New light on the biology and developmental potential of haematopoietic stem cells and progenitor cells

Journal of Internal Medicine

Volumn 266, Issue 4, 2009, Pages 311-324

  Sigvardsson, M ^a,b  

^a Experimental Hematology   (Sweden)

^b LINKÖPING UNIVERSITY   (Sweden)

Author keywords

Blood cells; Development; Hematopoiesis; Stem cells

Indexed keywords

BLOOD CELL; BONE MARROW; CELL DIVISION; CELL LINEAGE; CELL MATURATION; CELL THERAPY; CONFERENCE PAPER; EPIGENETICS; HEMATOLOGIC DISEASE; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; MULTIPOTENT STEM CELL; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SOMATIC CELL; STEM CELL; STEM CELL TRANSPLANTATION;

ANIMALS; BONE MARROW CELLS; GENE THERAPY; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HUMANS; STEM CELLS;

EID: 70349223032     PISSN: 09546820     EISSN: 13652796     Source Type: Journal    
DOI: 10.1111/j.1365-2796.2009.02154.x     Document Type: Conference Paper

References (141)

1. Ogawa M. Differentiation and proliferation of hematopoietic stem cells. Blood 1993 81 : 2844 2853.
2. Lorenz E, Uphoff D, Reid TR, Shelton E. Modification of irradiation injury in mice and guinea pigs by bone marrow injections. J Natl Cancer Inst 1951 12 : 197 201.
3. Becker AJ, McCulloch CE, Till JE. Cytological demonstration of the clonal nature of spleen colonies derived from transplanted mouse marrow cells. Nature 1963 197 : 452 454.
4. Till JE, McCulloch CE. A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res 1961 14 : 213 222.
5. Juraskova V, Tkadlecek L. Character of primary and secondary colonies of haematopoiesis in the spleen of irradiated mice. Nature 1965 206 : 951 952.
6. Jones RJ, Wagner JE, Celano P, Zicha MS, Sharkis SJ. Separation of pluripotent haematopoietic stem cells from spleen colony-forming cells. Nature 1990 347 : 188 189.
7. Lemischka IR, Raulet DH, Mulligan RC. Developmental potential and dynamic behavior of hematopoietic stem cells. Cell 1986 45 : 917 927.
8. Keller G, Paige C, Gilboa E, Wagner EF. Expression of a foreign gene in myeloid and lymphoid cells derived from multipotent haematopoietic precursors. Nature 1985 318 : 149 154.
9. Dick JE, Magli MC, Huszar D, Phillips RA, Bernstein A. Introduction of a selectable gene into primitive stem cells capable of long-term reconstitution of the hemopoietic system of W/Wv mice. Cell 1985 42 : 71 9.
10. Smith LG, Weissman IL, Heimfeld S. Clonal analysis of hematopoietic stem-cell differentiation in vivo. Proc Natl Acad Sci U S A 1991 88 : 2788 2792.
11. Wagers AJ, Weissman IL. Plasticity of adult stem cells. Cell 2004 116 : 639 648.
12. Nygren JM, Liuba K, Breitbach M et al. Myeloid and lymphoid contribution to non-haematopoietic lineages through irradiation-induced heterotypic cell fusion. Nat Cell Biol 2008 10 : 584 592.
13. Bradford GB, Williams B, Rossi R, Bertoncello I. Quiescence, cycling, and turnover in the primitive hematopoietic stem cell compartment. Exp Hematol 1997 25 : 445 453.
14. Cheshier SH, Morrison SJ, Liao X, Weissman IL. In vivo proliferation and cell cycle kinetics of long-term self-renewing hematopoietic stem cells. Proc Natl Acad Sci U S A 1999 96 : 3120 3125.
15. Wilson A, Laurenti E, Oser G et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 2008 135 : 1118 1129.
16. Zhang J, Niu C, Ye L et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003 425 : 836 841.
