BMP4: Its role in development of the hematopoietic system and potential as a hematopoietic growth factor

Stem Cells

Volumn 22, Issue 4, 2004, Pages 457-474

  Sadlon, Timothy J ^a   Lewis, Ian D ^b   D'Andrea, Richard J ^a,c  

^a CHILD HEALTH RESEARCH INSTITUTE   (Australia)

^b INSTITUTE OF MEDICAL AND VETERINARY SCIENCE   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Cytokines; Ex vivo expansion; Hematopoietic development; Hematopoietic stem cells (HSCs); Umbilical cord blood

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; GROWTH FACTOR;

BONE MARROW; BONE MARROW TRANSPLANTATION; CORD BLOOD STEM CELL TRANSPLANTATION; ENDODERM; EX VIVO STUDY; GENE IDENTIFICATION; HEMATOLOGIC MALIGNANCY; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNE DEFICIENCY; IN VIVO STUDY; MESODERM; MESONEPHROS; NONHUMAN; PROTEIN FUNCTION; SHORT SURVEY; UMBILICAL CORD BLOOD; XENOPUS; YOLK SAC;

MAMMALIA;

EID: 3543035189     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.22-4-457     Document Type: Short Survey

References (173)

1. Palis J, Yoder MC. Yolk-sac hematopoiesis: the first blood cells of mouse and man. Exp Hematol 2001; 29:927-936.
2. Marshall CJ, Thrasher AJ. The embryonic origins of human haematopoiesis. Br J Haematol 2001;112: 838-850.
3. Palis J, Robertson S, Kennedy M et al. Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development 1999; 126:5073-5084.
4. Palis J, Chan RJ, Koniski A et al. Spatial and temporal emergence of high proliferative potential hematopoietic precursors during murine embryogenesis. Proc Natl Acad Sci U S A 2001;98:4528-4533.
5. Tavian M, Robin C, Coulombel L et al. The human embryo, but not its yolk sac, generates lymphomyeloid stem cells: mapping multipotent hematopoietic cell fate in intraembryonic mesoderm. Immunity 2001;15:487-495.
6. Tavian M, Hallais MF, Peault B. Emergence of intraembryonic hematopoietic precursors in the pre-liver human embryo. Development 1999;126:793-803.
7. Kumaravelu P, Hook L, Morrison AM et al. Quantitative developmental anatomy of definitive haematopoietic stem cells/long-term repopulating units (HSC/RUs): role of the aorta-gonad-mesonephros (AGM) region and the yolk sac in colonisation of the mouse embryonic liver. Development 2002;129:4891-4899.
8. Johnson GR, Moore MA. Role of stem cell migration in initiation of mouse foetal liver haemopoiesis. Nature 1975;258:726-728.
9. Clapp DW, Freie B, Lee WH et al. Molecular evidence that in situ-transduced fetal liver hematopoietic stem/progenitor cells give rise to medullary hematopoiesis in adult rats. Blood 1995;86:2113-2122.
10. Zanjani ED, Ascensao JL, Tavassoli M. Liver-derived fetal hematopoietic stem cells selectively and preferentially home to the fetal bone marrow. Blood 1993;81: 399-404.
11. Dieterlen-Lièvre F. Hemopoiesis during avian ontogeny. Poultry Sci Rev 1994;5:273-305.
12. Ciau-Uitz A, Walmsley M, Patient R. Distinct origins of adult and embryonic blood in Xenopus. Cell 2000; 102:787-796.
13. Cumano A, Godin I. Pluripotent hematopoietic stem cell development during embryogenesis. Curr Opin Immunol 2001;13:166-171.
14. de Bruijn MF, Speck NA, Peeters MC et al. Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo. EMBO J 2000; 19:2465-2474.
15. + cells throughout ontogeny but display distinct distribution patterns in adult hematopoietic and nonhematopoietic tissues. Blood 2000;95:3113-3124.
