Cancer stem cells: The challenges ahead

Nature Cell Biology

Volumn 15, Issue 4, 2013, Pages 338-344

  Medema, Jan Paul ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

NESTIN; TRANSCRIPTOME; TUMOR MARKER;

CANCER CELL; CANCER GENETICS; CANCER IMMUNOLOGY; CANCER RESEARCH; CANCER STEM CELL; CARCINOGENESIS; CELL DIFFERENTIATION; CELL INVASION; DISEASE MARKER; EPIGENETICS; GENE MUTATION; HUMAN; METASTASIS; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; REVIEW; TUMOR MICROENVIRONMENT; XENOTRANSPLANTATION;

ANIMALS; HUMANS; MICE; NEOPLASM METASTASIS; NEOPLASMS; NEOPLASTIC STEM CELLS;

EID: 84876489727     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2717     Document Type: Review

References (81)

1. Clarke, M. F. et al. Cancer stem cells-perspectives on current status and future directions: AACR workshop on cancer stem cells. Cancer Res. 66, 9339-9344 (2006). (Pubitemid 44623625)
2. Vermeulen, L., Sprick, M. R., Kemper, K., Stassi, G. & Medema, J. P. Cancer stem cells-old concepts, new insights. Cell Death Differ. 15, 947-958 (2008). (Pubitemid 351712600)
3. 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. 13, e83-e89 (2012).
4. Heppner, G. H. & Miller, F. R. The cellular basis of tumor progression. Int. Rev. Cytol. 177, 1-56 (1998). (Pubitemid 128716720)
5. Wicha, M. S., Liu, S. & Dontu, G. Cancer stem cells: an old idea-a paradigm shift. Cancer Res. 66, 1883-1890 (2006).
6. Lapidot, T. et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367, 645-648 (1994). (Pubitemid 24067706)
7. Hill, R. P. Identifying cancer stem cells in solid tumors: case not proven. Cancer Res. 66, 1891-1895 (2006).
8. 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)
9. Masters, J. R., Kane, C., Yamamoto, H. & Ahmed, A. Prostate cancer stem cell therapy: hype or hope? Prostate Cancer Prostatic Dis. 11, 316-319 (2008).
10. Kemper, K., Grandela, C. & Medema, J. P. Molecular identification and targeting of colorectal cancer stem cells. Oncotarget 1, 387-395 (2010).
11. Quintana, E. et al. Efficient tumour formation by single human melanoma cells. Nature 456, 593-598 (2008).
12. Chen, J. et al. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 488, 522-526 (2012).
13. Driessens, G., Beck, B., Caauwe, A., Simons, B. D. & Blanpain, C. Defining the mode of tumour growth by clonal analysis. Nature 488, 527-530 (2012).
14. Schepers, A. G. et al. Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adenomas. Science 337, 730-735 (2012).
15. Visvader, J. E. Cells of origin in cancer. Nature 469, 314-322 (2011).
16. Magee, J. A., Piskounova, E. & Morrison, S. J. Cancer stem cells: impact, heterogeneity, and uncertainty. Cancer Cell 21, 283-296 (2012).
17. Kemper, K. et al. The AC133 epitope, but not the CD133 protein, is lost upon cancer stem cell differentiation. Cancer Res. 70, 719-729 (2010).
18. Mak, A. B. et al. CD133 protein N-glycosylation processing contributes to cell surface recognition of the primitive cell marker AC133 epitope. J. Biol. Chem. 286, 41046-41056 (2011).
19. Ricci-Vitiani, L. et al. Identification and expansion of human colon-cancer-initiating cells. Nature 445, 111-115 (2007). (Pubitemid 46067311)
20. O'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)
21. Dalerba, P. et al. Phenotypic characterization of human colorectal cancer stem cells. Proc. Natl Acad. Sci. USA 104, 10158-10163 (2007). (Pubitemid 47175279)
22. Al-Hajj, M., Wicha, M. S., Ito-Hernandez, A., Morrison, S. J. & Clarke, M. F. Prospective identification of tumo-rigenic breast cancer cells. Proc. Natl Acad. Sci. USA 100, 3983-3988 (2003). (Pubitemid 36418143)
23. Jijiwa, M. et al. CD44v6 regulates growth of brain tumor stem cells partially through the AKT-mediated pathway. PLoS ONE 6, e24217 (2011).
24. Snyder, E. L., Bailey, D., Shipitsin, M., Polyak, K. & Loda, M. Identification of CD44v6(+)/CD24-breast carcinoma cells in primary human tumors by quantum dot-conjugated antibodies. Lab Invest. 89, 857-866 (2009).
