Normal and leukaemic stem cells

British Journal of Haematology

Volumn 130, Issue 4, 2005, Pages 469-479

  Bonnet, Dominique ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Haematopoietic stem cell; Leukaemic stem cell; Non obese diabetic severe combined immunodeficient; Self renewal; Transcription factors; Xenotransplantation model

Indexed keywords

HOMEODOMAIN PROTEIN; TRANSCRIPTION FACTOR;

CELL CYCLE REGULATION; CELL FATE; CELL ISOLATION; CELL MATURATION; CELL PROLIFERATION; CELL TRANSFORMATION; HEMATOPOIETIC STEM CELL; HUMAN; LEUKEMIA CELL; MESODERM; NONHUMAN; PRIORITY JOURNAL; REVIEW; ACUTE DISEASE; CANCER STEM CELL; CELL CYCLE; CELL LINEAGE; CHRONIC MYELOID LEUKEMIA; GENE EXPRESSION REGULATION; GENETICS; HOMEOBOX; MUTATION; MYELOID LEUKEMIA; PATHOLOGY;

ACUTE DISEASE; CELL CYCLE; CELL LINEAGE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, HOMEOBOX; HEMATOPOIETIC STEM CELLS; HUMANS; LEUKEMIA, MYELOID; LEUKEMIA, MYELOID, CHRONIC; MUTATION; TUMOR STEM CELLS;

EID: 24944508703     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2005.05596.x     Document Type: Review

References (116)

1. Al-Hajj M. Wicha M.S. Benito-Hernandez A. Morrison S.J. Clarke M.F. ( 2003) Prospective identification of tumorigenic breast cancer cells. Proceedings of the National Academy of Sciences of the United States of America, 100, 3983 3988.
2. Amsellem S. Pflumio F. Bardinet D. Izac B. Charneau P. Romeo P.H. Dubart-Kupperschmitt A. Fichelson S. ( 2003) Ex vivo expansion of human hematopoietic stem cells by direct delivery of the HOXB4 homeoprotein. Nature Medicine, 9, 1423 1427.
3. Arai F. Hirao A. Ohmura M. Sato H. Matsuoka S. Takubo K. Ito K. Koh G.Y. Suda T. ( 2004) Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell, 118, 149 161.
4. Artavanis-Tsakonas S. Matsuno K. Fortini M. ( 1995) Notch signalling. Science, 268, 225 232.
5. Baum C.M. Weissman I.L. Tsukamoto A.S. Buckle A.M. Peault B. ( 1992) Isolation of a candidate human hematopoietic stem cell population. Proceedings of the National Academy of Sciences of the United States of America, 89, 2804 2810.
6. Bhardwaj G. Murdoch B. Wu D. Baker D.P. Williams K.P. Chadwick K. Ling L.E. Karanu F.N. Bhatia M. ( 2001) Sonic hedgehog induces the proliferation of primitive human hematopoietic cells via BMP regulation. Nature Immunology, 2, 172 180.
7. Bhatia M. ( 2001) AC133 expression in human stem cells. Leukemia, 15, 1685 1688.
8. Bhatia M. Wang J.C.Y. Kapp U. Bonnet D. Dick J.E. ( 1997) Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Proceedings of the National Academy of Sciences of the United States of America, 94, 5320 5325.
9. Bhatia M. Bonnet D. Wu D. Murdoch B. Wrana J. Gallacher L. Dick J.E. ( 1999) Bone morphogenetic proteins regulate the developmental program of human hematopoietic stem cells. Journal of Experimental Medicine, 189, 1139 1147.
10. Blair A. Sutherland H.J. ( 2000) Primitive acute myeloid leukemia cells with long-term proliferative ability in vitro and in vivo lack surface expression of c-kit (CD117). Experimental Haematology, 28, 660 671.
11. Blair A. Hogge D.E. Ailles L.E. Lansdorp P.M. Sutherland H.J. ( 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 3112.
12. Blair A. Hogge D.E. Sutherland H.J. ( 1998) Most acute myeloid leukemia progenitor cells with long-term proliferative ability in vitro and in vivo have the phenotype CD34(+)/CD71(-)/HLA-DR-. Blood, 92, 4325 4335.
