Cancer stem cells: A reality, a myth, a fuzzy concept or a misnomer? An analysis

Carcinogenesis

Volumn 31, Issue 2, 2010, Pages 149-158

  Maenhaut, C ^a   Dumont, J E ^a   Roger, P P ^a   van Staveren, W C G ^a  

^a ERASME HOSPITAL   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER;

ANEUPLOIDY; APOPTOSIS; CANCER CELL; CANCER CELL CULTURE; CANCER GROWTH; CANCER STEM CELL; CARCINOGENICITY; CELL DIFFERENTIATION; CELL POPULATION; CELL RENEWAL; EMBRYONIC STEM CELL; GENE MUTATION; HUMAN; MALIGNANT NEOPLASTIC DISEASE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; REVIEW; SOMATIC CELL; NEOPLASM; PATHOLOGY;

HUMANS; NEOPLASMS; NEOPLASTIC STEM CELLS;

EID: 77649208749     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgp259     Document Type: Review

References (130)

1. Al Hajj, M. et al. (2003) Prospective identification of tumorigenic breast cancer cells. Proc. Natl Acad. Sci. USA, 100, 3983-3988.
2. Lapidot, T. et al. (1994) A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature, 367, 645-648.
3. Bonnet, D. et al. (1997) Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med., 3, 730-737.
4. Kelly, P.N. et al. (2007) Tumor growth need not be driven by rare cancer stem cells. Science, 317, 337.
5. Hong, D. et al. (2008) Initiating and cancer-propagating cells in TELAML1-associated childhood leukemia. Science, 319, 336-339.
6. Shipitsin, M. et al. (2007) Molecular definition of breast tumor heterogeneity. Cancer Cell, 11, 259-273.
7. Marotta, L.L. et al. (2009) Cancer stem cells: a model in the making. Curr. Opin. Genet. Dev., 19, 44-50.
8. Klonisch, T. et al. (2008) Cancer stem cell markers in common cancers-therapeutic implications. Trends Mol. Med., 14, 450-460.
9. Charafe-Jauffret, E. et al. (2008) Cancer stem cells in breast: current opinion and future challenges. Pathobiology, 75, 75-84.
10. Korkaya, H. et al. (2008) HER2 regulates the mammary stem/progenitor cell population driving tumorigenesis and invasion. Oncogene, 27, 6120-6130.
11. Marusyk, A. et al. (2008) Declining cellular fitness with age promotes cancer initiation by selecting for adaptive oncogenic mutations. Biochim. Biophys Acta, 1785, 1-11.
12. Werbowetski-Ogilvie, T.E. et al. (2008) Pluripotent human stem cell lines: what we can learn about cancer initiation. Trends Mol. Med., 14, 323-332.
13. Barker, N. et al. (2009) Crypt stem cells as the cells-of-origin of intestinal cancer. Nature, 457, 608-611.
14. Xin, L. et al. (2006) Progression of prostate cancer by synergy of AKT with genotropic and nongenotropic actions of the androgen receptor. Proc. Natl Acad. Sci. USA, 103, 7789-7794.
15. Polyak, K. et al. (2006) Roots and stems: stem cells in cancer. Nat. Med., 12, 296-300.
16. Morrison, S.J. et al. (2008) Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell, 132, 598-611.
17. Krtolica, A. (2005) Stem cell: balancing aging and cancer. Int. J. Biochem. Cell Biol., 37, 935-941.
18. Sanchez, A.A. (2008) Stem cells: time to check our premises. Cell Stem Cell, 3, 25-29.
19. Sato, T. et al. (2009) Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature, 459, 262-265.
20. Jaks, V. et al. (2008) Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat. Genet., 40, 1291-1299.
21. Ying, Q.L. et al. (2008) The ground state of embryonic stem cell self-renewal. Nature, 453, 519-523.
22. Sell, S. et al. (2008) Liver cancer stem cells. J. Clin. Oncol., 26, 2800-2805.
23. Orkin, S.H. (2000) Diversification of haematopoietic stem cells to specific lineages. Nat. Rev. Genet., 1, 57-64.
