Developmental hematopoiesis: Ontogeny, genetic programming and conservation

Experimental Hematology

Volumn 42, Issue 8, 2014, Pages 669-683

  Ciau Uitz, Aldo ^a   Monteiro, Rui ^a,b   Kirmizitas, Arif ^a   Patient, Roger ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROSTAGLANDIN E2; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR TAL1; VASCULOTROPIN A;

CELL DIFFERENTIATION; CELL DIVISION; CELL MIGRATION; CELL POPULATION; CELL RENEWAL; EMBRYO DEVELOPMENT; ENDOTHELIUM; GENETIC CONSERVATION; HEART MUSCLE CELL; HEMANGIOBLAST; HEMATOPOIESIS; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL; HUMAN; LYMPHOPOIESIS; MESODERM; METAMORPHOSIS; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; STEM CELL; YOLK SAC;

ANIMALS; CELL DIFFERENTIATION; ENDOTHELIAL CELLS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; XENOPUS; ZEBRAFISH;

EID: 84905185118     PISSN: 0301472X     EISSN: 18732399     Source Type: Journal    
DOI: 10.1016/j.exphem.2014.06.001     Document Type: Review

References (206)

1. Medvinsky A., Rybtsov S., Taoudi S. Embryonic origin of the adult hematopoietic system: advances and questions. Development 2011, 138:1017-1031.
2. Johnson G.R., Moore M.A. Role of stem cell migration in initiation of mouse foetal liver haemopoiesis. Nature 1975, 258:726-728.
3. Moore M.A., Metcalf D. Ontogeny of the haemopoietic system: yolk sac origin of invivo and invitro colony forming cells in the developing mouse embryo. Br J Haematol 1970, 18:279-296.
4. Dzierzak E., Medvinsky A., de Bruijn M. Qualitative and quantitative aspects of haematopoietic cell development in the mammalian embryo. Immunol Today 1998, 19:228-236.
5. Fontaine-Perus J.C., Calman F.M., Kaplan C., Le Douarin N.M. Seeding of the 10-day mouse embryo thymic rudiment by lymphocyte precursors invitro. J Immunol 1981, 126:2310-2316.
6. Owen J.J., Ritter M.A. Tissue interaction in the development of thymus lymphocytes. J Exp Med 1969, 129:431-442.
7. LeDouarin N.M., Jotereau F.V. Origin and renewal of lymphocytes in avian embryo thymuses studied in interspecific combinations. Nat New Biol 1973, 246:25-27.
8. Pardanaud L., Yassine F., Dieterlen-Lievre F. Relationship between vasculogenesis, angiogenesis and haemopoiesis during avian ontogeny. Development 1989, 105:473-485.
9. Houssaint E. Differentiation of the mouse hepatic primordium: II. Extrinsic origin of the haemopoietic cell line. Cell Differ 1981, 10:243-252.
10. 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.
11. Dieterlen-Lievre F., Martin C. Diffuse intraembryonic hemopoiesis in normal and chimeric avian development. Dev Biol 1981, 88:180-191.
12. Kau C.L., Turpen J.B. 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.
13. Maéno M., Todate A., Katagiri C. The localization of precursor cells for larval and adult hematopoietic cells of Xenopus laevis in two regions of embryos. Dev Growth Differ 1985, 27:137-148.
14. Bechtold T.E., Smith P.B., Turpen J.B. Differential stem cell contributions to thymocyte succession during development of Xenopus laevis. J Immunol 1992, 148:2975-2982.
15. Chen X.D., Turpen J.B. Intraembryonic origin of hepatic hematopoiesis in Xenopus laevis. J Immunol 1995, 154:2557-2567.
16. Smith P.B., Flajnik M.F., Turpen J.B. Experimental analysis of ventral blood island hematopoiesis in Xenopus embryonic chimeras. Dev Biol 1989, 131:302-312.
17. Medvinsky A.L., Samoylina N.L., Muller A.M., Dzierzak E.A. An early pre-liver intraembryonic source of CFU-S in the developing mouse. Nature 1993, 364:64-67.
18. Tavian M., Robin C., Coulombel L., Peault B. The human embryo, but not its yolk sac, generates lympho-myeloid stem cells: mapping multipotent hematopoietic cell fate in intraembryonic mesoderm. Immunity 2001, 15:487-495.
19. 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.
20. Tavian M., Coulombel L., Luton D., Clemente H.S., Dieterlen-Lievre F., Peault B. Aorta-associated CD34+ hematopoietic cells in the early human embryo. Blood 1996, 87:67-72.
21. Ivanovs A., Rybtsov S., Anderson R.A., Turner M.L., Medvinsky A. Identification of the niche and phenotype of the first human hematopoietic stem cells. Stem Cell Rep 2014, 2:449-456.
22. Medvinsky A., Dzierzak E. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 1996, 86:897-906.
23. Boiers C., Carrelha J., Lutteropp M., et al. Lymphomyeloid contribution of an immune-restricted progenitor emerging prior to definitive hematopoietic stem cells. Cell Stem Cell 2013, 13:535-548.