13. Bonnet D. Dick J.E. ( 1997) Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nature Medicine, 3, 730 737.
14. Bradford G.B. Williams B. Rossi R. Bertoncello I. ( 1997) Quiescence, cycling and turnover in the primitive hematopoietic stem cell compartment. Experimental Hematology, 25, 445 453.
15. Breems D.A. Blokland E.A.W. Neben S. Ploemacher R.E. ( 1994) Frequency analysis of human primitive haematopoietic stem cell subsets using a cobblestone area forming cell assay. Leukemia, 8, 1095 1102.
16. Brown D. Kogan S. Lagasse E. Weissman I. Alcalay M. Pelicci P.G. Atwater S. Bishop J.M. ( 1997) A PML/RAR alpha transgene initiates murine acute promyelocytic leukemia. Proceedings of the National Academy of Sciences of the United States of America, 94, 2551 2556.
17. Bullinger L. Dohner K. Bair E. Frohling S. Schlenk R.F. Tibshirani R. Dohner H. Pollack J.R. ( 2004) Use of gene-expression profiling to identify prognostic subclasses in adult acute myeloid leukemia. New England Journal of Medicine, 350, 1605 1616.
18. Calvi L.M. Adams G.B. Weibrecht K.W. Weber J.M. Olson D.P. Knight M.C. Martin R.P. Schipani E. Divieti P. Bringhurst F.R. Milner L.A. Kronenberg H.M. Scadden D.T. ( 2003) Osteoblastic cells regulate the haematopoietic stem cell niche. Nature, 425, 841 846.
19. Cantor A.B. Orkin S.H. ( 2001) Hematopoietic development: a balancing act. Current Opinion in Genetics and Development, 11, 513 519.
20. Cheng T. Rodrigues N. Shen H. Yang Y. Dombkowski D. Sykes M. Scadden D.T. ( 2000a) Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science, 287, 1804 1808.
21. Cheng T. Rodrigues N. Dombkowski D. Stier S. Scadden D.T. ( 2000b) Stem cell repopulation efficiency but not pool size is governed by p27(kip1). Nature Medicine, 6, 1235 1240.
22. Cheng T. Shen H. Rodrigues N. Stier S. Scadden D.T. ( 2001) Transforming growth factor beta 1 mediates cell-cycle arrest of primitive hematopoietic cells independent of p21 (Cip1/Waf1) or p27 (Kip1). Blood, 98, 3643 3649.
23. Cozzio A. Passegue E. Ayton P.M. Karsunky H. Cleary M.L. Weissman I.L. ( 2003) Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes and Development, 24, 3029 3035.
24. Craig W. Kay R. Cutler R.B. Lansdorp P.M. ( 1993) Expression of Thy-1 on human hematopoietic progenitor cells. Journal of Experimental Medicine, 177, 1331 1342.
25. Dick J.E. ( 1996) Normal and leukemic human stem cells assayed in SCID mice. Seminar of Immunology, 8, 197 206.
26. Duncan A.W. Rattis F.M. DiMascio L.N. Congdon K.L. Paazianos G. Zhao C. Yoon K. Cook J.M. Willert K. Gaino N. Reya T. ( 2005) Integration of Notch and Wnt signalling in hematopoietic stem cell maintenance. Nature Immunology, 6, 314 322.
27. Fabbro D. Ruetz S. Buchdunger E. Cowan-Jacob S.W. Fendrich G. Liebetanz J. Mestan J. O'Reilly T. Traxler P. Chaudhuri B. Fretz H. Zimmermann J. Meyer T. Caravatti G. Furet P. Manley P.W. ( 2002) Protein kinases as targets in cancer therapy: successes and failures. Pharmacological Therapy, 93, 79 98.
28. Feuring-Buske M. Frankel A.E. Alexander R.L. Gerhard B. Hogge D.E. ( 2002) A diphtheria toxin-interleukin 3 fusion protein is cytotoxic to primitive acute myeloid leukemia progenitors but spares normal progenitors. Cancer Research, 62, 1730 1736.
