanoma initiating cells and their differentiated progeny. Oncogene 30: 2307-2318.
20. Chen, Y., Y. Hu, S. Michaels, D. Segal, D. Brown, and S. Li. 2009. Inhibitory effects of omacetaxine on leukemic stem cells and BCR-ABL-induced chronic myeloid leukemia and acute lymphoblastic leukemia in mice. Leukemia 23: 1446-1454.
21. Chen, Y., Y. Hu, H. Zhang, C. Peng, and S. Li. 2009. Loss of the Alox5 gene impairs leukemia stem cells and prevents chronic myeloid leukemia. Nat Genet 41: 783-792.
22. Chen, Y., D. Li, and S. Li. 2009. The Alox5 gene is a novel therapeutic target in cancer stem cells of chronic myeloid leukemia. Cell Cycle 8: 3488-3492.
23. de Sousa, E.M.F., S. Colak, J. Buikhuisen, J. Koster, K. Cameron, J.H. de Jong, J.B. Tuynman, P.R. Prasetyanti, E. Fessler, S.P. van den Bergh, H. Rodermond, E. Dekker, C.M. van der Loos, S.T. Pals, M.J. van de Vijver, R. Versteeg, D.J. Richel, L. Vermeulen, and J.P. Medema. 2011. Methylation of cancer-stem-cell-associated wnt target genes predicts poor prognosis in colorectal cancer patients. Cell Stem Cell 9: 476-485.
24. Dick, J.E. 2008. Stem cell concepts renew cancer research. Blood 112: 4793-4807.
25. Diehn, M., R.W. Cho, N.A. Lobo, T. Kalisky, M.J. Dorie, A.N. Kulp, D. Qian, J.S. Lam, L. E. Ailles, M. Wong, B. Joshua, M.J. Kaplan, I. Wapnir, F.M. Dirbas, G. Somlo, C. Garberoglio, B. Paz, J. Shen, S.K. Lau, S.R. Quake, J.M. Brown, I.L. Weissman, and M. F. Clarke. 2009. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458: 780-783.
26. Dierks, C., R. Beigi, G.R. Guo, K. Zirlik, M.R. Stegert, P. Manley, C. Trussell, A. Schmitt-Graeff, K. Landwerlin, H. Veelken, and M. Warmuth. 2008. Expansion of Bcr-Abl-positive leukemic stem cells is dependent on Hedgehog pathway activation. Cancer Cell 14: 238-249.
27. Ding, L., T.J. Ley, D.E. Larson, C.A. Miller, D.C. Koboldt, J.S. Welch, J.K. Ritchey, M.A. Young, T. Lamprecht, M.D. McLellan, J.F. McMichael, J.W. Wallis, C. Lu, D. Shen, C.C. Harris, D. J. Dooling, R.S. Fulton, L.L. Fulton, K. Chen, H. Schmidt, J. Kalicki-Veizer, V.J. Magrini, L. Cook, S.D. McGrath, T.L. Vickery, M.C. Wendl, S. Heath, M.A. Watson, D.C. Link, M. H. Tomasson, W.D. Shannon, J.E. Payton, S. Kulkarni, P. Westervelt, M.J. Walter, T.A. Graubert, E.R. Mardis, R.K. Wilson, and J.F. Dipersio. 2012. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature 481: 157-163.
28. Donahue, T.R., and D.W. Dawson. 2011. Nodal/Activin signaling: a novel target for pancreatic cancer stem cell therapy. Cell Stem Cell 9: 383-384.
29. Ellisen, L.W., J. Bird, D.C. West, A.L. Soreng, T.C. Reynolds, S.D. Smith, and J. Sklar. 1991. TAN-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. Cell 66: 649-661.
30. Eppert, K., K. Takenaka, E.R. Lechman, L. Waldron, B. Nilsson, P. van Galen, K.H. Metzeler, A. Poeppl, V. Ling, J. Beyene, A.J. Canty, J.S. Danska, S.K. Bohlander, C. Buske, M.D. Minden, T.R. Golub, I. Jurisica, B.L. Ebert, and J.E. Dick. 2011. Stem cell gene expression programs influence clinical outcome in human leukemia. Nat Med 17: 1086-1093.
31. Erler, J.T., K.L. Bennewith, T.R. Cox, G. Lang, D. Bird, A. Koong, Q.T. Le, and A.J. Giaccia. 2009. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche. Cancer Cell 15: 35-44.
32. Essers, M.A., S. Offner, W.E. Blanco-Bose, Z. Waibler, U. Kalinke, M.A. Duchosal, and A. Trumpp. 2009. IFNalpha activates dormant haematopoietic stem cells in vivo. Nature 458: 904-908.
33. Etzioni, R., N. Urban, S. Ramsey, M. McIntosh, S. Schwartz, B. Reid, J. Radich, G. Anderson, and L. Hartwell. 2003. The case for early detection. Nat Rev Cancer 3: 243-252.
