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Original

First among equals: The cancer cell hierarchy

&
Pages 2017-2027 | Received 27 Jan 2006, Accepted 30 Mar 2006, Published online: 01 Jul 2009

References

  • Hope K J, Jin L, Dick J E. Acute myeloid leukemia originates from a hierarchy of leukemic stem cell classes that differ in self-renewal capacity. Nat Immunol 2004; 5: 738–743
  • 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) 2003; 100: 3983–3988
  • Singh S K, Clarke I D, Terasaki M, Bonn V E, Hawkins C, Squire J, Dirks P B. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63: 5821–5828
  • Bonnet D, Dick J E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997; 3: 730–737
  • Collins A T, Berry P A, Hyde C, Stower M J, Maitland N J. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 2005; 65: 10946–10951
  • Mendelsohn M L. The growth fraction: a new concept applied to tumors. Science 1960; 132: 1496
  • Mendelsohn M L. Chronic infusion of iritiated ihymidine into mice with tumors. Science 1962; 135: 213
  • Mendelsohn M L. Autoradiographic analysis of cell proliferation in spontaneous breast cancer of C3H mouse. III. The growth fraction. J Natl Cancer Inst 1962; 28: 1015
  • Wylie C V, Nakane P K, Pierce G B. Degree of differentiation in nonproliferating cells of mammary carcinoma. Differentiation 1973; 1: 11–20
  • Steel G G, Lamerton L F. The growth rate of human tumors. Br J Cancer 1966; 20: 74–86
  • Steel G G. Cell loss as a factor in the growth rate of human tumors. Eur J Cancer 1967; 3: 381–387
  • Clarkson B. Consideration of the cell cycle in chemotherapy of acute leukemia. Current concepts in the management of lymphoma and leukemia, J E Ultmann, M L Griem, W H Kirsten, R W Wissler. Springer-Verlag, Berlin 1970; 88–118
  • Clarkson B D. Review of recent studies of cellular proliferation in acute leukemia. Natl Cancer Inst Monogr 1969; 30: 81–120
  • Frei E, Freireich E J. Progress and perspectives in the chemotherapy of acute leukemia. Advances in chemotherapy, F H Goldlin, R J Schnitzer. Academic Press, New York 1965; 269
  • Clarkson B, Fried J, Strife A, Sakai Y, Ota K, Okita T. Studies of cellular proliferation in human leukemia. 3. Behavior of leukemic cells in three adults with acute leukemia given continuous infusions of 3H-thymidine for 8 or 10 days. Cancer 1970; 25: 1237–1260
  • Burchenal J H. Long-term survivors in acute leukemia and Burkitt's tumor. Cancer 1968; 21: 595–599
  • Bush R S, Hill R P. Biologic discussions augmenting radiation effects and model systems. Laryngoscope 1975; 85: 1119–1133
  • Moore J V, Hendry J H, Hunter R D. Dose-incidence curves for tumour control and normal tissue injury, in relation to the response of clonogenic cells. Radiother Oncol 1983; 1: 143–157
  • Salmon S E, Hamburger A W, Soehnlen B, Durie B G, Alberts D S, Moon T E. Quantitation of differential sensitivity of human-tumor stem cells to anticancer drugs. N Engl J Med 1978; 298: 1321–1327
  • Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994; 367: 645–648
  • Singh S K, Hawkins C, Clarke I D, Squire J A, Bayani J, Hide T, et al. Identification of human brain tumour initiating cells. Nature 2004; 432: 396–401
  • Southam C M, Brunschwig A, Dizon Q. Autologous and homologous transplantation of human cancer. Biological interactions in normal and neoplastic growth, M J Brennan, W L Simpson. Little, Brown and Company, Boston, MA 1962; 723–738
  • Southam C M, Brunschwig A. Quantitative studies of autotransplantation of human cancer—preliminary report. Cancer 1961; 14: 971
  • Bennett J M, Catovsky D, Daniel M T, Flandrin G, Galton D A, Gralnick H R, Sultan C. Proposals for the classification of the acute leukaemias. French-American-British (FAB) co-operative group. Br J Haematol 1976; 33: 451–458
  • Bennett J M, Catovsky D, Daniel M T, Flandrin G, Galton D A, Gralnick H R, Sultan C. Proposed revised criteria for the classification of acute myeloid leukemia. A report of the French-American-British Cooperative Group. Ann Intern Med 1985; 103: 620–625