16. Godin I, Garcia-Porrero JA, Dieterlen-Lievre F et al. Stem cell emergence and hemopoietic activity are incompatible in mouse intraembryonic sites. J Exp Med 1999;190:43-52.
17. Kyba M, Daley GQ. Hematopoiesis from embryonic stem cells: lessons from and for ontogeny. Exp Hematol 2003;31:994-1006.
18. Godin I, Cumano A. The hare and the tortoise: an embryonic haematopoietic race. Nat Rev Immunol 2002;2:593-604.
19. Cumano A, Ferraz JC, Klaine M et al. Intraembryonic, but not yolk sac hematopoietic precursors, isolated before circulation, provide long-term multilineage reconstitution. Immunity 2001;15:477-485.
20. Cumano A, Dieterlen-Lievre F, Godin I. Lymphoid potential, probed before circulation in mouse, is restricted to caudal intraembryonic splanchnopleura. Cell 1996;86:907-916.
21. Nishikawa SI, Nishikawa S, Kawamoto H et al. In vitro generation of lymphohematopoietic cells from endothelial cells purified from murine embryos. Immunity 1998;8:761-769.
22. Matsuoka S, Tsuji K, Hisakawa H et al. Generation of definitive hematopoietic stem cells from murine early yolk sac and paraaortic splanchnopleures by aortagonad-mesonephros region-derived stromal cells. Blood 2001;98:6-12.
23. Yoder MC, Hiatt K, Dutt P et al. Characterization of definitive lymphohematopoietic stem cells in the day 9 murine yolk sac. Immunity 1997;7:335-344.
24. Yoder MC, Hiatt K, Mukherjee P. In vivo repopulating hematopoietic stem cells are present in the murine yolk sac at day 9.0 postcoitus. Proc Natl Acad Sci U S A 1997;94:6776-6780.
25. Yoder MC, Hiatt K. Engraftment of embryonic hematopoietic cells in conditioned newborn recipients. Blood 1997;89:2176-2183.
26. Orkin SH, Zon LI. Hematopoiesis and stem cells: plasticity versus developmental heterogeneity. Nat Immunol 2002;3:323-328.
27. Tam PP, Behringer RR. Mouse gastrulation: the formation of a mammalian body plan. Mech Dev 1997; 68:3-25.
28. Marshall CJ, Moore RL, Thorogood P et al. Detailed characterization of the human aorta-gonad-meso-nephros region reveals morphological polarity resembling a hematopoietic stromal layer. Dev Dyn 1999; 215:139-147.
29. Manaia A, Lemarchandel V, Klaine M et al. Lm02 and GATA-3 associated expression in intraembryonic hemogenic sites. Development 2000;127:643-653.
30. Garcia-Porrero JA, Manaia A, Jimeno J et al. Antigenic profiles of endothelial and hemopoietic lineages in murine intraembryonic hemogenic sites. Dev Comp Immunol 1998;22:303-319.
31. Shalaby F, Ho J, Stanford WL et al. A requirement for Flk 1 in primitive and definitive hematopoiesis and vasculogenesis. Cell 1997;89:981-990.
32. Carmeliet P, Ferreira V, Breier G et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996;380:435-439.
33. Lacaud G, Robertson S, Palis J et al. Regulation of hemangioblast development. Ann N Y Acad Sci 2001; 938:96-107.
34. Sabin FR. Preliminary note on the differentiation of angioblasts and the method by which they produce blood-vessels, blood-plasma and red blood-cells as seen in the living chick. J Hematother Stem Cell Res 2002;11:5-7.
35. Choi K. The hemangioblast: a common progenitor of hematopoietic and endothelial cells. J Hematother Stem Cell Res 2002;11:91-101.
36. Dang SM, Kyba M, Perlingeiro R et al. Efficiency of embryoid body formation and hematopoietic development from embryonic stem cells in different culture systems. Biotechnol Bioeng 2002;78:442-453.
37. Kennedy M, Firpo M, Choi K et al. A common precursor for primitive erythropoiesis and definitive haematopoiesis. Nature 1997;386:488-493.