34. Fialkow, PJ., R.J. Jacobson, and T. Papayannopoulou. 1977. Chronic myelocytic leukemia: clonal origin in a stem cell common to the granulocyte, erythrocyte, platelet and monocyte/ macrophage. Am J Med 63: 125-130.
35. Frangioni, J.V. 2008. New technologies for human cancer imaging. J Clin Oncol 26: 4012-4021.
36. Gao, J., S. Graves, U. Koch, S. Liu, V. Jankovic, S. Buonamici, A. El Andaloussi, S.D. Nimer, B. L. Kee, R. Taichman, F. Radtke, and I. Aifantis. 2009. Hedgehog signaling is dispensable for adult hematopoietic stem cell function. Cell Stem Cell 4: 548-558.
37. Gattinoni, L., E. Lugli, Y. Ji, Z. Pos, C.M. Paulos, M.F. Quigley, J.R. Almeida, E. Gostick, Z. Yu, C. Carpenito, E. Wang, D.C. Douek, D.A. Price, C.H. June, F.M. Marincola, M. Roederer, and N.P Restifo. 2011. A human memory T cell subset with stem cell-like properties. Nat Med 17:1290-1297.
38. Gentles, A.J., S.K. Plevritis, R. Majeti, and A.A. Alizadeh. 2010. Association of a leukemic stem cell gene expression signature with clinical outcomes in acute myeloid leukemia. JAMA 304: 2706-2715.
39. Gobaa, S., S. Hoehnel, M. Roccio, A. Negro, S. Kobel, and M.P. Lutolf. 2011. Artificial niche microarrays for probing single stem cell fate in high throughput. Nat Methods 8:949-955.
40. Goff, D., and C. Jamieson. 2010. Cycling toward elimination of leukemic stem cells. Cell Stem Cell 6: 296-297.
41. Goldstein, A.S., J. Huang, C. Guo, I.P. Garraway, and O.N. Witte. 2010. Identification of a cell of origin for human prostate cancer. Science 329: 568-571.
42. Goss, P.E., and A.F. Chambers. 2010. Does tumour dormancy offer a therapeutic target? Nat Rev Cancer 10: 871-877.
43. Greaves, M. 2010. Cancer stem cells: back to Darwin? Semin Cancer Biol 20: 65-70.
44. Greaves, M. 2011. Cancer stem cells renew their impact. Nat Med 17: 1046-1048.
45. Gregory, M.A., T.L. Phang, P Neviani, F. Alvarez-Calderon, C.A. Eide, T. O'Hare, V. Zaberezhnyy, R.T. Williams, B.J. Druker, D. Perrotti, and J. Degregori. 2010. Wnt/ Ca2+/NFAT signaling maintains survival of Ph+ leukemia cells upon inhibition of Bcr-Abl. Cancer Cell 18: 74-87.
46. Gupta, P.B., C.M. Fillmore, G. Jiang, S.D. Shapira, K. Tao, C. Kuperwasser, and E.S. Lander. 2011. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 146: 633-644.
47. Gupta, P.B., T.T. Onder, G. Jiang, K. Tao, C. Kuperwasser, R.A. Weinberg, and E.S. Lander. 2009. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138: 645-659.
48. Guzman, M.L., X. Li, C.A. Corbett, R.M. Rossi, T. Bushnell, J.L. Liesveld, J. Hebert, F. Young, and C.T. Jordan. 2007. Rapid and selective death of leukemia stem and progenitor cells induced by the compound 4-benzyl, 2-methyl, 1,2,4-thiadiazolidine, 3,5 dione (TDZD-8). Blood 110: 4436-4444.
49. Guzman, M.L., R.M. Rossi, L. Karnischky, X. Li, D.R. Peterson, D.S. Howard, and C.T. Jordan. 2005. The sesquiterpene lactone parthenolide induces apoptosis of human acute myelogenous leukemia stem and progenitor cells. Blood 105: 4163-4169.
50. Guzman, M.L., C.F. Swiderski, D.S. Howard, B.A. Grimes, R.M. Rossi, S.J. Szilvassy, and C.T. Jordan. 2002. Preferential induction of apoptosis for primary human leukemic stem cells. Proc Natl Acad Sci USA 99: 16220-16225.
51. Hamburger, A., and S.E. Salmon. 1977. Primary bioassay of human myeloma stem cells. J Clin Invest 60: 846-854.
52. Han, Y.C., C.Y. Park, G. Bhagat, J. Zhang, Y. Wang, J.B. Fan, M. Liu, Y. Zou, I.L. Weissman, and H. Gu. 2010. microRNA-29a induces aberrant self-renewal capacity in hematopoietic progenitors, biased myeloid development, and acute myeloid leukemia. J Exp Med 207: 475-489.
53. Hassane, D.C., M.L. Guzman, C. Corbett, X. Li, R. Abboud, F. Young, J.L. Liesveld, M. Carroll, and C.T. Jordan. 2008. Discovery of agents that eradicate leukemia stem cells using an in silico screen of public gene expression data. Blood 111: 5654-5662.