  • Freeman J A. The ultrastructure and genesis of Auer bodies. Blood 1960; 15: 449–465
  • Stass S A, Lanham G R, Butler D, Williams D L, Peiper S C, Kalwinsky D K, Dahl G V. Auer rods in mature granulocytes: a unique morphologic feature of acute myelogenous leukemia with maturation. Am J Clin Pathol 1984; 81: 662–665
  • Davies A R. Auer bodies in mature neutrophils. Jama 1968; 203: 895
  • Bainton D F, Friedlander L M, Shohet S B. Abnormalities in granule formation in acute myelogenous leukemia. Blood 1977; 49: 693–704
  • Fialkow P J, Singer J W, Adamson J W, Vaidya K, Dow L W, Ochs J, Moohr J W. Acute nonlymphocytic leukemia: heterogeneity of stem cell origin. Blood 1981; 57: 1068–1073
  • Fearon E R, Burke P J, Schiffer C A, Zehnbauer B A, Vogelstein B. Differentiation of leukemia cells to polymorphonuclear leukocytes in patients with acute nonlymphocytic leukemia. N Engl J Med 1986; 315: 15–24
  • Jacobson R J, Temple M J, Singer J W, Raskind W, Powell J, Fialkow P J. A clonal complete remission in a patient with acute nonlymphocytic leukemia originating in a multipotent stem cell. N Engl J Med 1984; 310: 1513–1517
  • Fialkow P J, Singer J W, Raskind W H, Adamson J W, Jacobson R J, Bernstein I D, et al. Clonal development, stem-cell differentiation, and clinical remissions in acute nonlymphocytic leukemia. N Engl J Med 1987; 317: 468–473
  • Lajtha L G. Which are the leukaemic cells. Blood Cells 1981; 7: 45–62
  • Foulds L. The experimental study of tumor progression: a review. Cancer Res 1954; 14: 327–339
  • van Duuren B L, Sivak A, Katz C, Seidman I, Melchionne S. The effect of aging and interval between primary and secondary treatment in two-stage carcinogenesis on mouse skin. Cancer Res 1975; 35: 502–505
  • Horton S J, Grier D G, McGonigle G J, Thompson A, Morrow M, de Silva I, et al. Continuous MLL-ENL expression is necessary to establish a ‘Hox Code’ and maintain immortalization of hematopoietic progenitor cells. Cancer Res 2005; 65: 9245–9252
  • Cozzio A, Passegue E, Ayton P M, Karsunky H, Cleary M L, Weissman I L. Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev 2003; 17: 3029–3035
  • Huntly B J, Shigematsu H, Deguchi K, Lee B H, Mizuno S, Duclos N, et al. MOZ-TIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell 2004; 6: 587–596
  • Jamieson C H, Ailles L E, Dylla S J, Muijtjens M, Jones C, Zehnder J L, et al. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med 2004; 351: 657–667
  • Miyamoto T, Nagafuji K, Akashi K, Harada M, Kyo T, Akashi T, et al. Persistence of multipotent progenitors expressing AML1/ETO transcripts in long-term remission patients with t(8;21) acute myelogenous leukemia. Blood 1996; 87: 4789–4796
  • Biernaux C, Loos M, Sels A, Huez G, Stryckmans P. Detection of major bcr-abl gene expression at a very low level in blood cells of some healthy individuals. Blood 1995; 86: 3118–3122
  • Bose S, Deininger M, Gora-Tybor J, Goldman J M, Melo J V. The presence of typical and atypical BCR-ABL fusion genes in leukocytes of normal individuals: biologic significance and implications for the assessment of minimal residual disease. Blood 1998; 92: 3362–3367
  • Limpens J, de Jong D, van Krieken J H, Price C G, Young B D, van Ommen G J, Kluin P M. Bcl-2/JH rearrangements in benign lymphoid tissues with follicular hyperplasia. Oncogene 1991; 6: 2271–2276
  • Trumper L, Pfreundschuh M, Bonin F V, Daus H. Detection of the t(2;5)-associated NPM/ALK fusion cDNA in peripheral blood cells of healthy individuals. Br J Haematol 1998; 103: 1138–1144
  • Maes B, Vanhentenrijk V, Wlodarska I, Cools J, Peeters B, Marynen P, de Wolf-Peeters C. The NPM-ALK and the ATIC-ALK fusion genes can be detected in non-neoplastic cells. Am J Pathol 2001; 158: 2185–2193
  • Marcucci G, Strout M P, Bloomfield C D, Caligiuri M A. Detection of unique ALL1 (MLL) fusion transcripts in normal human bone marrow and blood: distinct origin of normal versus leukemic ALL1 fusion transcripts. Cancer Res 1998; 58: 790–793
  • Disperati P, Ichim C V, Tkachuk D, Chun K, Schuh A C, Wells R A. Progression of myelodysplasia to acute lymphoblastic leukaemia: Implications for disease biology. Leuk Res 2006; 30: 233–239