24. Yoshimoto M., Montecino-Rodriguez E., Ferkowicz M.J., et al. Embryonic day 9 yolk sac and intra-embryonic hemogenic endothelium independently generate a B-1 and marginal zone progenitor lacking B-2 potential. Proc Natl Acad Sci U S A 2011, 108:1468-1473.
25. Yoder M.C., Hiatt K., Dutt P., Mukherjee P., Bodine D.M., Orlic D. Characterization of definitive lymphohematopoietic stem cells in the day 9 murine yolk sac. Immunity 1997, 7:335-344.
26. Murayama E., Kissa K., Zapata A., et al. Tracing hematopoietic precursor migration to successive hematopoietic organs during zebrafish development. Immunity 2006, 25:963-975.
27. Kissa K., Murayama E., Zapata A., et al. Live imaging of emerging hematopoietic stem cells and early thymus colonization. Blood 2008, 111:1147-1156.
28. Jin H., Sood R., Xu J., et al. Definitive hematopoietic stem/progenitor cells manifest distinct differentiation output in the zebrafish VDA and PBI. Development 2009, 136:647-654.
29. Monteiro R., Pouget C., Patient R. The gata1/pu.1 lineage fate paradigm varies between blood populations and is modulated by tif1gamma. EMBO J 2011, 30:1093-1103.
30. Bertrand J.Y., Chi N.C., Santoso B., Teng S., Stainier D.Y., Traver D. Haematopoietic stem cells derive directly from aortic endothelium during development. Nature 2010, 464:108-111.
31. Traver D., Paw B.H., Poss K.D., Penberthy W.T., Lin S., Zon L.I. Transplantation and invivo imaging of multilineage engraftment in zebrafish bloodless mutants. Nat Immunol 2003, 4:1238-1246.
32. Traver D., Winzeler A., Stern H.M., et al. Effects of lethal irradiation in zebrafish and rescue by hematopoietic cell transplantation. Blood 2004, 104:1298-1305.
33. Ma D., Zhang J., Lin H.F., Italiano J., Handin R.I. The identification and characterization of zebrafish hematopoietic stem cells. Blood 2011, 118:289-297.
34. Turpen J.B., Smith P.B. Location of hemopoietic stem cells influences frequency of lymphoid engraftment in Xenopus embryos. J Immunol 1989, 143:3455-3460.
35. Rollins-Smith L.A., Blair P. Contribution of ventral blood island mesoderm to hematopoiesis in postmetamorphic and metamorphosis-inhibited Xenopus laevis. Dev Biol 1990, 142:178-183.
36. Palis J., Malik J., McGrath K.E., Kingsley P.D. Primitive erythropoiesis in the mammalian embryo. Int J Dev Biol 2010, 54:1011-1018.
37. Palis J., Robertson S., Kennedy M., Wall C., Keller G. Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development 1999, 126:5073-5084.
38. Rampon C., Huber P. Multilineage hematopoietic progenitor activity generated autonomously in the mouse yolk sac: analysis using angiogenesis-defective embryos. Int J Dev Biol 2003, 47:273-280.
39. Lux C.T., Yoshimoto M., McGrath K., Conway S.J., Palis J., Yoder M.C. All primitive and definitive hematopoietic progenitor cells emerging before E10 in the mouse embryo are products of the yolk sac. Blood 2008, 111:3435-3438.
40. Bertrand J.Y., Kim A.D., Violette E.P., Stachura D.L., Cisson J.L., Traver D. Definitive hematopoiesis initiates through a committed erythromyeloid progenitor in the zebrafish embryo. Development 2007, 134:4147-4156.
41. Sugiyama D., Ogawa M., Nakao K., et al. B cell potential can be obtained from pre-circulatory yolk sac, but with low frequency. Dev Biol 2007, 301:53-61.
42. Li Z., Lan Y., He W., et al. Mouse embryonic head as a site for hematopoietic stem cell development. Cell Stem Cell 2012, 11:663-675.
43. Nakano H., Liu X., Arshi A., et al. Haemogenic endocardium contributes to transient definitive haematopoiesis. Nat Commun 2013, 4:1564.
44. Dzierzak E., Speck N.A. Of lineage and legacy: the development of mammalian hematopoietic stem cells. Nat Immunol 2008, 9:129-136.
45. Yoder M.C., Hiatt K., Mukherjee P. Invivo 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.
46. Toles J.F., Chui D.H., Belbeck L.W., Starr E., Barker J.E. Hemopoietic stem cells in murine embryonic yolk sac and peripheral blood. Proc Natl Acad Sci U S A 1989, 86:7456-7459.
47. Turpen J.B., Kelley C.M., Mead P.E., Zon L.I. Bipotential primitive-definitive hematopoietic progenitors in the vertebrate embryo. Immunity 1997, 7:325-334.
48. Gordon-Keylock S., Sobiesiak M., Rybtsov S., Moore K., Medvinsky A. Mouse extraembryonic arterial vessels harbor precursors capable of maturing into definitive HSCs. Blood 2013, 122:2338-2345.
