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Development, Vol 126, Issue 22 5073-5084, Copyright © 1999 by Company of Biologists

JOURNAL ARTICLES

Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse

J Palis, S Robertson, M Kennedy, C Wall and G Keller
University of Rochester Medical Center, Department of Pediatrics and Cancer Center, Box 777, Rochester, NY 14642, USA. James_Palis@URMC. Rochester.edu.

In this study, we have mapped the onset of hematopoietic development in the mouse embryo using colony-forming progenitor assays and PCR-based gene expression analysis. With this approach, we demonstrate that commitment of embryonic cells to hematopoietic fates begins in proximal regions of the egg cylinder at the mid-primitive streak stage (E7.0) with the simultaneous appearance of primitive erythroid and macrophage progenitors. Development of these progenitors was associated with the expression of SCL/tal-1 and GATA-1, genes known to be involved in the development and maturation of the hematopoietic system. Kinetic analysis revealed the transient nature of the primitive erythroid lineage, as progenitors increased in number in the developing yolk sac until early somite-pair stages of development (E8.25) and then declined sharply to undetectable levels by 20 somite pairs (E9.0). Primitive erythroid progenitors were not detected in any other tissue at any stage of embryonic development. The early wave of primitive erythropoiesis was followed by the appearance of definitive erythroid progenitors (BFU-E) that were first detectable at 1-7 somite pairs (E8.25) exclusively within the yolk sac. The appearance of BFU-E was followed by the development of later stage definitive erythroid (CFU-E), mast cell and bipotential granulocyte/macrophage progenitors in the yolk sac. C-myb, a gene essential for definitive hematopoiesis, was expressed at low levels in the yolk sac just prior to and during the early development of these definitive erythroid progenitors. All hematopoietic activity was localized to the yolk sac until circulation was established (E8.5) at which time progenitors from all lineages were detected in the bloodstream and subsequently in the fetal liver following its development. This pattern of development suggests that definitive hematopoietic progenitors arise in the yolk sac, migrate through the bloodstream and seed the fetal liver to rapidly initiate the first phase of intraembryonic hematopoiesis. Together, these findings demonstrate that commitment to hematopoietic fates begins in early gastrulation, that the yolk sac is the only site of primitive erythropoiesis and that the yolk sac serves as the first source of definitive hematopoietic progenitors during embryonic development.
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C. Huang, F. Sheikh, M. Hollander, C. Cai, D. Becker, P.-H. Chu, S. Evans, and J. Chen
Embryonic atrial function is essential for mouse embryogenesis, cardiac morphogenesis and angiogenesis
Development, December 15, 2003; 130(24): 6111 - 6119.
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W. Li, S. A. Johnson, W. C. Shelley, M. Ferkowicz, P. Morrison, Y. Li, and M. C. Yoder
Primary endothelial cells isolated from the yolk sac and para-aortic splanchnopleura support the expansion of adult marrow stem cells in vitro
Blood, December 15, 2003; 102(13): 4345 - 4353.
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M. Alvarez-Silva, P. Belo-Diabangouaya, J. Salaun, and F. Dieterlen-Lievre
Mouse placenta is a major hematopoietic organ
Development, November 15, 2003; 130(22): 5437 - 5444.
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M. C. Puri and A. Bernstein
Requirement for the TIE family of receptor tyrosine kinases in adult but not fetal hematopoiesis
PNAS, October 28, 2003; 100(22): 12753 - 12758.
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M. J. Ferkowicz, M. Starr, X. Xie, W. Li, S. A. Johnson, W. C. Shelley, P. R. Morrison, and M. C. Yoder
CD41 expression defines the onset of primitive and definitive hematopoiesis in the murine embryo
Development, September 15, 2003; 130(18): 4393 - 4403.
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H. J. Fehling, G. Lacaud, A. Kubo, M. Kennedy, S. Robertson, G. Keller, and V. Kouskoff
Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation
Development, September 1, 2003; 130(17): 4217 - 4227.
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N. Minegishi, N. Suzuki, T. Yokomizo, X. Pan, T. Fujimoto, S. Takahashi, T. Hara, A. Miyajima, S.-i. Nishikawa, and M. Yamamoto
Expression and domain-specific function of GATA-2 during differentiation of the hematopoietic precursor cells in midgestation mouse embryos
Blood, August 1, 2003; 102(3): 896 - 905.
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D. Sugiyama, M. Ogawa, I. Hirose, T. Jaffredo, K.-i. Arai, and K. Tsuji
Erythropoiesis from acetyl LDL incorporating endothelial cells at the preliver stage
Blood, June 15, 2003; 101(12): 4733 - 4738.
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X. Chu, J. Chen, M. C. Reedy, C. Vera, K.-L. P. Sung, and L. A. Sung
E-Tmod capping of actin filaments at the slow-growing end is required to establish mouse embryonic circulation
Am J Physiol Heart Circ Physiol, May 1, 2003; 284(5): H1827 - H1838.
[Abstract] [Full Text] [PDF]

