Blood cell generation from the hemangioblast

Journal of Molecular Medicine

Volumn 88, Issue 2, 2010, Pages 167-172

  Lancrin, Christophe ^a   Sroczynska, Patrycja ^a   Serrano, Alicia G ^a   Gandillet, Arnaud ^a   Ferreras, Cristina ^a   Kouskoff, Valerie ^a   Lacaud, Georges ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Hemangioblast; Hematopoiesis; Hemogenic endothelium; Leukemia; Stem cells; Transcription factors

Indexed keywords

NOTCH RECEPTOR; STEM CELL ANTIGEN 1; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR RUNX1; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN RECEPTOR 2;

BLOOD CELL; CELL LINEAGE; CELL MATURATION; COLONY FORMING CELL; ECTODERM; EMBRYONIC STEM CELL; ERYTHROCYTE; ERYTHROID CELL; ERYTHROPOIESIS; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCUS; GENE TRANSLOCATION; HEMANGIOBLAST; MESODERM; NONHUMAN; PROGENY; REVIEW;

ANIMALS; BLOOD CELLS; CELL DIFFERENTIATION; CELL LINEAGE; HEMANGIOBLASTS; HEMATOPOIESIS; HUMANS; LEUKEMIA; MICE; TRANSCRIPTION FACTORS;

EID: 77951204123     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00109-009-0554-0     Document Type: Review

References (63)