17. Xie Y, Yin T, Wiegraebe W et al. Detection of functional haematopoietic stem cell niche using real-time imaging. Nature 2009 457 : 97 101.
18. Lo Celso C, Fleming HE, Wu JW et al. Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature 2009 457 : 92 6.
19. Wilson A, Trumpp A. Bone-marrow haematopoietic-stem-cell niches. Nat Rev Immunol 2006 6 : 93 106.
20. Rizo A, Vellenga E, de Haan G, Schuringa JJ. Signaling pathways in self-renewing hematopoietic and leukemic stem cells: do all stem cells need a niche? Hum Mol Genet 2006 15 : R210 9.
21. Tothova Z, Kollipara R, Huntly BJ et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 2007 128 : 325 339.
22. Ito K, Hirao A, Arai F et al. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat Med 2006 12 : 446 451.
23. Parmar K, Mauch P, Vergilio JA, Sackstein R, Down JD. Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci U S A 2007 104 : 5431 5436.
24. Kiel MJ, Yilmaz OH, Iwashita T, Yilmaz OH, Terhorst C, Morrison SJ. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 2005 121 : 1109 1121.
25. Kopp HG, Avecilla ST, Hooper AT, Rafii S. The bone marrow vascular niche: home of HSC differentiation and mobilization. Physiology (Bethesda) 2005 20 : 349 356.
26. Morrison SJ, Uchida N, Weissman IL. The biology of hematopoietic stem cells. Annu Rev Cell Dev Biol 1995 11 : 35 71.
27. Cumano A, Godin I. Pluripotent hematopoietic stem cell development during embryogenesis. Curr Opin Immunol 2001 13 : 166 171.
28. Cumano A, Ferraz JC, Klaine M, Di Santo JP, Godin I. Intraembryonic, but not yolk sac hematopoietic precursors, isolated before circulation, provide long-term multilineage reconstitution. Immunity 2001 15 : 477 485.
29. Medvinsky A, Dzierzak E. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 1996 86 : 897 906.
30. Moore MA, Metcalf D. Ontogeny of the haemopoietic system: yolk sac origin of in vivo and in vitro colony forming cells in the developing mouse embryo. Br J Haematol 1970 18 : 279 296.
31. Samokhvalov IM, Samokhvalova NI, Nishikawa S. Cell tracing shows the contribution of the yolk sac to adult haematopoiesis. Nature 2007 446 : 1056 1061.
32. Ueno H, Weissman IL. Stem cells: blood lines from embryo to adult. Nature 2007 446 : 996 997.
33. Palis J, Chan RJ, Koniski A, Patel R, Starr M, Yoder MC. Spatial and temporal emergence of high proliferative potential hematopoietic precursors during murine embryogenesis. Proc Natl Acad Sci U S A 2001 98 : 4528 4533.
34. Godin I, Garcia-Porrero JA, Dieterlen-Lievre F, Cumano A. Stem cell emergence and hemopoietic activity are incompatible in mouse intraembryonic sites. J Exp Med 1999 190 : 43 52.
35. Dieterlen-Lievre F. On the origin of haemopoietic stem cells in the avian embryo: an experimental approach. J Embryol Exp Morphol 1975 33 : 607 619.
36. Alvarez-Silva M, Belo-Diabangouaya P, Salaun J, Dieterlen-Lievre F. Mouse placenta is a major hematopoietic organ. Development 2003 130 : 5437 5444.
37. Ottersbach K, Dzierzak E. The murine placenta contains hematopoietic stem cells within the vascular labyrinth region. Dev Cell 2005 8 : 377 387.
38. Gekas C, Dieterlen-Lievre F, Orkin SH, Mikkola HK. The placenta is a niche for hematopoietic stem cells. Dev Cell 2005 8 : 365 375. (Pubitemid 40309807)
39. Rossi DJ, Jamieson CH, Weissman IL. Stems cells and the pathways to aging and cancer. Cell 2008 132 : 681 696.
