Is cancer a stem cell disease? Theory, evidence and implications

Veterinary and Comparative Oncology

Volumn 5, Issue 2, 2007, Pages 76-89

  Blacking, T M ^a   Wilson, H ^b   Argyle, David J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 42449096121     PISSN: 14765810     EISSN: 14765829     Source Type: Journal    
DOI: 10.1111/j.1476-5829.2007.00127.x     Document Type: Review

References (77)

1. Moore KA and Lemischka IR. Stem cells and their niches. Science 2006; 311: 1880-1885.
2. Pierce GB and Johnson LD. Differentiation and cancer. In Vitro 1971; 7: 140-145.
3. Potter VR. Phenotypic diversity in experimental hepatomas: The concept of partially blocked ontogeny. The 10 th Walter Hubert Lecture. British Journal of Cancer 1978; 38: 1-23.
4. Failkow PJ, Jacobson RJ and Papayannopoulou T. Chronic myelocytic leukaemia: Clonal origin in a stem cell common to the granulocyte, erythrocyte, platelet and macrophage/monocyte. American Journal of Medicine 1977; 63: 125-130.
5. Al-Hajj M and Clarke MF. Self-renewal and solid tumor stem cells. Oncogene 2004; 23: 7274-7282.
6. Reya T, Morrison SJ, Clarke MF and Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001; 414: 105-111.
7. Park CH, Bergsage DE and McCulloc EA. Mouse myeloma tumour stem cells: primary cell culture assay. Journal of the National Cancer Institute 1971; 46: 411.
8. Huntly BJ and Gilliland DG. Leukaemia stem cells and the evolution of cancer-stem-cell research. Nature Reviews. Cancer 2005; 5: 311-321.
9. Kamel-Reid S, Letarte M, Sirard C, Doedens M, Grunberger T, Fulop G, Freedman MH, Phillips RA and Dick JE. A model of human acute lymphoblastic leukemia in immune-deficient SCID mice. Science 1989; 246: 1597-1600.
10. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, Minden M, Paterson B, Caligiuri MA and Dick JE. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994; 367: 645-648.
11. Sirard C, Lapidot T, Vormoor J, Cashman JD, Doedens M, Murdoch B, Jamal N, Messnor H, Addey L, Minden M, Laraya P, Keating A, Eaves A, Lansdorp PM, Eaves CJ and Dick JE. Normal and leukemic SCID-repopulating cells (SRC) coexist in the bone marrow and peripheral blood from CML patients in chronic phase, whereas leukemic SRC are detected in blast crisis. Blood 1996; 87: 1539-1548.
12. Bonnet D and Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nature Medicine 1997; 3: 730-737.
13. Fidler IJ and Kripke ML. Metastasis results from preexisting variant cells within a malignant tumor. Science 1977; 197: 893-895.
14. Fidler IJ and Hart IR. Biological diversity in metastatic neoplasms: origins and implications. Science 1982; 217: 998-1003.
15. Heppner GH. Tumor heterogeneity. Cancer Research 1984; 44: 2259-2265.
16. Nowell PC. Mechanisms of tumor progression. Cancer Research 1986; 46: 2203-2207.
17. Southam CM and Brunschwig A. Quantitative studies of autotransplantation of human cancer. Cancer 1961; 14: 971-978.
18. Reynolds BA, Tetzlaff W and Weiss S. A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. Journal of Neuroscience 1992; 12: 4565-4574.
19. Ignatova TN, Kukevov VG, Laywell ED, Suslov ON, Vrionis FD and Steindler DA. Human cortical glial tumors contain neural stem-like cells expressing astroglial and neuronal markers in vitro. Glia 2002; 39: 193-206.
20. Gibbs CP, Kukekov VG, Reith JD, Tchigrinova O, Suslov ON, Scott EW, Ghivizzani SC, Ignatova TN and Steindler DA. Stem-like cells in bone sarcomas: Implications for tumorigenesis. Neoplasia 2005; 7: 967-976.