1. FR Sabin 1920 Studies on the origin of blood vessels and of red corpuscules as seen in the living blastoderm of the chick during the second day of incubation: contributions to embryology Contrib Embryol 9 213 262
2. PDF Murray 1932 The development in vitro of the blood of the early chick embryo Proc R Soc Lond 11 497 521 10.1098/rspb.1932.0070
3. J Palis S Robertson M Kennedy C Wall G Keller 1999 Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse Development 126 5073 5084 1:CAS:528:DyaK1MXotV2lsbs%3D 10529424
4. O Klimchenko M Mori A Distefano T Langlois F Larbret Y Lecluse O Feraud W Vainchenker F Norol N Debili 2009 A common bipotent progenitor generates the erythroid and megakaryocyte lineages in embryonic stem cell-derived primitive hematopoiesis Blood 114 1506 1517 10.1182/blood-2008-09-178863 1:CAS:528:DC%2BD1MXhtVyiur3P 19478046
5. J Tober A Koniski KE McGrath R Vemishetti R Emerson KK de Mesy-Bentley R Waugh J Palis 2007 The megakaryocyte lineage originates from hemangioblast precursors and is an integral component both of primitive and of definitive hematopoiesis Blood 109 1433 1441 10.1182/blood-2006-06-031898 1:CAS:528:DC%2BD2sXjt1Cgs7w%3D 17062726 (Pubitemid 46239574)
6. M Kennedy M Firpo K Choi C Wall S Robertson N Kabrun G Keller 1997 A common precursor for primitive erythropoiesis and definitive haematopoiesis Nature 386 488 493 10.1038/386488a0 1:CAS:528:DyaK2sXisVWjsro%3D 9087406 (Pubitemid 27164073)
7. K Choi M Kennedy A Kazarov JC Papadimitriou G Keller 1998 A common precursor for hematopoietic and endothelial cells Development 125 725 732 1:CAS:528:DyaK1cXhvFWmtbw%3D 9435292
8. HJ Fehling G Lacaud A Kubo M Kennedy S Robertson G Keller V Kouskoff 2003 Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation Development 130 4217 4227 10.1242/dev.00589 1:CAS:528:DC%2BD3sXntFejsL4%3D 12874139 (Pubitemid 37063436)
9. C Lancrin P Sroczynska C Stephenson T Allen V Kouskoff G Lacaud 2009 The haemangioblast generates haematopoietic cells through a haemogenic endothelium stage Nature 457 892 895 10.1038/nature07679 1:CAS:528:DC%2BD1MXht1eht74%3D 19182774
10. TL Huber V Kouskoff HJ Fehling J Palis G Keller 2004 Haemangioblast commitment is initiated in the primitive streak of the mouse embryo Nature 432 625 630 10.1038/nature03122 1:CAS:528:DC%2BD2cXhtVeht7rI 15577911 (Pubitemid 39626269)
11. KM Vogeli SW Jin GR Martin DY Stainier 2006 A common progenitor for haematopoietic and endothelial lineages in the zebrafish gastrula Nature 443 337 339 10.1038/nature05045 1:CAS:528:DC%2BD28Xpslaksr4%3D 16988712 (Pubitemid 44435152)
12. H Ueno IL Weissman 2006 Clonal analysis of mouse development reveals a polyclonal origin for yolk sac blood islands Dev Cell 11 519 533 10.1016/j.devcel.2006.08.001 1:CAS:528:DC%2BD28XhtFWqtLzL 17011491 (Pubitemid 44430897)
13. JJ Lugus C Park YD Ma K Choi 2009 Both primitive and definitive blood cells are derived from Flk-1+ mesoderm Blood 113 563 566 10.1182/blood-2008-06- 162750 1:CAS:528:DC%2BD1MXht1Wns7c%3D 18957687
14. E Gunsilius HC Duba AL Petzer CM Kahler K Grunewald G Stockhammer C Gabl S Dirnhofer J Clausen G Gastl 2000 Evidence from a leukaemia model for maintenance of vascular endothelium by bone-marrow-derived endothelial cells Lancet 355 1688 1691 10.1016/S0140-6736(00)02241-8 1:CAS:528: DC%2BD3cXjvFSkurc%3D 10905245
15. E Pelosi M Valtieri S Coppola R Botta M Gabbianelli V Lulli G Marziali B Masella R Muller C Sgadari U Testa G Bonanno C Peschle 2002 Identification of the hemangioblast in postnatal life Blood 100 3203 3208 10.1182/blood-2002-05- 1511 1:CAS:528:DC%2BD38XosVSisLc%3D 12384418 (Pubitemid 35217068)
16. AS Bailey S Jiang M Afentoulis CI Baumann DA Schroeder SB Olson MH Wong WH Fleming 2004 Transplanted adult hematopoietic stems cells differentiate into functional endothelial cells Blood 103 13 19 10.1182/blood-2003-05-1684 1:CAS:528:DC%2BD2cXhsFCrtA%3D%3D 12958072 (Pubitemid 38029913)