24. Nakagawa, M. et al. (2008) Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat. Biotechnol., 26, 101-106.
25. Yu, J. et al. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science, 318, 1917-1920.
26. Dalerba, P. et al. (2007) Cancer stem cells: models and concepts. Annu. Rev. Med., 58, 267-284.
27. Moserle, L. et al. (2008) The side population of ovarian cancer cells is a primary target of IFN-alpha antitumor effects. Cancer Res., 68, 5658-5668.
28. Addla, S.K. et al. (2008) Characterization of the Hoechst 33342 side population from normal and malignant human renal epithelial cells. Am. J. Physiol. Renal Physiol., 295, F680-F687.
29. Zabierowski, S.E. et al. (2008) Learning the ABCs of melanoma-initiating cells. Cancer Cell, 13, 185-187.
30. Hermann, P.C. et al. (2008) Metastatic cancer stem cells: a new target for anti-cancer therapy? Cell Cycle, 7, 188-193.
31. Rich, J.N. (2007) Cancer stem cells in radiation resistance. Cancer Res., 67, 8980-8984.
32. Wicha, M.S. et al. (2006) Cancer stem cells: an old idea-a paradigm shift. Cancer Res., 66, 1883-1890.
33. Ashworth, A. (2008) Drug resistance caused by reversion mutation. Cancer Res., 68, 10021-10023.
34. Olivotto, M. et al. (2008) Environmental restrictions within tumor ecosystems select for a convergent, hypoxia-resistant phenotype of cancer stem cells. Cell Cycle, 7, 176-187.
35. Vermeulen, L. et al. (2008) Single-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacity. Proc. Natl Acad. Sci. USA, 105, 13427-13432.
36. Croker, A.K. et al. (2008) Cancer stem cells: implications for the progression and treatment of metastatic disease. J. Cell. Mol. Med., 12, 374-390.
37. Pietersen, A.M. et al. (2008) Stem cell regulation by polycomb repressors: postponing commitment. Curr. Opin. Cell Biol., 20, 201-207.
38. Hope, K.J. et al. (2004) Acute myeloid leukemia originates from a hierarchy of leukemic stem cell classes that differ in self-renewal capacity. Nat. Immunol., 5, 738-743.
39. Pronk, C.J. et al. (2007) Elucidation of the phenotypic, functional, and molecular topography of a myeloerythroid progenitor cell hierarchy. Cell Stem Cell, 1, 428-442.
40. Hill, R.P. (2006) Identifying cancer stem cells in solid tumors: case not proven. Cancer Res., 66, 1891-1895.
41. Adams, J.M. et al. (2008) Is tumor growth sustained by rare cancer stem cells or dominant clones? Cancer Res., 68, 4018-4021.
42. Zhou, J. et al. (2008) Cancer stem cells: models, mechanisms and implications for improved treatment. Cell Cycle, 7, 1360-1370.
43. Visvader, J.E. et al. (2008) Cancer stem cells in solid tumours: accumulating evidence and unresolved questions. Nat. Rev. Cancer, 8, 755-768.
44. Reya, T. et al. (2001) Stem cells, cancer, and cancer stem cells. Nature, 414, 105-111.
45. Zucchi, I. et al. (2007) The properties of a mammary gland cancer stem cell. Proc. Natl Acad. Sci. USA, 104, 10476-10481.
46. O'Brien, C.A. et al. (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature, 445, 106-110.
47. Blagosklonny, M.V. (2007) Cancer stem cell and cancer stemloids: from biology to therapy. Cancer Biol. Ther., 6, 1684-1690.
48. Furth, J. et al. (1937) The transmission of leukemia of mice with a single cell. Am. J. Cancer, 31, 276-282.
49. Schatton, T. et al. (2008) Cancer stem cells and human malignant melanoma. Pigment Cell Melanoma Res., 21, 39-55.
50. Quintana, E. et al. (2008) Efficient tumour formation by single human melanoma cells. Nature, 456, 593-598.