40. Rossi DJ, Bryder D, Weissman IL. Hematopoietic stem cell aging: mechanism and consequence. Exp Gerontol 2007 42 : 385 390.
41. Bryder D, Rossi DJ, Weissman IL. Hematopoietic stem cells: the paradigmatic tissue-specific stem cell. Am J Pathol 2006 169 : 338 346.
42. Pronk CJ, Attema J, Rossi DJ, Sigvardsson M, Bryder D. Deciphering developmental stages of adult myelopoiesis. Cell Cycle 2008 7 : 706 713.
43. Dick JE, Bhatia M, Gan O, Kapp U, Wang JC. Assay of human stem cells by repopulation of NOD/SCID mice. Stem Cells 1997 15 (Suppl. 1 199 204.
44. - population. Blood 2007 109 : 543 545.
45. Ikuta K, Weissman IL. Evidence that hematopoietic stem cells express mouse c-kit but do not depend on steel factor for their generation. Proc Natl Acad Sci U S A 1992 89 : 1502 1506.
46. Li CL, Johnson GR. Murine hematopoietic stem and progenitor cells: I. Enrichment and biologic characterization. Blood 1995 85 : 1472 1479.
47. Chen CZ, Li M, de Graaf D et al. Identification of endoglin as a functional marker that defines long-term repopulating hematopoietic stem cells. Proc Natl Acad Sci U S A 2002 99 : 15468 15473.
48. Spangrude GJ, Heimfeld S, Weissman IL. Purification and characterization of mouse hematopoietic stem cells. Science 1988 241 : 58 62.
49. Osawa M, Hanada K, Hamada H, Nakauchi H. Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 1996 273 : 242 245. (Pubitemid 26285891)
50. Christensen JL, Weissman IL. Flk-2 is a marker in hematopoietic stem cell differentiation: a simple method to isolate long-term stem cells. Proc Natl Acad Sci U S A 2001 98 : 14541 14546.
51. Adolfsson J, Borge OJ, Bryder D et al. Upregulation of Flt3 expression within the bone marrow Lin(-)Sca1(+)c-kit(+) stem cell compartment is accompanied by loss of self-renewal capacity. Immunity 2001 15 : 659 669. (Pubitemid 33016450)
52. Wolf NS, Kone A, Priestley GV, Bartelmez SH. In vivo and in vitro characterization of long-term repopulating primitive hematopoietic cells isolated by sequential Hoechst 33342-rhodamine 123 FACS selection. Exp Hematol 1993 21 : 614 622.
53. Akashi K, Traver D, Miyamoto T, Weissman IL. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 2000 404 : 193 197.
54. Kondo M, Weissman IL, Akashi K. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 1997 91 : 661 672.
55. + lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell 2005 121 : 295 306.
56. Arinobo Y, Mizuno S, Chong Y et al. Reciprocal activation of Gata-1 and PU.1 marks initial specification of hematopoietic stem cells into myeloerythroid and myelolymphoid lineages. Cell Stem Cell 2007 1 : 416 427.
57. Nutt SL, Metcalf D, D'Amico A, Polli M, Wu L. Dynamic regulation of PU.1 expression in multipotent hematopoietic progenitors. J Exp Med 2005 201 : 221 231.
58. Yoshida T, Ng SY, Zuniga-Pflucker JC, Georgopoulos K. Early hematopoietic lineage restrictions directed by Ikaros. Nat Immunol 2006 7 : 382 391.
59. Hartenstein V. Blood cells and blood cell development in the animal kingdom. Annu Rev Cell Dev Biol 2006 22 : 677 712.
60. Harrison F, De vos L. Microscopic anatomy of Invertebrates-Porifera. New York : Wiley, 1991 2 : 29 90.
61. Miller MA, Technau U, Smith KM, Steele RE. Oocyte development in Hydra involves selection from competent precursor cells. Dev Biol 2000 224 : 326 338.