17. MB Grant WS May S Caballero GA Brown SM Guthrie RN Mames BJ Byrne T Vaught PE Spoerri AB Peck EW Scott 2002 Adult hematopoietic stem cells provide functional hemangioblast activity during retinal neovascularization Nat Med 8 607 612 10.1038/nm0602-607 1:CAS:528:DC%2BD38XktVyit70%3D 12042812 (Pubitemid 34633439)
18. S Jiang AS Bailey DC Goldman JR Swain MH Wong PR Streeter WH Fleming 2008 Hematopoietic stem cells contribute to lymphatic endothelium PLoS ONE 3 e3812 10.1371/journal.pone.0003812 19043576 (Pubitemid 352749428)
19. AL Medvinsky NL Samoylina AM Muller EA Dzierzak 1993 An early pre-liver intraembryonic source of CFU-S in the developing mouse Nature 364 64 67 10.1038/364064a0 1:STN:280:DyaK3szgt1ymsw%3D%3D 8316298 (Pubitemid 23233456)
20. MF de Bruijn NA Speck MC Peeters E Dzierzak 2000 Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo Embo J 19 2465 2474 10.1093/emboj/19.11.2465 10835345
21. KE Rhodes C Gekas Y Wang CT Lux CS Francis DN Chan S Conway SH Orkin MC Yoder HK Mikkola 2008 The emergence of hematopoietic stem cells is initiated in the placental vasculature in the absence of circulation Cell Stem Cell 2 252 263 10.1016/j.stem.2008.01.001 1:CAS:528:DC%2BD1cXjslegtro%3D 18371450 (Pubitemid 351298590)
22. BM Zeigler D Sugiyama M Chen Y Guo KM Downs NA Speck 2006 The allantois and chorion, when isolated before circulation or chorio-allantoic fusion, have hematopoietic potential Development 133 4183 4192 10.1242/dev.02596 1:CAS:528:DC%2BD28XhtlehsLfO 17038514 (Pubitemid 44830662)
23. F Dieterlen-Lievre C Martin 1981 Diffuse intraembryonic hemopoiesis in normal and chimeric avian development Dev Biol 88 180 191 10.1016/0012-1606(81) 90228-1 1:STN:280:DyaL38%2FivVejsg%3D%3D 7286444
24. JA Garcia-Porrero IE Godin F Dieterlen-Lievre 1995 Potential intraembryonic hemogenic sites at pre-liver stages in the mouse Anat Embryol (Berl) 192 425 435 1:STN:280:DyaK287is1elsQ%3D%3D
25. M Tavian L Coulombel D Luton HS Clemente F Dieterlen-Lievre B Peault 1996 Aorta-associated CD34+ hematopoietic cells in the early human embryo Blood 87 67 72 1:CAS:528:DyaK28XitF2qtA%3D%3D 8547678
26. T Jaffredo R Gautier V Brajeul F Dieterlen-Lievre 2000 Tracing the progeny of the aortic hemangioblast in the avian embryo Dev Biol 224 204 214 10.1006/dbio.2000.9799 1:CAS:528:DC%2BD3cXltlCjt7c%3D 10926760 (Pubitemid 30661005)
27. T Jaffredo R Gautier A Eichmann F Dieterlen-Lievre 1998 Intraaortic hemopoietic cells are derived from endothelial cells during ontogeny Development 125 4575 4583 1:CAS:528:DyaK1MXhtFaltA%3D%3D 9778515
28. SI Nishikawa S Nishikawa H Kawamoto H Yoshida M Kizumoto H Kataoka Y Katsura 1998 In vitro generation of lymphohematopoietic cells from endothelial cells purified from murine embryos Immunity 8 761 769 10.1016/S1074-7613(00) 80581-6 1:CAS:528:DyaK1cXktFOkt7s%3D 9655490 (Pubitemid 28294523)
29. HM Eilken S Nishikawa T Schroeder 2009 Continuous single-cell imaging of blood generation from haemogenic endothelium Nature 457 896 900 10.1038/nature07760 1:CAS:528:DC%2BD1MXhslCnt7c%3D 19212410
30. MJ Chen T Yokomizo BM Zeigler E Dzierzak NA Speck 2009 Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter Nature 457 887 891 10.1038/nature07619 1:CAS:528:DC%2BD1MXht1ehsbw%3D 19129762
31. AC Zovein JJ Hofmann M Lynch WJ French KA Turlo Y Yang MS Becker L Zanetta E Dejana JC Gasson MD Tallquist ML Iruela-Arispe 2008 Fate tracing reveals the endothelial origin of hematopoietic stem cells Cell Stem Cell 3 625 636 10.1016/j.stem.2008.09.018 1:CAS:528:DC%2BD1cXhsFCqsLjK 19041779
32. E Lecuyer T Hoang 2004 SCL: from the origin of hematopoiesis to stem cells and leukemia Exp Hematol 32 11 24 10.1016/j.exphem.2003.10.010 1:CAS:528:DC%2BD2cXjsFemug%3D%3D 14725896 (Pubitemid 38064397)
33. RA Shivdasani EL Mayer SH Orkin 1995 Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL Nature 373 432 434 10.1038/373432a0 1:CAS:528:DyaK2MXjsFCjs7Y%3D 7830794
34. C Porcher W Swat K Rockwell Y Fujiwara FW Alt SH Orkin 1996 The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages Cell 86 47 57 10.1016/S0092-8674(00)80076-8 1:CAS:528: DyaK28XktlGnsLs%3D 8689686 (Pubitemid 26256577)