49. Samokhvalov I.M., Samokhvalova N.I., Nishikawa S. Cell tracing shows the contribution of the yolk sac to adult haematopoiesis. Nature 2007, 446:1056-1061.
50. Ciau-Uitz A., Walmsley M., Patient R. Distinct origins of adult and embryonic blood in Xenopus. Cell 2000, 102:787-796.
51. Muller A.M., Medvinsky A., Strouboulis J., Grosveld F., Dzierzak E. Development of hematopoietic stem cell activity in the mouse embryo. Immunity 1994, 1:291-301.
52. de Bruijn M.F., Speck N.A., Peeters M.C., Dzierzak E. Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo. EMBO J 2000, 19:2465-2474.
53. de Bruijn M.F., Ma X., Robin C., Ottersbach K., Sanchez M.J., Dzierzak E. Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta. Immunity 2002, 16:673-683.
54. Cormier F., Dieterlen-Lievre F. The wall of the chick embryo aorta harbours M-CFC, G-CFC, GM-CFC and BFU-E. Development 1988, 102:279-285.
55. Cormier F., de Paz P., Dieterlen-Lievre F. Invitro detection of cells with monocytic potentiality in the wall of the chick embryo aorta. Dev Biol 1986, 118:167-175.
56. Taoudi S., Medvinsky A. Functional identification of the hematopoietic stem cell niche in the ventral domain of the embryonic dorsal aorta. Proc Natl Acad Sci U S A 2007, 104:9399-9403.
57. Jordan H.E. Aortic cell clusters in vertebrate embryos. Proc Natl Acad Sci U S A 1917, 3:149-156.
58. Jordan H.E. Evidence of hemogenic capacity of endothelium. Anat Rec 1916, 10:417-420.
59. Emmel V.E. The cell clusters in the dorsal aorta of mammalian embryos. Am J Anat 1916, 19:401-421.
60. Jaffredo T., Gautier R., Brajeul V., Dieterlen-Lievre F. Tracing the progeny of the aortic hemangioblast in the avian embryo. Dev Biol 2000, 224:204-214.
61. Jaffredo T., Gautier R., Eichmann A., Dieterlen-Lievre F. Intraaortic hemopoietic cells are derived from endothelial cells during ontogeny. Development 1998, 125:4575-4583.
62. Oberlin E., Tavian M., Blazsek I., Peault B. Blood-forming potential of vascular endothelium in the human embryo. Development 2002, 129:4147-4157.
63. Wasteson P., Johansson B.R., Jukkola T., et al. Developmental origin of smooth muscle cells in the descending aorta in mice. Development 2008, 135:1823-1832.
64. Zovein A.C., Hofmann J.J., Lynch M., et al. Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell 2008, 3:625-636.
65. Zovein A.C., Turlo K.A., Ponec R.M., et al. Vascular remodeling of the vitelline artery initiates extravascular emergence of hematopoietic clusters. Blood 2010, 116:3435-3444.
66. Kissa K., Herbomel P. Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 2010, 464:112-115.
67. Boisset J.C., van Cappellen W., Andrieu-Soler C., Galjart N., Dzierzak E., Robin C. Invivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 2010, 464:116-120.
68. Mizuochi C., Fraser S.T., Biasch K., et al. Intra-aortic clusters undergo endothelial to hematopoietic phenotypic transition during early embryogenesis. PloS One 2012, 7:e35763.
69. Swiers G., Baumann C., O'Rourke J., et al. Early dynamic fate changes in haemogenic endothelium characterized at the single-cell level. Nat Commun 2013, 4:2924.
70. Lam E.Y., Hall C.J., Crosier P.S., Crosier K.E., Flores M.V. Live imaging of Runx1 expression in the dorsal aorta tracks the emergence of blood progenitors from endothelial cells. Blood 2010, 116:909-914.
71. Ciau-Uitz A., Liu F., Patient R. Genetic control of hematopoietic development in Xenopus and zebrafish. Int J Dev Biol 2010, 54:1139-1149.
72. Porcher C., Liao E.C., Fujiwara Y., Zon L.I., Orkin S.H. Specification of hematopoietic and vascular development by the bHLH transcription factor SCL without direct DNA binding. Development 1999, 126:4603-4615.
73. Porcher C., Swat W., Rockwell K., Fujiwara Y., Alt F.W., Orkin S.H. The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages. Cell 1996, 86:47-57.
74. Gering M., Rodaway A.R., Gottgens B., Patient R.K., Green A.R. The SCL gene specifies haemangioblast development from early mesoderm. EMBO J 1998, 17:4029-4045.
75. Liao E.C., Paw B.H., Oates A.C., Pratt S.J., Postlethwait J.H., Zon L.I. SCL/Tal-1 transcription factor acts downstream of cloche to specify hematopoietic and vascular progenitors in zebrafish. Genes Dev 1998, 12:621-626.
76. Dooley K.A., Davidson A.J., Zon L.I. Zebrafish scl functions independently in hematopoietic and endothelial development. Dev Biol 2005, 277:522-536.
77. Ng Y.K., George K.M., Engel J.D., Linzer D.I. GATA factor activity is required for the trophoblast-specific transcriptional regulation of the mouse placental lactogen I gene. Development 1994, 120:3257-3266.