62. Bode HR The interstitial cell lineage of hydra: a stem cell system that arose early in evolution. J Cell Sci 1996 109 (Pt 6 1155 1164.
63. Theopold U, Li D, Fabbri M, Scherfer C, Schmidt O. The coagulation of insect hemolymph. Cell Mol Life Sci 2002 59 : 363 372.
64. Kanost MR, Jiang H, Yu XQ. Innate immune responses of a lepidopteran insect, Manduca sexta. Immunol Rev 2004 198 : 97 105.
65. + multipotent hematopoietic progenitors. Cell 2006 126 : 415 426.
66. Pronk C, Rossi D, Månsson R et al. Elucidation of the phenotype, functional, and molecular topography of a myeloerythroid progenitor cell hierarchy. Cell Stem Cell 2007 1 : 428 442.
67. Mansson R, Hultquist A, Luc S et al. Molecular evidence for hierarchical transcriptional lineage priming in fetal and adult stem cells and multipotent progenitors. Immunity 2007 26 : 407 419.
68. Igarashi H, Gregory SC, Yokota T, Sakaguchi N, Kincade PW. Transcription from the RAG1 locus marks the earliest lymphocyte progenitors in bone marrow. Immunity 2002 17 : 117 130.
69. Krueger A, von Boehmer H. Identification of a T lineage-committed progenitor in adult blood. Immunity 2007 26 : 105 116.
70. Mansson R, Zandi S, Andersson K et al. B-lineage commitment prior to surface expression of B220 and CD19 on hematopoietic progenitor cells. Blood 2008 112 : 1048 1055.
71. Dias S, Mansson R, Gurbuxani S, Sigvardsson M, Kee BL. E2A proteins promote development of lymphoid-primed multipotent progenitors. Immunity 2008 29 : 217 227.
72. Allman D, Sambandam A, Kim S et al. Thymopoiesis independent of common lymphoid progenitors. Nat Immunol 2003 4 : 168 174.
73. Mansson R, Zandi S, Anderson K et al. B-lineage commitment prior to surface expression of B220 and CD19 on hematopoietic progenitor cells. Blood 2008 112 : 1048 1055.
74. Morrison SJ, Kimble J. Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 2006 441 : 1068 1074.
75. Attar EC, Scadden DT. Regulation of hematopoietic stem cell growth. Leukemia 2004 18 : 1760 1768.
76. Wu H, Liu X, Jaenisch R, Lodish HF. Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell 1995 83 : 59 67.
77. Lieschke GJ, Grail D, Hodgson G et al. Mice lacking granulocyte colony-stimulating factor have chronic neutropenia, granulocyte and macrophage progenitor cell deficiency, and impaired neutrophil mobilization. Blood 1994 84 : 1737 1746.
78. Stanley E, Lieschke GJ, Grail D et al. Granulocyte/macrophage colony-stimulating factor-deficient mice show no major perturbation of hematopoiesis but develop a characteristic pulmonary pathology. Proc Natl Acad Sci U S A 1994 91 : 5592 5596.
79. Seymour JF, Lieschke GJ, Grail D, Quilici C, Hodgson G, Dunn AR. Mice lacking both granulocyte colony-stimulating factor (CSF) and granulocyte-macrophage CSF have impaired reproductive capacity, perturbed neonatal granulopoiesis, lung disease, amyloidosis, and reduced long-term survival. Blood 1997 90 : 3037 3049.
80. Lieschke GJ, Stanley E, Grail D et al. Mice lacking both macrophage- and granulocyte-macrophage colony-stimulating factor have macrophages and coexistent osteopetrosis and severe lung disease. Blood 1994 84 : 27 35.
81. McArthur GA, Rohrschneider LR, Johnson GR. Induced expression of c-fms in normal hematopoietic cells shows evidence for both conservation and lineage restriction of signal transduction in response to macrophage colony-stimulating factor. Blood 1994 83 : 972 981.