38. Choi K, Kennedy M, Kazarov A et al. A common precursor for hematopoietic and endothelial cells. Development 1998;125:725-732.
39. Labastie MC, Cortes F, Romeo PH et al. Molecular identity of hematopoietic precursor cells emerging in the human embryo. Blood 1998;92:3624-3635.
40. North TE, de Bruijn MF, Stacy T et al. Runx1 expression marks long-term repopulating hematopoietic stem cells in the midgestation mouse embryo. Immunity 2002;16:661-672.
41. North T, Gu TL, Stacy T et al. Cbfa2 is required for the formation of intra-aortic hematopoietic clusters. Development 1999;126:2563-2575.
42. Takakura N, Huang XL, Naruse T et al. Critical role of the TIE2 endothelial cell receptor in the development of definitive hematopoiesis. Immunity 1998; 9:677-686.
43. Jaffredo T, Gautier R, Brajeul V et al. Tracing the progeny of the aortic hemangioblast in the avian embryo. Dev Biol 2000;224:204-214.
44. Jaffredo T, Gautier R, Eichmann A et al. Intraaortic hemopoietic cells are derived from endothelial cells during ontogeny. Development 1998;125:4575-4583.
45. de Bruijn MF, Ma X, Robin C et al. Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta. Immunity 2002;16:673-6837.
46. Oberlin E, Tavian M, Blazsek I et al. Blood-forming potential of vascular endothelium in the human embryo. Development 2002;129:4147-4157.
47. + cells at a diverging point of endothelial and hemopoietic lineages. Development 1998;125:1747-1757.
48. Fujimoto T, Ogawa M, Minegishi N et al. Step-wise divergence of primitive and definitive haematopoietic and endothelial cell lineages during embryonic stem cell differentiation. Genes Cells 2001;6:1113-1127.
49. Sugiyama D, Ogawa M, Hirose I et al. Erythropoiesis from acetyl LDL incorporating endothelial cells at the pre-liver stage. Blood 2003;101:4733-4738.
50. Davidson AJ, Zon LI. Turning mesoderm into blood: the formation of hematopoietic stem cells during embryogenesis. Curr Top Dev Biol 2000;50:45-60.
51. Wiles MV, Johansson BM. Analysis of factors controlling primary germ layer formation and early hematopoiesis using embryonic stem cell in vitro differentiation. Leukemia 1997;11(suppl 3):454-456.
52. Johansson BM, Wiles MV. Evidence for involvement of activin A and bone morphogenetic protein 4 in mammalian mesoderm and hematopoietic development. Mol Cell Biol 1995;15:141-151.
53. Dale L, Wardle FC. A gradient of BMP activity specifies dorsal-ventral fates in early Xenopus embryos. Semin Cell Dev Biol 1999;10:319-326.
54. Dale L, Jones CM. BMP signaling in early Xenopus development. Bioessays 1999;21:751-760.
55. Zhao GQ. Consequences of knocking out BMP signaling in the mouse. Genesis 2003;35:43-56.
56. Derynck R, Zhang YE. Smad-dependent and Smad-independent pathways in TGF-β family signaling. Nature 2003;425:577-584.
57. Massague J, Blain SW, Lo RS. TGFβ signaling in growth control, cancer, and heritable disorders. Cell 2000;103:295-309.
58. Attisano L, Wrana JL. Signal transduction by the TGF-β superfamily. Science 2002;296:1646-1647.
59. Chang H, Brown CW, Matzuk MM. Genetic analysis of the mammalian transforming growth factor-β superfamily. Endocr Rev 2002;23:787-823.
60. Balemans W, Van Hul W. Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev Biol 2002;250:231-250.
61. Piek E, Heldin CH, Ten Dijke P. Specificity, diversity, and regulation in TGF-β superfamily signaling. FASEB J 1999;13:2105-2124.
62. Miyazawa K, Shinozaki M, Hara T et al. Two major Smad pathways in TGF-β superfamily signaling. Genes Cells 2002;7:1191-1204.
