Hematopoiesis: A human perspective

Cell Stem Cell

Volumn 10, Issue 2, 2012, Pages 120-136

  Doulatov, Sergei ^a,b   Notta, Faiyaz ^a,b   Laurenti, Elisa ^a,b   Dick, John E ^a,b  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ISOLATION; DENDRITIC CELL; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; LYMPHOID CELL; LYMPHOMA; NONHUMAN; PRIORITY JOURNAL; PURIFICATION; REVIEW;

ANIMALS; CELL LINEAGE; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HUMANS; MICE; MICE, SCID; MODELS, ANIMAL; REGENERATIVE MEDICINE;

MUS;

EID: 84856738988     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2012.01.006     Document Type: Review

References (172)

1. J.L. Abkowitz, S.N. Catlin, and P. Guttorp Evidence that hematopoiesis may be a stochastic process in vivo Nat. Med. 2 1996 190 197 (Pubitemid 26054982)
2. J. Adolfsson, O.J. Borge, D. Bryder, K. Theilgaard-Monch, I. Astrand-Grundstrom, E. Sitnicka, Y. Sasaki, and S.E. Jacobsen Upregulation of Flt3 expression within the bone marrow Lin(-)Sca1(+)c-kit(+) stem cell compartment is accompanied by loss of self-renewal capacity Immunity 15 2001 659 669 (Pubitemid 33016450)
3. J. Adolfsson, R. Mansson, N. Buza-Vidas, A. Hultquist, K. Liuba, C.T. Jensen, D. Bryder, L. Yang, O.J. Borge, and L.A. Thoren Identification of Flt3+ lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment Cell 121 2005 295 306 (Pubitemid 40546396)
4. K. Akashi, D. Traver, T. Miyamoto, and I.L. Weissman A clonogenic common myeloid progenitor that gives rise to all myeloid lineages Nature 404 2000 193 197 (Pubitemid 30154488)
5. S. Amsellem, F. Pflumio, D. Bardinet, B. Izac, P. Charneau, P.H. Romeo, A. Dubart-Kupperschmitt, and S. Fichelson Ex vivo expansion of human hematopoietic stem cells by direct delivery of the HOXB4 homeoprotein Nat. Med. 9 2003 1423 1427 (Pubitemid 37466194)
6. J. Antonchuk, G. Sauvageau, and R.K. Humphries HOXB4-induced expansion of adult hematopoietic stem cells ex vivo Cell 109 2002 39 45 (Pubitemid 34327515)
7. F. Barabe, J.A. Kennedy, K.J. Hope, and J.E. Dick Modeling the initiation and progression of human acute leukemia in mice Science 316 2007 600 604 (Pubitemid 46683146)
8. C.M. Baum, I.L. Weissman, A.S. Tsukamoto, A.M. Buckle, and B. Peault Isolation of a candidate human hematopoietic stem-cell population Proc. Natl. Acad. Sci. USA 89 1992 2804 2808
9. A.J. Becker, E.A. McCulloch, and J.E. Till Cytological Demonstration of the Clonal Nature of Spleen Colonies Derived from Transplanted Mouse Marrow Cells Nature 197 1963 452 454
10. J.J. Bell, and A. Bhandoola The earliest thymic progenitors for T cells possess myeloid lineage potential Nature 452 2008 764 767 (Pubitemid 351521083)
11. P. Benveniste, C. Frelin, S. Janmohamed, M. Barbara, R. Herrington, D. Hyam, and N.N. Iscove Intermediate-term hematopoietic stem cells with extended but time-limited reconstitution potential Cell Stem Cell 6 2010 48 58
12. B.E. Bernstein, T.S. Mikkelsen, X. Xie, M. Kamal, D.J. Huebert, J. Cuff, B. Fry, A. Meissner, M. Wernig, and K. Plath A bivalent chromatin structure marks key developmental genes in embryonic stem cells Cell 125 2006 315 326
13. M. Bhatia, J.C.Y. Wang, U. Kapp, D. Bonnet, and J.E. Dick Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice Proc. Natl. Acad. Sci. USA 94 1997 5320 5325 (Pubitemid 27214781)
14. M. Bhatia, D. Bonnet, B. Murdoch, O.I. Gan, and J.E. Dick A newly discovered class of human hematopoietic cells with SCID- repopulating activity Nat. Med. 4 1998 1038 1045 (Pubitemid 28417336)
15. V. Bigley, M. Haniffa, S. Doulatov, X.N. Wang, R. Dickinson, N. McGovern, L. Jardine, S. Pagan, I. Dimmick, and I. Chua The human syndrome of dendritic cell, monocyte, B and NK lymphoid deficiency J. Exp. Med. 208 2011 227 234
16. L.G. Billips, D. Petitte, K. Dorshkind, R. Narayanan, C.P. Chiu, and K.S. Landreth Differential roles of stromal cells, interleukin-7, and kit-ligand in the regulation of B lymphopoiesis Blood 79 1992 1185 1192
17. A.E. Boitano, J. Wang, R. Romeo, L.C. Bouchez, A.E. Parker, S.E. Sutton, J.R. Walker, C.A. Flaveny, G.H. Perdew, and M.S. Denison Aryl hydrocarbon receptor antagonists promote the expansion of human hematopoietic stem cells Science 329 2010 1345 1348
18. G.C. Bosma, R.P. Custer, and M.J. Bosma A severe combined immunodeficiency mutation in the mouse Nature 301 1983 527 530 (Pubitemid 13160576)
19. S.W. Boyer, A.V. Schroeder, S. Smith-Berdan, and E.C. Forsberg All hematopoietic cells develop from hematopoietic stem cells through Flk2/Flt3-positive progenitor cells Cell Stem Cell 9 2011 64 73