51. Hahn, W.C. et al. (2002) Rules for making human tumor cells. N. Engl. J. Med., 347, 1593-1603.
52. Hu, T. et al. (2008) Octamer 4 small interfering RNA results in cancer stem cell-like cell apoptosis. Cancer Res., 68, 6533-6540.
53. Soeda, A. et al. (2008) Epidermal growth factor plays a crucial role in mitogenic regulation of human brain tumor stem cells. J. Biol. Chem., 283, 10958-10966.
54. Kirkland, S.C. et al. (2008) Alpha2beta1 integrin regulates lineage commitment in multipotent human colorectal cancer cells. J. Biol. Chem., 283, 27612-27619.
55. van Staveren, W.C. et al. (2009) Human cancer cell lines: experimental models for cancer cells in situ? For cancer stem cells? Biochim. Biophys. Acta, 1795, 92-103.
56. Ju, Z. et al. (2006) Telomeres and telomerase in stem cells during aging and disease. Genome Dyn., 1, 84-103.
57. Flores, I. et al. (2008) The longest telomeres: a general signature of adult stem cell compartments. Genes Dev., 22, 654-667.
58. Clarke, M.F. et al. (2006) Stem cells and cancer: two faces of eve. Cell, 124, 1111-1115.
59. Boyer, L.A. et al. (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature, 441, 349-353.
60. Boman, B.M. et al. (2008) Cancer stem cells: a step toward the cure. J. Clin. Oncol., 26, 2795-2799.
61. Harris, H. (2005) A long view of fashions in cancer research. Bioessays, 27, 833-838.
62. Kasper, S. (2008) Stem cells: the root of prostate cancer? J. Cell. Physiol., 216, 332-336.
63. Sotiriou, C. et al. (2009) Gene-expression signatures in breast cancer. N. Engl. J. Med., 360, 790-800.
64. Lee, M. et al. (2008) Cell polarity and cancer-cell and tissue polarity as a non-canonical tumor suppressor. J. Cell Sci., 121, 1141-1150.
65. Godar, S. et al. (2008) Growth-inhibitory and tumor-suppressive functions of p53 depend on its repression of CD44 expression. Cell, 134, 62-73.
66. Naor, D. et al. (2008) Involvement of CD44, a molecule with a thousand faces, in cancer dissemination. Semin. Cancer Biol., 18, 260-267.
67. Weinberg, R.A. (2008) Twisted epithelial-mesenchymal transition blocks senescence. Nat. Cell Biol., 10, 1021-1023.
68. Ginestier, C. et al. (2007) ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell, 1, 555-567.
69. Eramo, A. et al. (2008) Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ., 15, 504-514.
70. Hermann, P.C. et al. (2007) Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell, 1, 313-323.
71. Du, L. et al. (2008) CD44 is of functional importance for colorectal cancer stem cells. Clin. Cancer Res., 14, 6751-6760.
72. Leong, K.G. et al. (2008) Generation of a prostate from a single adult stem cell. Nature, 456, 804-808.
73. Pallini, R. et al. (2008) Cancer stem cell analysis and clinical outcome in patients with glioblastoma multiforme. Clin. Cancer Res., 14, 8205-8212.
74. Baumann, M. et al. (2008) Exploring the role of cancer stem cells in radioresistance. Nat. Rev. Cancer, 8, 545-554.
75. Phillips, T.M. et al. (2006) The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J. Natl Cancer Inst., 98, 1777-1785.
76. Sager, R. et al. (1985) Gene amplification: an example of accelerated evolution in tumorigenic cells. Proc. Natl Acad. Sci. USA, 82, 7015-7019.
77. Baumann, M. et al. (2009) Cancer stem cells and radiotherapy. Int. J. Radiat. Biol., 85, 391-402.
78. Viale, A. et al. (2009) Cell-cycle restriction limits DNA damage and maintains self-renewal of leukaemia stem cells. Nature, 457, 51-56.