29. Foley K.P. McArthur G.A. Queva C. Hurlin P.J. Soriano P. Eisenman R.N. ( 1998) Targeted disruption of Myc antagonist MAD1 inhibits cell cycle exit during granulocyte differentiation. EMBO Journal, 17, 774 785.
30. Frank D.A. ( 2003) Stat signaling in cancer: insights into the pathogenesis and treatment strategies. Cancer Treatment and Research, 115, 267 291.
31. Goodell M.A. Brose K. Paradis G. Connors A.S. Mulligan R.C. ( 1996) Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. Journal of Experimental Medicine, 183, 1797 1806.
32. Goodell M.A. Rosenzweig M. Kim H. Marks D.F. DeMaria M. Paradis G. Grupp S.A. Sieff C.A. Mulligan R.C. Johnson R.P. ( 1997) Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nature Medicine, 3, 1337 1345.
33. Graham S.M. Jorgensen H.G. Allan E. Pearson C. Alcorn M.J. Richmond L. Holyoake T.L. ( 2002) Primitive, quiescent, Philadelphia-positive stem cells from patients with chronic myeloid leukemia are insensitive to STI571 in vitro. Blood, 99, 319 325.
34. Griffin J.D. Linch D. Sabbath K. Larcom P. Schlossman S.F. ( 1984) A monoclonal antibody reactive with normal and leukaemic human myeloid progenitor cells. Leukaemia Research, 8, 521 534.
35. Guenechea G. Gan O.I. Dorrell C. Dick J.E. ( 2001) Distinct classes of human stem cells that differ in proliferative and self-renewal potential. Nature of Immunology, 1, 75 82.
36. Guzman M.L. Jordan C.T. ( 2004) Considerations for targeting malignant stem cells in leukemia. Cancer Control, 11, 97 104.
37. Hao Q.L. Thiemann F.T. Petersen D. Smogorzewska E.M. Crooks G.M. ( 1996) Extended long term culture reveals a highly quiescent and primitive human hematopoietic progenitor population. Blood, 88, 3306 3310.
38. - cells with both lymphoid and myeloid potential. Blood, 91, 4145 4152.
39. Hess D.A. Meyerrose T.E. Wirthlin L. Craft T.P. Herrbrich P.E. Creer M.H. Nolta J.A. ( 2004) Functional characterization of highly purified human hematopoietic repopulating cells isolated based on aldehyde dehydrogenase activity. Blood, 104, 1648 1655.
40. Ho A.D. ( 2005) Kinetics and symmetry divisions of hematopoietic stem cells. Experimental Hematology, 33, 1 8.
41. Hock H. Hamblen M.J. Rooke H.M. Schindler J.W. Saleque S. Fujiwara Y. Orkin S.H. ( 2004) Gli-1 restricts proliferation and preserves functional integrity of hematopoietic stem cells. Nature, 431, 1002 1007.
42. Hope K.J. Jin L. Dick J.E. ( 2004) Acute myeloid leukemia originates from a hierarchy of leukemic stem cell classes that differ in self-renewal capacity. Nature of Immunology, 7, 738 743.
43. Huntly B.J. Shigematsu H. Deguchi K. Lee B.H. Mizuno S. Duclos N. Rowan R. Amaral S. Curley D. Williams I.R. Akashi K. Gilliland D.G. ( 2004) MOZ-TIF2, but not BCR-ABL, confers properties of leukemic stem cells to committed murine hematopoietic progenitors. Cancer Cell, 6, 587 596.
44. Jaiswal S. Traver D. Miyamoto T. Akashi K. Lagasse E. Weissman I.L. ( 2003) Expression of BCR/ABL and BCL-2 in myeloid progenitors leads to myeloid leukemias. Proceedings of the National Academy of Sciences of the United States of America, 100, 10002 10007.
45. Jamieson C.H. Ailles L.E. Dylla S.J. Muijtjens M. Jones C. Zehnder J.L. Gotlib J. Li K. Manz M.G. Keating A. Sawyers C.L. Weissman I.L. ( 2004) Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. New England Journal of Medicine, 351, 657 667.