  • Blackstock A M, Garson O M. Direct evidence for involvement of erythroid cells in acute myeloblastic leukaemia. Lancet 1974; 2: 1178–1179
  • Ferraris A M, Raskind W H, Bjornson B H, Jacobson R J, Singer J W, Fialkow P J. Heterogeneity of B cell involvement in acute nonlymphocytic leukemia. Blood 1985; 66: 342–344
  • Jensen M K, Killmann S A. Additional evidence for chromosome abnormalities in the erythroid precursors in acute leukaemia. Acta Med Scand 1971; 189: 97–100
  • Keinanen M, Griffin J D, Bloomfield C D, Machnicki J, de la Chapelle A. Clonal chromosomal abnormalities showing multiple-cell-lineage involvement in acute myeloid leukemia. N Engl J Med 1988; 318: 1153–1158
  • Suciu S, Zeller W, Weh H J, Hossfeld D K. Immunophenotype of mitotic cells with clonal chromosome abnormalities demonstrating multilineage involvement in acute myeloid leukemia. Cancer Genet Cytogenet 1993; 70: 1–5
  • Blair A, Hogge D E, Sutherland H J. Most acute myeloid leukemia progenitor cells with long-term proliferative ability in vitro and in vivo have the phenotype CD34(+)/CD71(−)/HLA-DR. Blood 1998; 92: 4325–4335
  • Curtis J E, Messner H A, Hasselback R, Elhakim T M, McCulloch E A. Contributions of host- and disease-related attributes to the outcome of patients with acute myelogenous leukemia. J Clin Oncol 1984; 2: 253–259
  • Sutherland H, Blair A, Vercauteren S, Zapf R. Detection and clinical significance of human acute myeloid leukaemia progenitors capable of long-term proliferation in vitro. Br J Haematol 2001; 114: 296–306
  • Hill R P, Milas L. The proportion of stem cells in murine tumors. Int J Radiat Oncol Biol Phys 1989; 16: 513–518
  • Sawyers C L, Hochhaus A, Feldman E, Goldman J M, Miller C B, Ottmann O G, et al. Imatinib induces hematologic and cytogenetic responses in patients with chronic myelogenous leukemia in myeloid blast crisis: results of a phase II study. Blood 2002; 99: 3530–3539
  • Talpaz M, Silver R T, Druker B J, Goldman J M, Gambacorti-Passerini C, Guilhot F, et al. Imatinib induces durable hematologic and cytogenetic responses in patients with accelerated phase chronic myeloid leukemia: results of a phase 2 study. Blood 2002; 99: 1928–1937
  • Bhatia R, Holtz M, Niu N, Gray R, Snyder D S, Sawyers C L, et al. Persistence of malignant hematopoietic progenitors in chronic myelogenous leukemia patients in complete cytogenetic remission following imatinib mesylate treatment. Blood 2003; 101: 4701–4707
  • Chu S, Xu H, Shah N P, Snyder D S, Forman S J, Sawyers C L, Bhatia R. Detection of BCR-ABL kinase mutations in CD34+ cells from chronic myelogenous leukemia patients in complete cytogenetic remission on imatinib mesylate treatment. Blood 2005; 105: 2093–2098
  • Michor F, Hughes T P, Iwasa Y, Branford S, Shah N P, Sawyers C L, Nowak M A. Dynamics of chronic myeloid leukaemia. Nature 2005; 435: 1267–1270
  • Friend C, Scher W, Holland J G, Sato T. Hemoglobin synthesis in murine virus-induced leukemic cells in vitro: stimulation of erythroid differentiation by dimethyl sulfoxide. Proc Natl Acad Sci (USA) 1971; 68: 378–382
  • Andreeff M, Stone R, Michaeli J, Young C W, Tong W P, Sogoloff H, et al. Hexamethylene bisacetamide in myelodysplastic syndrome and acute myelogenous leukemia: a phase II clinical trial with a differentiation-inducing agent. Blood 1992; 80: 2604–2609
  • Lichtman M A. Differentiation versus maturation of neoplastic hematopoietic cells: an important distinction. Blood Cells Mol Dis 2001; 27: 649–652
  • Siminovitch L, McCulloch E A, Till J E. The distribution of colony-forming cells among spleen colonies. J Cell Comp Physiol 1963; 62: 327–336
  • Till J E, McCulloch E A, Siminovitch L. A stochastic model of stem cell proliferation based on the growth of spleen colony-forming cells. Proc Natl Acad Sci (USA) 1964; 51: 29–36
  • Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 1978; 4: 7–25
  • Lord B I. The architecture of bone marrow cell populations. Int J Cell Cloning 1990; 8: 317–331
