The cancer stem cell: Premises, promises and challenges

Nature Medicine

Volumn 17, Issue 3, 2011, Pages 313-319

  Clevers, Hans ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER B5; CD133 ANTIGEN; CD19 ANTIGEN; CD20 ANTIGEN; CD24 ANTIGEN; CD34 ANTIGEN; CD38 ANTIGEN; CELL MARKER; EPITHELIAL CELL ADHESION MOLECULE; HERMES ANTIGEN; THY 1 ANTIGEN; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ARTICLE; B CELL LEUKEMIA; BRAIN CANCER; BREAST CANCER; CANCER RELAPSE; CANCER RESEARCH; CANCER STEM CELL; CARCINOGENESIS; COLON CANCER; COLORECTAL CANCER; DRUG TARGETING; FLUORESCENCE ACTIVATED CELL SORTING; GENE MUTATION; HEAD AND NECK CANCER; HEMATOLOGIC MALIGNANCY; HUMAN; LEUKEMIA; LIVER CANCER; LUNG CANCER; MELANOMA; METASTASIS POTENTIAL; NONHUMAN; ONCOGENE; PANCREAS CANCER; PRIORITY JOURNAL; TUMOR SUPPRESSOR GENE; TUMOR XENOGRAFT;

ANIMALS; HUMANS; MICE; NEOPLASMS; NEOPLASTIC STEM CELLS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 79952370202     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.2304     Document Type: Article

References (82)