82. Pharr PN, Ogawa M, Hofbauer A, Longmore GD. Expression of an activated erythropoietin or a colony-stimulating factor 1 receptor by pluripotent progenitors enhances colony formation but does not induce differentiation. Proc Natl Acad Sci U S A 1994 91 : 7482 7486.
83. Semerad CL, Poursine-Laurent J, Liu F, Link DC. A role for G-CSF receptor signaling in the regulation of hematopoietic cell function but not lineage commitment or differentiation. Immunity 1999 11 : 153 161.
84. Stoffel R, Ziegler S, Ghilardi N, Ledermann B, de Sauvage FJ, Skoda RC. Permissive role of thrombopoietin and granulocyte colony-stimulating factor receptors in hematopoietic cell fate decisions in vivo. Proc Natl Acad Sci U S A 1999 96 : 698 702.
85. Kondo M, Scherer DC, Miyamoto T et al. Cell-fate conversion of lymphoid-committed progenitors by instructive actions of cytokines. Nature 2000 407 : 383 386.
86. Pui JC, Allman D, Xu L et al. Notch1 expression in early lymphopoiesis influences B versus T lineage determination. Immunity 1999 11 : 299 308.
87. Kondo M, Akashi K, Domen J, Sugamura K, Weissman IL. Bcl-2 rescues T lymphopoiesis, but not B or NK cell development, in common gamma chain-deficient mice. Immunity 1997 7 : 155 162.
88. Fujiwara Y, Browne CP, Cunniff K, Goff SC, Orkin SH. Arrested development of embryonic red cell precursors in mouse embryos lacking transcription factor GATA-1. Proc Natl Acad Sci U S A 1996 93 : 12355 12358.
89. Kitajima K, Zheng J, Yen H, Sugiyama D, Nakano T. Multipotential differentiation ability of GATA-1-null erythroid-committed cells. Genes Dev 2006 20 : 654 659.
90. Iwasaki H, Mizuno S, Wells RA, Cantor AB, Watanabe S, Akashi K. GATA-1 converts lymphoid and myelomonocytic progenitors into the megakaryocyte/ erythrocyte lineages. Immunity 2003 19 : 451 462.
91. Iwasaki H, Mizuno S, Arinobu Y et al. The order of expression of transcription factors directs hierarchical specification of hematopoietic lineages. Genes Dev 2006 20 : 3010 3021.
92. Zhang P, Behre G, Pan J et al. Negative cross-talk between hematopoietic regulators: GATA proteins repress PU.1. Proc Natl Acad Sci U S A 1999 96 : 8705 8710.
93. Nerlov C, Graf T. PU.1 induces myeloid lineage commitment in multipotent hematopoietic progenitors. Genes Dev 1998 12 : 2403 2412.
94. Rekhtman N, Radparvar F, Evans T, Skoultchi AI. Direct interaction of hematopoietic transcription factors PU.1 and GATA-1: functional antagonism in erythroid cells. Genes Dev 1999 13 : 1398 1411.
95. Chen H, Ray-Gallet D, Zhang P et al. PU.1 (Spi-1) autoregulates its expression in myeloid cells. Oncogene 1995 11 : 1549 1560.
96. Kafri T, Ariel M, Brandeis M et al. Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line. Genes Dev 1992 6 : 705 714.
97. Pradhan S, Bacolla A, Wells RD, Roberts RJ. Recombinant human DNA (cytosine-5) methyltransferase. I. Expression, purification, and comparison of de novo and maintenance methylation. J Biol Chem 1999 274 : 33002 33010.
98. Rajasekhar VK, Begemann M. Concise review: roles of polycomb group proteins in development and disease: a stem cell perspective. Stem Cells 2007 25 : 2498 2510.
99. Park IK, Qian D, Kiel M et al. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 2003 423 : 302 305.
100. Iwama A, Oguro H, Negishi M et al. Enhanced self-renewal of hematopoietic stem cells mediated by the polycomb gene product Bmi-1. Immunity 2004 21 : 843 851.