63. Hata A, Lagna G, Massague J et al. Smad6 inhibits BMP/Smad1 signaling by specifically competing with the Smad4 tumor suppressor. Genes Dev 1998;12: 186-197.
64. Hayashi H, Abdollah S, Qiu Y et al. The MAD-related protein Smad7 associates with the TGFβ receptor and functions as an antagonist of TGFβ signaling. Cell 1997;89:1165-1173.
65. Attisano L, Silvestri C, Izzi L et al. The transcriptional role of Smads and FAST (FoxH 1) in TGFβ and activin signaling. Mol Cell Endocrinol 2001;180:3-11.
66. Labbe E, Silvestri C, Hoodless PA et al. Smad2 and Smad3 positively and negatively regulate TGF β-dependent transcription through the forkhead DNA-binding protein FAST2. Mol Cell 1998;2:109-120.
67. Bond HM, Mesuraca M, Carbone E et al. Early hematopoietic zinc finger protein (EHZF), the human homologue to mouse Evi3, is highly expressed in primitive human hematopoietic cells. Blood 2004;103:2062-2070.
68. Hata A, Seoane J, Lagna G et al. OAZ uses distinct DNA- and protein-binding zinc fingers in separate BMP-Smad and Olf signaling pathways. Cell 2000; 100:229-240.
69. Lee HS, Park MJ, Lee SY et al. Transcriptional regulation of Xbr-1a/Xvent-2 homeobox gene: analysis of its promoter region. Biochem Biophys Res Commun 2002;298:815-823.
70. Henningfeld KA, Friedle H, Rastegar S et al. Autoregulation of Xvent-2B; direct interaction and functional cooperation of Xvent-2 and Smad1. J Biol Chem 2002; 277:2097-2103.
71. Miyazono K, Kusanagi K, Inoue H. Divergence and convergence of TGF-β/BMP signaling. J Cell Physiol 2001;187:265-276.
72. Zhang W, Yatskievych TA, Cao X et al. Regulation of Hex gene expression by a Smads-dependent signaling pathway. J Biol Chem 2002;277:45435-45441.
73. Korchynskyi O, Ten Dijke P. Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J Biol Chem 2002; 277:4883-4891.
74. Dennler S, Itoh S, Vivien D et al. Direct binding of Smad3 and Smad4 to critical TGF β-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J 1998;17:3091-3100.
75. Zawel L, Dai JL, Buckhaults P et al. Human Smad3 and Smad4 are sequence-specific transcription activators. Mol Cell 1998;1:611-617.
76. Lane MC, Sheets MD. Rethinking axial patterning in amphibians. Dev Dyn 2002;225:434-447.
77. Agius E, Oelgeschlager M, Wessely O et al. Endodermal Nodal-related signals and mesoderm induction in Xenopus. Development 2000;127:1173-1183.
78. Clements D, Friday RV, Woodland HR. Mode of action of Veg T in mesoderm and endoderm formation. Development 1999;126:4903-4911.
79. Eimon PM, Harland RM. Effects of heterodimerization and proteolytic processing on Derriere and Nodal activity: implications for mesoderm induction in Xenopus. Development 2002;129:3089-3103.
80. Sun BI, Bush SM, Collins-Racie LA et al. derriere: a TGF-β family member required for posterior development in Xenopus. Development 1999;126:1467-1482.
81. Munoz-Sanjuan I, Brivanlou A. Early posterior/ventral fate specification in the vertebrate embryo. Dev Biol 2001;237:1-17.
82. Harland R, Gerhart J. Formation and function of Spemann's organizer. Annu Rev Cell Dev Biol 1997;13: 611-667.
83. Walmsley M, Ciau-Uitz A, Patient R. Adult and embryonic blood and endothelium derive from distinct precursor populations which are differentially programmed by BMP in Xenopus. Development 2002; 129:5683-5695.
84. Kumano G, Belluzzi L, Smith WC. Spatial and temporal properties of ventral blood island induction in Xenopus laevis. Development 1999;126:5327-5337.