20. A.M. Broske, L. Vockentanz, S. Kharazi, M.R. Huska, E. Mancini, M. Scheller, C. Kuhl, A. Enns, M. Prinz, and R. Jaenisch DNA methylation protects hematopoietic stem cell multipotency from myeloerythroid restriction Nat. Genet. 41 2009 1207 1215
21. C.G. Brunstein, and J.E. Wagner Umbilical cord blood transplantation and banking Annu. Rev. Med. 57 2006 403 417 (Pubitemid 43261998)
22. C. Buske, M. Feuring-Buske, C. Abramovich, K. Spiekermann, C.J. Eaves, L. Coulombel, G. Sauvageau, D.E. Hogge, and R.K. Humphries Deregulated expression of HOXB4 enhances the primitive growth activity of human hematopoietic cells Blood 100 2002 862 868 (Pubitemid 34832611)
23. N. Buza-Vidas, P. Woll, A. Hultquist, S. Duarte, M. Lutteropp, T. Bouriez-Jones, H. Ferry, S. Luc, and S.E. Jacobsen FLT3 expression initiates in fully multipotent mouse hematopoietic progenitor cells Blood 118 2011 1544 1548
24. S. Carotta, L. Wu, and S.L. Nutt Surprising new roles for PU.1 in the adaptive immune response Immunol. Rev. 238 2010 63 75
25. S.N. Catlin, L. Busque, R.E. Gale, P. Guttorp, and J.L. Abkowitz The replication rate of human hematopoietic stem cells in vivo Blood 117 2011 4460 4466
26. S.H. Cheshier, S.J. Morrison, X. Liao, and I.L. Weissman In vivo proliferation and cell cycle kinetics of long-term self-renewing hematopoietic stem cells Proc. Natl. Acad. Sci. USA 96 1999 3120 3125 (Pubitemid 29148854)
27. L. Chicha, D. Jarrossay, and M.G. Manz Clonal type I interferon-producing and dendritic cell precursors are contained in both human lymphoid and myeloid progenitor populations J. Exp. Med. 200 2004 1519 1524 (Pubitemid 39657299)
28. C.I. Civin, L.C. Strauss, C. Brovall, M.J. Fackler, J.F. Schwartz, and J.H. Shaper Antigenic analysis of hematopoiesis. III. A hematopoietic progenitor cell surface antigen defined by a monoclonal antibody raised against KG-1a cells J. Immunol. 133 1984 157 165 (Pubitemid 14076703)
29. L.S. Collins, and K. Dorshkind A stromal cell line from myeloid long-term bone marrow cultures can support myelopoiesis and B lymphopoiesis J. Immunol. 138 1987 1082 1087 (Pubitemid 17017888)
30. E. Conneally, J. Cashman, A. Petzer, and C. Eaves 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 1997 9836 9841 (Pubitemid 27408151)
31. P.D. Cravens, M.W. Melkus, A. Padgett-Thomas, M. Islas-Ohlmayer, P.M.M. Del, and J.V. Garcia Development and activation of human dendritic cells in vivo in a xenograft model of human hematopoiesis Stem Cells 23 2005 264 278 (Pubitemid 40239521)
32. C. Delaney, S. Heimfeld, C. Brashem-Stein, H. Voorhies, R.L. Manger, and I.D. Bernstein Notch-mediated expansion of human cord blood progenitor cells capable of rapid myeloid reconstitution Nat. Med. 16 2010 232 236
33. T.M. Dexter, and L.G. Lajtha Proliferation of haemopoietic stem cells in vitro Br. J. Haematol. 28 1974 525 530
34. J.E. Dick Stem cell concepts renew cancer research Blood 112 2008 4793 4807
35. R.E. Dickinson, H. Griffin, V. Bigley, L.N. Reynard, R. Hussain, M. Haniffa, J.H. Lakey, T. Rahman, X.N. Wang, and N. McGovern Exome sequencing identifies GATA-2 mutation as the cause of dendritic cell, monocyte, B and NK lymphoid deficiency Blood 118 2011 2656 2658
36. S. Doulatov, F. Notta, K.L. Rice, L. Howell, A. Zelent, J.D. Licht, and J.E. Dick PLZF is a regulator of homeostatic and cytokine-induced myeloid development Genes Dev. 23 2009 2076 2087
37. S. Doulatov, F. Notta, K. Eppert, L.T. Nguyen, P.S. Ohashi, and J.E. Dick Revised map of the human progenitor hierarchy shows the origin of macrophages and dendritic cells in early lymphoid development Nat. Immunol. 11 2010 585 593
38. K. Eppert, K. Takenaka, E.R. Lechman, L. Waldron, B. Nilsson, P. van Galen, K.H. Metzeler, A. Poeppl, V. Ling, and J. Beyene Stem cell gene expression programs influence clinical outcome in human leukemia Nat. Med. 17 2011 1086 1093
39. P. Ernst, J.K. Fisher, W. Avery, S. Wade, D. Foy, and S.J. Korsmeyer Definitive hematopoiesis requires the mixed-lineage leukemia gene Dev. Cell 6 2004 437 443 (Pubitemid 38364574)
40. D.K. Fogg, C. Sibon, C. Miled, S. Jung, P. Aucouturier, D.R. Littman, A. Cumano, and F. Geissmann A clonogenic bone marrow progenitor specific for macrophages and dendritic cells Science 311 2006 83 87 (Pubitemid 43063063)
41. A. Foudi, K. Hochedlinger, D. Van Buren, J.W. Schindler, R. Jaenisch, V. Carey, and H. Hock Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells Nat. Biotechnol. 27 2009 84 90
42. G.M. Fulop, and R.A. Phillips The scid mutation in mice causes a general defect in DNA repair Nature 347 1990 479 482