21. Fults D, Pedone C, Dai C and Holland EC. MYC expression promotes the proliferation of neural progenitor cells in culture and in vivo. Neoplasia 2002; 4: 32-39.
22. Holland EC, Celestino J, Dai C, Schaefer L, Sawaya RE and Fuller GN. Combined activation of Ras and Akt in neural progenitors induces glioblastoma formation in mice. Nature Genetics 2000; 25: 55-57.
23. Dai C, Celestino JC, Okada Y, Louis DN, Fuller GN and Holland EC. PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas and oligoastrocytomas from neural progenitors and astrocytes in vivo. Genes and Development 2001; 15: 1913-1925.
24. Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M and Kornblum HI. Cancerous stem cells can arise from pediatric brain tumors. Proceedings of the National Academy of Sciences of the United States of America 2003; 100: 15178-15183.
25. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J and Dirks PB. Identification of a cancer stem cell in human brain tumors. Cancer Research 2003; 63: 5821-5828.
26. Singh SK, Hawking C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelmen RM, Cusimano MD and Dirks PB. Identification of human brain tumour initiating cells. Nature 2004; 432: 396-401.
27. Galli R, Binda E, Ortanelli U, Gritti A, De Vitis S, Fiocco R, Foroni C, Dimeco F and Vescovi A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Research 2004; 64: 7011-7021.
28. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ and Wicha MS. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes and Development 2003; 17: 1253-1270.
29. Dontu G, Jackson KW, McNicholas E, Kawamura MJ, Adallah WM and Wicha MS. Role of Notch signaling in cell-fate determination of human mammary stem/ progenitor cells. Breast Cancer Research 2004; 6: R605-R615.
30. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ and Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proceedings of the National Academy of Sciences of the United States of America 2003; 100: 3983-3988.
31. Abraham BK, Fritz P, McClellan M, Hauptvogel P, Athelogou M and Brauch H. Prevalence of CD44+/CD24-/low cells in breast cancer may not be associated with clinical outcome but may favor distant metastasis. Clin Cancer Res 2005; 11: 1154-1159.
32. Balic M, Lin H, Young L, Hawes D, Guiliano A, McNamara G, Datar RH and Cote RJ. Most early disseminated cancer cells detected in bone marrow of breast cancer patients have a putative breast cancer stem cell phenotype. Clin Cancer Res 2006; 12: 5615-5621.
33. Seaberg RM and Van der Kooy D. Stem and progenitor cells: The premature desertion of rigorous definitions Trends in Neurosciences 2003; 26: 125-131.
34. Reynolds BA and Rietze RL. Neural stem cells and neurospheres-re-evaluating the relationship. Nat Methods 2005; 2: 333-336.
35. O'Brien CA, Pollett A, Gallinger S and Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2006.
36. Ricci-Vitiani L, Lombardi DG, Pilozzi E, Biffoni M, Todaro M, Peschle C and De Maria R. Identification and expansion of human colon-cancer-initiating cells. Nature 2006.
37. Goodell MA, Rosenzweig M, Kim H, Marks DF, DeMaria M, Paradis G, Grupp SA, Sieff CA, Mulligan RC and Johnson RP. Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nature Medicine 1997; 3: 1337-1345.
38. Zhou S, Schuetz JD, Bunting KD, Colapietro AM, Sampath J, Morris JJ, Lagutina I, Grosveld GC, Osawa M, Nakauchi H and Sorrentino BP. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nature Medicine 2001; 7: 1028-1034.
39. Scharenberg CW, Harkey MA and Torok-Storb B. The ABCG2 transporter is an efficient Hoechst 33342 efflux pump and is preferentially expressed by immature human hematopoietic progenitors. Blood 2002; 99: 507-512.
40. Bunting KD. ABC transporters as phenotypic markers and functional regulators of stem cells. Stem Cells 2002; 20: 11-20.
41. Doyle LA and Ross DD. Multidrug resistance mediated by the breast cancer resistance protein BCRP (ABCG2). Oncogene 2003; 22: 7340-7358.
