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

Palis, James, Robertson, Scott, Kennedy, Marion, Wall, Charles, Keller, Gordon·1999·Development
DOI 10.1242/dev.126.22.5073
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Abstract

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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Research works printed but not linked: 47

  1. Barker, 1968, Development of the mouse hematopoietic system: I. Types of hemoglobin produced in embryonic yolk sac and liver, Dev. Biol, 18, 14, 10.1016/0012-1606(68)90020-1 · DOI
  2. Beaupain, 1979, Are developmental hemoglobin changes related to the origin of stem cells and site of hematopoiesis?, Blood, 53, 212, 10.1182/blood.V53.2.212.212 · DOI
  3. Begley, 1999, The SCL gene: from case report to critical hematopoietic regulator, Blood, 93, 2760, 10.1182/blood.V93.9.2760.409k44_2760_2770 · DOI
  4. Belaousoff, 1999, Hematopoietic induction and respecification of A-P identity by visceral endoderm signaling in the mouse embryo, Development, 125, 5009, 10.1242/dev.125.24.5009 · DOI
  5. Brady, 1990, Representative in vitro cDNA amplification from individual hematopoietic cells and colonies, Meth. Mol. Cell. Biol, 2, 17
  6. Brotherton, 1979, Hemoglobin ontogeny during normal mouse fetal development, Proc. Natl. Acad. Sci. USA, 76, 2853, 10.1073/pnas.76.6.2853 · DOI
  7. Caprioli, 1998, Blood-bourne seeding by hematopoietic and endothelial precursors from the allantois, Proc. Natl. Acad Sci. USA, 95, 1641, 10.1073/pnas.95.4.1641 · DOI
  8. Choi, 1998, A common precursor for hematopoietic and endothelial cells, Development, 125, 725, 10.1242/dev.125.4.725 · DOI
  9. Copp, 1995, Death before birth: clues from gene knockouts and mutations, Trends Genet, 11, 87, 10.1016/S0168-9525(00)89008-3 · DOI
  10. Cormier, 1988, The wall of the chick embryo aorta harbours M-CFC, G-CFC, GM-CFC and BFU-E, Development, 102, 279, 10.1242/dev.102.2.279 · DOI
  11. Cudennec, 1981, In vitro induction of adult erythropoiesis in early mouse yolk sac, Proc. Natl. Acad. Sci. USA, 78, 2412, 10.1073/pnas.78.4.2412 · DOI
  12. Cumano, 1996, Lymphoid potential, probed before circulation in mouse, is restricted to caudal intraembryonic splanchnopleura, Cell, 86, 907, 10.1016/S0092-8674(00)80166-X · DOI
  13. Dieterlen-Lievre, 1975, On the origin of hematopoietic stem cells in the avian embryo: an experimental approach, J. Embryol. Exp. Morph, 33, 607
  14. Downs, 1993, Staging of gastrulating mouse embryos by morphological landmarks in the dissecting microscope, Development, 118, 1255, 10.1242/dev.118.4.1255 · DOI
  15. Downs, 1998, Vascularizationin the murine allantois occurs by vasculogenesis without accompanying erythropoiesis, Development, 125, 4507, 10.1242/dev.125.22.4507 · DOI
  16. Dzierzak, 1998, Qualitative and quantitative aspects of haemopoietic cell development in the mammalian embryo, Immunology Today, 19, 228, 10.1016/S0167-5699(98)01258-4 · DOI
  17. Godin, 1995, Emergence of multipotent hemopoietic cells in the yolk sac and paraaortic splanchnopleura in mouse embryos, beginning at 8.5 days postcoitus, Proc. Natl. Acad. Sci., USA, 92, 773, 10.1073/pnas.92.3.773 · DOI
  18. Haar, 1971, A phase and electron microscopic study of vasculogenesis and erythropoiesis in the yolk sac of the mouse, Anat. Rec, 170, 199, 10.1002/ar.1091700206 · DOI
  19. Hagopian, 1971, Developmental changes of erythropoiesis in cultured chick blastoderms, J. Cell Biol, 51, 440, 10.1083/jcb.51.2.440 · DOI
  20. Houssaint, 1981, Differentiation of the mouse hepatic primordium. II. Extrinsic origin of the haemopoietic cell line, Cell Differentiation, 10, 243, 10.1016/0045-6039(81)90007-5 · DOI
  21. Johnson, 1985, Erythroid progenitor cells and stimulating factors during murine embryonic and fetal development, Exp. Hematol, 13, 200
  22. Karasuyama, 1988, Establishment of mouse cell lines which constitutively secrete large quantities of interleukin 2, 3, 4 or 5, using modified cDNA expression vectors, Eur. J. Immunol, 18, 97, 10.1002/eji.1830180115 · DOI
  23. Keller, 1993, Hematopoietic commitment during embryonic stem cell differentiation in culture, Mol. Cell. Biol, 13, 473
  24. Kennedy, 1997, Identification of a common precursor for primitive and definitive hematopoiesis, Nature, 386, 488, 10.1038/386488a0 · DOI