35. M Endoh M Ogawa S Orkin S Nishikawa 2002 SCL/tal-1-dependent process determines a competence to select the definitive hematopoietic lineage prior to endothelial differentiation EMBO J 21 6700 6708 10.1093/emboj/cdf674 1:CAS:528:DC%2BD38XpslOgsr8%3D 12485991 (Pubitemid 36014542)
36. SL D'Souza AG Elefanty G Keller 2005 SCL/Tal-1 is essential for hematopoietic commitment of the hemangioblast but not for its development Blood 105 3862 3870 10.1182/blood-2004-09-3611 15677567 (Pubitemid 40656129)
37. TM Schlaeger HK Mikkola C Gekas HB Helgadottir SH Orkin 2005 Tie2Cre-mediated gene ablation defines the stem-cell leukemia gene (SCL/tal1)-dependent window during hematopoietic stem-cell development Blood 105 3871 3874 10.1182/blood-2004-11-4467 1:CAS:528:DC%2BD2MXktlSrsL0%3D 15677556 (Pubitemid 40656130)
38. M Gering AR Rodaway B Gottgens RK Patient AR Green 1998 The SCL gene specifies haemangioblast development from early mesoderm EMBO J 17 4029 4045 10.1093/emboj/17.14.4029 1:CAS:528:DyaK1cXltFygtL0%3D 9670018 (Pubitemid 28333987)
39. I Ismailoglu G Yeamans GQ Daley RC Perlingeiro M Kyba 2008 Mesodermal patterning activity of SCL Exp Hematol 36 1593 1603 10.1016/j.exphem.2008.07.005 1:CAS:528:DC%2BD1cXhtlyhsr%2FO 18809240
40. H Miyoshi K Shimizu T Kozu N Maseki Y Kaneko M Ohki 1991 t(8;21) breakpoints on chromosome 21 in acute myeloid leukemia are clustered within a limited region of a single gene, AML1 Proc Natl Acad Sci USA 88 10431 10434 10.1073/pnas.88.23.10431 1:CAS:528:DyaK3sXhs1Kht78%3D 1720541
41. AT Look 1997 Oncogenic transcription factors in the human acute leukemias Science 278 1059 1064 10.1126/science.278.5340.1059 1:CAS:528: DyaK2sXnt1Wju74%3D 9353180 (Pubitemid 27517875)
42. JW Schindler D Van Buren A Foudi O Krejci J Qin SH Orkin H Hock 2009 TEL-AML1 corrupts hematopoietic stem cells to persist in the bone marrow and initiate leukemia Cell Stem Cell 5 43 53 10.1016/j.stem.2009.04.019 1:CAS:528:DC%2BD1MXoslCnsrc%3D 19570513
43. T Okuda J van Deursen SW Hiebert G Grosveld JR Downing 1996 AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis Cell 84 321 330 10.1016/S0092-8674(00) 80986-1 1:CAS:528:DyaK28Xnt1egug%3D%3D 8565077 (Pubitemid 26042836)
44. T Yokomizo K Hasegawa H Ishitobi M Osato M Ema Y Ito M Yamamoto S Takahashi 2008 Runx1 is involved in primitive erythropoiesis in the mouse Blood 111 4075 4080 10.1182/blood-2007-05-091637 1:CAS:528:DC%2BD1cXkvFeis7w%3D 18250229
45. G Lacaud L Gore M Kennedy V Kouskoff P Kingsley C Hogan L Carlsson N Speck J Palis G Keller 2002 Runx1 is essential for hematopoietic commitment at the hemangioblast stage of development in vitro Blood 100 458 466 10.1182/blood-2001-12-0321 1:CAS:528:DC%2BD38XlsVWgtrY%3D 12091336 (Pubitemid 34761107)
46. Z Li MJ Chen T Stacy NA Speck 2006 Runx1 function in hematopoiesis is required in cells that express Tek Blood 107 106 110 10.1182/blood-2005-05-1955 1:CAS:528:DC%2BD28XhsVGgtQ%3D%3D 16174759 (Pubitemid 43053530)
47. A Liakhovitskaia R Gribi E Stamateris G Villain T Jaffredo R Wilkie D Gilchrist J Yang J Ure A Medvinsky 2009 Restoration of Runx1 expression in the Tie2 cell compartment rescues definitive hematopoietic stem cells and extends life of Runx1 knockout animals until birth Stem Cells 27 1616 1624 10.1002/stem.71 1:CAS:528:DC%2BD1MXhtVGjsbzP 19544462
48. M Hoogenkamp M Lichtinger H Krysinska C Lancrin D Clarke A Williamson L Mazzarella R Ingram H Jorgensen A Fisher DG Tenen V Kouskoff G Lacaud C Bonifer 2009 Early chromatin unfolding by RUNX1: a molecular explanation for differential requirements during specification versus maintenance of the hematopoietic gene expression program Blood 114 299 309 10.1182/blood-2008-11- 191890 1:CAS:528:DC%2BD1MXovVKmu7k%3D 19339695
49. X Cheng TL Huber VC Chen P Gadue GM Keller 2008 Numb mediates the interaction between Wnt and Notch to modulate primitive erythropoietic specification from the hemangioblast Development 135 3447 3458 10.1242/dev.025916 1:CAS:528:DC%2BD1cXhsVarurzI 18799543