42. Patrawala L, Calhoun T, Schneider-Broussard R, Zhou J, Claypool K and Tang DG. Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2-cancer cells are similarly tumorigenic. Cancer Research 2005; 65: 6207-6219.
43. Taipale J and Beachy PA. The Hedgehog and Wnt signalling pathways in cancer. Nature 2001; 411: 349-354.
44. Pardal R, Clarke MF and Morrison SJ. Applying the principles of stem-cell biology to cancer. Nature Reviews. Cancer 2003; 3: 895-902.
45. Behbod F and Rosen JM. Will cancer stem cells provide new therapeutic targets? Carcinogenesis 2005; 26: 703-711.
46. Jacobs JJ, Kieboom K, Marino S, DePinho RA and Van Lohuizen M. The oncogene and Polycomb-group gene bmi-1 regulates cell proliferation and senescence through the ink4a locus. Nature 1999; 397: 164-168.
47. Lessard J and Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 2003; 423: 255-260.
48. Glinsky GV, Berezovska O and Glinskii AB. Microarray analysis identifies a death-from-cancer signature predicting therapy failure in patients with multiple types of cancer. The Journal of Clinical Investigation 2005; 115: 1503-1521.
49. Weng AP and Aster JC. Multiple niches for Notch in cancer: Context is everything. Current Opinion in Genetics and Development 2004; 14: 48-54.
50. Hoemann CD, Beaulieu N, Girard L, Rebai N and Jolicoeur P. Two distinct Notch1 mutant alleles are involved in the induction of T-cell leukemia in c-myc transgenic mice. Molecular and Cell Biology 2000; 20(11): P. 3831-42
51. Dievart A, Beaulieu N and Jolicoeur P. Involvement of Notch1 in the development of mouse mammary tumors. Oncogene 1999; 18: 5973-5981.
52. Nicolas M, Wolfer A, Raj K, Kummer JA, Mill P, Van Noort M, Hui CC, Clevers H, Dotto GP and Radtke F. Notch1 functions as a tumor suppressor in mouse skin. Nature Genetics 2003; 33: 416-421.
53. Hanahan D and Weinberg RA. The hallmarks of cancer. Cell 2000; 100: 57-70.
54. Argyle DJ and Nasir L. Telomerase: A potential diagnostic and therapeutic tool in canine oncology. Veterinary Pathology 2003; 40: 1-7.
55. Ju Z and Rudolph KL. Telomeres and telomerase in cancer stem cells. European Journal of Cancer 2006; 42: 1197-1203.
56. Lendahl U, Zimmerman LB and McKay RD. CNS stem cells express a new class of intermediate filament protein. Cell 1990; 60: 585-595.
57. Polyak K and Hahn WC. Roots and stems: Stem cells in cancer. Nature Medicine 2006; 12: 296-300.
58. Reya T and Clevers H. Wnt signalling in stem cells and cancer. Nature 2005; 434: 843-850.
59. Cozzio A, Passegue E, Ayton PM, Karsunky H, Cleary ML and Weissman IL. Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes and Development 2003; 17: 3029-3035.
60. Jamieson CH, Aillies LE, Dylla SJ, Muijtjens M, Jones C, Zehnder JL, Gotlib J, Li K, Manz MG, Keating A, Sawyers CL and Weissman IL. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. New England Journal of Medicine 2004; 351: 657-667.
61. Kai T and Spradling A. Differentiating germ cells can revert into functional stem cells in Drosophila melanogaster ovaries. Nature 2004; 428: 564-569.
62. Passegue E, Jamieson CH, Ailles LE and Weissman IL. Normal and leukemic hematopoiesis: Are leukemias a stem cell disorder or a reacquisition of stem cell characteristics? Proceedings of the National Academy of Sciences of the United States of America 2003; 100(Suppl. 1): 11842-11849.
63. Gunsilius E, Duba HC, Petzer AL, Kahnler CM, Grunewald K, Stockhammer G, Gabl C, Dirnhofer S, Clausen J and Gastl G. Evidence from a leukaemia model for maintenance of vascular endothelium by bone-marrow-derived endothelial cells. Lancet 2000; 355: 1688-1691.