46. Jones R.J. Barber J.P. Vala M.S. Collector M.I. Kaufmann S.H. Ludeman S.M. Colvin O.M. Hilton J. ( 1995) Assessment of aldehyde dehydrogenase in viable cells. Blood, 85, 2742 2746.
47. Jordan C.T. Yamasaki G. Minamoto D. ( 1996) High resolution cell cycle analysis of defined phenotypic subsets within primitive hematopoietic stem cell populations. Experimental Hematology, 24, 1347 1355.
48. Jordan C.T. Upchurch D. Szilvassy S.J. Guzman M.L. Howard D.S. Pettigrew A.L. Meyerrose T. Rossi R. Grimes B. Rizzieri D.A. Luger S.M. Phillips G.L. ( 2000) The interleukin-3 receptor alpha chain is a unique marker for human acute myelogenous leukemia stem cells. Leukemia, 10, 1777 1784.
49. Karanu F.N. Murdoch B. Gallacher L. Wu D.M. Koremoto M. Sakano S. Bhatia M. ( 2000) The Notch ligand jagged-1 represents a novel growth factor of human hematopoietic stem cells. Journal of Experimental Medicine, 192, 1365 1372.
50. Krause D.S. Fackler M.J. Civin C.I. May W.S. ( 1996) CD34: structure, biology, and clinical utility (see comments). Blood, 87, 1 13.
51. Krosl J. Austin P. Beslu N. Kroon E. Humphries R.K. Sauvageau G. ( 2003) In vitro expansion of hematopoietic stem cells by recombinant TAT-HOXB4 protein. Nature Medicine, 9, 1428 1432.
52. Lapidot T. Sirard C. Vormoor J. Murdoch B. Hoang T. Caceres-Cortes J. Minden M. Paterson B. Caligiuri M.A. Dick J.E. ( 1994) A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature, 367, 645 648.
53. Lawrence H.J. Sauvageau G. Ahmadi N. Lopez A.R. Lebeau M.M. Link M. Humphries K. Largman C. ( 1995) Stage- and lineage-specific expression of the HOXA10 homeobox gene in normal and leukemic hematopoietic cells. Experimental Hematology, 23, 1160 1166.
54. Lemischka I. Raulet D. Mulligan R.C. ( 1986) Developmental potential and dynamic behaviour of hematopoietic stem cells. Cell, 45, 915 927.
55. Lessard J. Sauvageau G. ( 2003) Bim-1 determines the proliferative capacity of normal and leukemic stem cells. Nature, 423, 255 260.
56. Lessard J. Baban S. Sauvageau G. ( 1998) Stage-specific expression of polycomb group genes in human bone marrow cells. Blood, 91, 1216 1224.
57. Look T.A. ( 1996) Oncogenic transcription factors in human acute leukemias. Science, 278, 1059 1064.
58. McArthur G. Foley K.P. Fero M.L. Walkley C.R. Deans A.J. Roberts J.M. Eisenman R.N. ( 2002) MAD1 and p27 cooperate to promote terminal differentiation of granulocytes and inhibit Myc expression and cyclin E-CDK2 activity. Molecular and Cellular Biology, 22, 3014 3023.
59. - progenitors give rise to NK cells, B-lineage cells, dendritic cells and myeloid cells. Blood, 93, 96 105.
60. Minden M.D. Buick R.N. McCulloch E.A. ( 1979) Separation of blast cell and T-lymphocyte progenitors in the blood of patients with acute myeloblastic leukemia. Blood, 54, 186 195.
61. Miwa H. Bearn M. Saunders G.F. ( 1992) Expression of the Wilm's tumor (WT) gene in human leukemia. Leukemia, 6, 405 408.
62. Moore M.A. Metcalf D. ( 1973) Cytogenetic analysis of human acute and chronic myeloid leukemic cells cloned in agar culture. International Journal of Cancer, 11, 143 152.
63. Moreau-Gachelin F. Ray D. Mattei M.G. Tambourin P. Tavitian A. ( 1998) Spi-1 is a putative oncogene in virally induced murine erythroleukemias. Nature, 331, 277 279.
