Cancer stem cells: Models and concepts

Annual Review of Medicine

Volumn 58, Issue , 2007, Pages 267-284

  Dalerba, Piero ^a   Cho, Robert W ^a   Clarke, Michael F ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aberrant differentiation; Functional heterogeneity of tumor tissues; Self renewal; Targeting of antitumor treatments

Indexed keywords

BLOOD CELL; BRAIN CANCER; BREAST CANCER; CANCER CELL; CANCER GROWTH; CANCER IMMUNOTHERAPY; CANCER STEM CELL; CARCINOGENESIS; CELL CLONING; CELL DIFFERENTIATION; CELL FATE; CELL RENEWAL; CELL SUBPOPULATION; CELL TRANSFORMATION; CYTOLOGY; GENETIC VARIABILITY; HEMATOPOIETIC STEM CELL; HUMAN; METASTASIS; MYELOID LEUKEMIA; NONHUMAN; PRIORITY JOURNAL; REVIEW; SOMATIC MUTATION; TARGET CELL DESTRUCTION; TREATMENT OUTCOME; BIOLOGICAL MODEL; NEOPLASM; PATHOLOGY; PHYSIOLOGY;

HUMANS; MODELS, BIOLOGICAL; NEOPLASMS; TUMOR STEM CELLS;

EID: 34047096557     PISSN: 00664219     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.med.58.062105.204854     Document Type: Review

References (92)