54. Hegde, S., N. Kaushal, K.C. Ravindra, C. Chiaro, K.T. Hafer, U.H. Gandhi, J.T. Thompson, J.P. van den Heuvel, M.J. Kennett, P. Hankey, R.F. Paulson, and K.S. Prabhu. 2011. (Delta)12-prostaglandin J3, an omega-3 fatty acid-derived metabolite, selectively ablates leukemia stem cells in mice. Blood 118: 6909-6919.
55. Hermann, P.C., S. Bhaskar, M. Cioffi, and C. Heeschen. 2010. Cancer stem cells in solid tumors. Semin Cancer Biol 20: 77-84.
56. Heuser, M., H. Yun, T. Berg, E. Yung, B. Argiropoulos, F. Kuchenbauer, G. Park, I. Hamwi, L. Palmqvist, C.K. Lai, M. Leung, G. Lin, A. Chaturvedi, B.K. Thakur, M. Iwasaki, M. Bilenky, N. Thiessen, G. Robertson, M. Hirst, D. Kent, N.K. Wilson, B. Gottgens, C. Eaves, M.L. Cleary, M. Marra, A. Ganser, and R.K. Humphries. 2011. Cell of origin in AML: susceptibility to MN1-induced transformation is regulated by the MEIS1/AbdB-like HOX protein complex. Cancer Cell 20: 39-52.
57. Hoey, T., W.C. Yen, F. Axelrod, J. Basi, L. Donigian, S. Dylla, M. Fitch-Bruhns, S. Lazetic, I.K. Park, A. Sato, S. Satyal, X. Wang, M.F. Clarke, J. Lewicki, and A. Gurney. 2009. DLL4 blockade inhibits tumor growth and reduces tumor-initiating cell frequency. Cell Stem Cell 5: 168-177.
58. Hofmann, I., E.H. Stover, D.E. Cullen, J. Mao, K.J. Morgan, B.H. Lee, M.G. Kharas, PG. Miller, M.G. Cornejo, R. Okabe, S.A. Armstrong, N. Ghilardi, S. Gould, FJ. de Sauvage, A.P. McMahon, and D.G. Gilliland. 2009. Hedgehog signaling is dispensable for adult murine hematopoietic stem cell function and hematopoiesis. Cell Stem Cell 4: 559-567.
59. Huang, S. 2011. On the intrinsic inevitability of cancer: from foetal to fatal attraction. Semin Cancer Biol 21: 183-199.
60. Hurtz, C., K. Hatzi, L. Cerchietti, M. Braig, E. Park, Y.M. Kim, S. Herzog, P Ramezani-Rad, H. Jumaa, M.C. Muller, W.K. Hofmann, A. Hochhaus, B.H. Ye, A. Agarwal, B.J. Druker, N. P Shah, A.M. Melnick, and M. Muschen. 2011. BCL6-mediated repression of p53 is critical for leukemia stem cell survival in chronic myeloid leukemia. J Exp Med 11:2163-2174.
61. Husemann, Y., J.B. Geigl, F. Schubert, P. Musiani, M. Meyer, E. Burghart, G. Forni, R. Eils, T. Fehm, G. Riethmuller, and C.A. Klein. 2008. Systemic spread is an early step in breast cancer. Cancer Cell 13: 58-68.
62. Iliopoulos, D., M. Lindahl-Allen, C. Polytarchou, H.A. Hirsch, PN. Tsichlis, and K. Struhl. 2010. Loss of miR-200 inhibition of Suz12 leads to polycomb-mediated repression required for the formation and maintenance of cancer stem cells. Mol Cell 39: 761-772.
63. Ishikawa, F., S. Yoshida, Y. Saito, A. Hijikata, H. Kitamura, S. Tanaka, R. Nakamura, T. Tanaka, H. Tomiyama, N. Saito, M. Fukata, T. Miyamoto, B. Lyons, K. Ohshima, N. Uchida, S. Taniguchi, O. Ohara, K. Akashi, M. Harada, and L.D. Shultz. 2007. Chemotherapy-resistant human AML stem cells home to and engraft within the bone-marrow endosteal region. Nat Biotechnol 25: 1315-1321.
64. Ishimoto, T., O. Nagano, T. Yae, M. Tamada, T. Motohara, H. Oshima, M. Oshima, T. Ikeda, R. Asaba, H. Yagi, T. Masuko, T. Shimizu, T. Ishikawa, K. Kai, E. Takahashi, Y. Imamura, Y. Baba, M. Ohmura, M. Suematsu, H. Baba, and H. Saya. 2011. CD44 variant regulates redox status in cancer cells by stabilizing the xCT subunit of system xc(-) and thereby promotes tumor growth. Cancer Cell 19: 387-400.