85. Lane MC, Smith WC. The origins of primitive blood in Xenopus: implications for axial patterning. Development 1999;126:423-434.
86. Lane MC, Sheets MD. Primitive and definitive blood share a common origin in Xenopus: a comparison of lineage techniques used to construct fate maps. Dev Biol 2002;248:52-67.
87. Kumano G, Smith WC. Revisions to the Xenopus gastrula fate map: implications for mesoderm induction and patterning. Dev Dyn 2002;225:409-421.
88. Kau CL, Turpen JB. Dual contribution of embryonic ventral blood island and dorsal lateral plate mesoderm during ontogeny of hemopoietic cells in Xenopus laevis. J Immunol 1983;131:2262-2266.
89. Tracey WD Jr., Pepling ME, Horb ME et al. A Xenopus homologue of aml-1 reveals unexpected patterning mechanisms leading to the formation of embryonic blood. Development 1998;125:1371-1380.
90. Dale L, Howes G, Price BM et al. Bone morphogenetic protein 4: a ventralizing factor in early Xenopus development. Development 1992;115:573-585.
91. Jones CM, Lyons KM, Lapan PM et al. DVR-4 (bone morphogenetic protein-4) as a posterior-ventralizing factor in Xenopus mesoderm induction. Development 1992;115:639-647.
92. Maeno M, Ong RC, Suzuki A et al. A truncated bone morphogenetic protein 4 receptor alters the fate of ventral mesoderm to dorsal mesoderm: roles of animal pole tissue in the development of ventral mesoderm. Proc Natl Acad Sci U S A 1994;91:10260-10264.
93. Maeno M, Ong RC, Xue Y et al. Regulation of primary erythropoiesis in the ventral mesoderm of Xenopus gastrula embryo: evidence for the expression of a stimulatory factor(s) in animal pole tissue. Dev Biol 1994; 161:522-529.
94. Graff JM, Thies RS, Song JJ et al. Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo. Cell 1994;79:169-179.
95. Schmerer M, Evans T. Primitive erythropoiesis is regulated by Smad-dependent signaling in postgastrulation mesoderm. Blood 2003;102:3196-3205.
96. Kikkawa M, Yamazaki M, Izutsu Y et al. Two-step induction of primitive erythrocytes in Xenopus laevis embryos: signals from the vegetal endoderm and the overlying ectoderm. Int J Dev Biol 2001;45:387-396.
97. Walters MJ, Wayman GA, Notis JC et al. Calmodulin-dependent protein kinase IV mediated antagonism of BMP signaling regulates lineage and survival of hematopoietic progenitors. Development 2002;129:1455-1466.
98. Keller R. Early embryonic development of Xenopus laevis. In: Kay BK, Peng HB, eds. Methods in Cell Biology. San Diego: Academic Press, 1991:62-109.
99. Maeda R, Kobayashi A, Sekine R et al. Xmsx-1 modifies mesodermal tissue pattern along dorsoventral axis in Xenopus laevis embryo. Development 1997;124: 2553-2560.
100. Henningfeld KA, Rastegar S, Adler G et al. Smad1 and Smad4 are components of the bone morphogenetic protein-4 (BMP-4)-induced transcription complex of the Xvent-2B promoter. J Biol Chem 2000;275: 21827-21835.
101. Gawantka V, Delius H, Hirschfeld K et al. Antagonizing the Spemann organizer: role of the homeobox gene Xvent-1. EMBO J 1995;14:6268-62790.
102. Ault KT, Dirksen ML, Jamrich M. A novel homeobox gene PV.1 mediates induction of ventral mesoderm in Xenopus embryos. Proc Natl Acad Sci U S A 1996;93:6415-6420.
103. Mead PE, Brivanlou IH, Kelley CM et al. BMP-4-responsive regulation of dorsal-ventral patterning by the homeobox protein Mix. 1. Nature 1996;382:357-360.
104. Hemmati-Brivanlou A, Thomsen GH. Ventral mesodermal patterning in Xenopus embryos: expression patterns and activities of BMP-2 and BMP-4. Dev Genet 1995;17:78-89.