78. Tsai F.Y., Keller G., Kuo F.C., et al. An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature 1994, 371:221-226.
79. Pimanda J.E., Ottersbach K., Knezevic K., et al. Gata2, Fli1, and Scl form a recursively wired gene-regulatory circuit during early hematopoietic development. Proc Natl Acad Sci U S A 2007, 104:17692-17697.
80. Wilson N.K., Foster S.D., Wang X., et al. Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators. Cell Stem Cell 2010, 7:532-544.
81. 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.
82. Patterson L.J., Gering M., Eckfeldt C.E., et al. The transcription factors Scl and Lmo2 act together during development of the hemangioblast in zebrafish. Blood 2007, 109:2389-2398.
83. Ciau-Uitz A., Pinheiro P., Kirmizitas A., Zuo J., Patient R. VEGFA-dependent and -independent pathways synergise to drive Scl expression and initiate programming of the blood stem cell lineage in Xenopus. Development 2013, 140:2632-2642.
84. Lim K.C., Hosoya T., Brandt W., et al. Conditional Gata2 inactivation results in HSC loss and lymphatic mispatterning. J Clin Invest 2012, 122:3705-3717.
85. Gao X., Johnson K.D., Chang Y.I., et al. Gata2 cis-element is required for hematopoietic stem cell generation in the mammalian embryo. J Exp Med 2013, 210:2833-2842.
86. de Pater E., Kaimakis P., Vink C.S., et al. Gata2 is required for HSC generation and survival. J Exp Med 2013, 210:2843-2850.
87. Patterson L.J., Gering M., Patient R. Scl is required for dorsal aorta as well as blood formation in zebrafish embryos. Blood 2005, 105:3502-3511.
88. Zhen F., Lan Y., Yan B., Zhang W., Wen Z. Hemogenic endothelium specification and hematopoietic stem cell maintenance employ distinct Scl isoforms. Development 2013, 140:3977-3985.
89. North T.E., de Bruijn M.F., Stacy T., et al. Runx1 expression marks long-term repopulating hematopoietic stem cells in the midgestation mouse embryo. Immunity 2002, 16:661-672.
90. Tober J., Yzaguirre A.D., Piwarzyk E., Speck N.A. Distinct temporal requirements for Runx1 in hematopoietic progenitors and stem cells. Development 2013, 140:3765-3776.
91. Okuda T., van Deursen J., Hiebert S.W., Grosveld G., Downing J.R. AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 1996, 84:321-330.
92. Wang Q., Stacy T., Miller J.D., et al. The CBFbeta subunit is essential for CBFalpha2 (AML1) function invivo. Cell 1996, 87:697-708.
93. Wang Q., Stacy T., Binder M., Marin-Padilla M., Sharpe A.H., Speck N.A. Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc Natl Acad Sci U S A 1996, 93:3444-3449.
94. Chen M.J., Yokomizo T., Zeigler B.M., Dzierzak E., Speck N.A. Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 2009, 457:887-891.
95. North T., Gu T.L., Stacy T., et al. Cbfa2 is required for the formation of intra-aortic hematopoietic clusters. Development 1999, 126:2563-2575.
96. Cai X., Gaudet J.J., Mangan J.K., et al. Runx1 loss minimally impacts long-term hematopoietic stem cells. PloS One 2011, 6:e28430.
97. Chen M.J., Li Y., De Obaldia M.E., et al. Erythroid/myeloid progenitors and hematopoietic stem cells originate from distinct populations of endothelial cells. Cell Stem Cell 2011, 9:541-552.
98. Lancrin C., Sroczynska P., Stephenson C., Allen T., Kouskoff V., Lacaud G. The haemangioblast generates haematopoietic cells through a haemogenic endothelium stage. Nature 2009, 457:892-895.
99. Eilken H.M., Nishikawa S., Schroeder T. Continuous single-cell imaging of blood generation from haemogenic endothelium. Nature 2009, 457:896-900.
100. Garriock R.J., Czeisler C., Ishii Y., Navetta A.M., Mikawa T. An anteroposterior wave of vascular inhibitor downregulation signals aortae fusion along the embryonic midline axis. Development 2010, 137:3697-3706.
101. Lawson N.D., Vogel A.M., Weinstein B.M. Sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Dev Cell 2002, 3:127-136.
102. Quillien A., Moore J.C., Shin M., et al. Distinct Notch signaling outputs pattern the developing arterial system. Development 2014, 141:1544-1552.
103. Lawson N.D., Scheer N., Pham V.N., et al. Notch signaling is required for arterial-venous differentiation during embryonic vascular development. Development 2001, 128:3675-3683.
104. Krebs L.T., Shutter J.R., Tanigaki K., Honjo T., Stark K.L., Gridley T. Haploinsufficient lethality and formation of arteriovenous malformations in Notch pathway mutants. Genes Dev 2004, 18:2469-2473.
105. Benedito R., Trindade A., Hirashima M., et al. Loss of Notch signalling induced by Dll4 causes arterial calibre reduction by increasing endothelial cell response to angiogenic stimuli. BMC Dev Biol 2008, 8:117.