43. A. Galy, M. Travis, D. Cen, and B. Chen Human T, B, natural killer, and dendritic cells arise from a common bone marrow progenitor cell subset Immunity 3 1995 459 473
44. S. Gartner, and H.S. Kaplan Long-term culture of human bone marrow cells Proc. Natl. Acad. Sci. USA 77 1980 4756 4759
45. R.W. Georgantas 3rd, V. Tanadve, M. Malehorn, S. Heimfeld, C. Chen, L. Carr, F. Martinez-Murillo, G. Riggins, J. Kowalski, and C.I. Civin Microarray and serial analysis of gene expression analyses identify known and novel transcripts overexpressed in hematopoietic stem cells Cancer Res. 64 2004 4434 4441 (Pubitemid 38856914)
46. H. Glimm, W. Eisterer, K. Lee, J. Cashman, T.L. Holyoake, F. Nicolini, L.D. Shultz, C. von Kalle, and C.J. Eaves Previously undetected human hematopoietic cell populations with short-term repopulating activity selectively engraft NOD/SCID-beta2 microglobulin-null mice J. Clin. Invest. 107 2001 199 206 (Pubitemid 32096836)
47. N. Goardon, E. Marchi, A. Atzberger, L. Quek, A. Schuh, S. Soneji, P. Woll, A. Mead, K.A. Alford, and R. Rout Coexistence of LMPP-like and GMP-like leukemia stem cells in acute myeloid leukemia Cancer Cell 19 2011 138 152
48. W. Goessling, T.E. North, S. Loewer, A.M. Lord, S. Lee, C.L. Stoick-Cooper, G. Weidinger, M. Puder, G.Q. Daley, and R.T. Moon Genetic interaction of PGE2 and Wnt signaling regulates developmental specification of stem cells and regeneration Cell 136 2009 1136 1147
49. W. Goessling, R.S. Allen, X. Guan, P. Jin, N. Uchida, M. Dovey, J.M. Harris, M.E. Metzger, A.C. Bonifacino, and D. Stroncek Prostaglandin E2 enhances human cord blood stem cell xenotransplants and shows long-term safety in preclinical nonhuman primate transplant models Cell Stem Cell 8 2011 445 458
50. R. Gupta, D. Hong, F. Iborra, S. Sarno, and T. Enver NOV (CCN3) functions as a regulator of human hematopoietic stem or progenitor cells Science 316 2007 590 593 (Pubitemid 46683143)
51. R. Haddad, F. Guimiot, E. Six, F. Jourquin, N. Setterblad, E. Kahn, M. Yagello, C. Schiffer, I. Andre-Schmutz, and M. Cavazzana-Calvo Dynamics of thymus-colonizing cells during human development Immunity 24 2006 217 230 (Pubitemid 43214590)
52. W.C. Hahn, and R.A. Weinberg Rules for making human tumor cells N. Engl. J. Med. 347 2002 1593 1603 (Pubitemid 35315841)
53. S. Hambleton, S. Salem, J. Bustamante, V. Bigley, S. Boisson-Dupuis, J. Azevedo, A. Fortin, M. Haniffa, L. Ceron-Gutierrez, and C.M. Bacon IRF8 mutations and human dendritic-cell immunodeficiency N. Engl. J. Med. 365 2011 127 138
54. J. Hanna, M. Wernig, S. Markoulaki, C.W. Sun, A. Meissner, J.P. Cassady, C. Beard, T. Brambrink, L.C. Wu, and T.M. Townes Treatment of sickle cell anemia mouse model with iPS cells generated from autologous skin Science 318 2007 1920 1923
55. Q.L. Hao, F.T. Thiemann, D. Petersen, E.M. Smogorzewska, and G.M. Crooks Extended long-term culture reveals a highly quiescent and primitive human hematopoietic progenitor population Blood 88 1996 3306 3313 (Pubitemid 26365563)
56. Q.L. Hao, J. Zhu, M.A. Price, K.J. Payne, L.W. Barsky, and G.M. Crooks Identification of a novel, human multilymphoid progenitor in cord blood Blood 97 2001 3683 3690
57. H.A. Himburg, G.G. Muramoto, P. Daher, S.K. Meadows, J.L. Russell, P. Doan, J.T. Chi, A.B. Salter, W.E. Lento, and T. Reya Pleiotrophin regulates the expansion and regeneration of hematopoietic stem cells Nat. Med. 16 2010 475 482
58. I. Hoebeke, M. De Smedt, F. Stolz, K. Pike-Overzet, F.J. Staal, J. Plum, and G. Leclercq T-, B- and NK-lymphoid, but not myeloid cells arise from human CD34(+)CD38(-)CD7(+) common lymphoid progenitors expressing lymphoid-specific genes Leukemia 21 2007 311 319 (Pubitemid 46158125)
59. A.P. Hsu, E.P. Sampaio, J. Khan, K.R. Calvo, J.E. Lemieux, S.Y. Patel, D.M. Frucht, D.C. Vinh, R.D. Auth, and A.F. Freeman Mutations in GATA2 are associated with the autosomal dominant and sporadic monocytopenia and mycobacterial infection (MonoMAC) syndrome Blood 118 2011 2653 2655
60. K. Ikuta, and I.L. Weissman Evidence that hematopoietic stem cells express mouse c-kit but do not depend on steel factor for their generation Proc. Natl. Acad. Sci. USA 89 1992 1502 1506
61. M. Ishii, Y. Matsuoka, Y. Sasaki, R. Nakatsuka, M. Takahashi, T. Nakamoto, K. Yasuda, K. Matsui, H. Asano, and Y. Uemura Development of a high-resolution purification method for precise functional characterization of primitive human cord blood-derived CD34-negative SCID-repopulating cells Exp. Hematol 39 2011 203 213 e201
62. M. Ito, H. Hiramatsu, K. Kobayashi, K. Suzue, M. Kawahata, K. Hioki, Y. Ueyama, Y. Koyanagi, K. Sugamura, and K. Tsuji NOD/SCID/gamma(c)(null) mouse: an excellent recipient mouse model for engraftment of human cells Blood 100 2002 3175 3182 (Pubitemid 35217065)