1. Aguirre-Ghiso, J.A. Models, mechanisms and clinical evidence for cancer dormancy. Nat. Rev. Cancer 7, 834-846 (2007). (Pubitemid 350006258)
2. Dick, J.E. Stem cell concepts renew cancer research. Blood 112, 4793-4807 (2008).
3. Furth, J. & Kahn, M. The transmission of leukemia of mice with a single cell. Am. J. Cancer 31, 276-282 (1937).
4. Makino, S. Further evidence favoring the concept of the stem cell in ascites tumors of rats. Ann. NY Acad. Sci. 63, 818-830 (1956).
5. Hewitt, H.B. Studies of the dissemination and quantitative transplantation of a lymphocytic leukaemia of CBA mice. Br. J. Cancer 12, 378-401 (1958).
6. Bruce, W.R. & Van Der Gaag, H. A quantitative assay for the number of murine lymphoma cells capable of proliferation in vivo. Nature 199, 79-80 (1963).
7. Kleinsmith, L.J. & Pierce, G.B. Jr. Multipotentiality of single embryonal carcinoma cells. Cancer Res. 24, 1544-1551 (1964).
8. Belanger, L.F. & Leblond, C.P. A method for locating radioactive elements in tissues by covering histological sections with a photographic emulsion. Endocrinology 39, 8-13 (1946).
9. Clermont, Y. & Leblond, C.P. Renewal of spermatogonia in the rat. Am. J. Anat. 93, 475-501 (1953).
10. Pierce, G.B. & Wallace, C. Differentiation of malignant to benign cells. Cancer Res. 31, 127-134 (1971).
11. Pierce, G.B. & Speers, W.C. Tumors as caricatures of the process of tissue renewal: prospects for therapy by directing differentiation. Cancer Res. 48, 1996-2004 (1988).
12. Clarkson, B. et al. Studies of cellular proliferation in human leukemia. Behavior of leukemic cells in three adults with acute leukemia given continuous infusions of 3H-thymidine for 8 or 10 days. Cancer 25, 1237-1260 (1970).
13. Killmann, S.A., Cronkite, E.P., Robertson, J.S., Fliedner, T.M. & Bond, V.P. Estimation of phases of the life cycle of leukemic cells from labeling in human beings in vivo with tritiated thymidine. Lab. Invest. 12, 671-684 (1963).
14. Clarkson, B.D. Review of recent studies of cellular proliferation in acute leukemia. Natl. Cancer Inst. Monogr. 30, 81-120 (1969).
15. Clarkson, B. The survival value of the dormant state in neoplastic and normal populations. in Control of Proliferation in Animal Cells (eds. Clarkson, B., Baserga, R.) 945-972 (Cold Spring Harbor Laboratory, New York, NY, 1974).
16. Clarkson, B.D. & Fried, J. Changing concepts of treatment in acute leukemia. Med. Clin. North Am. 55, 561-600 (1971).
17. Cronkite, E.P. Acute leukemia: is there a relationship between cell growth kinetics and response to chemotherapy? Proc. Natl. Cancer Conf. 6, 113-117 (1970).
18. Clarkson, B.D., Dowling, M.D., Gee, T.S., Cunningham, I.B. & Burchenal, J.H. Treatment of acute leukemia in adults. Cancer 36, 775-795 (1975).
19. Nowell, P.C. The clonal evolution of tumor cell populations. Science 194, 23-28 (1976).
20. Fearon, E.R. & Vogelstein, B. A genetic model for colorectal tumorigenesis. Cell 61 759-767 1990).
21. Uckun, F.M. et al. Leukemic cell growth in SCID mice as a predictor of relapse in high-risk B-lineage acute lymphoblastic leukemia. Blood 85, 873-878 (1995).
22. Lapidot, T. et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367, 645-648 (1994). (Pubitemid 24067706)
23. Bonnet, D. & Dick, J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 3, 730-737 (1997). (Pubitemid 27298715)
24. Al-Hajj, M., Wicha, M.S., Benito-Hernandez, A., Morrison, S.J. & Clarke, M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. USA 100, 3983-3988 (2003). (Pubitemid 36418143)
25. Singh, S.K. et al. Identification of human brain tumour initiating cells. Nature 432, 396-401 (2004). (Pubitemid 39551674)
26. Dalerba, P. et al. Phenotypic characterization of human colorectal cancer stem cells. Proc. Natl. Acad. Sci. USA 104, 10158-10163 (2007). (Pubitemid 47175279)
27. Brien, C.A., Pollett, A., Gallinger, S. & Dick, J.E. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445 106-110 (2007). (Pubitemid 46067310)
28. Ricci-Vitiani, L. et al. Identification and expansion of human colon-cancer-initiating cells. Nature 445, 111-115 (2007). (Pubitemid 46067311)
29. Ebben, J.D. et al. The cancer stem cell paradigm: a new understanding of tumor development and treatment. Expert Opin. Ther. Targets 14, 621-632 (2010).
30. Quintana, E. et al. Efficient tumour formation by single human melanoma cells. Nature 456, 593-598 (2008).
31. Shackleton, M., Quintana, E., Fearon, E.R. & Morrison, S.J. Heterogeneity in cancer: cancer stem cells versus clonal evolution. Cell 138, 822-829 (2009).
32. Quintana, E. et al. Phenotypic heterogeneity among tumorigenic melanoma cells from patients that is reversible and not hierarchically organized. Cancer Cell 18, 510-523 (2010).
33. Roesch, A. et al. A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell 141, 583-594 (2010).
34. Sharma, S.V. et al. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 141, 69-80 (2010).
35. Ill, C.R., Brehm, T., Lydersen, B.K., Hernandez, R. & Burnett, K.G. Species specificity of iron delivery in hybridomas. In Vitro Cell. Dev. Biol. 24, 413-419 (1988).
36. Feuring-Buske, M. et al. Improved engraftment of human acute myeloid leukemia progenitor cells in 2-microglobulin-deficient NOD/SCID mice and in NOD/SCID mice transgenic for human growth factors. Leukemia 17, 760-763 (2003). (Pubitemid 36519373)
37. Karnoub, A.E. et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449, 557-563 (2007). (Pubitemid 47525152)
38. Kennedy, J.A., Barabe, F., Poeppl, A.G., Wang, J.C. & Dick, J.E. Comment on "Tumor growth need not be driven by rare cancer stem cells". Science 318, 1722 (2007).
39. Kelly, P.N., Dakic, A., Adams, J.M., Nutt, S.L. & Strasser, A. Tumor growth need not be driven by rare cancer stem cells. Science 317, 337 (2007). (Pubitemid 47106366)
40. Krivtsov, A.V. et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature 442, 818-822 (2006). (Pubitemid 44258912)
41. Yilmaz, O.H. et al. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Nature 441, 475-482 (2006). (Pubitemid 44050144)