79. Diehn, M. et al. (2009) Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature, 458, 780-783.
80. Eyler, C.E. et al. (2008) Survival of the fittest: cancer stem cells in therapeutic resistance and angiogenesis. J. Clin. Oncol., 26, 2839-2845.
81. Ishii, H. et al. (2008) Cancer stem cells and chemoradiation resistance. Cancer Sci., 99, 1871-1877.
82. Kern, S.E. et al. (2007) The fuzzy math of solid tumor stem cells: a perspective. Cancer Res., 67, 8985-8988.
83. Blagosklonny, M.V. (2005) Why therapeutic response may not prolong the life of a cancer patient: selection for oncogenic resistance. Cell Cycle, 4, 1693-1698.
84. Shibata, D.K. et al. (2008) Ancestral trees for modeling stem cell lineages genetically rather than functionally: understanding mutation accumulation and distinguishing the restrictive cancer stem cell propagation theory and the unrestricted cell propagation theory of human tumorigenesis. Breast Dis., 29, 15-25.
85. Gupta, P.B. et al. (2009) Cancer stem cells: mirage or reality? Nat. Med., 15, 1010-1012.
86. Malaise, E.P. et al. (1973) The relationship between growth rate, labelling index and histological type of human solid tumours. Eur. J. Cancer, 9, 305-312.
87. d'Adda, dF. (2008) Living on a break: cellular senescence as a DNA-damage response. Nat. Rev. Cancer, 8, 512-522.
88. Zhuang, D. et al. (2008) C-MYC overexpression is required for continuous suppression of oncogene-induced senescence in melanoma cells. Oncogene, 27, 6623-6634.
89. Cahill, D.P. et al. (1999) Genetic instability and darwinian selection in tumours. Trends Cell Biol., 9, M57-M60.
90. Loeb, L.A. et al. (2008) Cancers exhibit a mutator phenotype: clinical implications. Cancer Res., 68, 3551-3557.
91. Elena, S.F. et al. (1997) Test of synergistic interactions among deleterious mutations in bacteria. Nature, 390, 395-398.
92. Eyre-Walker, A. et al. (2007) The distribution of fitness effects of new mutations. Nat. Rev. Genet., 8, 610-618.
93. Williams, B.R. et al. (2008) Aneuploidy affects proliferation and spontaneous immortalization in mammalian cells. Science, 322, 703-709.
94. Wang, Q. et al. (2008) Mechanisms of resistance to ErbB-targeted cancer therapeutics. J. Clin. Invest., 118, 2389-2392.
95. Ye, C.J. et al. (2009) Genome based cell population heterogeneity promotes tumorigenicity: the evolutionary mechanism of cancer. J. Cell. Physiol., 219, 288-300.
96. Greaves, M. (2001) Cancer, The Evolutionary Legacy. Oxford University Press, UK, 1-276.
97. Murgia, C. et al. (2006) Clonal origin and evolution of a transmissible cancer. Cell, 126, 477-487.
98. Baker, N.E. et al. (2008) Cell competition and its possible relation to cancer. Cancer Res., 68, 5505-5507.
99. Rhiner, C. et al. (2009) Super competition as a possible mechanism to pioneer precancerous fields. Carcinogenesis, 30, 723-728.
100. Rubin, H. (2008) Cell-cell contact interactions conditionally determine suppression and selection of the neoplastic phenotype. Proc. Natl Acad. Sci. USA, 105, 6215-6221.
101. Johnston, L.A. (2009) Competitive interactions between cells: death, growth, and geography. Science, 324, 1679-1682.
102. Kramer, B.S. et al. (2009) Cancer screening: the clash of science and intuition. Annu. Rev. Med., 60, 125-137.
103. Frumkin, D. et al. (2008) Cell lineage analysis of a mouse tumor. Cancer Res., 68, 5924-5931.
104. Jovanovic, L. et al. (2008) Most multifocal papillary thyroid carcinomas acquire genetic and morphotype diversity through subclonal evolution following the intra-glandular spread of the initial neoplastic clone. J. Pathol., 215, 145-154.
