Primitive erythropoiesis in the mammalian embryo

International Journal of Developmental Biology

Volumn 54, Issue 6-7, 2010, Pages 1011-1018

  Palis, James ^a   Malik, Jeffrey ^a   McGrath, Kathleen E ^a   Kingsley, Paul D ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Enucleation; Erythropoiesis; Yolk sac

Indexed keywords

BETA GLOBIN; ERYTHROPOIETIN RECEPTOR; JANUS KINASE 2; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR GATA 2; TRANSCRIPTION FACTOR RUNX1;

ANIMAL EMBRYO; ARTICLE; CELL FUNCTION; CELL LINEAGE; CELL MATURATION; CELL SPECIFICITY; EMBRYO DEVELOPMENT; ERYTHROCYTE LIFESPAN; ERYTHROID CELL; ERYTHROID PRECURSOR CELL; ERYTHROPOIESIS; GENE TARGETING; HEMANGIOBLAST; HEMATOPOIESIS; HUMAN; NONHUMAN; PERIPHERAL BLOOD STEM CELL; PRIMITIVE STREAK; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; TRANSCRIPTION REGULATION; YOLK SAC;

ANIMALS; EMBRYO, MAMMALIAN; ERYTHROID CELLS; ERYTHROPOIESIS; GATA1 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, KNOCKOUT;

MAMMALIA;

EID: 77954853923     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.093056jp     Document Type: Article

References (106)

1. BASU P, MORRIS PE, HAAR JL, WANI MA, LINGREL JB, GAENSLER KM, LLOYD JA (2005). KLF2 is essential for primitive erythropoiesis and regulates the human and murine embryonic beta-like globin genes in vivo. Blood 106: 2566-2571.
2. BATEMAN AE, COLE RJ (1971). Stimulation of haem synthesis by erythropoietin in mouse yolk-sac-stage embryonic cells. J Emb Exp Morph 26: 475-480.
3. BARKER JE (1968). Development of the mouse hematopoietic system: I. Types of hemoglobin produced in embryonic yolk sac and liver. Dev Biol 18: 14-29.
4. BELAOUSOFF M, FARRINGTON SM, BARON MH (1999). Hematopoietic induction and respecification of A-P identity by visceral endoderm signaling in the mouse embryo. Development 125: 5009-5018.
5. BETHLENFALVAY NC, BLOCK M (1970). Fetal erythropoiesis. Maturation in megaloblastic (yolk sac) erythropoiesis in the C57Bl/6J mouse. Acta Haematol 44: 240-245.
6. BIELINSKA M, NARITA N, HEIKINHEIMO M, PORTER SB, WILSON DB (1996). Erythropoiesis and vasculogenesis in embryoid bodies lacking visceral yolk sac endoderm. Blood 88: 3720-3730.
7. BOCKAMP E, ANTUNES C, LIEBNER S, SCHMITT S, CABEZAS-WALLSCHEID N, HECK R, OHNNGEMACH S, OESCH-BARTLOMOWICZ B, RICKERT C, SANCHEZ MJ, HENGSTLER J, KAINA B, WILSON A, TRUMPP A, ESHKIND L (2009). In vivo fate mapping with SCL regulatory elements identifies progenitors for primitive and definitive hematopoiesis in mice. Mech Dev 126: 863-872.
8. BOUSSIOS T, BERTLES JF, GOLDWASSER E (1988). Erythropoietin-receptor characteristics during the ontogeny of hamster yolk sac erythroid cells. J Biol Chem 264: 16017-16021.
9. BROTHERTON TW, CHUI DHK, GAULDIE J, PATTERSON M (1979). Hemoglobin ontogeny during normal mouse fetal development. Proc Natl Acad Sci USA 76: 2853-2857.
10. CHENG X, HUBER TL, CHEN VC, GADUE P, KELLER GM (2008). Numb mediates the interaction between Wnt and Notch to modulate primitive erythropoietic specification from the hemangioblast. Development 135: 3447-3458.