65. Ito, K., R. Bernardi, and P.P. Pandolfi. 2009. A novel signaling network as a critical rheostat for the biology and maintenance of the normal stem cell and the cancer-initiating cell. Curr Opin Genet Dev 19: 51-59.
66. Jaiswal, S., C.H. Jamieson, W.W. Pang, C.Y. Park, M.P. Chao, R. Majeti, D. Traver, N. van Rooijen, and I.L. Weissman. 2009. CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell 138: 271-285.
67. Jin, L., E.M. Lee, H.S. Ramshaw, S.J. Busfield, A.G. Peoppl, L. Wilkinson, M.A. Guthridge, D. Thomas, E.F. Barry, A. Boyd, D.P. Gearing, G. Vairo, A.F. Lopez, J.E. Dick, and R.B. Lock. 2009. Monoclonal antibody-mediated targeting of CD123, IL-3 receptor alpha chain, eliminates human acute myeloid leukemic stem cells. Cell Stem Cell 5: 31-42.
68. Jordan, C.T. 2008. Can we finally target the leukemic stem cells? Best Pract Res Clin Haematol 21: 615-620.
69. Kasinski, A.L., and FJ. Slack. 2011. Epigenetics and genetics. MicroRNAs en route to the clinic: progress in validating and targeting microRNAs for cancer therapy. Nat Rev Cancer 11: 849-864.
70. Kikushige, Y., T. Shima, S. Takayanagi, S. Urata, T. Miyamoto, H. Iwasaki, K. Takenaka, T. Teshima, T. Tanaka, Y. Inagaki, and K. Akashi. 2010. TIM-3 is a promising target to selectively kill acute myeloid leukemia stem cells. Cell Stem Cell 7: 708-717.
71. Koch, U., M. Krause, and M. Baumann. 2010. Cancer stem cells at the crossroads of current cancer therapy failures-radiation oncology perspective. Semin Cancer Biol 20: 116-124.
72. Kuster, L., R. Grausenburger, G. Fuka, U. Kaindl, G. Krapf, A. Inthal, G. Mann, M. Kauer, J. Rainer, R. Kofler, A. Hall, M. Metzler, L.H. Meyer, C. Meyer, J. Harbott, R. Marschalek, S. Strehl, O.A. Haas, and R. Panzer-Grumayer. 2011. ETV6/RUNX1-positive relapses evolve from an ancestral clone and frequently acquire deletions of genes implicated in glucocorticoid signaling. Blood 117: 2658-2667.
73. Lane, S.W., and D.G. Gilliland. 2010. Leukemia stem cells. Semin Cancer Biol 20: 71-76.
74. Lathia, J.D., J. Gallagher, J.M. Heddleston, J. Wang, C.E. Eyler, J. Macswords, Q. Wu, A. Vasanji, R.E. McLendon, A.B. Hjelmeland, and J.N. Rich. 2010. Integrin alpha 6 regulates glioblastoma stem cells. Cell Stem Cell 6: 421-432.
75. Le Viseur, C., M. Hotfilder, S. Bomken, K. Wilson, S. Rottgers, A. Schrauder, A. Rosemann, J. Irving, R.W. Stam, L.D. Shultz, J. Harbott, H. Jurgens, M. Schrappe, R. Pieters, and J. Vormoor. 2008. In childhood acute lymphoblastic leukemia, blasts at different stages of immunophenotypic maturation have stem cell properties. Cancer Cell 14: 47-58.
76. Leder, K., E.C. Holland, and F. Michor. 2010. The therapeutic implications of plasticity of the cancer stem cell phenotype. PLoS One 5: e14366.
77. Lee, H.E., J.H. Kim, Y.J. Kim, S.Y. Choi, S.W. Kim, E. Kang, I.Y. Chung, I.A. Kim, E.J. Kim, Y. Choi, H.S. Ryu, and S.Y. Park. 2011. An increase in cancer stem cell population after primary systemic therapy is a poor prognostic factor in breast cancer. Br J Cancer 104: 1730-1738.
78. Lee, Y.S., and A. Dutta. 2009. MicroRNAs in cancer. Annu Rev Pathol 4: 199-227.
79. Lessard, J., and G. Sauvageau. 2003. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 423: 255-260.
80. Li, Y., A. Li, M. Glas, B. Lal, M. Ying, Y. Sang, S. Xia, D. Trageser, H. Guerrero-Cazares, C. G. Eberhart, A. Quinones-Hinojosa, B. Scheffler, and J. Laterra. 2011. c-Met signaling induces a reprogramming network and supports the glioblastoma stem-like phenotype. Proc Natl Acad Sci USA 108: 9951-9956.
81. Li, Z., S. Bao, Q. Wu, H. Wang, C. Eyler, S. Sathornsumetee, Q. Shi, Y. Cao, J. Lathia, R.E. McLendon, A.B. Hjelmeland, and J.N. Rich. 2009. Hypoxia-inducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 15: 501-513.