63. K. Itoh, H. Tezuka, H. Sakoda, M. Konno, K. Nagata, T. Uchiyama, H. Uchino, and K.J. Mori Reproducible establishment of hemopoietic supportive stromal cell lines from murine bone marrow Exp. Hematol. 17 1989 145 153 (Pubitemid 19056039)
64. N.B. Ivanova, J.T. Dimos, C. Schaniel, J.A. Hackney, K.A. Moore, and I.R. Lemischka A stem cell molecular signature Science 298 2002 601 604
65. S. Jaiswal, C.H. Jamieson, W.W. Pang, C.Y. Park, M.P. Chao, R. Majeti, D. Traver, N. van Rooijen, and I.L. Weissman CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis Cell 138 2009 271 285
66. H. Ji, L.I. Ehrlich, J. Seita, P. Murakami, A. Doi, P. Lindau, H. Lee, M.J. Aryee, R.A. Irizarry, and K. Kim Comprehensive methylome map of lineage commitment from haematopoietic progenitors Nature 467 2010 338 342
67. C.D. Jude, L. Climer, D. Xu, E. Artinger, J.K. Fisher, and P. Ernst Unique and independent roles for MLL in adult hematopoietic stem cells and progenitors Cell Stem Cell 1 2007 324 337 (Pubitemid 47355322)
68. S. Kamel-Reid, and J.E. Dick Engraftment of immune-deficient mice with human hematopoietic stem cells Science 242 1988 1706 1709 (Pubitemid 19022179)
69. Y. Kang, N.J. Chao, and F. Aversa Unmanipulated or CD34 selected haplotype mismatched transplants Curr. Opin. Hematol. 15 2008 561 567
70. H. Kawamoto, K. Ohmura, S. Fujimoto, and Y. Katsura Emergence of T cell progenitors without B cell or myeloid differentiation potential at the earliest stage of hematopoiesis in the murine fetal liver J. Immunol. 162 1999 2725 2731 (Pubitemid 29309295)
71. H. Kawamoto, T. Ikawa, K. Masuda, H. Wada, and Y. Katsura A map for lineage restriction of progenitors during hematopoiesis: the essence of the myeloid-based model Immunol. Rev. 238 2010 23 36
72. N.I. Kerkvliet, D.M. Shepherd, and L. Baecher-Steppan T lymphocytes are direct, aryl hydrocarbon receptor (AhR)-dependent targets of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD): AhR expression in both CD4+ and CD8+ T cells is necessary for full suppression of a cytotoxic T lymphocyte response by TCDD Toxicol. Appl. Pharmacol. 185 2002 146 152 (Pubitemid 36062805)
73. M.J. Kiel, O.H. Yilmaz, T. Iwashita, C. Terhorst, and S.J. Morrison SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells Cell 121 2005 1109 1121 (Pubitemid 40884400)
74. M.J. Kiel, S. He, R. Ashkenazi, S.N. Gentry, M. Teta, J.A. Kushner, T.L. Jackson, and S.J. Morrison Haematopoietic stem cells do not asymmetrically segregate chromosomes or retain BrdU Nature 449 2007 238 242 (Pubitemid 47402371)
75. C. Klein Genetic defects in severe congenital neutropenia: emerging insights into life and death of human neutrophil granulocytes Annu. Rev. Immunol. 29 2011 399 413
76. U. Koch, A. Wilson, M. Cobas, R. Kemler, H.R. Macdonald, and F. Radtke Simultaneous loss of beta- and gamma-catenin does not perturb hematopoiesis or lymphopoiesis Blood 111 2008 160 164
77. M. Kondo, I.L. Weissman, and K. Akashi Identification of clonogenic common lymphoid progenitors in mouse bone marrow Cell 91 1997 661 672 (Pubitemid 27513657)
78. A.V. Krivtsov, and S.A. Armstrong MLL translocations, histone modifications and leukaemia stem-cell development Nat. Rev. Cancer 7 2007 823 833 (Pubitemid 350006257)
79. M. Kyba, R.C. Perlingeiro, and G.Q. Daley HoxB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors Cell 109 2002 29 37 (Pubitemid 34327514)
80. R.N. La Motte-Mohs, E. Herer, and J.C. Zuniga-Pflucker Induction of T cell development from human cord blood hematopoietic stem cells by Delta-like 1 in vitro Blood 105 2004 1431 1439
81. C. Lagresle-Peyrou, E.M. Six, C. Picard, F. Rieux-Laucat, V. Michel, A. Ditadi, C. Demerens-de Chappedelaine, E. Morillon, F. Valensi, and K.L. Simon-Stoos Human adenylate kinase 2 deficiency causes a profound hematopoietic defect associated with sensorineural deafness Nat. Genet. 41 2009 106 111
82. P.M. Lansdorp, H.J. Sutherland, and C.J. Eaves Selective expression of CD45 isoforms on functional subpopulations of CD34+ hemopoietic cells from human bone marrow J. Exp. Med. 172 1990 363 366 (Pubitemid 20217280)
83. T. Lapidot, F. Pflumio, M. Doedens, B. Murdoch, D.E. Williams, and J.E. Dick Cytokine stimulation of multilineage hematopoiesis from immature human cells engrafted in scid mice Science 255 1992 1137 1141
84. A. Larochelle, M. Savona, M. Wiggins, S. Anderson, B. Ichwan, K. Keyvanfar, S.J. Morrison, and C.E. Dunbar Human and rhesus macaque hematopoietic stem cells cannot be purified based only on SLAM family markers Blood 117 2011 1550 1554