11. CHENG Y, WU W, KUMAR SA, YU D, DENG W, TRIPIC T, KING DC, CHEN KB, ZHANG Y, DRAUTZ D, GIARDINE B, SCHUSTER SC, MILLER W, CHIAROMONTE F, ZHANG Y, BLOBEL GA, WEISS MJ, HARDISON RC (2009). Erythroid GATA1 function revealed by genome-wide analysis of transcription factor occupancy, histone modifications, and mRNA expression. Genome Res 19: 2172-2184.
12. COLE RJ, PAUL J (1966). The effects of erythropoietin on haem synthesis in mouse yolk sac and cultured foetal liver cells. J Emb Exp Morph 15: 245-260.
13. DE LA CHAPELLE A, FANTONI A, MARKS P (1969). Differentiation of mammalian somatic cells: DNA and hemoglobin synthesis in fetal mouse yolk sac erythroid cells. Proc Natl Acad Sci USA 63: 812-819.
14. DYER MA, FARRINGTON SM, MOHN D, MONDY JR, BARON MH (2001). Indian hedgehog activates hematopoiesis and vasculogenesis and can respecify neurectodermal cell fate in the mouse embryo. Development 128: 1717-1730.
15. EMA M, YOKOMIZO T, WAKAMATSU A, TERUNUMA T, YAMAMOTO M, TAKAHASHI S (2006). Primitive erythropoiesis from mesodermal precursors expressing VE-cadherin, PECAM-1, Tie2, endoglin, and CD34 in the mouse embryo. Blood 108: 4018-4024.
16. EILKEN HM, NISHIKAWA S, SCHROEDER T (2009). Continuous single-cell imaging of blood generation from haemogenic endothelium. Nature 12: 896-900.
17. FANTONI A, DE LA CHAPELLE A, RIFKIND RA, MARKS PA (1968). Erythroid cell development in fetal mice: synthetic capacity for different proteins. J Mol Biol 33: 79-91.
18. FANTONI A, DE LA CHAPELLE A, MARKS PA (1969). Synthesis of embryonic hemoglobins during erythroid cell development in fetal mice. J Biol Chem 244: 675-681.
19. FARACE MG, BROWN BA, RASCHELLA G, ALEXANDER J, GAMBARI R, FANTONI A, HARDIES SC, HUTCHISON CA 3RD, EDGELL MH (1984). The mouse bh1 gene codes for the z chain of embryonic hemoglobin. J Biol Chem 259: 7123-7128.
20. FERKOWICZ MJ, STARR M, XIE X, LI W, JOHNSON SA, SHELLEY WC, MORRISON PR, YODER MC (2003). CD41 expression defines the onset of primitive and definitive hematopoiesis in the murine embryo. Development 130: 4393-4403.
21. FERKOWICZ MJ, YODER MC (2005). Blood island formation: longstanding observations and modern interpretations. Exp Hematol 33: 1041-1047.
22. FRASER ST, ISERN J, BARON MH (2007). Maturation and enucleation of primitive erythroblasts during mouse embryogenesis is accompanied by changes in cellsurface antigen expression. Blood 109: 343-352.
23. FUJIWARA Y, BROWNE CP, CUNNIFF K, GOFF SC, ORKIN SH (1996). Arrested development of embryonic red cell precursors in mouse embryos lacking transcription factor GATA-1. Proc Natl Acad Sci USA 93: 12355-12358.
24. FUJIWARA T, O'GEEN H, KELES S, BLAHNIK K, LINNEMANN AK, KANG YA, CHOI K, FARNHAM PJ, BRESNICK EH (2009) Discovering hematopoietic mechanisms through genome-wide analysis of GATA factor chromatin occupancy. Mol Cell 36: 667-681.
25. FURUTA C, EMA H, TAKAYANAGI S, OGAERI T, OKAMURA D, MATSUI Y, NAKAUCHI H (2006). Discordant developmental waves of angioblasts and hemangioblasts in the early gastrulating mouse embryo. Development 133: 2771-2779.