82. Liu, C., J.C. Sage, M.R. Miller, R.G. Verhaak, S. Hippenmeyer, H. Vogel, O. Foreman, R. T. Bronson, A. Nishiyama, L. Luo, and H. Zong. 2011. Mosaic analysis with double markers reveals tumor cell of origin in glioma. Cell 146: 209-221.
83. Liu, H., A.W. Chi, K.L. Arnett, M.Y. Chiang, L. Xu, O. Shestova, H. Wang, Y.M. Li, A. Bhandoola, J.C. Aster, S.C. Blacklow, and W.S. Pear. 2010. Notch dimerization is required for leukemogenesis and T-cell development. Genes Dev 24: 2395-2407.
84. Lobry, C., P. Oh, and I. Aifantis. 2011. Oncogenic and tumor suppressor functions of Notch in cancer: it's NOTCH what you think. J Exp Med 208: 1931-1935.
85. Lonardo, E., P.C. Hermann, M.T. Mueller, S. Huber, A. Balic, I. Miranda-Lorenzo, S. Zagorac, S. Alcala, I. Rodriguez-Arabaolaza, J.C. Ramirez, R. Torres-Ruiz, E. Garcia, M. Hidalgo, D. A. Cebrian, R. Heuchel, M. Lohr, F. Berger, P. Bartenstein, A. Aicher, and C. Heeschen. 2011. Nodal/Activin signaling drives self-renewal and tumorigenicity of pancreatic cancer stem cells and provides a target for combined drug therapy. Cell Stem Cell 9: 433-446.
86. Luckey, C.J., D. Bhattacharya, A.W. Goldrath, I.L. Weissman, C. Benoist, and D. Mathis. 2006. Memory T and memory B cells share a transcriptional program of self-renewal with long-term hematopoietic stem cells. Proc Natl Acad Sci USA 103: 3304-3309.
87. Luis, T.C., B.A. Naber, P.P. Roozen, M.H. Brugman, E.F. de Haas, M. Ghazvini, W.E. Fibbe, J.J. van Dongen, R. Fodde, and F.J. Staal. 2011. Canonical wnt signaling regulates hematopoiesis in a dosage-dependent fashion. Cell Stem Cell 9: 345-356.
88. Majeti, R., M.P. Chao, A.A. Alizadeh, W.W. Pang, S. Jaiswal, K.D. Gibbs, Jr., N. van Rooijen, and I.L. Weissman. 2009. CD47 is an adverse prognostic factor and therapeutic antibody target on human acute myeloid leukemia stem cells. Cell 138: 286-299.
89. Malanchi, I., A. Santamaria-Martinez, E. Susanto, H. Peng, H.A. Lehr, J.F. Delaloye, and J. Huelsken. 2012. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 481: 85-89.
90. Marder, J. 2010. Cancer research. Childhood's cures haunted by adulthood's 'late effects'. Science 328: 1474-1475.
91. Marshall, E. 2011. Cancer research and the $90 billion metaphor. Science 331: 1540-1541.
92. McDermott, S.P., K. Eppert, F. Notta, M. Isaac, A. Datti, R. Al-Awar, J. Wrana, M.D. Minden, and J.E. Dick. 2011. A small molecule screening strategy with validation on human leukemia stem cells uncovers the therapeutic efficacy of kinetin riboside. Blood doi: 10.1182/blood-2011-01-330019
93. Merlos-Suarez, A., F.M. Barriga, P. Jung, M. Iglesias, M.V. Cespedes, D. Rossell, M. Sevillano, X. Hernando-Momblona, V. da Silva-Diz, P. Munoz, H. Clevers, E. Sancho, R. Mangues, and E. Batlle. 2011. The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse. Cell Stem Cell 8: 511-524.
94. Meyer, L.H., S.M. Eckhoff, M. Queudeville, J.M. Kraus, M. Giordan, J. Stursberg, A. Zangrando, E. Vendramini, A. Moricke, M. Zimmermann, A. Schrauder, G. Lahr, K. Holzmann, M. Schrappe, G. Basso, K. Stahnke, H.A. Kestler, G. Te Kronnie, and K.M. Debatin. 2011. Early relapse in all is identified by time to leukemia in NOD/SCID mice and is characterized by a gene signature involving survival pathways. Cancer Cell 19: 206-217.
95. Molyneux, G., F.C. Geyer, F.A. Magnay, A. McCarthy, H. Kendrick, R. Natrajan, A. Mackay, A. Grigoriadis, A. Tutt, A. Ashworth, J.S. Reis-Filho, and M.J. Smalley. 2010. BRCA1 basal-like breast cancers originate from luminal epithelial progenitors and not from basal stem cells. Cell Stem Cell 7: 403-417.
96. Mullighan, C.G., L.A. Phillips, X. Su, J. Ma, C.B. Miller, S.A. Shurtleff, and J.R. Downing. 2008. Genomic analysis of the clonal origins of relapsed acute lymphoblastic leukemia. Science 322: 1377-1380.