85. J.D. Lathia, J. Gallagher, J.M. Heddleston, J. Wang, C.E. Eyler, J. Macswords, Q. Wu, A. Vasanji, R.E. McLendon, and A.B. Hjelmeland Integrin alpha 6 regulates glioblastoma stem cells Cell Stem Cell 6 2010 421 432
86. J. Lessard, and G. Sauvageau Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells Nature 423 2003 255 260 (Pubitemid 40852690)
87. E. Lorenz, D. Uphoff, T.R. Reid, and E. Shelton Modification of irradiation injury in mice and guinea pigs by bone marrow injections J. Natl. Cancer Inst. 12 1951 197 201
88. I. Maillard, U. Koch, A. Dumortier, O. Shestova, L. Xu, H. Sai, S.E. Pross, J.C. Aster, A. Bhandoola, and F. Radtke Canonical notch signaling is dispensable for the maintenance of adult hematopoietic stem cells Cell Stem Cell 2 2008 356 366 (Pubitemid 351455243)
89. R. Majeti, C.Y. Park, and I.L. Weissman Identification of a hierarchy of multipotent hematopoietic progenitors in human cord blood Cell Stem Cell 1 2007 635 645 (Pubitemid 350215330)
90. R. Mansson, A. Hultquist, S. Luc, L. Yang, K. Anderson, S. Kharazi, S. Al-Hashmi, K. Liuba, L. Thoren, and J. Adolfsson Molecular evidence for hierarchical transcriptional lineage priming in fetal and adult stem cells and multipotent progenitors Immunity 26 2007 407 419 (Pubitemid 46603001)
91. M.G. Manz, T. Miyamoto, K. Akashi, and I.L. Weissman Prospective isolation of human clonogenic common myeloid progenitors Proc. Natl. Acad. Sci. USA 99 2002 11872 11877 (Pubitemid 34994491)
92. A. Maximow Der Lymphozyt als gemeinsame Stammzelle der verschiedenen Blutelemente in der embryonalen Entwicklung und im postfetalen Leben der Säugetiere Folia Haematol. (Frankf.) 8 1909 125 134
93. F. Mazurier, M. Doedens, O.I. Gan, and J.E. Dick Rapid myeloerythroid repopulation after intrafemoral transplantation of NOD-SCID mice reveals a new class of human stem cells Nat. Med. 9 2003 959 963 (Pubitemid 36889941)
94. J.M. McCune, R. Namikawa, H. Kaneshima, L.D. Shultz, M. Lieberman, and I.L. Weissman The SCID-hu mouse: murine model for the analysis of human hematolymphoid differentiation and function Science 241 1988 1632 1639
95. J. Mestas, and C.C. Hughes Of mice and not men: differences between mouse and human immunology J. Immunol. 172 2004 2731 2738 (Pubitemid 38263654)
96. C.L. Miller, J. Audet, and C.J. Eaves Ex vivo expansion of human and murine hematopoietic stem cells Methods Mol. Med. 63 2002 189 208
97. M. Milyavsky, O.I. Gan, M. Trottier, M. Komosa, O. Tabach, F. Notta, E. Lechman, K.G. Hermans, K. Eppert, and Z. Konovalova A distinctive DNA damage response in human hematopoietic stem cells reveals an apoptosis-independent role for p53 in self-renewal Cell Stem Cell 7 2010 186 197
98. M. Mohrin, E. Bourke, D. Alexander, M.R. Warr, K. Barry-Holson, M.M. Le Beau, C.G. Morrison, and E. Passegue Hematopoietic stem cell quiescence promotes error-prone DNA repair and mutagenesis Cell Stem Cell 7 2010 174 185
99. M.A. Moore, N. Williams, and D. Metcalf In vitro colony formation by normal and leukemic human hematopoietic cells: characterization of the colony-forming cells J. Natl. Cancer Inst. 50 1973 603 623
100. S.J. Morrison, A.M. Wandycz, H.D. Hemmati, D.E. Wright, and I.L. Weissman Identification of a lineage of multipotent hematopoietic progenitors Development 124 1997 1929 1939 (Pubitemid 27270262)
101. D.E. Mosier, R.J. Gulizia, S.M. Baird, and D.B. Wilson Transfer of a functional human immune system to mice with severe combined immunodeficiency Nature 335 1988 256 259
102. D. Mosier, R. Gulizia, S. Baird, D. Wilson, D. Spector, and S. Spector Human Immunodeficiency virus infection of human-PBL-SCID mice Science 251 1991 791 794 (Pubitemid 21926171)
103. C.G. Mullighan, X. Su, J. Zhang, I. Radtke, L.A. Phillips, C.B. Miller, J. Ma, W. Liu, C. Cheng, and B.A. Schulman Deletion of IKZF1 and prognosis in acute lymphoblastic leukemia N. Engl. J. Med. 360 2009 470 480
104. L. Murray, B. Chen, A. Galy, S. Chen, R. Tushinski, N. Uchida, R. Negrin, G. Tricot, S. Jagannath, and D. Vesole Enrichment of human hematopoietic stem cell activity in the CD34+Thy-1+Lin- subpopulation from mobilized peripheral blood Blood 85 1995 368 378
105. R. Namikawa, H. Kaneshima, M. Lieberman, I.L. Weissman, and J.M. McCune Infection of the SCID-hu mouse by HIV-1 Science 242 1988 1684 1686 (Pubitemid 19022172)
106. R.S. Negrin, K. Atkinson, T. Leemhuis, E. Hanania, C. Juttner, K. Tierney, W.W. Hu, L.J. Johnston, J.A. Shizurn, and K.E. Stockerl-Goldstein Transplantation of highly purified CD34+Thy-1+ hematopoietic stem cells in patients with metastatic breast cancer Biol. Blood Marrow Transplant. 6 2000 262 271