64. Morrison S.J. Weissman I.L. ( 1994) The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity, 1, 661 673.
65. Morrison S.J. Shah N.M. Anderson D.J. ( 1997) Regulatory mechanisms in stem cell biology. Cell, 88, 287 298.
66. Nerlov C. Querfurth E. Kulessa H. Graf T. ( 2000) GATA-1 interacts with the myeloid PU-1 transcription factor and represses PU-1 dependent transcription. Blood, 95, 2543 2551.
67. Nilsson S.K. Johnston H.M. Coverdale J.A. ( 2001) Spatial localization of transplanted hematopoietic stem cells: interferences for the localization of stem cell niches. Blood, 97, 2293 2299.
68. Ohta H. Sawada A. Kim J.Y. Tokimasa S. Nishiguchi S. Humphries R.K. Hara J. Takihara Y. ( 2002) Polycomb group gene Rae28 is required for sustaining activity of hematopietic stem cells. Journal of Experimental Medicine, 195, 759 770.
69. Orkin S.H. ( 1995) Transcription factors and hematopoietic development. Journal of Biological Chemistry, 270, 4955 4958.
70. Park I.K. Qian D. Kiel M. Becker M.W. Pihalja M. Weissman I.L. Morrison S.J. Clarke M.F. ( 2003) Bim-1 is required for maintenance of adult self-renewing stem cells. Nature, 423, 302 305.
71. Passegue E. Jamieson C.H.M. Ailles L.E. Weissman I.L. ( 2003) 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, 100, 11842 11849.
72. Passegue E. Wagner E.F. Weissman I.L. ( 2004) JunB deficiency leads to a myeloproliferative disorder arising from hematopoietic stem cells. Cell, 119, 431 443.
73. Pearce D.J. Ridler C.M. Simpson C. Bonnet D. ( 2004) Multiparameter analysis of murine bone marrow side population cells. Blood, 103, 2541 2546.
74. Phillips R. ( 1991) Hematopoietic stem cells: concepts, assays, and controversies. Seminar of Immunology, 3, 337 347.
75. Ploemacher R.E. van der Sluijs J.P. Voerman J.S. Brons N.H. ( 1989) An in vitro limiting dilution assay of long-term repopulating hematopoietic stem cells in the mouse. Blood, 74, 2755 2764.
76. Potocnik A.J. Brakebusch C. Fassler R. ( 2000) Fetal and adult hematopoietic stem cells require beta 1 integrin function for colonizing fetal liver, spleen and bone marrow. Immunity, 12, 653 663.
77. Punzel M. Wissink J.S. Miller K.A. Moore K.A. Lemiscka I.R. Verfaillie C.M. ( 1999) The myeloid-lymphoid initiating cell (ML-IC) assay assesses the fate of multipotent human progenitors in vitro. Blood, 93, 3750 3756.
78. Rabbitts T.H. ( 1994) Chromosomal translocations in human cancer. Nature, 372, 143 145.
79. Rafii S. Mohle R. Shapiro F. Frey B.M. Moore M.A. ( 1997) Regulation of hematopoiesis by microvascular endothelium. Leukemia and Lymphoma, 27, 357 386.
80. Rekhtman N. Radparvar F. Evans T. Skoultchi A.L. ( 1999) Direct interaction of hematopoietic transcription factors PU.1 and GATA.1 functional antagonism in erythroid cells. Genes and Development, 13, 1398 1411.
81. Reya T. Morrison S.J. Clarke M.F. Weissman I.L. ( 2001) Stem cells, cancer, and cancer stem cells. Nature, 414, 105 111.
82. Reya T. Duncan A.W. Ailles L. Domen J. Scherer D.C. Willert K. Hintz L. Nusse R. Weissman I.L. ( 2003) A role of Wnt signalling in self-renewal of haematopoietic stem cells. Nature, 423, 409 414.
83. Robb L. Lyons I. Li R. Hartley L. Kontgen F. Harvey R.P. Metcalf D. Begley C.G. ( 1995) Absence of yolk sac hematopoiesis from mice with a targeted disruption of the scl gene. Proceedings of the National Academy of Sciences of the United States of America, 92, 7075 7079.
