Acute myeloid leukemia originates from a hierarchy of leukemic stem cell classes that differ in self-renewal capacity

Nature Immunology

Volumn 5, Issue 7, 2004, Pages 738-743

  Hope, Kristin J ^a   Jin, Liqing ^a   Dick, John E ^a  

^a UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL COMPARTMENTALIZATION; CELL DIVISION; CELL FATE; CELL HETEROGENEITY; CELL RENEWAL; CONTROLLED STUDY; DIABETES MELLITUS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; HYPOTHESIS; IMMUNE DEFICIENCY; LEUKEMIA CELL; LEUKEMOGENESIS; MOUSE; MOUSE MUTANT; NONHUMAN; PRIORITY JOURNAL; RECIPIENT; STEM CELL; STEM CELL TRANSPLANTATION; ANIMAL; CANCER STEM CELL; CANCER TRANSPLANTATION; CELL CLONE; CELL CULTURE; CELL LINEAGE; CLASSIFICATION; FLOW CYTOMETRY; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; KINETICS; LENTIVIRINAE; NONOBESE DIABETIC MOUSE; PATHOLOGY; TRANSPLANTATION;

ANIMALS; CELL DIVISION; CELL LINEAGE; CLONE CELLS; FLOW CYTOMETRY; GENETIC VECTORS; HUMANS; KINETICS; LENTIVIRUS; LEUKEMIA, MYELOCYTIC, ACUTE; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASM TRANSPLANTATION; TRANSDUCTION, GENETIC; TUMOR CELLS, CULTURED; TUMOR STEM CELLS;

EID: 3242754448     PISSN: 15292908     EISSN: None     Source Type: Journal    
DOI: 10.1038/ni1080     Document Type: Article

References (39)