1. Clarke MF, Fuller M. 2006. Stem cells and cancer: two faces of Eve. Cell 124:1111-15
2. Reya T, Morrison SJ, Clarke MF, Weissman IL. 2001. Stem cells, cancer, and cancer stem cells. Nature 414:105-11
3. Fearon ER, Vogelstein B. 1990. A genetic model for colorectal tumorigenesis. Cell 61:759-67
4. Clarke MF. 2005. A self-renewal assay for cancer stem cells. Cancer Chemother. Pharmacol. 56(Suppl. 1):64-68
5. Till JE, McCulloch EA. 1961. A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat. Res. 14:213-22
6. Kondo M, Wagers AJ, Manz MG, et al. 2003. Biology of hematopoietic stem cells and progenitors: implications for clinical application. Annu. Rev. Immunol. 21:759-806
7. Spangrude GJ, Heimfeld S, Weissman IL. 1988. Purification and characterization of mouse hematopoietic stem cells. Science 241:58-62
8. Morrison SJ, Weissman IL. 1994. The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1:661-73
9. Morrison SJ, Wandycz AM, Hemmati HD, et al. 1997. Identification of a lineage of multipotent hematopoietic progenitors. Development 124:1929-39
10. Kiel MJ, Yilmaz OH, Iwashita T, et al. 2005. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121:1109-21
11. Passegue E, Jamieson CH, Ailles LE, Weissman IL. 2003. Normal and leukemic hematopoiesis: Are leukemias a stem cell disorder or a reacquisition of stem cell characteristics? Proc. Natl. Acad. Sci. USA 100(Suppl. 1):11842-49
12. Dick JE, Bhatia M, Gan O, et al. 1997. Assay of human stem cells by repopulation of NOD/SCID mice. Stem Cells 15(Suppl. 1):199-203; discussion 204-7
13. Bhatia M, Wang JC, Kapp U, et al. 1997. Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Proc. Natl. Acad. Sci. USA 94:5320-25
14. Manz MG, Miyamoto T, Akashi K, Weissman IL. 2002. Prospective isolation of human clonogenic common myeloid progenitors. Proc. Natl. Acad. Sci. USA 99:11872-77
15. Terstappen LW, Huang S, Safford M, et al. 1991. Sequential generations of hematopoietic colonies derived from single nonlineage-committed CD34+CD38- progenitor cells. Blood 77:1218-27
16. Baum CM, Weissman IL, Tsukamoto AS, et al. 1992. Isolation of a candidate human hematopoietic stem-cell population. Proc. Natl. Acad. Sci. USA 89:2804-8
17. Shizuru JA, Negrin RS, Weissman IL. 2005. Hematopoietic stem and progenitor cells: clinical and preclinical regeneration of the hematolymphoid system. Annu. Rev. Med. 56:509-38
18. Fialkow PJ, Faguet GB, Jacobson RJ, et al. 1981. Evidence that essential thrombocythemia is a clonal disorder with origin in a multipotent stem cell. Blood 58:916-19
19. Fialkow PJ, Jacobson RJ, Papayannopoulou T. 1977. Chronic myelocytic leukemia: clonal origin in a stem cell common to the granulocyte, erythrocyte, platelet and monocyte/macrophage. Am. J. Med. 63:125-30
20. Adamson JW, Fialkow PJ, Murphy S, et al. 1976. Polycythemia vera: stem-cell and probable clonal origin of the disease. N. Engl. J. Med. 295:913-16
21. Fialkow PJ, Singer JW, Adamson JW, et al. 1981. Acute nonlymphocytic leukemia: heterogeneity of stem cell origin. Blood 57:1068-73
22. Bonnet D, Dick JE. 1997. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 3:730-37
23. Lapidot T, Sirard C, Vormoor J, et al. 1994. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367:645-48
24. Turhan AG, Lemoine FM, Debert C, et al. 1995. Highly purified primitive hematopoietic stem cells are PML-RARA negative and generate nonclonal progenitors in acute promyelocytic leukemia. Blood 85:2154-61
25. Miyamoto T, Weissman IL, Akashi K. 2000. AML1/ETO-expressing nonleukemic stem cells in acute myelogenous leukemia with 8;21 chromosomal translocation. Proc. Natl. Acad. Sci. USA 97:7521-26
26. Blair A, Hogge DE, Ailles LE, et al. 1997. Lack of expression of Thy-1 (CD90) on acute myeloid leukemia cells with long-term proliferative ability in vitro and in vivo. Blood 89:3104-12
27. Weissman IL. 2005. Stem cell research: paths to cancer therapies and regenerative medicine. JAMA 294:1359-66
28. Takahashi N, Miura I, Saitoh K, Miura AB. 1998. Lineage involvement of stem cells bearing the Philadelphia chromosome in chronic myeloid leukemia in the chronic phase as shown by a combination of fluorescence-activated cell sorting and fluorescence in situ hybridization. Blood 92:4758-63
29. Primo D, Sanchez ML, Espinosa AB, et al. 2006. Lineage involvement in chronic myeloid leukaemia: comparison between MBCR/ABL and mBCR/ABL cases. Br. J. Haematol. 132:736-9