105. Xu RH, Kim J, Taira M et al. Differential regulation of neurogenesis by the two Xenopus GATA-1 genes. Mol Cell Biol 1997;17:436-443.
106. Maeno M, Mead PE, Kelley C et al. The role of BMP-4 and GATA-2 in the induction and differentiation of hematopoietic mesoderm in Xenopus laevis. Blood 1996;88:1965-1972.
107. Mead PE, Kelley CM, Hahn PS et al. SCL specifies hematopoietic mesoderm in Xenopus embryos. Development 1998;125:2611-2620.
108. Mead PE, Deconinck AE, Huber TL et al. Primitive erythropoiesis in the Xenopus embryo: the synergistic role of LMO-2, SCL and GATA-binding proteins. Development 2001;128:2301-2308.
109. Hoppler S, Moon RT. BMP-2/-4 and Wnt-8 cooperatively pattern the Xenopus mesoderm. Mech Dev 1998; 71:119-129.
110. Shim S, Bae N, Han JK. Bone morphogenetic protein-4-induced activation of Xretpos is mediated by Smads and Olf-1/EBF associated zinc finger (OAZ). Nucleic Acids Res 2002;30:3107-3117.
111. Rastegar S, Friedle H, Frommer G et al. Transcriptional regulation of Xvent homeobox genes. Mech Dev 1999; 81:139-149.
112. Friedle H, Knochel W. Cooperative interaction of Xvent-2 and GATA-2 in the activation of the ventral homeobox gene Xvent-1B. J Biol Chem 2002;277: 23872-23881.
113. Friedle H, Rastegar S, Paul H et al. Xvent-1 mediates BMP-4-induced suppression of the dorsal-lip-specific early response gene XFD-1′ in Xenopus embryos. EMBO J 1998;17:2298-2307.
114. Imai Y, Gates MA, Melby AE et al. The homeobox genes vox and vent are redundant repressors of dorsal fates in zebrafish. Development 2001;128:2407-2420.
115. Trindade M, Tada M, Smith JC. DNA-binding specificity and embryological function of Xom (Xvent-2). Dev Biol 1999;216:442-456.
116. Kawahara A, Wilm T, Solnica-Krezel L et al. Functional interaction of vega2 and goosecoid homeobox genes in zebrafish. Genesis 2000;28:58-67.
117. Kawahara A, Wilm T, Solnica-Krezel L et al. Antagonistic role of vegal and bozozok/dharma homeobox genes in organizer formation. Proc Natl Acad Sci U S A 2000;97:12121-12126.
118. Melby AE, Beach C, Mullins M et al. Patterning the early zebrafish by the opposing actions of bozozok and vox/vent. Dev Biol 2000;224:275-285.
119. Kozmik Z, Holland LZ, Schubert M et al. Characterization of Amphioxus AmphiVent, an evolutionarily conserved marker for chordate ventral mesoderm. Genesis 2001;29:172-179.
120. Moretti PA, Davidson AJ, Baker E et al. Molecular cloning of a human Vent-like homeobox gene. Genomics 2001;76:21-29.
121. Melby AE, Clements WK, Kimelman D. Regulation of dorsal gene expression in Xenopus by the ventralizing homeodomain gene Vox. Dev Biol 1999;211:293-305.
122. Schuler-Metz A, Knochel S, Kaufmann E et al. The homeodomain transcription factor Xvent-2 mediates autocatalytic regulation of BMP-4 expression in Xenopus embryos. J Biol Chem 2000;275:34365-34374.
123. Xu RH, Ault KT, Kim J et al. Opposite effects of FGF and BMP-4 on embryonic blood formation: roles of PV.1 and GATA-2. Dev Biol 1999;208:352-361.
124. Deramaudt TB, Remy P, Stiegler P. Identification of interaction partners for two closely-related members of the ETS protein family, FLI and ERG. Gene 2001;274:169-177.