26. GARDINER MR, GONGORA MM, GRIMMOND SM, PERKINS AC (2007). A global role for zebrafish klf4 in embryonic erythropoiesis. Mech Dev 124: 762-774.
27. GRASS JA, BOYER ME, PAL S, WU J, WEISS MJ, BRESNICK EH (2003). GATA-1-dependent transcriptional repression of GATA-2 via disruption of positive autoregulation and domain-wide chromatin remodeling. Proc Natl Acad Sci USA 100: 8811-8816.
28. GRASS JA, JING H, KIM SI, MARTOWICZ ML, PAL S, BLOBEL GA, BRESNICK EH (2006). Distinct functions of dispersed GATA factor complexes at an endogenous gene locus. Mol Cell Biol 26: 7056-7067.
29. GRIFFIN CT, BRENNAN J, MAGNUSON T (2008). The chromatin-remodeling enzyme BRG1 plays an essential role in primitive erythropoiesis and vascular development. Development 135: 493-500.
30. HAAR JL, ACKERMAN GA (1971). A phase and electron microscopic study of vasculogenesis and erythropoiesis in the yolk sac of the mouse. Anat Rec 170: 199-224.
31. HADLAND BK, HUPPERT SS, KANUNGO J, XUE Y, JIANG R, GRIDLEY T, CONLON RA, CHENG AM, KOPAN R, LONGMORE GD (2004). A requirement for Notch1 distinguishes 2 phases of definitive hematopoiesis during development. Blood 104: 3097-3105.
32. HODGE D, COGHILL E, KEYS J, MAGUIRE T, HARTMANN B, MCDOWALL A, WEISS M, GRIMMOND S, PERKINS A (2006). A global role for EKLF in definitive and primitive erythropoiesis. Blood 107: 3359-3370.
33. HUBER K, KOUSKOFF V, FEHLING HJ, PALIS J, KELLER G (2004). Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 432: 625-630.
34. ISERN J, FRASER ST, HE Z, BARON MH (2008). The fetal liver is a niche for maturation of primitive erythroid cells. Proc Natl Acad Sci USA 105: 6662-6667.
35. JI RP, PHOON CK, ARISTIZABAL O, MCGRATH KE, PALIS J, TURNBULL DH (2003). Onset of cardiac function during early mouse embryogenesis coincides with entry of primitive erythroblasts into the embryo proper. Circ Res 92: 133-135.
36. JOHANSSON BM, WILES MV (1995). Evidence for involvement of activin A and bone morphogenetic protein 4 in mammalian mesoderm and hematopoietic development. Mol Cell Biol 15: 141-151.
37. JOLLIE WP (1990). Development, morphology, and function of the yolk-sac placenta of laboratory rodents. Teratology 41: 361-381.
38. KALLIANPUR AR, JORDAN JE, BRANDT SJ (1994). The SCL/TAL-1 gene is expressed in progenitors of both the hematopoietic and vascular systems during embryogenesis. Blood 83: 1200-1208.
39. KENNEDY M, D'SOUZA SL, LYNCH-KATTMAN M, SCHWANTZ S, KELLER G (2007). Development of the hemangioblast defines the onset of hematopoiesis in human ES cell differentiation cultures. Blood 109: 2679-2687.
40. KIERAN MW, PERKINS AC, ORKIN SH, ZON LZ (1996). Thrombopoietin rescues in vitro erythroid colony formation from mouse embryos lacking the erythropoietin receptor. Proc Natl Acad Sci USA 93: 9126-9131.
41. KIMURA T, SONODA Y, IWAI N, SATOH M, YAMAGUCHI-TSUKIO M, IZUI T, SUDA M, SASAKI K, NAKANO T (2000). Proliferation and cell death of embryonic primitive erythrocytes. Exp Hematol 28: 635-641.
42. KINGSLEY PD, MALIK J, FANTAUZZO KA, PALIS J (2004). Yolk sac-derived primitive erythroblasts enucleate during mammalian embryogenesis. Blood 104: 19-25.