42. Deshpande, A.J. et al. Acute myeloid leukemia is propagated by a leukemic stem cell with lymphoid characteristics in a mouse model of CALM/AF10-positive leukemia. Cancer Cell 10, 363-374 (2006). (Pubitemid 44693467)
43. Cho, R.W. et al. Isolation and molecular characterization of cancer stem cells in MMTV-Wnt-1 murine breast tumors. Stem Cells 26, 364-371 (2008). (Pubitemid 351413596)
44. Vaillant, F. et al. The mammary progenitor marker CD61/3 integrin identifies cancer stem cells in mouse models of mammary tumorigenesis. Cancer Res. 68, 7711-7717 (2008).
45. Zhang, M. et al. Identification of tumor-initiating cells in a p53-null mouse model of breast cancer. Cancer Res. 68, 4674-4682 (2008).
46. Malanchi, I. et al. Cutaneous cancer stem cell maintenance is dependent on -catenin signalling. Nature 452, 650-653 (2008). (Pubitemid 351483363)
47. Williams, R.T., den Besten, W. & Sherr, C.J. Cytokine-dependent imatinib resistance in mouse BCR-ABL+, Arf-null lymphoblastic leukemia. Genes Dev. 21, 2283-2287 (2007). (Pubitemid 47443334)
48. Blanpain, C., Horsley, V. & Fuchs, E. Epithelial stem cells: turning over new leaves. Cell 128, 445-458 (2007). (Pubitemid 46198895)
49. Bonfanti, P. et al. Microenvironmental reprogramming of thymic epithelial cells to skin multipotent stem cells. Nature 466, 978-982 (2010).
50. Shmelkov, S.V. et al. CD133 expression is not restricted to stem cells, and both CD133+ and CD133? metastatic colon cancer cells initiate tumors. J. Clin. Invest. 118, 2111-2120 (2008). (Pubitemid 351872330)
51. Bao, S. et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444, 756-760 (2006). (Pubitemid 44949604)
52. Joo, K.M. et al. Clinical and biological implications of CD133-positive and CD133-negative cells in glioblastomas. Lab. Invest. 88, 808-815 (2008).
53. Ogden, A.T. et al. Identification of A2B5+CD133? tumor-initiating cells in adult human gliomas. Neurosurgery 62, 505-514 (2008). (Pubitemid 351489297)
54. Wang, J. et al. CD133 negative glioma cells form tumors in nude rats and give rise to CD133 positive cells. Int. J. Cancer 122, 761-768 (2008).
55. Chen, R. et al. A hierarchy of self-renewing tumor-initiating cell types in glioblastoma. Cancer Cell 17, 362-375 (2010).
56. Boiko, A.D. et al. Human melanoma-initiating cells express neural crest nerve growth factor receptor CD271. Nature 466, 133-137 (2010).
57. Schatton, T. et al. Identification of cells initiating human melanomas. Nature 451, 345-349 (2008).
58. Fuchs, E. The tortoise and the hair: slow-cycling cells in the stem cell race. Cell 137, 811-819 (2009).
59. Essers, M.A. & Trumpp, A. Targeting leukemic stem cells by breaking their dormancy. Mol. Oncol. 4, 443-450 (2010).
60. Pece, S. et al. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 140, 62-73 (2010).
61. Zhou, B.B. et al. Tumour-initiating cells: challenges and opportunities for anticancer drug discovery. Nat. Rev. Drug Discov. 8, 806-823 (2009).
62. Li, X. et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J. Natl. Cancer Inst. 100, 672-679 (2008).
63. Diehn, M. et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458, 780-783 (2009).
64. O'Hare, T., Corbin, A.S. & Druker, B.J. Targeted CML therapy: controlling drug resistance, seeking cure. Curr. Opin. Genet. Dev. 16, 92-99 (2006). (Pubitemid 43089618)
65. Oravecz-Wilson, K.I. et al. Persistence of leukemia-initiating cells in a conditional knockin model of an imatinib-responsive myeloproliferative disorder. Cancer Cell 16, 137-148 (2009).
66. Masters, J.R. & Koberle, B. Curing metastatic cancer: lessons from testicular germ-cell tumours. Nat. Rev. Cancer 3, 517-525 (2003). (Pubitemid 37328839)
67. Sikic, B.I. Natural and acquired resistance to cancer therapies. in The Molecular Basis of Cancer (eds. J. Mendelsohn, P.M. Howley, M.A. Israel, J.W. Gray and C.B. Thompson) 583-592 (Saunders Elsevier, Philadelphia, 2008).
68. Chiu, P.P., Jiang, H. & Dick, J.E. Leukemia-initiating cells in human T-lymphoblastic leukemia exhibit glucocorticoid resistance. Blood 116, 5268-5279 (2010).
69. Hermann, P.C. et al. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 1, 313-323 (2007). (Pubitemid 47355323)
70. Balic, M. et al. Most early disseminated cancer cells detected in bone marrow of breast cancer patients have a putative breast cancer stem cell phenotype. Clin. Cancer Res. 12, 5615-5621 (2006). (Pubitemid 44629587)
71. Saito, Y. et al. Induction of cell cycle entry eliminates human leukemia stem cells in a mouse model of AML. Nat. Biotechnol. 28, 275-280 (2010).
72. Goldman, J.M. et al. Chronic myeloproliferative diseases with and without the Ph chromosome: some unresolved issues. Leukemia 23, 1708-1715 (2009).
73. Charames, G.S. & Bapat, B. Genomic instability and cancer. Curr. Mol. Med. 3, 589-596 (2003). (Pubitemid 37236402)
74. Vogelstein, B. & Kinzler, K.W. Cancer genes and the pathways they control. Nat. Med. 10, 789-799 (2004). (Pubitemid 39070849)
75. Shah, N.P. et al. Sequential ABL kinase inhibitor therapy selects for compound drug-resistant BCR-ABL mutations with altered oncogenic potency. J. Clin. Invest. 117, 2562-2569 (2007). (Pubitemid 47494357)
76. Calabretta, B. & Perrotti, D. The biology of CML blast crisis. Blood 103, 4010-4022 (2004). (Pubitemid 38685338)
77. Kristensen, V. & Borresen-Dale, A.L. Mutations for the people. EMBO Mol Med 2, 143-145 (2010).
78. Mardis, E.R. & Wilson, R.K. Cancer genome sequencing: a review. Hum. Mol. Genet. 18, R163-R168 (2009).
79. Shah, S.P. et al. Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution. Nature 461, 809-813 (2009).
80. Ding, L. et al. Genome remodelling in a basal-like breast cancer metastasis and xenograft. Nature 464, 999-1005 (2010).
81. Campbell, P.J. et al. The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature 467, 1109-1113 (2010).
82. Yachida, S. et al. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 467, 1114-1117 (2010).