125. Kelley C, Yee K, Harland R et al. Ventral expression of GATA-1 and GATA-2 in the Xenopus embryo defines induction of hematopoietic mesoderm. Dev Biol 1994;165:193-205.
126. Gottgens B, Nastos A, Kinston S et al. Establishing the transcriptional programme for blood: the SCL stem cell enhancer is regulated by a multiprotein complex containing Ets and GATA factors. EMBO J 2002;21:3039-3050.
127. Sanchez M, Gottgens B, Sinclair AM et al. An SCL 3′ enhancer targets developing endothelium together with embryonic and adult haematopoietic progenitors. Development 1999;126:3891-3904.
128. Tracey WD, Speck NA. Potential roles for RUNX 1 and its orthologs in determining hematopoietic cell fate. Semin Cell Dev Biol 2000;11:337-342.
129. Hanai J, Chen LF, Kanno T et al. Interaction and functional cooperation of PEBP2/CBF with Smads. Synergistic induction of the immunoglobulin germline Cα promoter. J Biol Chem 1999;274:31577-31582.
130. Zaidi SK, Sullivan AJ, van Wijnen AJ et al. Integration of Runx and Smad regulatory signals at transcriptionally active subnuclear sites. Proc Natl Acad Sci U S A 2002;99:8048-8053.
131. Ito Y, Miyazono K. RUNX transcription factors as key targets of TGF-β superfamily signaling. Curr Opin Genet Dev 2003;13:43-47.
132. Winnier G, Blessing M, Labosky PA et al. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev 1995;9: 2105-2116.
133. Beppu H, Kawabata M, Hamamoto T et al. BMP type II receptor is required for gastrulation and early development of mouse embryos. Dev Biol 2000;221:249-258.
134. Dyer MA, Farrington SM, Mohn D et al. Indian hedgehog activates hematopoiesis and vasculogenesis and can respecify prospective neurectodermal cell fate in the mouse embryo. Development 2001;128:1717-1730.
135. Belaoussoff M, Farrington SM, Baron MH. Hematopoietic induction and respecification of A-P identity by visceral endoderm signaling in the mouse embryo. Development 1998;125:5009-5018.
136. Baron M. Induction of embryonic hematopoietic and endothelial stem/progenitor cells by hedgehog-mediated signals. Differentiation 2001;68:175-185.
137. Marshall CJ, Kinnon C, Thrasher AJ. Polarized expression of bone morphogenetic protein-4 in the human aortagonad-mesonephros region. Blood 2000;96:1591-1593.
138. Pardanaud L, Dieterlen-Lievre F. Ontogeny of the endothelial system in the avian model. Adv Exp Med Biol 2000;476:67-78.
139. Pardanaud L, Dieterlen-Lievre F. Manipulation of the angiopoietic/ hemangiopoietic commitment in the avian embryo. Development 1999;126:617-627.
140. Ingham PW, McMahon AP. Hedgehog signaling in animal development: paradigms and principles. Genes Dev 2001;15:3059-3087.
141. Becker S, Wang ZJ, Massey H et al. A role for Indian hedgehog in extraembryonic endoderm differentiation in F9 cells and the early mouse embryo. Dev Biol 1997; 187:298-310.
142. Hammerschmidt M, Brook A, McMahon AP. The world according to hedgehog. Trends Genet 1997;13: 14-21.
143. Pardanaud L, Luton D, Prigent M et al. Two distinct endothelial lineages in ontogeny, one of them related to hemopoiesis. Development 1996;122:1363-1371.
144. Nakayama N, Lee J, Chiu L. Vascular endothelial growth factor synergistically enhances bone morphogenetic protein-4-dependent lymphohematopoietic cell generation from embryonic stem cells in vitro. Blood 2000;95:2275-2283.
145. Adelman CA, Chattopadhyay S, Bieker JJ. The BMP/BMPR/Smad pathway directs expression of the erythroid-specific EKLF and GATA1 transcription factors during embryoid body differentiation in serum-free media. Development 2002;129:539-549.
146. Wiles MV, Johansson BM. Embryonic stem cell development in a chemically defined medium. Exp Cell Res 1999;247:241-248.