  • Calvi L M, Adams G B, Weibrecht K W, Weber J M, Olson D P, Knight M C, et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003; 425: 841–846
  • Lord B I, Hendry J H. The distribution of haemopoietic colony-forming units in the mouse femur, and its modification by x rays. Br J Radiol 1972; 45: 110–115
  • Lord B I, Testa N G, Hendry J H. The relative spatial distributions of CFUs and CFUc in the normal mouse femur. Blood 1975; 46: 65–72
  • Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, Takubo K, et al. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 2004; 118: 149–161
  • Zhang J, Niu C, Ye L, Huang H, He X, Tong W G, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003; 425: 836–841
  • Reya T, Duncan A W, Ailles L, Domen J, Scherer D C, Willert K, et al. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 2003; 423: 409–414
  • Jian H, Shen X, Liu I, Semenov M, He X, Wang X F. Smad3-dependent nuclear translocation of beta-catenin is required for TGF-beta1-induced proliferation of bone marrow-derived adult human mesenchymal stem cells. Genes Dev 2006; 20: 666–674
  • Alexson T O, Hitoshi S, Coles B L, Bernstein A, van der Kooy D. Notch signaling is required to maintain all neural stem cell populations – irrespective of spatial or temporal niche. Dev Neurosci 2006; 28: 34–48
  • Duncan A W, Rattis F M, DiMascio L N, Congdon K L, Pazianos G, Zhao C, et al. Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat Immunol 2005; 6: 314–322
  • Lessard J, Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 2003; 423: 255–260
  • Nakauchi H, Oguro H, Negishi M, Iwama A. Polycomb gene product Bmi-1 regulates stem cell self-renewal. Ernst Schering Res Found Workshop 2005; 85–100
  • Iwama A, Oguro H, Negishi M, Kato Y, Morita Y, Tsukui H, et al. Enhanced self-renewal of hematopoietic stem cells mediated by the polycomb gene product Bmi-1. Immunity 2004; 21: 843–851
  • Beslu N, Krosl J, Laurin M, Mayotte N, Humphries K R, Sauvageau G. Molecular interactions involved in HOXB4-induced activation of HSC self-renewal. Blood 2004; 104: 2307–2314
  • Ema H, Sudo K, Seita J, Matsubara A, Morita Y, Osawa M, et al. Quantification of self-renewal capacity in single hematopoietic stem cells from normal and Lnk-deficient mice. Dev Cell 2005; 8: 907–914
  • Zeng H, Yucel R, Kosan C, Klein-Hitpass L, Moroy T. Transcription factor Gfi1 regulates self-renewal and engraftment of hematopoietic stem cells. Embo J 2004; 3: 4116–4125
  • Hock H, Hamblen M J, Rooke H M, Schindler J W, Saleque S, Fujiwara Y, Orkin S H. Gfi-1 restricts proliferation and preserves functional integrity of haematopoietic stem cells. Nature 2004; 431: 1002–1007
  • Kato Y, Iwama A, Tadokoro Y, Shimoda K, Minoguchi M, Akira S, et al. Selective activation of STAT5 unveils its role in stem cell self-renewal in normal and leukemic hematopoiesis. J Exp Med 2005; 202: 169–179
  • Burns C E, Traver D, Mayhall E, Shepard J L, Zon L I. Hematopoietic stem cell fate is established by the Notch-Runx pathway. Genes Dev 2005; 19: 2331–2342
  • Zhu J, Zhang Y, Joe G J, Pompetti R, Emerson S G. NF-Ya activates multiple hematopoietic stem cell (HSC) regulatory genes and promotes HSC self-renewal. Proc Natl Acad Sci (USA) 2005; 102: 11728–11733
  • Iwasaki H, Somoza C, Shigematsu H, Duprez E A, Iwasaki-Arai J, Mizuno S, et al. Distinctive and indispensable roles of PU.1 in maintenance of hematopoietic stem cells and their differentiation. Blood 2005; 106: 1590–1600
  • Blair A, Sutherland H J. Primitive acute myeloid leukemia cells with long-term proliferative ability in vitro and in vivo lack surface expression of c-kit (CD117). Exp Hematol 2000; 28: 660–671
  • Blair A, Hogge D E, Ailles L E, Lansdorp P M, Sutherland H J. Lack of expression of Thy-1 (CD90) on acute myeloid leukemia cells with long-term proliferative ability in vitro and in vivo. Blood 1997; 89: 3104–3112
  • Jordan C T, Upchurch D, Szilvassy S J, Guzman M L, Howard D S, Pettigrew A L, et al. The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells. Leukemia 2000; 14: 1777–1784

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