64. Mueller MM and Fusenig NE. Friends or foes -bipolar effects of the tumour stroma in cancer. Nature Reviews. Cancer 2004; 4: 839-849.
65. Bjerkvig R, Tysnes BB, Aboody KS, Najbauer J and Terzis AJ. Opinion: The origin of the cancer stem cell: Current controversies and new insights. Nature Reviews. Cancer 2005; 5: 899-904.
66. Lapidot T, Dar A and Kollet O. How do stem cells find their way home? Blood 2005; 106: 1901-1910.
67. Terskikh AV, Easterday MC, Li L, Hood L, Kornblum HI, Geschwind DH and Weissman IL. From hematopoiesis to neuropoiesis: Evidence of overlapping genetic programs. Proceedings of the National Academy of Sciences of the United States of America 2001; 98: 7934-7939.
68. Kucia MM, Reca R, Miekus K, Wanzeck J, Wojakowski W, Janowska-Wieczorek A, Ratajczak J and Ratajczak MZ. Trafficking of normal stem cells and metastasis of cancer stem cells involve similar mechanisms: Pivotal role of the SDF-1-CXCR4 axis. Stem Cells 2005; 23: 879-894.
69. Macpherson H, Keir P, Webb S, Samuel K, Boyle S, Bickmore W, Forrester L and Dorin J. Bone marrow-derived SP cells can contribute to the respiratory tract of mice in vivo. Journal of Cell Science 2005; 118(Pt 11): 2441-2450.
70. Brabletz T, Jung A, Spaderna S, Hlubek F and Kirchner T. Opinion: migrating cancer stem cells - an integrated concept of malignant tumour progression. Nature Reviews. Cancer 2005; 5: 744-749.
71. Sell S. Stem cell origin of cancer and differentiation therapy. Critical Reviews in Oncology/Hematology 2004; 51: 1-28.
72. Guzman ML, Swiderski CF, Howard DS, Grimls BA, Rossi RM, Szilvassy SJ and Jordan CT. Preferential induction of apoptosis for primary human leukemic stem cells. Proceedings of the National Academy of Sciences of the United States of America 2002; 99: 16220-16225.
73. Jain M, Arvanitis C, Chu K, Dewey W, Leonhardt E, Trinh M, Sundberg CD, Bishop JM and Felsher DW. Sustained loss of a neoplastic phenotype by brief inactivation of MYC. Science 2002; 297: 102-104.
74. Jones RJ, Matsui WH and Smith BD. Cancer stem cells - are we missing the target? Journal of the National Cancer Institute, 2004; 96: 583-585.
75. Bhatia R, Holtz M, Niu N, Gray R, Snyder DS, Sawyers CL, Arber DA, Slovak ML and Forman SJ. Persistence of malignant hematopoietic progenitors in chronic myelogenous leukemia patients in complete cytogenetic remission following imatinib mesylate treatment. Blood 2003; 101: 4701-4707.
76. Gorlick R, Anderson P, Andrulis I, Arndt C, Beardsley GP, Bernstein M, Bridge J, Cheung NK, Dome JS, Ebb D, Gardner T, Gebhardt M, Grier H, Hansen M, Healey J, Helman L, Hock J, Houghton J, Houghton P, Huvos A, Khanna C, Kieran M, Kleinerman E, Ladanyi M, Lau C, Malkin D, Marina N, Meltzer P, Meyers P, Schofield D, Schwartz C, Smith MA, Toretsky J, Tsokos M, Wexler L, Wigginton J, Withrow S, Schoenfeldt M and Anderson B. Biology of childhood osteogenic sarcoma and potential targets for therapeutic development: Meeting summary. Clinical Cancer Research 2003; 9: 5442-5453.
77. Khanna C, Lindblad-Toh K, Vail D, London C, Bergman P, Barber L, Breen M, Kitchell B, McNeil E, Modiano JF, Niemi S, Comstock KE, Ostrander E, Westmoreland S and Withrow S. The dog as a cancer model. Nature Biotechnology 2006; 24: 1065-1066.