105. McKenna, E.S. et al. (2008) Loss of the epigenetic tumor suppressor SNF5 leads to cancer without genomic instability. Mol. Cell. Biol., 28, 6223-6233.
106. Brock, A. et al. (2009) Non-genetic heterogeneity-a mutation-independent driving force for the somatic evolution of tumours. Nat. Rev. Genet., 10, 336-342.
107. Spencer, S.L. et al. (2009) Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis. Nature, 459, 428-432.
108. Greenman, C. et al. (2007) Patterns of somatic mutation in human cancer genomes. Nature, 446, 153-158.
109. Jones, S. et al. (2008) Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science, 321, 1801-1806.
110. Stratton, M.R. et al. (2009) The cancer genome. Nature, 458, 719-724.
111. Baudot, A. et al. (2009) From cancer genomes to cancer models: bridging the gaps. EMBO Rep., 10, 359-366.
112. Rapp, U.R. et al. (2008) Oncogene-induced plasticity and cancer stem cells. Cell Cycle, 7, 45-51.
113. Shipitsin, M. et al. (2008) The cancer stem cell hypothesis: in search of definitions, markers, and relevance. Lab. Invest., 88, 459-463.
114. Chang, H.H. et al. (2008) Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature, 453, 544-547.
115. Baptist, M. et al. (1991) Various facets of the intercellular heterogeneity in thyroid primary culture. Thyroidology, 3, 109-113.
116. Rosen, J.M. et al. (2009) The increasing complexity of the cancer stem cell paradigm. Science, 324, 1670-1673.
117. Goymer, P. (2008) Natural selection: the evolution of cancer. Nature, 454, 1046-1048.
118. Ma, S. et al. (2008) Aldehyde dehydrogenase discriminates the CD133 liver cancer stem cell populations. Mol. Cancer Res., 6, 1146-1153.
119. Fang, J.S. et al. (2008) Adaptation to hypoxia and acidosis in carcinogenesis and tumor progression. Semin. Cancer Biol., 18, 330-337.
120. Piccirillo, S.G. et al. (2009) Distinct pools of cancer stem-like cells coexist within human glioblastomas and display different tumorigenicity and independent genomic evolution. Oncogene, 28, 1807-1811.
121. Unger, K. et al. (2008) Array CGH demonstrates characteristic aberration signatures in human papillary thyroid carcinomas governed by RET/PTC. Oncogene, 27, 4592-4602.
122. Karoui, M. et al. (2004) Loss of heterozygosity on 10q and mutational status of PTEN and BMPR1A in colorectal primary tumours and metastases. Br. J. Cancer, 90, 1230-1234.
123. Fox, E.J. et al. (2009) Cancer genome sequencing-an interim analysis. Cancer Res., 69, 4948-4950.
124. Siegmund, K.D. et al. (2009) Inferring clonal expansion and cancer stem cell dynamics from DNA methylation patterns in colorectal cancers. Proc. Natl Acad. Sci. USA, 106, 4828-4833.
125. Odoux, C. et al. (2008) A stochastic model for cancer stem cell origin in metastatic colon cancer. Cancer Res., 68, 6932-6941.
126. Gonzalez-Garcia, I. et al. (2002) Metapopulation dynamics and spatial heterogeneity in cancer. Proc. Natl Acad. Sci. USA, 99, 13085-13089.
127. Mullighan, C.G. et al. (2008) Genomic analysis of the clonal origins of relapsed acute lymphoblastic leukemia. Science, 322, 1377-1380.
128. Shackleton, M. et al. (2006) Generation of a functional mammary gland from a single stem cell. Nature, 439, 84-88.
129. Epstein, S.S. (2009) Microbial awakenings. Nature, 457, 1083.
130. Thomas, R. (1978) Logical analysis of systems comprising feedback loops. J. Theor. Biol., 73, 631-656.