25. Yi, J. M. et al. Abnormal DNA methylation of CD133 in colorectal and glioblastoma tumors. Cancer Res. 68, 8094-8103 (2008).
26. Douville, J., Beaulieu, R. & Balicki, D. ALDH1 as a functional marker of cancer stem and progenitor cells. Stem Cells Dev. 18, 17-25 (2009).
27. Ginestier, C. et al. 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 (2007). (Pubitemid 350056407)
28. Deng, S. et al. Distinct expression levels and patterns of stem cell marker, aldehyde dehydrogenase isoform 1 (ALDH1), in human epithelial cancers. PLoS ONE 5, e10277 (2010).
29. Ma, I. & Allan, A. L. The role of human aldehyde dehy-drogenase in normal and cancer stem cells. Stem Cell Rev. 7, 292-306 (2011).
30. Ginestier, C. et al. Retinoid signaling regulates breast cancer stem cell differentiation. Cell Cycle 8, 3297-3302 (2009).
31. Schatton, T. et al. Identification of cells initiating human melanomas. Nature 451, 345-349 (2008).
32. Wilson, B. J. et al. ABCB5 identifies a therapy-refractory tumor cell population in colorectal cancer patients. Cancer Res. 71, 5307-5316 (2011).
33. Vermeulen, L. et al. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat. Cell Biol. 12, 468-476 (2010).
34. Lonardo, E. et al. 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 (2011).
35. Liu, S. et al. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 66, 6063-6071 (2006).
36. Sims-Mourtada, J., Izzo, J. G., Ajani, J. & Chao, K. S. Sonic Hedgehog promotes multiple drug resistance by regulation of drug transport. Oncogene 26, 5674-5679 (2007). (Pubitemid 47267845)
37. Van der Flier, L. G. The intestinal Wnt/TCF signature. Gastroenterology 132, 628-632 (2007).
38. Katoh, Y. & Katoh, M. Comparative genomics on PROM1 gene encoding stem cell marker CD133. Int. J. Mol. Med. 19, 967-970 (2007).
39. Valent, P. et al. Cancer stem cell definitions and terminology: the devil is in the details. Nat. Rev. Cancer 12, 767-775 (2012).
40. Medema, J. P. & Vermeulen, L. Microenvironmental regulation of stem cells in intestinal homeostasis and cancer. Nature 474, 318-326 (2011).
41. Shestopalov, I. A. & Zon, L. I. Stem cells: The right neighbour. Nature 481, 453-455 (2012).
42. Borovski, T., de Sousa e Melo, F., Vermeulen, L. & Medema, J. P. Cancer stem cell niche: the place to be. Cancer Res. 71, 634-639 (2011).
43. Calabrese, C. et al. A perivascular niche for brain tumor stem cells. Cancer Cell 11, 69-82 (2007). (Pubitemid 46054518)
44. Borovski, T. et al. Tumor microvasculature supports proliferation and expansion of glioma-propagating cells. Int. J. Cancer 125, 1222-1230 (2009).
45. Ricci-Vitiani, L. et al. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 468, 824-828 (2010).
46. Wang, R. et al. Glioblastoma stem-like cells give rise to tumour endothelium. Nature 468, 829-833 (2010).
47. Lonardo, E., Frias-Aldeguer, J., Hermann, P. C. & Heeschen, C. Pancreatic stellate cells form a niche for cancer stem cells and promote their self-renewal and invasiveness. Cell Cycle 11, 1282-1290 (2012).
48. Liu, S. et al. Breast cancer stem cells are regulated by mesenchymal stem cells through cytokine networks. Cancer Res. 71, 614-624 (2011).
49. Fodde, R. & Brabletz, T. Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr. Opin. Cell Biol. 19, 150-158 (2007). (Pubitemid 46386404)
50. Christensen, K., Schroder, H. D. & Kristensen, B. W. CD133+ niches and single cells in glioblastoma have different phenotypes. J. Neurooncol. 104, 129-143 (2011).
51. Buijs, J. T. et al. The BMP2/7 heterodimer inhibits the human breast cancer stem cell subpopulation and bone metastases formation. Oncogene 31, 2164-2174 (2012).
52. Lombardo, Y. et al. Bone morphogenetic protein 4 induces differentiation of colorectal cancer stem cells and increases their response to chemotherapy in mice. Gastroenterology 140, 297-309 (2011).