50. CE Burns D Traver E Mayhall JL Shepard LI Zon 2005 Hematopoietic stem cell fate is established by the Notch-Runx pathway Genes Dev 19 2331 2342 10.1101/gad.1337005 1:CAS:528:DC%2BD2MXhtFais7%2FL 16166372 (Pubitemid 41396910)
51. M Nakagawa M Ichikawa K Kumano S Goyama M Kawazu T Asai S Ogawa M Kurokawa S Chiba 2006 AML1/Runx1 rescues Notch1-null mutation-induced deficiency of para-aortic splanchnopleural hematopoiesis Blood 108 3329 3334 10.1182/blood-2006-04-019570 1:CAS:528:DC%2BD28Xht1ahsL7I 16888092
52. T Yokomizo S Takahashi N Mochizuki T Kuroha M Ema A Wakamatsu R Shimizu O Ohneda M Osato H Okada T Komori M Ogawa S Nishikawa Y Ito M Yamamoto 2007 Characterization of GATA-1(+) hemangioblastic cells in the mouse embryo Embo J 26 184 196 10.1038/sj.emboj.7601480 1:CAS:528:DC%2BD2sXivFOrtA%3D%3D 17159898 (Pubitemid 46094710)
53. JJ Lugus YS Chung JC Mills SI Kim J Grass M Kyba JM Doherty EH Bresnick K Choi 2007 GATA2 functions at multiple steps in hemangioblast development and differentiation Development 134 393 405 10.1242/dev.02731 1:CAS:528: DC%2BD2sXhvFGmsbs%3D 17166922
54. F Liu M Walmsley A Rodaway R Patient 2008 Fli1 acts at the top of the transcriptional network driving blood and endothelial development Curr Biol 18 1234 1240 10.1016/j.cub.2008.07.048 1:CAS:528:DC%2BD1cXhtVamtrbJ 18718762
55. Y Guo R Chan H Ramsey W Li X Xie WC Shelley JP Martinez-Barbera B Bort K Zaret M Yoder R Hromas 2003 The homeoprotein Hex is required for hemangioblast differentiation Blood 102 2428 2435 10.1182/blood-2003-02-0634 1:CAS:528:DC%2BD3sXnslyktLo%3D 12791650 (Pubitemid 37193579)
56. A Kubo V Chen M Kennedy E Zahradka GQ Daley G Keller 2005 The homeobox gene HEX regulates proliferation and differentiation of hemangioblasts and endothelial cells during ES cell differentiation Blood 105 4590 4597 10.1182/blood-2004-10-4137 1:CAS:528:DC%2BD2MXlsVWjtbw%3D 15728128 (Pubitemid 40807276)
57. D Lee C Park H Lee JJ Lugus SH Kim E Arentson YS Chung G Gomez M Kyba S Lin R Janknecht DS Lim K Choi 2008 ER71 acts downstream of BMP, Notch, and Wnt signaling in blood and vessel progenitor specification Cell Stem Cell 2 497 507 10.1016/j.stem.2008.03.008 1:CAS:528:DC%2BD1cXmt1WrsL8%3D 18462699 (Pubitemid 351598081)
58. LJ Patterson M Gering CE Eckfeldt AR Green CM Verfaillie SC Ekker R Patient 2007 The transcription factors Scl and Lmo2 act together during development of the hemangioblast in zebrafish Blood 109 2389 2398 10.1182/blood-2006-02-003087 1:CAS:528:DC%2BD2sXnslygs7s%3D 17090656 (Pubitemid 46425879)
59. RC Perlingeiro 2007 Endoglin is required for hemangioblast and early hematopoietic development Development 134 3041 3048 10.1242/dev.002907 1:CAS:528:DC%2BD2sXhtV2qtLvE 17634194 (Pubitemid 47386915)
60. JE Pimanda IJ Donaldson MF de Bruijn S Kinston K Knezevic L Huckle S Piltz JR Landry AR Green D Tannahill B Gottgens 2007 The SCL transcriptional network and BMP signaling pathway interact to regulate RUNX1 activity Proc Natl Acad Sci USA 104 840 845 10.1073/pnas.0607196104 1:CAS:528:DC%2BD2sXhtVegtrg%3D 17213321 (Pubitemid 46154698)
61. JE Pimanda WY Chan NK Wilson AM Smith S Kinston K Knezevic ME Janes JR Landry A Kolb-Kokocinski J Frampton D Tannahill K Ottersbach GA Follows G Lacaud V Kouskoff B Gottgens 2008 Endoglin expression in blood and endothelium is differentially regulated by modular assembly of the Ets/Gata hemangioblast code Blood 112 4512 4522 10.1182/blood-2008-05-157560 1:CAS:528:DC%2BD1cXhsVCltb3F 18805961
62. S Pearson P Sroczynska G Lacaud V Kouskoff 2008 The stepwise specification of embryonic stem cells to hematopoietic fate is driven by sequential exposure to Bmp4, activin A, bFGF and VEGF Development 135 1525 1535 10.1242/dev.011767 1:CAS:528:DC%2BD1cXmtFaksrs%3D 18339678 (Pubitemid 351753642)
63. J Yamashita H Itoh M Hirashima M Ogawa S Nishikawa T Yurugi M Naito K Nakao 2000 Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors Nature 408 92 96 10.1038/35040568 1:CAS:528: DC%2BD3cXotVaks7g%3D 11081514