106. Duarte A., Hirashima M., Benedito R., et al. Dosage-sensitive requirement for mouse Dll4 in artery development. Genes Dev 2004, 18:2474-2478.
107. Taylor K.L., Henderson A.M., Hughes C.C. Notch activation during endothelial cell network formation invitro targets the basic HLH transcription factor HESR-1 and downregulates VEGFR-2/KDR expression. Microvasc Res 2002, 64:372-383.
108. Holderfield M.T., Henderson Anderson A.M., Kokubo H., Chin M.T., Johnson R.L., Hughes C.C. HESR1/CHF2 suppresses VEGFR2 transcription independent of binding to E-boxes. Biochem Biophys Res Commun 2006, 346:637-648.
109. Davis R.B., Curtis C.D., Griffin C.T. BRG1 promotes COUP-TFII expression and venous specification during embryonic vascular development. Development 2013, 140:1272-1281.
110. Henderson A.M., Wang S.J., Taylor A.C., Aitkenhead M., Hughes C.C. The basic helix-loop-helix transcription factor HESR1 regulates endothelial cell tube formation. J Biol Chem 2001, 276:6169-6176.
111. Burns C.E., Traver D., Mayhall E., Shepard J.L., Zon L.I. Hematopoietic stem cell fate is established by the Notch-Runx pathway. Genes Dev 2005, 19:2331-2342.
112. Gering M., Patient R. Hedgehog signaling is required for adult blood stem cell formation in zebrafish embryos. Dev Cell 2005, 8:389-400.
113. Kumano K., Chiba S., Kunisato A., et al. Notch1 but not Notch2 is essential for generating hematopoietic stem cells from endothelial cells. Immunity 2003, 18:699-711.
114. Leung A., Ciau-Uitz A., Pinheiro P., et al. Uncoupling VEGFA functions in arteriogenesis and hematopoietic stem cell specification. Dev cell 2013, 24:144-158.
115. Richard C., Drevon C., Canto P.Y., et al. Endothelio-mesenchymal interaction controls runx1 expression and modulates the notch pathway to initiate aortic hematopoiesis. Dev Cell 2013, 24:600-611.
116. Lebestky T., Jung S.H., Banerjee U. A Serrate-expressing signaling center controls Drosophila hematopoiesis. Genes Dev 2003, 17:348-353.
117. Guiu J., Shimizu R., D'Altri T., et al. Hes repressors are essential regulators of hematopoietic stem cell development downstream of Notch signaling. J Exp Med 2013, 210:71-84.
118. Robert-Moreno A., Espinosa L., de la Pompa J.L., Bigas A. RBPjkappa-dependent Notch function regulates Gata2 and is essential for the formation of intra-embryonic hematopoietic cells. Development 2005, 132:1117-1126.
119. Robert-Moreno A., Guiu J., Ruiz-Herguido C., et al. Impaired embryonic haematopoiesis yet normal arterial development in the absence of the Notch ligand Jagged1. EMBO J 2008, 27:1886-1895.
120. Clements W.K., Kim A.D., Ong K.G., Moore J.C., Lawson N.D., Traver D. A somitic Wnt16/Notch pathway specifies haematopoietic stem cells. Nature 2011, 474:220-224.
121. Clements W.K., Traver D. Signalling pathways that control vertebrate haematopoietic stem cell specification. Nat Rev Immunol 2013, 13:336-348.
122. Wilkinson R.N., Pouget C., Gering M., et al. Hedgehog and Bmp polarize hematopoietic stem cell emergence in the zebrafish dorsal aorta. Dev Cell 2009, 16:909-916.
123. Pardanaud L., Luton D., Prigent M., Bourcheix L.M., Catala M., Dieterlen-Lievre F. Two distinct endothelial lineages in ontogeny, one of them related to hemopoiesis. Development 1996, 122:1363-1371.
124. Pouget C., Gautier R., Teillet M.A., Jaffredo T. Somite-derived cells replace ventral aortic hemangioblasts and provide aortic smooth muscle cells of the trunk. Development 2006, 133:1013-1022.
125. Sato Y., Watanabe T., Saito D., et al. Notch mediates the segmental specification of angioblasts in somites and their directed migration toward the dorsal aorta in avian embryos. Dev Cell 2008, 14:890-901.
126. Kataoka H., Hayashi M., Kobayashi K., Ding G., Tanaka Y., Nishikawa S.I. Region-specific Etv2 ablation revealed the critical origin of hemogenic capacity from Hox6-positive caudal-lateral primitive mesoderm. Exp Hematol 2013, 41:567-581.
127. Chong D.C., Koo Y., Xu K., Fu S., Cleaver O. Stepwise arteriovenous fate acquisition during mammalian vasculogenesis. Dev Dyn 2011, 240:2153-2165.
128. Cleaver O., Krieg P.A. VEGF mediates angioblast migration during development of the dorsal aorta in Xenopus. Development 1998, 125:3905-3914.