30. Jamieson CH, Ailles LE, Dylla SJ, et al. 2004. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N. Engl. J. Med. 351:657-67
31. Clarke MF. 2004. Chronic myelogenous leukemia - identifying the hydra's heads. N. Engl. J. Med. 351:634-36
32. Lessard J, Baban S, Sauvageau G. 1998. Stage-specific expression of polycomb group genes in human bone marrow cells. Blood 91:1216-24
33. Park IK, Qian D, Kiel M, et al. 2003. Bmi-1 is required for maintenance of adult self-renewing hematopoietic stem cells. Nature 423:302-5
34. Kroon E, Krosl J, Thorsteinsdottir U, et al. 1998. Hoxa9 transforms primary bone marrow cells through specific collaboration with Meis1a but not Pbx1b. EMBO J. 17:3714-25
35. Lessard J, Sauvageau G. 2003. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 423:255-60
36. Di Cristofano A, Pandolfi PP. 2000. The multiple roles of PTEN in tumor suppression. Cell 100:387-90
37. Yilmaz OH, Valdez R, Theisen BK, et al. 2006. Pten dependence distinguishes hematopoietic stem cells from leukaemia-initiating cells. Nature 441:475-82
38. Zhang J, Grindley JC, Yin T, et al. 2006. PTEN maintains hematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature 441:518-22
39. Dalerba P, Guiducci C, Poliani PL, et al. 2005. Reconstitution of human telomerase reverse transcriptase expression rescues colorectal carcinoma cells from in vitro senescence: evidence against immortality as a constitutive trait of tumor cells. Cancer Res. 65:2321-29
40. Shackleton M, Vaillant F, Simpson KJ, et al. 2006. Generation of a functional mammary gland from a single stem cell. Nature 439:84-88
41. Stingl J, Eirew P, Ricketson I, et al. 2006. Purification and unique properties of mammary epithelial stem cells. Nature 439:993-97
42. Brittan M, Wright NA. 2004. Stem cell in gastrointestinal structure and neoplastic development. Gut 53:899-910
43. Bach SP, Renehan AG, Potten CS. 2000. Stem cells: the intestinal stem cell as a paradigm. Carcinogenesis 21:469-76
44. Seery JP. 2002. Stem cells of the esophageal epithelium. J. Cell Sci. 115:1783-89
45. Watt FM. 2001. Stem cell fate and patterning in mammalian epidermis. Curr. Opin. Genet. Dev. 11:410-17
46. Sancho E, Batlle E, Clevers H. 2003. Live and let die in the intestinal epithelium. Curr. Opin. Cell Biol. 15:763-70
47. Alonso L, Fuchs E. 2003. Stem cells of the skin epithelium. Proc. Natl. Acad. Sci. USA 100(Suppl. 1):11830-35
48. Kim CF, Jackson EL, Woolfenden AE, et al. 2005. Identification of bronchioalveolar stem cells in normal lung and lung cancer. Cell 121:823-35
49. Otto WR. 2002. Lung epithelial stem cells. J. Pathol. 197:527-35
50. Gargett CE. 2004. Stem cells in gynaecology. Aust. NZ J. Obstet. Gynaecol. 44:380-86
51. Potten CS. 1998. Stem cells in gastrointestinal epithelium: numbers, characteristics and death. Philos. Trans. R. Soc. London Ser. B 353:821-30
52. Schalken JA, van Leenders G. 2003. Cellular and molecular biology of the prostate: stem cell biology. Urology 62:11-20
53. Ming GL, Song H. 2005. Adult neurogenesis in the mammalian central nervous system. Annu. Rev. Neurosci. 28:223-50
54. Collins CA, Olsen I, Zammit PS, et al. 2005. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 122:289-301
55. Luckey CJ, Bhattacharya D, Goldrath AW, et al. 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 103:3304-9
56. Al-Hajj M, Wicha MS, Benito-Hernandez A, et al. 2003. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. USA 100:3983-88
57. Stingl J, Raouf A, Emerman JT, Eaves CJ. 2005. Epithelial progenitors in the normal human mammary gland. J. Mammary Gland Biol. Neoplasia 10:49-59
58. Dontu G, Abdallah WM, Foley JM, et al. 2003. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 17:1253-70
59. Ponti D, Costa A, Zaffaroni N, et al. 2005. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res. 65:5506-11
60. Galli R, Binda E, Orfanelli U, et al. 2004. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 64:7011-21
61. Singh SK, Clarke ID, Terasaki M, et al. 2003. Identification of a cancer stem cell in human brain tumors. Cancer Res. 63:5821-28
62. Singh SK, Hawkins C, Clarke ID, et al. 2004. Identification of human brain tumor initiating cells. Nature 432:396-401
63. Vescovi AL, Galli R, Reynolds BA. 2006. Brain tumor stem cells. Nat. Rev. Cancer 6:425-36
64. Collins AT, Berry PA, Hyde C, et al. 2005. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res. 65:10946-51
65. Patrawala L, Calhoun T, Schneider-Broussard R, et al. 2006. Highly purified CD44+ prostate cancer cells from xenograft human tumors are enriched in tumorigenic and metastatic progenitor cells. Oncogene 25:1696-708