97. Naka, K., T. Hoshii, T. Muraguchi, Y. Tadokoro, T. Ooshio, Y. Kondo, S. Nakao, N. Motoyama, and A. Hirao. 2010. TGF-beta-FOXO signalling maintains leukaemia-initiating cells in chronic myeloid leukaemia. Nature 463: 676-680.
98. Nalls, D., S.N. Tang, M. Rodova, R.K. Srivastava, and S. Shankar. 2011. Targeting Epigenetic Regulation of miR-34a for Treatment of Pancreatic Cancer by Inhibition of Pancreatic Cancer Stem Cells. PLoS One 6: e24099.
99. Ng, J.M., and T. Curran. 2011. The Hedgehog's tale: developing strategies for targeting cancer. Nat Rev Cancer 11: 493-501.
100. Notta, F., C.G. Mullighan, J.C. Wang, A. Poeppl, S. Doulatov, L.A. Phillips, J. Ma, M.D. Minden, J.R. Downing, and J.E. Dick. 2011. Evolution of human BCR-ABL1 lymphoblastic leukaemia-initiating cells. Nature 469: 362-367.
101. Park, I.K., D. Qian, M. Kiel, M.W. Becker, M. Pihalja, I.L. Weissman, S.J. Morrison, and M.F. Clarke. 2003. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 423: 302-305.
102. Park, K.S., L.G. Martelotto, M. Peifer, M.L. Sos, A.N. Karnezis, M.R. Mahjoub, K. Bernard, J.F. Conklin, A. Szczepny, J. Yuan, R. Guo, B. Ospina, J. Falzon, S. Bennett, T.J. Brown, A. Markovic, W.L. Devereux, C.A. Ocasio, J.K. Chen, T. Stearns, R.K. Thomas, M. Dorsch, S. Buonamici, D.N. Watkins, C.D. Peacock, and J. Sage. 2011. A crucial requirement for Hedgehog signaling in small cell lung cancer. Nat Med 7: 1504-1508.
103. Pece, S., D. Tosoni, S. Confalonieri, G. Mazzarol, M. Vecchi, S. Ronzoni, L. Bernard, G. Viale, P.G. Pelicci, and P.P. Di Fiore. 2010. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 140: 62-73.
104. Penuelas, S., J. Anido, R.M. Prieto-Sanchez, G. Folch, I. Barba, I. Cuartas, D. Garcia-Dorado, M. A. Poca, J. Sahuquillo, J. Baselga, and J. Seoane. 2009. TGF-beta increases glioma-initiating cell self-renewal through the induction of LIF in human glioblastoma. Cancer Cell 15: 315-327.
105. Persson, A.I., C. Petritsch, F.J. Swartling, M. Itsara, F.J. Sim, R. Auvergne, D.D. Goldenberg, S.R. Vandenberg, K.N. Nguyen, S. Yakovenko, J. Ayers-Ringler, A. Nishiyama, W.B. Stallcup, M.S. Berger, G. Bergers, T.R. McKnight, S.A. Goldman, and W.A. Weiss. 2010. Non-stem cell origin for oligodendroglioma. Cancer Cell 18: 669-682.
106. Pietersen, A.M., and M. van Lohuizen. 2008. Stem cell regulation by polycomb repressors: postponing commitment. Curr Opin Cell Biol 20: 201-207.
107. Pui, C.H., L.L. Robison, and A.T. Look. 2008. Acute lymphoblastic leukaemia. Lancet 371: 1030-1043.
108. Quintana, E., M. Shackleton, H.R. Foster, D.R. Fullen, M.S. Sabel, T.M. Johnson, and S. J. Morrison. 2010. Phenotypic heterogeneity among tumorigenic melanoma cells from patients that is reversible and not hierarchically organized. Cancer Cell 18: 510-523.
109. Ranganathan, P., K.L. Weaver, and A.J. Capobianco. 2011. Notch signalling in solid tumours: a little bit of everything but not all the time. Nat Rev Cancer 11: 338-351.
110. Reynaud, D., E. Pietras, K. Barry-Holson, A. Mir, M. Binnewies, M. Jeanne, O. Sala-Torra, J.P. Radich, and E. Passegue. 2011. IL-6 controls leukemic multipotent progenitor cell fate and contributes to chronic myelogenous leukemia development. Cancer Cell 20: 661-673.
111. Ritchie, D.S., and M.J. Smyth. 2009. A new therapeutic target for leukemia comes to the surface. Cell 138: 226-8.
112. Roesch, A., M. Fukunaga-Kalabis, E.C. Schmidt, S.E. Zabierowski, P.A. Brafford, A. Vultur, D. Basu, P. Gimotty, T. Vogt, and M. Herlyn. 2010. A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell 141: 583-594.
113. Sagrera, A., J. Perez-Losada, M. Perez-Caro, R. Jimenez, I. Sanchez-Garcia, and C. Cobaleda 2009. Elimination of Cancer Stem Cells. Stem Cell Biology in Health and Disease. T. Dittmar and K. S. Zänker, Springer Science + Bussiness Media: 356-384.