101. Kamminga LM, Bystrykh LV, de Boer A et al. The Polycomb group gene Ezh2 prevents hematopoietic stem cell exhaustion. Blood 2006 107 : 2170 2179.
102. Vire E, Brenner C, Deplus R et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 2006 439 : 871 874.
103. Spivakov M, Fisher AG. Epigenetic signatures of stem-cell identity. Nat Rev Genet 2007 8 : 263 271.
104. Giadrossi S, Dvorkina M, Fisher AG. Chromatin organization and differentiation in embryonic stem cell models. Curr Opin Genet Dev 2007 17 : 132 138.
105. Ahmad K, Henikoff S. The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell 2002 9 : 1191 1200.
106. Meshorer E, Yellajoshula D, George E, Scambler PJ, Brown DT, Misteli T. Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. Dev Cell 2006 10 : 105 116. (Pubitemid 43025681)
107. Bernstein BE, Mikkelsen TS, Xie X et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006 125 : 315 326.
108. Azuara V, Perry P, Sauer S et al. Chromatin signatures of pluripotent cell lines. Nat Cell Biol 2006 8 : 532 538.
109. Attema JL, Papathanasiou P, Forsberg EC, Xu J, Smale ST, Weissman IL. Epigenetic characterization of hematopoietic stem cell differentiation using miniChIP and bisulfite sequencing analysis. Proc Natl Acad Sci U S A 2007 104 : 12371 12376.
110. Cui K, Zang C, Roh TY et al. Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell 2009 4 : 80 93.
111. Hu M, Krause D, Greaves M et al. Multilineage gene expression precedes commitment in the hemopoietic system. Genes Dev 1997 11 : 774 785.
112. Miyamoto T, Iwasaki H, Reizis B et al. Myeloid or lymphoid promiscuity as a critical step in hematopoietic lineage commitment. Dev Cell 2002 3 : 137 147.
113. Ye M, Iwasaki H, Laiosa CV et al. Hematopoietic stem cells expressing the myeloid lysozyme gene retain long-term, multilineage repopulation potential. Immunity 2003 19 : 689 699.
114. Antonchuk J, Sauvageau G, Humphries RK. HOXB4 overexpression mediates very rapid stem cell regeneration and competitive hematopoietic repopulation. Exp Hematol 2001 29 : 1125 1134.
115. Kimura S, Roberts AW, Metcalf D, Alexander WS. Hematopoietic stem cell deficiencies in mice lacking c-Mpl, the receptor for thrombopoietin. Proc Natl Acad Sci U S A 1998 95 : 1195 1200.
116. Solar GP, Kerr WG, Zeigler FC et al. Role of c-mpl in early hematopoiesis. Blood 1998 92 : 4 10.
117. Ema H, Sudo K, Seita J et al. Quantification of self-renewal capacity in single hematopoietic stem cells from normal and Lnk-deficient mice. Dev Cell 2005 8 : 907 914.
118. Buza-Vidas N, Antonchuk J, Qian H et al. Cytokines regulate postnatal hematopoietic stem cell expansion: opposing roles of thrombopoietin and LNK. Genes Dev 2006 20 : 2018 2023.
119. Seita J, Ema H, Ooehara J et al. Lnk negatively regulates self-renewal of hematopoietic stem cells by modifying thrombopoietin-mediated signal transduction. Proc Natl Acad Sci U S A 2007 104 : 2349 2354.
120. Bhatia M, Bonnet D, Wu D et al. Bone morphogenetic proteins regulate the developmental program of human hematopoietic stem cells. J Exp Med 1999 189 : 1139 1148.
121. Singbrant S, Moody JL, Blank U et al. Smad5 is dispensable for adult murine hematopoiesis. Blood 2006 108 : 3707 3712.
122. Sitnicka E, Ruscetti FW, Priestley GV, Wolf NS, Bartelmez SH. Transforming growth factor beta 1 directly and reversibly inhibits the initial cell divisions of long-term repopulating hematopoietic stem cells. Blood 1996 88 : 82 8.