147. Li F, Lu S, Vida L et al. Bone morphogenetic protein 4 induces efficient hematopoietic differentiation of rhesus monkey embryonic stem cells in vitro. Blood 2001;98:335-342.
148. Chadwick K, Wang L, Li L et al. Cytokines and BMP-4 promote hematopoietic differentiation of human embryonic stem cells. Blood 2003;102:906-915.
149. Jay KE, Gallacher L, Bhatia M. Emergence of muscle and neural hematopoiesis in humans. Blood 2002;100: 3193-3202.
150. Kyba M, Perlingeiro RC, Daley GQ. HoxB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors. Cell 2002;109:29-37.
151. 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.
152. Ohishi K, Katayama N, Shiku H et al. Notch signaling in hematopoiesis. Semin Cell Dev Biol 2003;14:143-150.
153. Bhardwaj G, Murdoch B, Wu D et al. Sonic hedgehog induces the proliferation of primitive human hematopoietic cells via BMP regulation. Nat Immunol 2001;2:172-180.
154. Ueno H, Sakita-Ishikawa M, Morikawa Y et al. A stromal cell-derived membrane protein that supports hematopoietic stem cells. Nat Immunol 2003;4:457-463.
155. Lessard J, Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 2003;423:255-260.
156. Antonchuk J, Sauvageau G, Humphries RK. HOXB4-induced expansion of adult hematopoietic stem cells ex vivo. Cell 2002;109:39-45.
157. 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.
158. Fuchs O, Simakova O, Klener P et al. Inhibition of Smad5 in human hematopoietic progenitors blocks erythroid differentiation induced by BMP4. Blood Cells Mol Dis 2002;28:221-233.
159. Detmer K, Walker AN. Bone morphogenetic proteins act synergistically with haematopoietic cytokines in the differentiation of haematopoietic progenitors. Cytokine 2002;17:36-42.
160. Maguer-Satta V, Bartholin L, Jeanpierre S et al. Regulation of human erythropoiesis by activin A, BMP2, and BMP4, members of the TGFβ family. Exp Cell Res 2003;282:110-120.
161. Devine SM, Lazarus HM, Emerson SG. Clinical application of hematopoietic progenitor cell expansion: current status and future prospects. Bone Marrow Transplant 2003;31:241-252.
162. Kondo M, Wagers AJ, Manz MG et al. Biology of hematopoietic stem cells and progenitors: implications for clinical application. Annu Rev Immunol 2003;21:759-806.
163. Gluckman E. Current status of umbilical cord blood hematopoietic stem cell transplantation. Exp Hematol 2000;28:1197-1205.
164. Cohen SB, Madrigal JA. Immunological and functional differences between cord and peripheral blood. Bone Marrow Transplant 1998;21 (suppl 3):S9-12.
165. Silberstein LE, Jefferies LC. Placental-blood banking: a new frontier in transfusion medicine. N Engl J Med 1996;335:199-201.
166. Rubinstein P, Carrier C, Scaradavou A et al. Outcomes among 562 recipients of placental-blood transplants from unrelated donors. N Engl J Med 1998;339: 1565-1577.
167. Ooi J, Iseki T, Takahashi S et al. Unrelated cord blood transplantation for adult patients with advanced myelodysplastic syndrome. Blood 2003;101:4711-4713.
168. Verfaillie CM. Hematopoietic stem cells for transplantation. Nat Immunol 2002;3:314-317.
169. Kojika S, Griffin JD. Notch receptors and hematopoiesis. Exp Hematol 2001;29:1041-1052.
170. 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.
171. Tsai RY, Kittappa R, McKay RD. Plasticity, niches, and the use of stem cells. Dev Cell 2002;2:707-712.
172. Dale L, Slack JM. Fate map for the 32-cell stage of Xenopus laevis. Development 1987;99:527-551.
173. Moody SA. Fates of the blastomeres of the 32-cell-stage Xenopus embryo. Dev Biol 1987;122:300-319.