129. Zhong T.P., Childs S., Leu J.P., Fishman M.C. Gridlock signalling pathway fashions the first embryonic artery. Nature 2001, 414:216-220.
130. Jin S.W., Beis D., Mitchell T., Chen J.N., Stainier D.Y. Cellular and molecular analyses of vascular tube and lumen formation in zebrafish. Development 2005, 132:5199-5209.
131. 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.
132. Kohli V., Schumacher J.A., Desai S.P., Rehn K., Sumanas S. Arterial and venous progenitors of the major axial vessels originate at distinct locations. Dev Cell 2013, 25:196-206.
133. Nimmo R., Ciau-Uitz A., Ruiz-Herguido C., et al. MiR-142-3p controls the specification of definitive hemangioblasts during ontogeny. Dev Cell 2013, 26:237-249.
134. Ciau-Uitz A., Wang L., Patient R., Liu F. ETS transcription factors in hematopoietic stem cell development. Blood Cells Mol Dis 2013, 51:248-255.
135. Ciau-Uitz A., Pinheiro P., Gupta R., Enver T., Patient R. Tel1/ETV6 specifies blood stem cells through the agency of VEGF signaling. Dev Cell 2010, 18:569-578.
136. Sabin F.R. Studies on the origin of blood vessels and of red blood corpuscules as seen in the living blastoderm of chicks during the second day of incubation. Contrib Embryol 1920, 9:213-262.
137. Murray P.D.F. The development invitro of the blood of the early chick embryo. Proc R Soc B 1932, 111:497-521.
138. Mandal L., Banerjee U., Hartenstein V. Evidence for a fruit fly hemangioblast and similarities between lymph-gland hematopoiesis in fruit fly and mammal aorta-gonadal-mesonephros mesoderm. Nat Genet 2004, 36:1019-1023.
139. Stainier D.Y., Weinstein B.M., Detrich H.W., Zon L.I., Fishman M.C. Cloche, an early acting zebrafish gene, is required by both the endothelial and hematopoietic lineages. Development 1995, 121:3141-3150.
140. Shalaby F., Ho J., Stanford W.L., et al. A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell 1997, 89:981-990.
141. Shalaby F., Rossant J., Yamaguchi T.P., et al. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 1995, 376:62-66.
142. Lee D., Park C., Lee H., et al. ER71 acts downstream of BMP, Notch, and Wnt signaling in blood and vessel progenitor specification. Cell Stem Cell 2008, 2:497-507.
143. Sumanas S., Gomez G., Zhao Y., Park C., Choi K., Lin S. Interplay among Etsrp/ER71, Scl, and Alk8 signaling controls endothelial and myeloid cell formation. Blood 2008, 111:4500-4510.
144. Vogeli K.M., Jin S.W., Martin G.R., Stainier D.Y. A common progenitor for haematopoietic and endothelial lineages in the zebrafish gastrula. Nature 2006, 443:337-339.
145. Weng W., Sukowati E.W., Sheng G. On hemangioblasts in chicken. PloS One 2007, 2:e1228.
146. Warga R.M., Kane D.A., Ho R.K. Fate mapping embryonic blood in zebrafish: multi- and unipotential lineages are segregated at gastrulation. Dev Cell 2009, 16:744-755.
147. Kennedy M., D'Souza S.L., Lynch-Kattman M., Schwantz S., Keller G. Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures. Blood 2007, 109:2679-2687.
148. Choi K., Kennedy M., Kazarov A., Papadimitriou J.C., Keller G. A common precursor for hematopoietic and endothelial cells. Development 1998, 125:725-732.
149. Huber T.L., Kouskoff V., Fehling H.J., Palis J., Keller G. Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 2004, 432:625-630.
150. Ferkowicz M.J., Yoder M.C. Blood island formation: longstanding observations and modern interpretations. Exp Hematol 2005, 33:1041-1047.
151. Ueno H., Weissman I.L. Clonal analysis of mouse development reveals a polyclonal origin for yolk sac blood islands. Dev Cell 2006, 11:519-533.
152. Myers C.T., Krieg P.A. BMP-mediated specification of the erythroid lineage suppresses endothelial development in blood island precursors. Blood 2013, 122:3929-3939.
153. Walmsley M., Cleaver D., Patient R. Fibroblast growth factor controls the timing of Scl, Lmo2, and Runx1 expression during embryonic blood development. Blood 2008, 111:1157-1166.
154. Fong G.H., Zhang L., Bryce D.M., Peng J. Increased hemangioblast commitment, not vascular disorganization, is the primary defect in flt-1 knock-out mice. Development 1999, 126:3015-3025.
155. Gering M., Yamada Y., Rabbitts T.H., Patient R.K. Lmo2 and Scl/Tal1 convert non-axial mesoderm into haemangioblasts which differentiate into endothelial cells in the absence of Gata1. Development 2003, 130:6187-6199.
156. Schneider V.A., Mercola M. Wnt antagonism initiates cardiogenesis in Xenopus laevis. Genes Dev 2001, 15:304-315.
157. Schoenebeck J.J., Keegan B.R., Yelon D. Vessel and blood specification override cardiac potential in anterior mesoderm. Dev Cell 2007, 13:254-267.