107. R.A. Neumuller, and J.A. Knoblich Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer Genes Dev. 23 2009 2675 2699
108. B. Niebuhr, G.B. Iwanski, M. Schwieger, S. Roscher, C. Stocking, and J. Cammenga Investigation of C/EBPalpha function in human (versus murine) myelopoiesis provides novel insight into the impact of CEBPA mutations in acute myelogenous leukemia (AML) Leukemia 23 2009 978 983
109. M. Noguchi, H. Yi, H.M. Rosenblatt, A.H. Filipovich, S. Adelstein, W.S. Modi, O.W. McBride, and W.J. Leonard Interleukin-2 receptor gamma chain mutation results in X-linked severe combined immunodeficiency in humans Cell 73 1993 147 157 (Pubitemid 23115456)
110. T.E. North, W. Goessling, C.R. Walkley, C. Lengerke, K.R. Kopani, A.M. Lord, G.J. Weber, T.V. Bowman, I.H. Jang, and T. Grosser Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis Nature 447 2007 1007 1011 (Pubitemid 46975751)
111. F. Notta, S. Doulatov, and J.E. Dick Engraftment of human hematopoietic stem cells is more efficient in female NOD/SCID/IL-2Rgc-null recipients Blood 115 2010 3704 3707
112. F. Notta, S. Doulatov, E. Laurenti, A. Poeppl, I. Jurisica, and J.E. Dick Isolation of single human hematopoietic stem cells capable of long-term multilineage engraftment Science 333 2011 218 221
113. N. Novershtern, A. Subramanian, L.N. Lawton, R.H. Mak, W.N. Haining, M.E. McConkey, N. Habib, N. Yosef, C.Y. Chang, and T. Shay Densely interconnected transcriptional circuits control cell states in human hematopoiesis Cell 144 2011 296 309
114. K. Ohishi, B. Varnum-Finney, and I.D. Bernstein Delta-1 enhances marrow and thymus repopulating ability of human CD34(+)CD38(-) cord blood cells J. Clin. Invest. 110 2002 1165 1174 (Pubitemid 35215897)
115. S.H. Orkin, and L.I. Zon Hematopoiesis: an evolving paradigm for stem cell biology Cell 132 2008 631 644 (Pubitemid 351260057)
116. M. Osawa, K. Hanada, H. Hamada, and H. Nakauchi Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell Science 273 1996 242 245 (Pubitemid 26285891)
117. C. Owen, M. Barnett, and J. Fitzgibbon Familial myelodysplasia and acute myeloid leukaemia-a review Br. J. Haematol. 140 2008 123 132 (Pubitemid 350265048)
118. K.V. Pajcini, N.A. Speck, and W.S. Pear Notch signaling in mammalian hematopoietic stem cells Leukemia 25 2011 1525 1532
119. B.L. Pike, and W.A. Robinson Human bone marrow colony growth in agar-gel J. Cell. Physiol. 76 1970 77 84
120. J.A. Prieyl, and T.W. LeBien Interleukin 7 independent development of human B cells Proc. Natl. Acad. Sci. USA 93 1996 10348 10353 (Pubitemid 26314625)
121. A. Puel, S.F. Ziegler, R.H. Buckley, and W.J. Leonard Defective IL7R expression in T(-)B(+)NK(+) severe combined immunodeficiency Nat. Genet. 20 1998 394 397 (Pubitemid 28541642)
122. M. Ramalho-Santos, S. Yoon, Y. Matsuzaki, R.C. Mulligan, and D.A. Melton "Stemness": transcriptional profiling of embryonic and adult stem cells Science 298 2002 597 600 (Pubitemid 35215313)
123. A. Raya, I. Rodriguez-Piza, G. Guenechea, R. Vassena, S. Navarro, M.J. Barrero, A. Consiglio, M. Castella, P. Rio, and E. Sleep Disease-corrected haematopoietic progenitors from Fanconi anaemia induced pluripotent stem cells Nature 460 2009 53 59
124. K. Raymond, M.A. Deugnier, M.M. Faraldo, and M.A. Glukhova Adhesion within the stem cell niches Curr. Opin. Cell Biol. 21 2009 623 629
125. T. Reya, S.J. Morrison, M.F. Clarke, and I.L. Weissman Stem cells, cancer, and cancer stem cells Nature 414 2001 105 111 (Pubitemid 33041634)
126. T. Reya, A.W. Duncan, L. Ailles, J. Domen, D.C. Scherer, K. Willert, L. Hintz, R. Nusse, and I.L. Weissman A role for Wnt signalling in self-renewal of haematopoietic stem cells Nature 423 2003 409 414 (Pubitemid 36626987)
127. L.I. Richie Ehrlich, T. Serwold, and I.L. Weissman In vitro assays misrepresent in vivo lineage potentials of murine lymphoid progenitors Blood 117 2011 2618 2624
128. A. Rizo, B. Dontje, E. Vellenga, G. de Haan, and J.J. Schuringa Long-term maintenance of human hematopoietic stem/progenitor cells by expression of BMI1 Blood 111 2008 2621 2630
129. A. Rizo, S. Olthof, L. Han, E. Vellenga, G. de Haan, and J.J. Schuringa Repression of BMI1 in normal and leukemic human CD34(+) cells impairs self-renewal and induces apoptosis Blood 114 2009 1498 1505
130. N.P. Rodrigues, V. Janzen, R. Forkert, D.M. Dombkowski, A.S. Boyd, S.H. Orkin, T. Enver, P. Vyas, and D.T. Scadden Haploinsufficiency of GATA-2 perturbs adult hematopoietic stem-cell homeostasis Blood 106 2005 477 484 (Pubitemid 40981241)