114. Saito, Y., N. Uchida, S. Tanaka, N. Suzuki, M. Tomizawa-Murasawa, A. Sone, Y. Najima, S. Takagi, Y. Aoki, A. Wake, S. Taniguchi, L.D. Shultz, and F. Ishikawa. 2010. Induction of cell cycle entry eliminates human leukemia stem cells in a mouse model of AML. Nat Biotechnol 28: 275-280.
115. Sanchez-Garcia, I. 2009. The crossroads of oncogenesis and metastasis. N Engl J Med 360: 297-299.
116. Sanchez-Garcia, I. 2010. Getting to the stem of cancer. Semin Cancer Biol 20: 63-64.
117. Sanchez-Garcia, I., C. Vicente-Duenas, and C. Cobaleda. 2007. The theoretical basis of cancer-stem-cell-based therapeutics of cancer: can it be put into practice? Bioessays 29: 1269-1280.
118. Schurch, C., C. Riether, M.S. Matter, A. Tzankov, and A.F. Ochsenbein. 2012. CD27 signaling on chronic myelogenous leukemia stem cells activates Wnt target genes and promotes disease progression. J Clin Invest doi: 10.1172/JCI45977.
119. Shackleton, M. 2010. Normal stem cells and cancer stem cells: similar and different. Semin Cancer Biol 20: 85-92.
120. Shah, N., and S. Sukumar. 2010. The Hox genes and their roles in oncogenesis. Nat Rev Cancer 10: 361-371.
121. Sharma, S.V., D.Y. Lee, B. Li, M.P. Quinlan, F. Takahashi, S. Maheswaran, U. McDermott, N. Azizian, L. Zou, M.A. Fischbach, K.K. Wong, K. Brandstetter, B. Wittner, S. Ramaswamy, M. Classon, and J. Settleman. 2010. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 141: 69-80.
122. Shats, I., M.L. Gatza, J.T. Chang, S. Mori, J. Wang, J. Rich, and J.R. Nevins. 2011. Using a stem cell-based signature to guide therapeutic selection in cancer. Cancer Res 71: 1772-1780.
123. Shimono, Y., M. Zabala, R.W. Cho, N. Lobo, P. Dalerba, D. Qian, M. Diehn, H. Liu, S.P. Panula, E. Chiao, F.M. Dirbas, G. Somlo, R.A. Pera, K. Lao, and M.F. Clarke. 2009. Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell 138: 592-603.
124. Smith, L.L., J. Yeung, B.B. Zeisig, N. Popov, I. Huijbers, J. Barnes, A.J. Wilson, E. Taskesen, R. Delwel, J. Gil, M. Van Lohuizen, and C.W. So. 2011. Functional crosstalk between Bmi1 and MLL/Hoxa9 axis in establishment of normal hematopoietic and leukemic stem cells. Cell Stem Cell 8: 649-662.
125. Somervaille, T.C., C.J. Matheny, G.J. Spencer, M. Iwasaki, J.L. Rinn, D.M. Witten, H.Y. Chang, S. A. Shurtleff, J.R. Downing, and M.L. Cleary. 2009. Hierarchical maintenance of MLL myeloid leukemia stem cells employs a transcriptional program shared with embryonic rather than adult stem cells. Cell Stem Cell 4: 129-140.
126. Tatarek, J., K. Cullion, T. Ashworth, R. Gerstein, J.C. Aster, and M.A. Kelliher. 2011. Notch1 inhibition targets the leukemia-initiating cells in a Tal1/Lmo2 mouse model of T-ALL. Blood 118: 1579-1590.
127. Tian, H., B. Biehs, S. Warming, K.G. Leong, L. Rangell, O.D. Klein, and F.J. de Sauvage. 2011. A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature 478: 255-259.
128. Uhr, J.W., and K. Pantel. 2011. Controversies in clinical cancer dormancy. Proc Natl Acad Sci USA 108: 12396-12400.
129. van Delft, F.W., S. Horsley, S. Colman, K. Anderson, C. Bateman, H. Kempski, J. Zuna, C. Eckert, V. Saha, L. Kearney, A. Ford, and M. Greaves. 2011. Clonal origins of relapse in ETV6-RUNX1 acute lymphoblastic leukemia. Blood 117: 6247-6254.
130. Van Keymeulen, A., A.S. Rocha, M. Ousset, B. Beck, G. Bouvencourt, J. Rock, N. Sharma, S. Dekoninck, and C. Blanpain. 2011. Distinct stem cells contribute to mammary gland development and maintenance. Nature 49: 189-193.
131. Varjosalo, M., and J. Taipale. 2008. Hedgehog: functions and mechanisms. Genes Dev 22: 2454-2472.
132. Veeman, M.T., J.D. Axelrod, and R.T. Moon. 2003. A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev Cell 5: 367-377.