43. KINGSLEY, PD, MALIK, J, EMERSON, RL, BUSHNELL, TP, MCGRATH, KE, BLOEDORN, LA, BULGER, M, PALIS, J (2006). "Maturational" globin switching in primary primitive erythroid cells. Blood 104: 1667-1672.
44. LACAUD G, GORE L, KENNEDY M, KOUSKOFF V, KINGSLEY P, HOGAN C, CARLSSON L, SPECK N, PALIS J, KELLER G (2002). Runx1 is essential for hematopoietic commitment at the hemangioblast stage of development in vitro. Blood 100: 548-466.
45. LANCRIN C, SROCZYNSKA P, STEPHENSON C, ALLEN T, KOUSKOFF V, LACAUD G (2009). The haemangioblast generates haematopoietic cells through a haemogenic endothelium stage. Nature 12: 892-895.
46. LANDRY JR, BONADIES N, KINSTON S, KNEZEVIC K, WILSON NK, ORAM SH, JANES M, PILTZ S, HAMMETT M, CARTER J, HAMILTON T, DONALDSON IJ, LACAUD G, FRAMPTON J, FOLLOWS G, KOUSKOFF V, GÖTTGENS B (2009). Expression of the leukemia oncogene Lmo2 is controlled by an array of tissue-specific elements dispersed over 100 kb and bound by Tal1/Lmo2, Ets, and Gata factors. Blood 113: 5783-5792.
47. LANDRY JR, KINSTON S, KNEZEVIC K, DE BRUIJN MF, WILSON N, NOTTINGHAM WT, PEITZ M, EDENHOFER F, PIMANDA JE, OTTERSBACH K, GÖTTGENS B (2008). Runx genes are direct targets of Scl/Tal1 in the yolk sac and fetal liver. Blood 111: 3005-3014.
48. LEE R, KERTESZ N, JOSEPH SB, JEGALIAN A, WU H (2001). Erythropoietin (Epo) and EpoR expression and 2 waves of erythropoiesis. Blood 98: 1408-1415.
49. LIN C-S, LIM S-K, D'AGATI V, CONSTANTINI F (1996). Differential effects of an erythropoietin receptor gene disruption on primitive and definitive erythropoiesis. Genes Dev 10: 154-164.
50. LUGUS JJ, PARK C, MA YD, CHOI K (2009). Both primitive and definitive blood cells are derived from Flk-1+ mesoderm. Blood 113: 563-566.
51. MAKITA T, HERNANDEZ-HOYOS G, CHEN TH, WU H, ROTHENBERG EV, SUCOV HM (2001). A developmental transition in definitive erythropoiesis: erythropoietin expression is sequentially regulated by retinoic acid receptors and HNF4. Genes Dev 15: 889-901.
52. MATSUMOTO N, KUBO A, LIU H, AKITA K, LAUB F, RAMIREZ F, KELLER G, FRIEDMAN SL (2006). Developmental regulation of yolk sac hematopoiesis by Kruppel-like factor 6. Blood 107: 1357-1365.
53. MAXIMOW AA (1909). Untersuchungen uber blut und bindegewebe 1. Die fruhesten entwicklungsstadien der blut- und binde- gewebszellan bein saugetierembryo, bis zum anfang der blutbilding unden leber. Arch Mikroskop Anat 73: 444-561.
54. MCGANN JK, SILVER L, LIESVELD J, PALIS J (1997). Erythropoietin-receptor expression and function during the initiation of murine yolk sac erythropoiesis. Exp Hematol 25: 1149-1157.
55. MCGRATH KE, KONISKI AD, MALIK J, PALIS J (2003). Circulation is established in a stepwise pattern in the mammalian embryo. Blood 101: 1669-1676.
56. MCGRATH KE, KINGSLEY PD, KONISKI AD, PORTER RL, BUSHNELL TP, PALIS J (2008). Enucleation of primitive erythroid cells generates a transient population of "pyrenocytes" in the mammalian fetus. Blood 111: 2409-2417.