131. A. Rongvaux, T. Willinger, H. Takizawa, C. Rathinam, W. Auerbach, A.J. Murphy, D.M. Valenzuela, G.D. Yancopoulos, E.E. Eynon, and S. Stevens Human thrombopoietin knockin mice efficiently support human hematopoiesis in vivo Proc. Natl. Acad. Sci. USA 108 2011 2378 2383
132. M.I. Rossi, T. Yokota, K.L. Medina, K.P. Garrett, P.C. Comp, A.H. Schipul Jr., and P.W. Kincade B lymphopoiesis is active throughout human life, but there are developmental age-related changes Blood 101 2003 576 584 (Pubitemid 36077580)
133. D.J. Rossi, C.H. Jamieson, and I.L. Weissman Stems cells and the pathways to aging and cancer Cell 132 2008 681 696 (Pubitemid 351253688)
134. R. Sakai, T. Kajiume, H. Inoue, R. Kanno, M. Miyazaki, Y. Ninomiya, and M. Kanno TCDD treatment eliminates the long-term reconstitution activity of hematopoietic stem cells Toxicol. Sci. 72 2003 84 91 (Pubitemid 36336437)
135. K. Sakamoto, S. Yamaguchi, R. Ando, A. Miyawaki, Y. Kabasawa, M. Takagi, C.L. Li, B. Perbal, and K. Katsube The nephroblastoma overexpressed gene (NOV/ccn3) protein associates with Notch1 extracellular domain and inhibits myoblast differentiation via Notch signaling pathway J. Biol. Chem. 277 2002 29399 29405 (Pubitemid 41079223)
136. V.G. Sankaran, J. Xu, T. Ragoczy, G.C. Ippolito, C.R. Walkley, S.D. Maika, Y. Fujiwara, M. Ito, M. Groudine, and M.A. Bender Developmental and species-divergent globin switching are driven by BCL11A Nature 460 2009 1093 1097
137. N. Saran, M. Lyszkiewicz, J. Pommerencke, K. Witzlau, R. Vakilzadeh, M. Ballmaier, H. von Boehmer, and A. Krueger Multiple extrathymic precursors contribute to T-cell development with different kinetics Blood 115 2010 1137 1144
138. S.M. Schlenner, V. Madan, K. Busch, A. Tietz, C. Laufle, C. Costa, C. Blum, H.J. Fehling, and H.R. Rodewald Fate mapping reveals separate origins of T cells and myeloid lineages in the thymus Immunity 32 2010 426 436
139. J.J. Schuringa, and E. Vellenga Role of the polycomb group gene BMI1 in normal and leukemic hematopoietic stem and progenitor cells Curr. Opin. Hematol. 17 2010 294 299
140. M. Schwieger, J. Lohler, M. Fischer, U. Herwig, D.G. Tenen, and C. Stocking A dominant-negative mutant of C/EBPalpha, associated with acute myeloid leukemias, inhibits differentiation of myeloid and erythroid progenitors of man but not mouse Blood 103 2004 2744 2752 (Pubitemid 38393033)
141. B.E. Shepherd, P. Guttorp, P.M. Lansdorp, and J.L. Abkowitz Estimating human hematopoietic stem cell kinetics using granulocyte telomere lengths Exp. Hematol. 32 2004 1040 1050 (Pubitemid 39469927)
142. F. Shojaei, J. Trowbridge, L. Gallacher, L. Yuefei, D. Goodale, F. Karanu, K. Levac, and M. Bhatia Hierarchical and ontogenic positions serve to define the molecular basis of human hematopoietic stem cell behavior Dev. Cell 8 2005 651 663 (Pubitemid 40585289)
143. K. Shortman, and S.H. Naik Steady-state and inflammatory dendritic-cell development Nat. Rev. Immunol. 7 2007 19 30 (Pubitemid 46020824)
144. L. Shultz, P. Schweitzer, S. Christianson, B. Gott, I. Schweitzer, B. Tennent, S. McKenna, L. Mobraaten, T. Rajan, and D. Greiner Multiple defects in innate and adaptive immunological function in NOD/LtSz-scid mice J. Immunol. 154 1995 180 191
145. L.D. Shultz, B.L. Lyons, L.M. Burzenski, B. Gott, X. Chen, S. Chaleff, M. Kotb, S.D. Gillies, M. King, and J. Mangada Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells J. Immunol. 174 2005 6477 6489 (Pubitemid 40663843)
146. L.D. Shultz, F. Ishikawa, and D.L. Greiner Humanized mice in translational biomedical research Nat. Rev. Immunol. 7 2007 118 130 (Pubitemid 46174859)
147. E. Sitnicka, N. Buza-Vidas, S. Larsson, J.M. Nygren, K. Liuba, and S.E. Jacobsen Human CD34+ hematopoietic stem cells capable of multilineage engrafting NOD/SCID mice express flt3: distinct flt3 and c-kit expression and response patterns on mouse and candidate human hematopoietic stem cells Blood 102 2003 881 886 (Pubitemid 36917779)
148. E.M. Six, D. Bonhomme, M. Monteiro, K. Beldjord, M. Jurkowska, C. Cordier-Garcia, A. Garrigue, L. Dal Cortivo, B. Rocha, and A. Fischer A human postnatal lymphoid progenitor capable of circulating and seeding the thymus J. Exp. Med. 204 2007 3085 3093
149. G.J. Spangrude, S. Heimfeld, and I.L. Weissman Purification and characterization of mouse hematopoietic stem cells Science 241 1988 58 62
150. J. Stingl, C.J. Eaves, U. Kuusk, and J.T. Emerman Phenotypic and functional characterization in vitro of a multipotent epithelial cell present in the normal adult human breast Differentiation 63 1998 201 213 (Pubitemid 28428734)