53. Piccirillo, S. G. et al. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 444, 761-765 (2006). (Pubitemid 44949605)
54. Kai, K. et al. Maintenance of HCT116 colon cancer cell line conforms to a stochastic model but not a cancer stem cell model. Cancer Sci. 100, 2275-2282 (2009).
55. Gupta, P. B. et al. Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell 146, 633-644 (2011).
56. Bryder, D., Rossi, D. J. & Weissman, I. L. Hematopoietic stem cells: the paradigmatic tissue-specific stem cell. Am. J. Pathol. 169, 338-346 (2006). (Pubitemid 44156296)
57. Yamanaka, S. & Blau, H. M. Nuclear reprogramming to a pluripotent state by three approaches. Nature 465, 704-712 (2010).
58. Van Es, J. H. et al. Dll1(+) secretory progenitor cells revert to stem cells upon crypt damage. Nat. Cell Biol. 14, 1099-1104 (2012).
59. Mani, S. A. et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133, 704-715 (2008). (Pubitemid 351636299)
60. Morel, A. P. et al. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS ONE 3, e2888 (2008).
61. Burk, U. et al. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 9, 582-589 (2008). (Pubitemid 351772923)
62. Scheel, C. et al. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell 145, 926-940 (2011).
63. Tsai, K. S. et al. Mesenchymal stem cells promote formation of colorectal tumors in mice. Gastroenterology 141, 1046-1056 (2011).
64. Friedmann-Morvinski, D. et al. Dedifferentiation of neurons and astrocytes by oncogenes can induce gliomas in mice. Science 338, 1080-1084 (2012).
65. Brabletz, T. To differentiate or not-routes towards metastasis. Nat. Rev. Cancer 12, 425-436 (2012).
66. Sottoriva, A. et al. Cancer stem cell tumor model reveals invasive morphology and increased phenotypical heterogeneity. Cancer Res. 70, 46-56 (2010).
67. Bruna, A. et al. TGFbeta induces the formation of tumour-initiating cells in claudinlow breast cancer. Nat. Commun. 3, 1055 (2012).
68. 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 5, 744-749 (2005). (Pubitemid 41486367)
69. Yang, J. & Weinberg, R. A. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev. Cell 14, 818-829 (2008). (Pubitemid 351757205)
70. Alix-Panabieres, C. et al. Detection and characterization of putative metastatic precursor cells in cancer patients. Clin. Chem. 53, 537-539 (2007). (Pubitemid 46447957)
71. 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)
72. Malanchi, I. et al. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 481, 85-89 (2012).
73. Gentles, A. J., Plevritis, S. K., Majeti, R. & Alizadeh, A. A. Association of a leukemic stem cell gene expression signature with clinical outcomes in acute myeloid leukemia. JAMA 304, 2706-2715 (2010).
74. Merlos-Suarez, A. et al. The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse. Cell Stem Cell 8, 511-524 (2011).
75. Pece, S. et al. Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell 140, 62-73 (2010).
76. de Sousa e Melo F. et al. Methylation of cancer-stem-cell-associated Wnt target genes predicts poor prognosis in colorectal cancer patients. Cell Stem Cell 9, 476-485 (2011).
77. 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)
78. Pang, R. et al. A subpopulation of CD26+ cancer stem cells with metastatic capacity in human colorectal cancer. Cell Stem Cell 6, 603-615 (2010).
79. Dieter, S. M. et al. Distinct types of tumor-initiating cells form human colon cancer tumors and metastases. Cell Stem Cell 9, 357-365 (2011).
80. Park, S. M., Gaur, A. B., Lengyel, E. & Peter, M. E. The miR-200 family determines the epithelial phe-notype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 22, 894-907 (2008). (Pubitemid 351482843)
81. Todaro, M., Francipane, M. G., Medema, J. P. & Stassi, G. Colon cancer stem cells: promise of targeted therapy. Gastroenterology 138, 2151-2162 (2010).