57. MILLER IJ, BIEKER JJ (1993). A novel, erythroid cell-specific murine transcription factor that binds to the CACCC element and is related to the Krüppel family of nuclear proteins. Mol Cell Biol 13: 2776-2786.
58. MORIOKA K, TONÉ S, MUKAIDA M, TAKANO-OHMURO H (1998). The apoptotic and nonapoptotic nature of the terminal differentiation of erythroid cells. Exp Cell Res 240: 206-217.
59. MOTOYAMA N, KIMURA T, TAKAHASHI T, WATANABE T, NAKANO T (1999). bcl-x prevents apoptotic cell death of both primitive and definitive erythrocytes at the end of maturation. J Exp Med 11: 1691-1698.
60. NEUBAUER H, CUMANO A, MÜLLER M, WU H, HUFFSTADT U, PFEFFER K (1998). Jak2 deficiency defines an essential developmental checkpoint in definitive hematopoiesis. Cell 93: 397-409.
61. NORTH T, GU T-L, STACEY T, WANG Q, HOWARD L, BINDER M, MARÍNPADILLA M, SPECK NA (1999). Cbfa is required for the formation of intra-aortic hematopoietic clusters. Development 126: 2563-2575.
62. NUEZ B, MICHALOVICH D, BYGRAVE A, PLOEMACHER R, GROSVELD F (1995). Defective haematopoiesis in fetal liver resulting from inactivation of the EKLF gene. Nature 375: 316-318.
63. PALIS J, KENNEDY M, ROBERTSON S, WALL C, KELLER G (1999): Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse embryo. Development 126: 5073-5084.
64. PALIS J, KINGSLEY PD, MCGRATH KE (1995): Initiation of hematopoiesis and vasculogenesis in murine yolk sac explants. Blood 86: 156-163.
65. PARK C, MA YD, CHOI K (2005). Evidence for the hemangioblast. Exp Hematol 33: 965-970.
66. PEARSON S, SROCZYNSKA P, LACAUD G, KOUSKOFF V (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.
67. PERKINS AC, SHARPE AH, ORKIN SH (1995). Lethal beta-thalassaemia in mice lacking the erythroid CACCC-transcription factor EKLF. Nature 375: 318-322.
68. PESCHLE C, MAVILIO F, CARÈ A, MIGLIACCIO G, MIGLIACCIO AR, SALVO G, SAMOGGIA P, PETTI S, GUERRIERO R, MARINUCCI M, LAZZARO D, RUSSO G, MASTROBERARDINO G (1985). Haemoglobin switching in human embryos: asynchrony of zeta‡ alpha and epsilon‡ gamma-globin switches in primitive and definite erythropoietic lineage. Nature 313: 235-238.
69. PILON AM, NILSON DG, ZHOU D, SANGERMAN J, TOWNES TM, BODINE DM, GALLAGHER PG (2006). Alterations in expression and chromatin configuration of the alpha hemoglobin-stabilizing protein gene in erythroid Kruppel-like factordeficient mice. Mol Cell Biol 26: 4368-4377.
70. QIU C, OLIVIER EN, VELHO M, BOUHASSIRA EE (2008). Globin switches in yolksac-like primitive and fetal-like definitive red blood cells produced from human embryonic stem cells. Blood 111: 2400-2408.
71. RICHMOND TD, CHOHAN M, BARBER DL (2005). Turning cells red: signal transduction mediated by erythropoietin. Trends Cell Biol 15: 146-155.
72. ROBB L, LYONS I, LI R, HARTLEY L, KÖNTGEN F, HARVEY RP, METCALF D, BEGLEY CG (1995). Absence of yolk sac hematopoiesis from mice with a targeted disruption of the scl gene. Proc Natl Acad Sci USA 92: 7075-7079.
73. ROBERT-MORENO A, ESPINOSA L, SANCHEZ MJ, DE LA POMPA JL, BIGAS A (2007). The notch pathway positively regulates programmed cell death during erythroid differentiation. Leukemia 21: 1496-1503.