123. Batard P, Monier MN, Fortunel N et al. TGF-(beta)1 maintains hematopoietic immaturity by a reversible negative control of cell cycle and induces CD34 antigen up-modulation. J Cell Sci 2000 113 (Pt 3 383 390.
124. Leveen P, Larsson J, Ehinger M et al. Induced disruption of the transforming growth factor beta type II receptor gene in mice causes a lethal inflammatory disorder that is transplantable. Blood 2002 100 : 560 568.
125. Yaswen L, Kulkarni AB, Fredrickson T et al. Autoimmune manifestations in the transforming growth factor-beta 1 knockout mouse. Blood 1996 87 : 1439 1445.
126. Larsson J, Blank U, Klintman J, Magnusson M, Karlsson S. Quiescence of hematopoietic stem cells and maintenance of the stem cell pool is not dependent on TGF-beta signaling in vivo. Exp Hematol 2005 33 : 592 596.
127. Larsson J, Blank U, Helgadottir H et al. TGF-beta signaling-deficient hematopoietic stem cells have normal self-renewal and regenerative ability in vivo despite increased proliferative capacity in vitro. Blood 2003 102 : 3129 3135.
128. Karanu FN, Murdoch B, Miyabayashi T et al. Human homologues of Delta-1 and Delta-4 function as mitogenic regulators of primitive human hematopoietic cells. Blood 2001 97 : 1960 1967. (Pubitemid 32239074)
129. Karanu FN, Murdoch B, Gallacher L et al. The notch ligand jagged-1 represents a novel growth factor of human hematopoietic stem cells. J Exp Med 2000 192 : 1365 1372.
130. Varnum-Finney B, Brashem-Stein C, Bernstein ID. Combined effects of Notch signaling and cytokines induce a multiple log increase in precursors with lymphoid and myeloid reconstituting ability. Blood 2003 101 : 1784 1789.
131. Calvi LM, Adams GB, Weibrecht KW et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003 425 : 841 846.
132. Maillard I, Koch U, Dumortier A et al. Canonical notch signaling is dispensable for the maintenance of adult hematopoietic stem cells. Cell Stem Cell 2008 2 : 356 366.
133. Duncan AW, Rattis FM, DiMascio LN et al. Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat Immunol 2005 6 : 314 322.
134. Willert K, Brown JD, Danenberg E et al. Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 2003 423 : 448 452.
135. Austin TW, Solar GP, Ziegler FC, Liem L, Matthews W. A role for the Wnt gene family in hematopoiesis: expansion of multilineage progenitor cells. Blood 1997 89 : 3624 3635.
136. Van Berg Den DJ, Sharma AK, Bruno E, Hoffman R. Role of members of the Wnt gene family in human hematopoiesis. Blood 1998 92 : 3189 3202.
137. Reya T, Duncan AW, Ailles L et al. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 2003 423 : 409 414.
138. Kirstetter P, Anderson K, Porse BT, Jacobsen SE, Nerlov C. Activation of the canonical Wnt pathway leads to loss of hematopoietic stem cell repopulation and multilineage differentiation block. Nat Immunol 2006 7 : 1048 1056.
139. Cobas M, Wilson A, Ernst B et al. Beta-catenin is dispensable for hematopoiesis and lymphopoiesis. J Exp Med 2004 199 : 221 229.
140. Zhang CC, Kaba M, Ge G et al. Angiopoietin-like proteins stimulate ex vivo expansion of hematopoietic stem cells. Nat Med 2006 12 : 240 245.
141. Gupta R, Hong D, Iborra F, Sarno S, Enver T. NOV (CCN3) functions as a regulator of human hematopoietic stem or progenitor cells. Science 2007 316 : 590 593.