158. Simoes F.C., Peterkin T., Patient R. Fgf differentially controls cross-antagonism between cardiac and haemangioblast regulators. Development 2011, 138:3235-3245.
159. Kattman S.J., Huber T.L., Keller G.M. Multipotent flk-1+ cardiovascular progenitor cells give rise to the cardiomyocyte, endothelial, and vascular smooth muscle lineages. Dev Cell 2006, 11:723-732.
160. Peterkin T., Gibson A., Patient R. Common genetic control of haemangioblast and cardiac development in zebrafish. Development 2009, 136:1465-1474.
161. Liu F., Kang I., Park C., et al. ER71 specifies Flk-1+ hemangiogenic mesoderm by inhibiting cardiac mesoderm and Wnt signaling. Blood 2012, 119:3295-3305.
162. Palencia-Desai S., Kohli V., Kang J., Chi N.C., Black B.L., Sumanas S. Vascular endothelial and endocardial progenitors differentiate as cardiomyocytes in the absence of Etsrp/Etv2 function. Development 2011, 138:4721-4732.
163. Van Handel B., Montel-Hagen A., Sasidharan R., et al. Scl represses cardiomyogenesis in prospective hemogenic endothelium and endocardium. Cell 2012, 150:590-605.
164. Parmar K., Mauch P., Vergilio J.A., Sackstein R., Down J.D. Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci U S A 2007, 104:5431-5436.
165. Winkler I.G., Barbier V., Wadley R., Zannettino A.C., Williams S., Levesque J.P. Positioning of bone marrow hematopoietic and stromal cells relative to blood flow invivo: serially reconstituting hematopoietic stem cells reside in distinct nonperfused niches. Blood 2010, 116:375-385.
166. Takubo K., Goda N., Yamada W., et al. Regulation of the HIF-1alpha level is essential for hematopoietic stem cells. Cell Stem Cell 2010, 7:391-402.
167. Gerber H.P., Malik A.K., Solar G.P., et al. VEGF regulates haematopoietic stem cell survival by an internal autocrine loop mechanism. Nature 2002, 417:954-958.
168. Rehn M., Olsson A., Reckzeh K., et al. Hypoxic induction of vascular endothelial growth factor regulates murine hematopoietic stem cell function in the low-oxygenic niche. Blood 2011, 118:1534-1543.
169. Imanirad P., Solaimani Kartalaei P., Crisan M., et al. HIF1alpha is a regulator of hematopoietic progenitor and stem cell development in hypoxic sites of the mouse embryo. Stem Cell Res 2014, 12:24-35.
170. Harris J.M., Esain V., Frechette G.M., et al. Glucose metabolism impacts the spatiotemporal onset and magnitude of HSC induction invivo. Blood 2013, 121:2483-2493.
171. Simsek T., Kocabas F., Zheng J., et al. The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell 2010, 7:380-390.
172. le Noble F., Moyon D., Pardanaud L., et al. Flow regulates arterial-venous differentiation in the chick embryo yolk sac. Development 2004, 131:361-375.
173. Adamo L., Naveiras O., Wenzel P.L., et al. Biomechanical forces promote embryonic haematopoiesis. Nature 2009, 459:1131-1135.
174. North T.E., Goessling W., Peeters M., et al. Hematopoietic stem cell development is dependent on blood flow. Cell 2009, 137:736-748.
175. Wang L., Zhang P., Wei Y., Gao Y., Patient R., Liu F. A blood flow-dependent klf2a-NO signaling cascade is required for stabilization of hematopoietic stem cell programming in zebrafish embryos. Blood 2011, 118:4102-4110.
176. Miller S.B. Prostaglandins in health and disease: an overview. Semin Arthritis Rheum 2006, 36:37-49.
177. Feher I., Gidali J. Prostaglandin E2 as stimulator of haemopoietic stem cell proliferation. Nature 1974, 247:550-551.
178. Gidali J., Feher I. The effect of E type prostaglandins on the proliferation of haemopoietic stem cells invivo. Cell Tissue Kinet 1977, 10:365-373.
179. Pelus L.M. Association between colony forming units-granulocyte macrophage expression of Ia-like (HLA-DR) antigen and control of granulocyte and macrophage production: A new role for prostaglandin E. J Clin Invest 1982, 70:568-578.
180. Hoggatt J., Singh P., Sampath J., Pelus L.M. Prostaglandin E2 enhances hematopoietic stem cell homing, survival, and proliferation. Blood 2009, 113:5444-5455.
181. Cutler C., Multani P., Robbins D., et al. Prostaglandin-modulated umbilical cord blood hematopoietic stem cell transplantation. Blood 2013, 122:3074-3081.
182. Verma D.S., Spitzer G., Zander A.R., McCredie K.B., Dicke K.A. Prostaglandin E1-mediated augmentation of human granulocyte-macrophage progenitor cell growth invitro. Leukemia Res 1981, 5:65-71.
183. Villablanca E.J., Pistocchi A., Court F.A., et al. Abrogation of prostaglandin E2/EP4 signaling impairs the development of rag1+ lymphoid precursors in the thymus of zebrafish embryos. J Immunol 2007, 179:357-364.