  25. Lassila, 1982, Erythropoiesis and lymphopoiesis in the chick yolk-sac-embryo chimeras: contribution of yolk sac and intraembryonic stem cells, Blood, 59, 377, 10.1182/blood.V59.2.377.377 · DOI
  26. Medvinsky, 1996, Development of day-8 colony-forming unit-spleen hematopoietic progenitors during early murine embryogenesis: Spatial and temporal mapping, Blood, 87, 557, 10.1182/blood.V87.2.557.bloodjournal872557 · DOI
  27. Metcalf, 1971, Haemopoietic Cells
  28. Millauer, 1993, High affinity VEGF binding and developmental expression suggest flk-1 as a major regulator of vasculogenesis and angiogenesis, Cell, 72, 835, 10.1016/0092-8674(93)90573-9 · DOI
  29. Moore, 1970, Ontogeny of the haemopoietic system: yolk sac origin in vivo and in vitro colony forming cells in the developing mouse embryo, Br. J. Haem, 18, 279, 10.1111/j.1365-2141.1970.tb01443.x · DOI
  30. Moore, 1967, Stem-cell migration in developing myeloid and lymphoid systems, Lancet, 1, 658, 10.1016/S0140-6736(67)90693-9 · DOI
  31. Moore, 1967, Chromosome marker studies in the irradiated chick embryo, Nature, 215, 1081, 10.1038/2151081a0 · DOI
  32. Mucenski, 1991, A functional c-myb gene is required for normal murine fetal hepatic hematopoiesis, Cell, 65, 677, 10.1016/0092-8674(91)90099-K · DOI
  33. Muller, 1994, Development of hematopoietic stem cell activity in the mouse embryo, Immunity, 1, 291, 10.1016/1074-7613(94)90081-7 · DOI
  34. Rich, 1992, The developmental biology of hemopoiesis: effect of growth factors on the colony formation of embryonic cells, Exp. Hematol, 20, 368
  35. Schuh, 1999, In vitro hematopoietic and endothelial potential of flk-1(-/-) embryonic stem cells and embryos, Proc. Natl. Acad. Sci. USA, 96, 2159, 10.1073/pnas.96.5.2159 · DOI
  36. Shalaby, 1997, A requirement for Flk-1 in primitive and definitive hematopoiesis and vasculogenesis, Cell, 89, 981, 10.1016/S0092-8674(00)80283-4 · DOI
  37. Silver, 1997, Initiation of murine embryonic erythropoiesis: a spatial analysis, Blood, 89, 1154, 10.1182/blood.V89.4.1154 · DOI
  38. Sonoda, 1983, Presence of mast cell precursors in the yolk sac of mice, Dev. Biol, 97, 89, 10.1016/0012-1606(83)90066-0 · DOI · Paper page
  39. Steiner, 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, 10.1002/jcp.1040810305 · DOI
  40. Turpen, 1981, The early ontogeny of hematopoietic cells studied by grafting cytogenetically labeled tissue anlagen: localization of a prospective stem cell compartment, Dev. Biol, 85, 99, 10.1016/0012-1606(81)90239-6 · DOI
  41. Turpen, 1997, Bipotential primitive-definitive hematopoietic progenitors in the vertebrate embryo, Immunity, 7, 325, 10.1016/S1074-7613(00)80354-4 · DOI
  42. Vandenbunder, 1989, Complementary patterns of expression of c-ets 1, c-myb and c-myc in the blood forming system of the chick embryo, Development, 106, 265, 10.1242/dev.107.2.265 · DOI
  43. Wilkinson, 1990, Expression pattern of the mouse embryo and its role in mesoderm formation, Nature, 343, 657, 10.1038/343657a0 · DOI
  44. Wong, 1986, Properties of the earliest clonogenic hematopoietic precursors to appear in the developing murine yolk sac, Proc. Natl. Acad. Sci. U.S.A, 83, 3851, 10.1073/pnas.83.11.3851 · DOI
  45. Wong, 1986, Hemoglobin switching during murine embryonic development: evidence for two populations of embryonic erythropoietic progenitor cells, Blood, 67, 716, 10.1182/blood.V67.3.716.716 · DOI
  46. Yamaguchi, 1993, flk-1, an flt-related tyrosine kinase is an early marker for endothelial cell precursors, Development, 118, 489, 10.1242/dev.118.2.489 · DOI
  47. Yoder, 1997, Characterization of definitive lymphohematopoietic stem cells in the day 9 murine yolk sac, Immunity, 7, 335, 10.1016/S1074-7613(00)80355-6 · DOI

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Metadata

Authors
Palis, J., Robertson, S., Kennedy, M., Wall, C., & Keller, G.
Affiliations
  • University of Rochester Medical Center 1 , Department of Pediatrics and Cancer Center, Box 777, 601 Elmwood Avenue, Rochester, NY 14642, USA
  • 2 National Jewish Medical and Research Center, Department of Medicine, 1400 Jackson Street, Denver, CO 80206, USA
Venue
Development
Publisher
The Company of Biologists
Published
1999-11-15
Volume
126
Issue
22
Pages
5073-5084
ISSN
  • 0950-1991
  • 1477-9129
DOI
10.1242/dev.126.22.5073
Cited by
965
References
2
Language
en
Licence
www.biologists.com/user-licence-1-1/ (vor)

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