74. SABIN FR (1920). Studies on the origin of blood vessels and red blood corpuscles as seen in the living blastoderm of chicks during the second day of incubation. Contrib Embryol 9: 213-262.
75. SANGIORGI F, WOODS CM, LAZARIDES E (1990). Vimentin downregulation is an inherent feature of murine erythropoiesis and occurs independently of lineage. Development 110: 85-96.
76. SASAKI K, KENDALL MD (1985). The morphology of the haematopoietic cells of the yolk sac in mice with particular reference to nucleolar changes. J Anat 140: 279-295.
77. SHIVDASANI RA, MAYER EL, ORKIN SH (1995). Absence of blood formation in mice lacking T-cell leukemia oncoprotein tal-1/SCL. Nature 373: 432-434.
78. SILVER L, PALIS J (1997). Initiation of murine embryonic erythropoiesis: a spatial analysis. Blood 89: 1154-1164.
79. SILVA M, BENITO A, SANZ C, PROSPER F, EKHTERAE D, NUÑEZ G, FERNANDEZ-LUNA JL (1999). Erythropoietin can induce the expression of bclx(L) through Stat5 in erythropoietin-dependent progenitor cell lines. J Biol Chem 274: 22165-22169.
80. SMITH RA, GLOMSKI CA (1977). Embryonic and fetal hemopoiesis in the Mongolian gerbil (Meriones unguiculatus). Anat Rec 189: 499-517.
81. SORENSON GD (1961). An electron microscopic study of hematopoiesis in the yolk sac. Lab Invest 10: 178-193.
82. SOUTHWOOD CM, DOWNS KM, BIEKER JJ (1996). Erythroid Krüppel-like factor exhibits an early and sequentially localized pattern of expression during mammalian erythroid ontogeny. Dev Dyn 206: 248-259.
83. STEINER R, VOGEL H (1973). On the kinetics of erythroid cell differentiation in fetal mice: I. Microspectrophotometric determination of the hemoglobin content in erythroid cells during gestation. J Cell Physiol 81: 323-338.
84. TAKASHINA T (1987). Haemopoiesis in the human yolk sac. J Anat 151: 125-135.
85. TEWARI R, GILLEMANS N, WIJGERDE M, NUEZ B, VON LINDERN M, GROSVELD F, PHILIPSEN S (1998). Erythroid Krüppel-like factor (EKLF) is active in primitive and definitive erythroid cells and is required for the function of 5'HS3 of the beta-globin locus control region. EMBO J 17: 2334-2341.
86. TIEDEMANN K (1977). On the yolk sac of the cat. Cell Tiss Res 183: 171-189.
87. TOBER J, KONISKI A, MCGRATH KE, VEMISHETTI R, EMERSON R, DE MESYBENTLEY KKL, WAUGH R, PALIS J (2007). The megakaryocyte lineage originates from hemangioblast precursors and is an integral component both of primitive and definitive hematopoiesis. Blood 109: 1433-1441.
88. TSANG AP, VISVADER JE, TURNER CA, FUJIWARA Y, YU C, WEISS MJ, CROSSLEY M, ORKIN SH (1997). FOG, a multitype zinc finger protein, acts as a cofactor for transcription factor GATA-1 in erythroid and megakaryocytic differentiation. Cell 90: 109-119.
89. TSANG AP, FUJIWARA Y, HOM DB, ORKIN SH (1998). Failure of megakaryopoiesis and arrested erythropoiesis in mice lacking the GATA-1 transcriptional cofactor FOG. Genes Dev 15: 1176-1188.
90. TSUJI-TAKAYAMA K, OTANI T, INOUE T, NAKAMURA S, MOTODA R, KIBATA M, ORITA K (2006). Erythropoietin induces sustained phosphorylation of STAT5 in primitive but not definitive erythrocytes generated from mouse embryonic stem cells. Exp Hematol 34: 1323-1332.