151. H. Sutherland, C. Eaves, A. Eaves, W. Dragowska, and P. Lansdorp Characterization and partial purification of human marrow cells capable of initiating long-term hematopoiesis in vitro Blood 74 1989 1563 1570 (Pubitemid 19251530)
152. H.J. Sutherland, C.J. Eaves, P.M. Lansdorp, J.D. Thacker, and D.E. Hogge Differential regulation of primitive human hematopoietic cells in long-term cultures maintained on genetically engineered murine stromal cells Blood 78 1991 666 672
153. K. Takenaka, T.K. Prasolava, J.C. Wang, S.M. Mortin-Toth, S. Khalouei, O.I. Gan, J.E. Dick, and J.S. Danska Polymorphism in Sirpa modulates engraftment of human hematopoietic stem cells Nat. Immunol. 8 2007 1313 1323 (Pubitemid 350138972)
154. D.G. Tenen Disruption of differentiation in human cancer: AML shows the way Nat. Rev. Cancer 3 2003 89 101 (Pubitemid 37328876)
155. J.E. Till, and E.A. McCulloch A direct measurement of the radiation sensitivity of normal mouse bone marrow cells Radiat. Res. 14 1961 213 222
156. J.E. Till, E.A. McCulloch, and L. Siminovitch A Stochastic Model of Stem Cell Proliferation Based on the Growth of Spleen Colony-Forming Cells Proc. Natl. Acad. Sci. USA 51 1964 29 36
157. J.J. Trowbridge, A. Xenocostas, R.T. Moon, and M. Bhatia Glycogen synthase kinase-3 is an in vivo regulator of hematopoietic stem cell repopulation Nat. Med. 12 2006 89 98 (Pubitemid 43050082)
158. F.Y. Tsai, and S.H. Orkin Transcription factor GATA-2 is required for proliferation/survival of early hematopoietic cells and mast cell formation, but not for erythroid and myeloid terminal differentiation Blood 89 1997 3636 3643 (Pubitemid 27227086)
159. L.T. van der Meer, J.H. Jansen, and B.A. van der Reijden Gfi1 and Gfi1b: key regulators of hematopoiesis Leukemia 24 2010 1834 1843
160. R. van Furth, and Z.A. Cohn The origin and kinetics of mononuclear phagocytes J. Exp. Med. 128 1968 415 435
161. B. Varnum-Finney, L. Xu, C. Brashem-Stein, C. Nourigat, D. Flowers, S. Bakkour, W.S. Pear, and I.D. Bernstein Pluripotent, cytokine-dependent, hematopoietic stem cells are immortalized by constitutive Notch1 signaling Nat. Med. 6 2000 1278 1281
162. D.C. Vinh, S.Y. Patel, G. Uzel, V.L. Anderson, A.F. Freeman, K.N. Olivier, C. Spalding, S. Hughes, S. Pittaluga, and M. Raffeld Autosomal dominant and sporadic monocytopenia with susceptibility to mycobacteria, fungi, papillomaviruses, and myelodysplasia Blood 115 2010 1519 1529
163. W. Vogel, S. Scheding, L. Kanz, and W. Brugger Clinical applications of CD34(+) peripheral blood progenitor cells (PBPC) Stem Cells 18 2000 87 92 (Pubitemid 30176802)
164. H. Wada, K. Masuda, R. Satoh, K. Kakugawa, T. Ikawa, Y. Katsura, and H. Kawamoto Adult T-cell progenitors retain myeloid potential Nature 452 2008 768 772 (Pubitemid 351521082)
165. J.C. Wang, M. Doedens, and J.E. Dick Primitive human hematopoietic cells are enriched in cord blood compared with adult bone marrow or mobilized peripheral blood as measured by the quantitative in vivo SCID-repopulating cell assay Blood 89 1997 3919 3924 (Pubitemid 27220934)
166. L. Wang, P. Menendez, F. Shojaei, L. Li, F. Mazurier, J.E. Dick, C. Cerdan, K. Levac, and M. Bhatia Generation of hematopoietic repopulating cells from human embryonic stem cells independent of ectopic HOXB4 expression J. Exp. Med. 201 2005 1603 1614 (Pubitemid 40721004)
167. J. Wei, M. Wunderlich, C. Fox, S. Alvarez, J.C. Cigudosa, J.S. Wilhelm, Y. Zheng, J.A. Cancelas, Y. Gu, and M. Jansen Microenvironment determines lineage fate in a human model of MLL-AF9 leukemia Cancer Cell 13 2008 483 495 (Pubitemid 351763903)
168. R.S. Welner, R. Pelayo, and P.W. Kincade Evolving views on the genealogy of B cells Nat. Rev. Immunol. 8 2008 95 106 (Pubitemid 351161301)
169. A.P. Weng, A.A. Ferrando, W. Lee, J.P.t. Morris, L.B. Silverman, C. Sanchez-Irizarry, S.C. Blacklow, A.T. Look, and J.C. Aster Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia Science 306 2004 269 271 (Pubitemid 39336870)
170. T. Willinger, A. Rongvaux, T. Strowig, M.G. Manz, and R.A. Flavell Improving human hemato-lymphoid-system mice by cytokine knock-in gene replacement Trends Immunol. 32 2011 321 327
171. A. Wilson, E. Laurenti, G. Oser, R.C. van der Wath, W. Blanco-Bose, M. Jaworski, S. Offner, C.F. Dunant, L. Eshkind, and E. Bockamp Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair Cell 135 2008 1118 1129
172. C.C. Zhang, M. Kaba, S. Iizuka, H. Huynh, and H.F. Lodish Angiopoietin-like 5 and IGFBP2 stimulate ex vivo expansion of human cord blood hematopoietic stem cells as assayed by NOD/SCID transplantation Blood 111 2008 3415 3423