66. Fang D, Nguyen TK, Leishear K, et al. 2005. A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res. 65:9328-37
67. Xin L, Lawson DA, Witte ON. 2005. The Sca-1 cell surface marker enriches for a prostate-regenerating cell subpopulation that can initiate prostate tumorigenesis. Proc. Natl. Acad. Sci. USA 102:6942-47
68. Matsui W, Huff CA, Wang Q, et al. 2004. Characterization of clonogenic multiple myeloma cells. Blood 103:2332-36
69. Brabletz T, Jung A, Spaderna S, et al. 2005. Opinion: migrating cancer stem cells - an integrated concept of malignant tumor progression. Nat. Rev. Cancer 5:744-49
70. Losi L, Baisse B, Bouzourene H, Benhattar J. 2005. Evolution of intratumoral genetic heterogeneity during colorectal cancer progression. Carcinogenesis 26:916-22
71. Brabletz T, Jung A, Reu S, et al. 2001. Variable beta-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc. Natl. Acad. Sci. USA 98:10356-61
72. Yan P, Benhattar J, Seelentag W, et al. 2 004. Immunohistochemical localization of hTERT protein in human tissues. Histochem. Cell Biol. 121:391-97
73. Hanahan D, Weinberg RA. 2000. The hallmarks of cancer. Cell 100:57-70
74. Shay JW, Wright WE. 2005. Senescence and immortalization: role of telomeres and telomerase. Carcinogenesis 26:867-74
75. Kyo S, Inoue M. 2002. Complex regulatory mechanisms of telomerase activity in normal and cancer cells: How can we apply them for cancer therapy? Oncogene 21:688-97
76. Morrison SJ, Prowse KR, Ho P, Weissman IL. 1996. Telomerase activity in hematopoietic cells is associated with self-renewal potential. Immunity 5:207-16
77. Dimri GP, Martinez JL, Jacobs JJL, et al. 2002. The Bmi-1 oncogene induces telomerase activity and immortalizes human mammary epithelial cells. Cancer Res. 62:4736-45
78. Yan P, Saraga EP, Bouzourene H, et al. 2001. Expression of telomerase genes correlates with telomerase activity in human colorectal carcinogenesis. J. Pathol. 193:21-26
79. Altieri DC. 2003. Survivin, versatile modulation of cell division and apoptosis in cancer. Oncogene 22:8581-89
80. Losi L, Benhattar J, Costa J. 1992. Stability of K-ras mutations throughout the natural history of human colorectal cancer. Eur. J. Cancer 28A:1115-20
81. Khan ZA, Jonas SK, Le-Marer N, et al. 2000. P53 mutations in primary and metastatic tumors and circulating tumor cells from colorectal carcinoma patients. Clin. Cancer Res. 6:3499-504
82. Zauber P, Sabbath-Solitare M, Marotta SP, Bishop DT. 2003. Molecular changes in the Ki-ras and APC genes in primary colorectal carcinoma and synchronous metastases compared with the findings in accompanying adenomas. Mol. Pathol. 56:137-40
83. Menon AG, Tollenaar RA, van de Velde CJ, et al. 2004. p53 and HLA class-I expression are not down-regulated in colorectal cancer liver metastases. Clin. Exp. Metastasis 21:79-85
84. Dalerba P, Ricci A, Russo V, et al. 1998. High homogeneity of MAGE, BAGE, GAGE, tyrosinase and Melan-A/MART-1 gene expression in clusters of multiple simultaneous metastases of human melanoma: implications for protocol design of therapeutic antigen-specific vaccination strategies. Int. J. Cancer 77:200-4
85. D'Arrigo A, Belluco C, Ambrosi A, et al. 2005. Metastatic transcriptional pattern revealed by gene expression profiling in primary colorectal carcinoma. Int. J. Cancer 115:256-62
86. Weigelt B, Glas AM, Wessels LF, et al. 2003. Gene expression profiles of primary breast tumors maintained in distant metastases. Proc. Natl. Acad. Sci. USA 100:15901-5
87. Weigelt B, Peterse JL, van't Veer LJ. 2005. Breast cancer metastasis: markers and models. Nat. Rev. Cancer 5:591-602
88. Guan Y, Gerhard B, Hogge DE. 2003. Detection, isolation, and stimulation of quiescent primitive leukemic progenitor cells from patients with acute myeloid leukemia (AML). Blood 101:3142-49
89. Guzman ML, Swiderski CF, Howard DS, et al. 2002. Preferential induction of apoptosis for primary human leukemic stem cells. Proc. Natl. Acad. Sci. USA 99:16220-25
90. Al-Hajj M, Becker MW, Wicha M, et al. 2004. Therapeutic implications of cancer stem cells. Curr. Opin. Genet. Dev. 14:43-47
91. Dalerba P, Maccalli C, Casati C, et al. 2003. Immunology and immunotherapy of colorectal cancer. Crit. Rev. Oncol. Hematol. 46:33-57
92. Parmiani G, Castelli C, Dalerba P, et al. 2002. Cancer immunotherapy with peptide-based vaccines: What have we achieved? Where are we going? J. Natl. Cancer Inst. 94:805-18