91. UEDA T, WATANABE-FUKUNAGA R, OGAWA H, FUKUYAMA H, HIGASHI Y, NAGATA S, FUKUNAGA R (2007). Critical role of the p400/mDomino chromatin-remodeling ATPase in embryonic hematopoiesis. Genes Cells 12: 581-592.
92. UENO H, WEISSMAN IL (2006). Clonal analysis of mouse development reveals a polyclonal origin of yolk sac blood islands. Dev Cell 11: 519-533.
93. WADMAN IA, OSADA H, GRÜTZ GG, AGULNICK AD, WESTPHAL H, FORSTER A, RABBITTS TH (1997). The LIM-only protein Lmo2 is a bridging molecule assembling an erythroid, DNA-binding complex which includes the TAL1, E47, GATA-1 and Ldb1/NLI proteins. EMBO J 16: 3145-3157.
94. WANG Q, STACY T, BINDER M, MARIN-PADILLA M, SHARPE AH, SPECK NA (1996). Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc Natl Acad Sci USA 93: 3444-3449.
95. WARREN AJ, COLLEDGE WH, CARLTON MB, EVANS MJ, SMITH AJ, RABBITTS TH (1994). The oncogenic cysteine-rich LIM domain protein is essential for erythroid development. Cell 78: 45-57.
96. WELLS RMG (1979). Hemoglobin-oxygen affinity in developing embryonic erythroid cells of the mouse. J Comp Physiol 129: 333-338.
97. WHITELAW E, TSAI SF, HOGBEN P, ORKIN SH (1990). Regulated expression of globin chains and the erythroid transcription factor GATA-1 during erythropoiesis in the developing mouse. Mol Cell Biol 10: 6596-6606,.
98. WINNIER G, BLESSING M, LABOSKY PA, HOGAN BL (1995). Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev 9: 2105-2116.
99. WONG PMC, CHUNG SW, CHUI DHK, EAVES CJ (1986). Properties of the earliest clonogenic hematopoietic precursors to appear in the developing murine yolk sac. Proc Natl Acad Sci USA 83: 3851-3854.
100. WU H, LIU X, JAENISCH R, LODISH HF (1995). Generation of committed erythroid BFU-E and CFU-E progenitors does not require erythropoietin or the erythropoietin receptor. Cell 83: 59-67.
101. YAMADA Y, WARREN AJ, DOBSON C, FORSTER A, PANNELL R, RABBITTS TH (2000). The oncogenic LIM-only transcription factor Lmo2 regulates angiogenesis but not vasculogenesis in mice. Proc Natl Acad Sci USA 97: 320-324.
102. YOKOMIZO T, HASEGAWA K, ISHITOBI H, OSATO M, EMA M, ITO Y, YAMAMOTO M, TAKAHASHI S (2008). Runx1 is involved in primitive erythropoiesis in the mouse. Blood 111: 4075-4080.
103. YOSHIDA H, KAWANE K, KOIKE M, MORI Y, UCHIYAMA Y, NAGATA S (2005). Phosphatidylserine-dependent engulfment by macrophages of nuclei from erythroid precursor cells. Nature 437: 754-758.
104. YU M, RIVA L, XIE H, SCHINDLER Y, MORAN TB, CHENG Y, YU D, HARDISON R, WEISS MJ, ORKIN SH, BERNSTEIN BE, FRAENKEL E, CANTOR AB (2009). Insights into GATA-1-mediated gene activation versus repression via genome-wide chromatin occupancy analysis. Mol Cell 36: 682-695.
105. ZAMBIDIS ET, PEAULT B, PARK TS, BUNZ F, CIVIN CI (2005). Hematopoietic differentiation of human embryonic stem cells progresses through sequential hematoendothelial, primitive, and definitive stages resembling human yolk sac development. Blood 106: 860-870.
106. ZIMMERMANN F, RICH IN (1997). Mammalian homeobox B6 expression can be correlated with erythropoietin production sites and erythropoiesis during development, but not with hematopoietic or nonhematopoietic stem cell populations. Blood 89: 2723-2739.