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M. Walmsley, A. Ciau-Uitz, and R. Patient
Adult and embryonic blood and endothelium derive from distinct precursor populations which are differentially programmed by BMP in Xenopus
Development, March 14, 2003; 129(24): 5683 - 5695.
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A. Damert, L. Miquerol, M. Gertsenstein, W. Risau, and A. Nagy
Insufficient VEGFA activity in yolk sac endoderm compromises haematopoietic and endothelial differentiation
Development, March 6, 2003; 129(8): 1881 - 1892.
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M. T. Mitjavila-Garcia, M. Cailleret, I. Godin, M. M. Nogueira, K. Cohen-Solal, V. Schiavon, Y. Lecluse, F. Le Pesteur, A. H. Lagrue, and W. Vainchenker
Expression of CD41 on hematopoietic progenitors derived from embryonic hematopoietic cells
Development, March 6, 2003; 129(8): 2003 - 2013.
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K. E. McGrath, A. D. Koniski, J. Malik, and J. Palis
Circulation is established in a stepwise pattern in the mammalian embryo
Blood, March 1, 2003; 101(5): 1669 - 1675.
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X. Xie, R. J. Chan, S. A. Johnson, M. Starr, J. McCarthy, R. Kapur, and M. C. Yoder
Thrombopoietin promotes mixed lineage and megakaryocytic colony-forming cell growth but inhibits primitive and definitive erythropoiesis in cells isolated from early murine yolk sacs
Blood, February 15, 2003; 101(4): 1329 - 1335.
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R. P. Ji, C. K.L. Phoon, O. Aristizabal, K. E. McGrath, J. Palis, and D. H. Turnbull
Onset of Cardiac Function During Early Mouse Embryogenesis Coincides With Entry of Primitive Erythroblasts Into the Embryo Proper
Circ. Res., February 7, 2003; 92(2): 133 - 135.
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M. Ema, P. Faloon, W. J. Zhang, M. Hirashima, T. Reid, W. L. Stanford, S. Orkin, K. Choi, and J. Rossant
Combinatorial effects of Flk1 and Tal1 on vascular and hematopoietic development in the mouse
Genes & Dev., February 1, 2003; 17(3): 380 - 393.
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K. M. McNagny and T. Graf
E26 leukemia virus converts primitive erythroid cells into cycling multilineage progenitors
Blood, February 1, 2003; 101(3): 1103 - 1110.
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H. K. A. Mikkola, Y. Fujiwara, T. M. Schlaeger, D. Traver, and S. H. Orkin
Expression of CD41 marks the initiation of definitive hematopoiesis in the mouse embryo
Blood, January 15, 2003; 101(2): 508 - 516.
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B. Liu, Y. Sun, F. Jiang, S. Zhang, Y. Wu, Y. Lan, X. Yang, and N. Mao
Disruption of Smad5 gene leads to enhanced proliferation of high-proliferative potential precursors during embryonic hematopoiesis
Blood, January 1, 2003; 101(1): 124 - 133.
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B. de Andres, P. Gonzalo, S. Minguet, J. A. Martinez-Marin, P. G. Soro, M. A. R. Marcos, and M. L. Gaspar
The first 3 days of B-cell development in the mouse embryo
Blood, December 1, 2002; 100(12): 4074 - 4081.
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G. Lacaud, L. Gore, M. Kennedy, V. Kouskoff, P. Kingsley, C. Hogan, L. Carlsson, N. Speck, J. Palis, and G. Keller
Runx1 is essential for hematopoietic commitment at the hemangioblast stage of development in vitro