84. Ruiz I. Altaba A. Sanchez P. Dahmane N. ( 2002) Gli and hedgehog in cancer: tumours, embryos and stem cells. Nature Review Cancer, 2, 361 372.
85. Sandberg M.L. Sutton S.E. Pletcher M.T. Wiltshire T. Tarantino L.M. Hogenesch J.B. Cooke M.I.P. ( 2005) c-Myb and p300 regulate hematopoietic stem cell proliferation and differentiation. Cell, 8, 153 166.
86. Sauvageau G. Lansdorp P.M. Eaves C.J. Hogge D.E. Dragowska W.H. Reid D.S. Largman C. Lawrence H.J. Humphries R.K. ( 1994) Differential expression of homeobox genes in functionally distinct CD34+ subpopulations of human bone marrow cells. Proceedings of the National Academy of Sciences of the United States of America, 91, 12223 12227.
87. Sauvageau G. Thorsteinsdottir U. Eaves C.J. Lawrence H.J. Largman C. Lansdorp P.M. Humphries R.K. ( 1995) Overexpression of HOXB4 in hematopoietic cells causes the selective expansion of more primitive populations in vitro and in vivo. Genes and Development, 9, 1753 1765.
88. Scott M.P. ( 1992) Vertebrate homeobox gene nomenclature. Cell, 71, 551 553.
89. Shivdasani R.A. Orkin S.H. ( 1996) The transcription control of hematopoiesis. Blood, 87, 4025 4029.
90. Singh S.K. Clarke I.D. Terasaki M. Bonn V.E. Hawkins C. Squire J. Dirks P.B. ( 2003) Identification of a cancer stem cell in human brain tumors. Cancer Research, 63, 5821 5828.
91. Singh S.K. Hawkins C. Clarke I.D. Squire J.A. Bayani J. Hide T. Henkelman R.M. Cusimano M.D. Dirks P.B. ( 2004a) Identification of human brain tumour initiating cells. Nature, 432, 396 401.
92. Singh S.K. Clarke I.D. Hide T. Dirks P.B. ( 2004b) Cancer stem cells in nervous system tumors. Oncogene, 23, 7267 7273.
93. So C.W. Karsunky H. Passegue E. Cozzio A. Weissman I.L. Cleary M.L. ( 2003) MLL-GAS7 transforms multipotent hematopoietic progenitors and induces mixed lineage leukemias in mice. Cancer Cell, 3, 161 171.
94. Spangrude G.J. Heimfield S. Weissman I.L. ( 1998) Purification and characterization of murine hematopoietic stem cells. Science, 241, 58 63.
95. Storms R.W. Trujillo A.P. Springer J.B. Shah L. Colvin O.M. Ludeman S.M. Smith C. ( 1999) Isolation of primitive human hematopoietic progenitors on the basis of aldehyde dehydrogenase activity. Proceedings of the National Academy of Sciences of the United States of America, 96, 9118 9123.
96. Sutherland H.J. Eaves C.J. Eaves A.C. ( 1989) Characterization and partial purification of human marrow cell capable of initiating long-term hematopoiesis in vitro. Blood, 74, 1563 1570.
97. Sutherland H.J. Lansdorp P.M. Henkelman D.H. Eaves A.C. Eaves C.J. ( 1990) Functional characterization of individual human hematopoietic stem cells cultured at limiting dilution on supportive marrow stromal layers. Proceedings of the National Academy of Sciences of the United States of America, 87, 3584 3588.
98. Sutherland H.J. Blair A. Zapf R.W. ( 1996) Characterization of a hierarchy in human acute myeloid leukemia progenitor cells. Blood, 87, 4754 4761.
99. Taichman R.S. Emerson S.G. ( 1998) The role of osteoblasts in the hematopoietic microenvironment. Stem Cells, 6, 7 15.
100. Tenen D.G. Hromas R. Licht J.D. Zhang D.E. ( 1997) Transcription factors, normal myeloid development, and leukemia. Blood, 90, 489 519.