133. Vicente-Duenas, C., C. Cobaleda, J. Perez-Losada, and I. Sanchez-Garcia. 2010. The evolution of cancer modeling: the shadow of stem cells. Dis Model Mech 3: 149-155.
134. Vicente-Duenas, C., M. Perez-Caro, F. Abollo-Jimenez, C. Cobaleda, and I. Sanchez-Garcia. 2009. Stem-cell driven cancer: "hands-off" regulation of cancer development. Cell Cycle 8: 1314-1318.
135. Visvader, J.E. 2011. Cells of origin in cancer. Nature 469: 314-322.
136. Wang, Y., A.V. Krivtsov, A.U. Sinha, T.E. North, W. Goessling, Z. Feng, L.I. Zon, and S.A. Armstrong. 2010. The Wnt/beta-catenin pathway is required for the development of leukemia stem cells in AML. Science 327: 1650-1653.
137. Wang, Y., Y. Liu, S.N. Malek, and P Zheng. 2011. Targeting HIF1alpha eliminates cancer stem cells in hematological malignancies. Cell Stem Cell 8: 399-411.
138. Warr, M.R., E.M. Pietras, and E. Passegue. 2011. Mechanisms controlling hematopoietic stem cell functions during normal hematopoiesis and hematological malignancies. Wiley Interdiscip Rev Syst Biol Med 3: 681-701.
139. Weng, A.P, A.A. Ferrando, W. Lee, J.P. T. Morris, L.B. Silverman, C. Sanchez-Irizarry, S.C. Blacklow, A.T. Look, and J.C. Aster. 2004. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 306: 269-271.
140. Wingo, PA., C.J. Cardinez, S.H. Landis, R.T. Greenlee, L.A. Ries, R.N. Anderson, and M.J. Thun. 2003. Long-term trends in cancer mortality in the United States, 1930-1998. Cancer 97: 3133-3275.
141. Yachida, S., S. Jones, I. Bozic, T. Antal, R. Leary, B. Fu, M. Kamiyama, R.H. Hruban, J.R. Eshleman, M.A. Nowak, V.E. Velculescu, K.W. Kinzler, B. Vogelstein, and C.A. Iacobuzio-Donahue. 2010. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 467: 1114-1117.
142. Yeung, J., M.T. Esposito, A. Gandillet, B.B. Zeisig, E. Griessinger, D. Bonnet, and C.W. So. 2010. beta-Catenin mediates the establishment and drug resistance of MLL leukemic stem cells. Cancer Cell 18: 606-618.
143. Yuan, J., M. Takeuchi, M. Negishi, H. Oguro, H. Ichikawa, and A. Iwama. 2011. Bmi1 is essential for leukemic reprogramming of myeloid progenitor cells. Leukemia 25: 1335-1343.
144. Zhang, B., A.C. Strauss, S. Chu, M. Li, Y. Ho, K.D. Shiang, D.S. Snyder, C.S. Huettner, L. Shultz, T. Holyoake, and R. Bhatia. 2010. Effective targeting of quiescent chronic myelogenous leukemia stem cells by histone deacetylase inhibitors in combination with imatinib mesylate. Cancer Cell 17: 427-442.
145. Zhang, N., P. Wei, A. Gong, W.T. Chiu, H.T. Lee, H. Colman, H. Huang, J. Xue, M. Liu, Y. Wang, R. Sawaya, K. Xie, W.K. Yung, R.H. Medema, X. He, and S. Huang. 2011. FoxM1 Promotes beta-Catenin Nuclear Localization and Controls Wnt Target-Gene Expression and Glioma Tumorigenesis. Cancer Cell 20: 427-442.
146. Zhang, W.C., N. Shyh-Chang, H. Yang, A. Rai, S. Umashankar, S. Ma, B.S. Soh, L.L. Sun, B.C. Tai, M.E. Nga, K.K. Bhakoo, S.R. Jayapal, M. Nichane, Q. Yu, D.A. Ahmed, C. Tan, W.P. Sing, J. Tam, A. Thirugananam, M.S. Noghabi, Y. Huei Pang, H.S. Ang, P. Robson, P. Kaldis, R.A. Soo, S. Swarup, E.H. Lim, and B. Lim. 2012. Glycine Decarboxylase Activity Drives Non-Small Cell Lung Cancer Tumor-Initiating Cells and Tumorigenesis. Cell 48: 259-272.
147. Zhao, C., A. Chen, C.H. Jamieson, M. Fereshteh, A. Abrahamsson, J. Blum, H.Y. Kwon, J. Kim, J.P. Chute, D. Rizzieri, M. Munchhof, T. VanArsdale, P.A. Beachy, and T. Reya. 2009. Hedgehog signalling is essential for maintenance of cancer stem cells in myeloid leukaemia. Nature 458: 776-769.
148. Zoller, M. 2011. CD44: can a cancer-initiating cell profit from an abundantly expressed molecule? Nat Rev Cancer 11: 254-267.