Blood, June 28, 2002; 100(2): 458 - 466.
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H. C. Masuoka and T. M. Townes
Targeted disruption of the activating transcription factor 4 gene results in severe fetal anemia in mice
Blood, February 1, 2002; 99(3): 736 - 745.
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Y. S. Chung, W. J. Zhang, E. Arentson, P. D. Kingsley, J. Palis, and K. Choi
Lineage analysis of the hemangioblast as defined by FLK1 and SCL expression
Development, January 12, 2002; 129(23): 5511 - 5520.
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E. C. Liao, N. S. Trede, D. Ransom, A. Zapata, M. Kieran, and L. I. Zon
Non-cell autonomous requirement for the bloodless gene in primitive hematopoiesis of zebrafish
Development, January 2, 2002; 129(3): 649 - 659.
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H. Hisakawa, D. Sugiyama, I. Nishijima, M.-j. Xu, H. Wu, K. Nakao, S. Watanabe, M. Katsuki, S. Asano, K.-i. Arai, et al.
Human granulocyte-macrophage colony-stimulating factor (hGM-CSF) stimulates primitive and definitive erythropoiesis in mouse embryos expressing hGM-CSF receptors but not erythropoietin receptors
Blood, December 15, 2001; 98(13): 3618 - 3625.
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M.-J. Sanchez, E.-O. Bockamp, J. Miller, L. Gambardella, and A. R. Green
Selective rescue of early haematopoietic progenitors in Scl-/- mice by expressing Scl under the control of a stem cell enhancer
Development, December 1, 2001; 128(23): 4815 - 4827.
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R. C. R. Perlingeiro, M. Kyba, and G. Q. Daley
Clonal analysis of differentiating embryonic stem cells reveals a hematopoietic progenitor with primitive erythroid and adult lymphoid-myeloid potential
Development, November 15, 2001; 128(22): 4597 - 4604.
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J. A. Martinez-M., S. Minguet, P. Gonzalo, P. G. Soro, B. de Andres, A. Izcue, M. A. R. Marcos, and M.-L. Gaspar
Long-lived polyclonal B-cell lines derived from midgestation mouse embryo lymphohematopoietic progenitors reconstitute adult immunodeficient mice
Blood, September 15, 2001; 98(6): 1862 - 1871.
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R. Lee, N. Kertesz, S. B. Joseph, A. Jegalian, and H. Wu
Erythropoietin (Epo) and EpoR expression and 2 waves of erythropoiesis
Blood, September 1, 2001; 98(5): 1408 - 1415.
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M. C. Yoder
Introduction: spatial origin of murine hematopoietic stem cells
Blood, July 1, 2001; 98(1): 3 - 5.
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S. Matsuoka, K. Tsuji, H. Hisakawa, M.-j. Xu, Y. Ebihara, T. Ishii, D. Sugiyama, A. Manabe, R. Tanaka, Y. Ikeda, et al.
Generation of definitive hematopoietic stem cells from murine early yolk sac and paraaortic splanchnopleures by aorta-gonad-mesonephros region-derived stromal cells
Blood, July 1, 2001; 98(1): 6 - 12.
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J. Palis, R. J. Chan, A. Koniski, R. Patel, M. Starr, and M. C. Yoder
Spatial and temporal emergence of high proliferative potential hematopoietic precursors during murine embryogenesis
PNAS, April 10, 2001; 98(8): 4528 - 4533.
[Abstract] [Full Text] [PDF]


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