101. Theunissen K. Verfaillie C.M. ( 2005) A multifactorial analysis of umbilical cord blood, adult bone marrow and mobilized peripheral blood progenitors using the improved ML-IC assay. Experimental Hematology, 33, 165 172.
102. Thorsteindottir U. Sauvageau G. Humphries R.K. ( 1999) Enhanced in vivo regenerative potential of Hox B4-transduced hematopoietic stem cells with regulation of their pool size. Blood, 94, 2605 2612.
103. Uchida N. Fujisaki T. Eaves A.C. Eaves C.J. ( 2001) Transplantable hematopoietic stem cells in human fetal liver have a CD34+ side population (SP) phenotype. Journal of Clinical Investigation, 108, 1071 1077.
104. Valk P.J. Verhaak R.G. Beijen M.A. Erpelinck C.A. Barjesteh van Waalwijk van Doorn-Khosrovani S. Boer J.M. Beverloo H.B. Moorhouse M.J. van der Spek P.J. Lowenberg B. Delwel R. ( 2004) Prognostically useful gene-expression profiles in acute myeloid leukemia. New England Journal of Medicine, 350, 1617 1628.
105. Valk P.J. Delwel R. Lowenberg B. ( 2005) Gene expression profiling in acute myeloid leukemia. Current Opinion in Hematology, 12, 76 81.
106. Varnum-Finney B. Xu L. Brashem-Stein C. Nourigat C. Flowers D. Bakkour S. Pear W. Bernstein I. ( 2000) Pluripotent, cytokine-dependent hematopoietic stem cells are immortalized by constitutive Notch 1 signalling. Nature Medicine, 6, 1278 1281.
107. Walkley C.R. Fero M.L. Chien W.M. Purton L.E. McArthur G.A. ( 2005) Negative cell-cycle regulators cooperatively control self-renewal and differentiation of hematopoietic stem cells. Nature Cell Biology, 7, 172 178.
108. Weissman I. ( 2000) Stem cells: units of development, units of regeneration, and units in evolution. Cell, 100, 157 168.
109. Whetton A.D. Graham G.J. ( 1999) Homing mobilization in the stem cell niche. Trends in Cell Biology, 9, 233 238.
110. Willert K. Brown J.D. Danenberg E. Duncan A.W. Weissman I.L. Reya T. Reya T. Yates J.R. Nusse R. ( 2003) Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature, 423, 448 452.
111. Wilson A. Murphy M.J. Oskarsson T. Kaloulis K. Bettess M.D. Oser G.M. Pasche A.C. Knabenhans C. MacDonald H.R. Trumpp A. ( 2005) C-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes and Development, 18, 2747 2763.
112. Yuan Y. Shen H. Franklin D.S. Scadden D.T. Cheng T. ( 2004) In vivo self-renewing divisions of haematopoietic stem cells are increased in the absence of the early G1-phase inhibitor, p18INK4C. Nature Cell Biology, 5, 436 442.
113. Zanjani E.D. Almeida-Porada G. Ascensao J.L. MacKintosh F.R. Flake A.W. ( 1997) Transplantation of hematopoietic stem cells in utero. Stem Cells, 15 ( Suppl. 1 79 84.
114. Zeng H. Yucel R. Kosan C. Klein-Hitpass L. Moroy T. ( 2004) Transcription factors Gli-1 regulates self-renewal and engraftment of hematopoietic stem cells. EMBO Journal, 23, 4116 4125.
115. Zhang P. Zhang X. Iwama A. Yu C. Smith K.A. Mueller B.U. Narravula S. Torbett B.E. Orkin S.H. Tenen D.G. ( 2000) PU.1 inhibits GATA-1 function and erythroid differentiation by blocking GATA-1 DNA binding. Blood, 96, 2641 2648.
116. Ziegler B.L. Valtieri M. Porada G.A. De Maria R. Muller R. Masella B. Gabbianelli M. Casella I. Pelosi E. Bock T. Peschle C. ( 1999) KDR receptor: a key marker defining hematopoietic stem cells. Science, 285, 553 558.