1. Dick, J.E. Breast cancer stem cells revealed. Proc. Natl. Acad. Sci. USA 100, 3547-3549 (2003).
2. McCulloch, E. Stem cells in normal and leukemic hemopoiesis (Henry Stratton Lecture). Blood 62, 1-13 (1983).
3. Griffin, J. & Löwenberg, B. Clonogenic cells in acute myeloblastic leukemia. Blood 68, 1185-1195 (1986).
4. Larochelle, A. et al. Identification of primitive human hematopoietic cells capable of repopulating NOD/SCID mouse bone marrow: implications for gene therapy. Nat. Med. 2, 1329-1337 (1996).
5. Kamel-Reid, S. & Dick, J.E. Engraftment of immune-deficient mice with human hematopoietic stem cells. Science 242, 1706-1709 (1988).
6. Kamel-Reid, S. et al. A model of human acute lymphoblastic leukemia in immune-deficient SCID mice. Science 246, 1597-1600 (1989).
7. Lapidot, T. et al. Cytokine stimulation of multilineage hematopoiesis from immature human cells engrafted in scid mice. Science 255, 1137-1141 (1992).
8. Lapidot, T. et al. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367, 645-648 (1994).
9. Ailles, L.E., Gerhard, B., Kawagoe, H. & Hogge, D.E. Growth characteristics of acute myelogenous leukemia progenitors that initiate malignant hematopoiesis in nonobese diabetic/severe combined immunodeficient mice. Blood 94, 1761-1772 (1999).
10. Rombouts, W.J., Martens, A.C. & Ploemacher, R.E. Identification of variables determining the engraftment potential of human acute myeloid leukemia in the immunodeficient NOD/SCID human chimera model. Leukemia 14, 889-897 (2000).
11. Bhatia, M., Wang, J.C.Y., Kapp, U., Bonnet, D. & Dick, J.E. Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Proc. Natl. Acad. Sci. USA 94, 5320-5325 (1997).
12. Conneally, E., Cashman, J., Petzer, A. & Eaves, C. Expansion in vitro of transplantable human cord blood stem cells demonstrated using a quantitative assay of their lympho-myeloid repopulating activity in nonobese diabetic-scid/scid mice. Proc. Natl. Acad. Sci. USA 94, 9836-9841 (1997).
13. Bonnet, D. & Dick, J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 3, 730-737 (1997).
14. Blair, A., Hogge, D.E., Allies, 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 89, 3104-3112 (1997).
15. Jordan, C.T. et al. The interleukin-3 receptor α chain is a unique marker for human acute myelogenous leukemia stem cells. Leukemia 14, 1777-1784 (2000).
16. -/HLA-DR. Blood 92, 4325-4335 (1998).
17. Brendel, C. et al. Detection of cytogenetic aberrations both in CD90 (Thy-1)-positive and (Thy-1)-negative stem cell (CD34) subtractions of patients with acute and chronic myeloid leukemias. Leukemia 13, 1770-1775 (1999).
18. Dick, J.E. Stem cells: Self-renewal writ in blood. Nature 423, 231-233 (2003).
19. Guenechea, G., Gan, O.I., Dorrell, C. & Dick, J.E. Distinct classes of human stem cells that differ in proliferative and self-renewal potential. Nat. Immunol. 2, 75-82 (2001).
20. Ailles, L.E., Humphries, R.K., Thomas, T.E. & Hogge, D.E. Retroviral marking of acute myelogenous leukemia progenitors that initiate long-term culture and growth in immunodeficient mice. Exp. Hematol. 27, 1609-1620 (1999).
21. Guzman, M.L. et al. Nuclear factor-κB is constitutively activated in primitive human acute myelogenous leukemia cells. Blood 98, 2301-2307 (2001).
22. Terpstra, W. et al. Fluorouracil selectively spares acute myeloid leukemia cells with long-term growth abilities in immunodeficient mice and in culture. Blood 88, 1944-1950 (1996).
23. Mazurier, F., Gan, O., McKenzie, J., Doedens, M. & Dick, J. Lentivector-mediated clonal tracking reveals intrinsic heterogeneity in the human hematopoietic stem cell compartment and culture-induced stem cell impairment. Blood 103, 545-552 (2004).
24. + cells that mediate long-term engraftment of NOD/SCID mice by HIV vectors. Science 283, 682-686 (1999).
25. - bone marrow and cord blood-derived SCID-repopulating cells with third-generation lentiviral vectors. Mol. Ther. 1, 566-573 (2000).
26. Terpstra, W. et al. Conditions for engraftment of human acute myeloid leukemia (AML) in SCID mice. Leukemia 9, 1573-1577 (1995).
27. Guan, Y., Gerhard, B. & Hogge, D.E. Detection, isolation, and stimulation of quiescent primitive leukemic progenitor cells from patients with acute myeloid leukemia (AML). Blood 101, 3142-3149 (2003).
28. Till, J.E. & McCulloch, E.A. Hemopoietic stem cell differentiation. Biochim. Biophys. Acta 605, 431-459 (1980).
29. Lessard, J. & Sauvageau, G. Bmi-1 determines the proliferative capacity of normal and leukemic stem cells. Nature 423, 455-460 (2003).
30. Greaves, M. Differentiation-linked leukemogenesis in lymphocytes. Science 234, 697-704 (1986).
31. Kamel-Reid, S. et al. Bone marrow from children in relapse with pre-B acute lymphoblastic leukemia proliferates and disseminates rapidly in scid mice. Blood 78, 2973-2981 (1991).
32. Guzman, M.L. et al. Preferential induction of apoptosis for primary human leukemic stem cells. Proc. Natl. Acad. Sci. USA 99, 16220-16225 (2002).
33. Al-Hajj, M., Wicha, M., Morrison, S.J. & Clarke, M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. USA 100, 3983-3988 (2003).
34. Reya, T., Morrison, S.J., Clarke, M.F. & Weissman, I.L. Stem cells, cancer, and cancer stem cells. Nature 414, 105-111 (2001).
35. Singh, S. et al. Identification of a cancer stem cell in human brain tumours. Cancer Res. 63, 5281-5288 (2003).
36. Marx, J. Cancer research. Mutant stem cells may seed cancer. Science 301, 1308-1310 (2003).
37. Bernards, R. & Weinberg, R.A. A progression puzzle. Nature 418, 823 (2002).
38. Follenzi, A., Ailles, L.E., Bakovic, S., Geuna, M. & Naldini, L. Gene transfer by lentiviral vectors is limited by nuclear translocation and rescued by HIV-1 pol sequences. Nat. Genet. 25, 217-222 (2000).
39. + cord blood cells. Blood 93, 1097-1105 (1999).