184. North T.E., Goessling W., Walkley C.R., et al. Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis. Nature 2007, 447:1007-1011.
185. Goessling W., North T.E., Loewer S., et al. Genetic interaction of PGE2 and Wnt signaling regulates developmental specification of stem cells and regeneration. Cell 2009, 136:1136-1147.
186. Speth J.M., Hoggatt J., Singh P., Pelus L.M. Pharmacologic increase in HIF1alpha enhances hematopoietic stem and progenitor homing and engraftment. Blood 2014, 123:203-207.
187. Safi R., Muramoto G.G., Salter A.B., et al. Pharmacological manipulation of the RAR/RXR signaling pathway maintains the repopulating capacity of hematopoietic stem cells in culture. Mol Endocrinol 2009, 23:188-201.
188. Chanda B., Ditadi A., Iscove N.N., Keller G. Retinoic acid signaling is essential for embryonic hematopoietic stem cell development. Cell 2013, 155:215-227.
189. Linnemann A.K., O'Geen H., Keles S., Farnham P.J., Bresnick E.H. Genetic framework for GATA factor function in vascular biology. Proc Natl Acad Sci U S A 2011, 108:13641-13646.
190. Greenfest-Allen E., Malik J., Palis J., Stoeckert C.J. Stat and interferon genes identified by network analysis differentially regulate primitive and definitive erythropoiesis. BMC Syst Biol 2013, 7:38.
191. Oostendorp R.A., Harvey K.N., Kusadasi N., et al. Stromal cell lines from mouse aorta-gonads-mesonephros subregions are potent supporters of hematopoietic stem cell activity. Blood 2002, 99:1183-1189.
192. Oostendorp R.A., Medvinsky A.J., Kusadasi N., et al. Embryonal subregion-derived stromal cell lines from novel temperature-sensitive SV40 T antigen transgenic mice support hematopoiesis. J Cell Sci 2002, 115:2099-2108.
193. Taoudi S., Gonneau C., Moore K., et al. Extensive hematopoietic stem cell generation in the AGM region via maturation of VE-cadherin+CD45+ pre-definitive HSCs. Cell Stem Cell 2008, 3:99-108.
194. Mirshekar-Syahkal B., Fitch S.R., Ottersbach K. From greenhouse to garden: The changing soil of the hematopoietic stem cell microenvironment during development. Stem Cells 2014, 32:1691-1700.
195. Mascarenhas M.I., Parker A., Dzierzak E., Ottersbach K. Identification of novel regulators of hematopoietic stem cell development through refinement of stem cell localization and expression profiling. Blood 2009, 114:4645-4653.
196. Magnusson M., Sierra M.I., Sasidharan R., et al. Expansion on stromal cells preserves the undifferentiated state of human hematopoietic stem cells despite compromised reconstitution ability. PloS One 2013, 8:e53912.
197. Durand C., Robin C., Bollerot K., Baron M.H., Ottersbach K., Dzierzak E. Embryonic stromal clones reveal developmental regulators of definitive hematopoietic stem cells. Proc Natl Acad Sci U S A 2007, 104:20838-20843.
198. Mirshekar-Syahkal B., Haak E., Kimber G.M., et al. Dlk1 is a negative regulator of emerging hematopoietic stem and progenitor cells. Haematologica 2013, 98:163-171.
199. Peeters M., Ottersbach K., Bollerot K., et al. Ventral embryonic tissues and Hedgehog proteins induce early AGM hematopoietic stem cell development. Development 2009, 136:2613-2621.
200. Fitch S.R., Kimber G.M., Wilson N.K., et al. Signaling from the sympathetic nervous system regulates hematopoietic stem cell emergence during embryogenesis. Cell Stem Cell 2012, 11:554-566.
201. Pandolfi P.P., Roth M.E., Karis A., et al. Targeted disruption of the GATA3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis. Nat Genet 1995, 11:40-44.
202. Jin H., Xu J., Wen Z. Migratory path of definitive hematopoietic stem/progenitor cells during zebrafish development. Blood 2007, 109:5208-5214.
203. Dieterlen-Lievre F., Pouget C., Bollerot K., Jaffredo T. Are intra-aortic hemopoietic cells derived from endothelial cells during ontogeny?. Trends Cardiovasc Med 2006, 16:128-139.
204. Grayfer L., Robert J. Colony-stimulating factor-1-responsive macrophage precursors reside in the amphibian (Xenopus laevis) bone marrow rather than the hematopoietic subcapsular liver. J Innate Immun 2013, 5:531-542.
205. Bertrand J.Y., Kim A.D., Teng S., Traver D. CD41+ cmyb+ precursors colonize the zebrafish pronephros by a novel migration route to initiate adult hematopoiesis. Development 2008, 135:1853-1862.
206. Nieuwkoop PD, Faber J. Normal table of Xenopus laevis (Daudin): A systematic and chronological survey of the development from the fertilized egg till the end of metamorphosis. Amsterdam: North-Holland Publishing;1967.