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Long-Term Reconstituting Hematopoietic Stem Cell Capacity in the Embryo

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Hematopoietic Stem Cell Development

Part of the book series: Medical Intelligence Unit ((MIUN))

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Abstract

Hematopoiesis is the dynamic process whereby all formed elements of the blood arise from multipotent precursor cells. In the adult mouse, hematopoiesis occurs primarily within the medullary cavity of bone and in the spleen. During murine development, however, hematopoiesis is found in numerous sites within and outside the embryo proper.1 The first blood cells in the mouse embryo arise between embryonic day 7 and 8 (E7-8) in the yolk sac.2, 3 Primitive erythroid progenitor production is restricted to the yolk sac and while these cells first differentiate into mature nucleated primitive red blood cells expressing embryonic globins, recent evidence indicates that eventually these cells enucleate intravascularly.4 Other recent evidence indicates that “definitive” erythroid and myeloid progenitors, including high proliferative potential colony-forming cells, are also produced in the yolk sac as early as E8.25.5, 6

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References

  1. Keller G, Lacaud G, Robertson S. Development of the hematopoietic system in the mouse. Exp Hematol 1999; 27:777–787.

    Article  CAS  PubMed  Google Scholar 

  2. Barker J. Development of the mouse hematopoietic system: I. Types of hemoglobin produced in embryonic yolk sac and liver. Dev Biol 1968; 18:14–29.

    Article  CAS  PubMed  Google Scholar 

  3. Haar J, Ackerman G. A phase and electron microscopic study of vasculogenesis and erythropoiesis in the yolk sac of the mouse. Anat Rec 1970; 170:199–224.

    Article  Google Scholar 

  4. Kingsley P, Malik J, Fantauzzo K et al. Yolk-sac-derived primitive erythroblasts enucleate during mammalian embryogenesis. Blood 2004; 104:19–25.

    Article  CAS  PubMed  Google Scholar 

  5. Palis J, Chan RJ, Koniski A et al. Spatial and temporal emergence of high proliferative potential hematopoietic precursors during murine embryogenesis. Proc Nat Acad Sci USA 2001; 98:4528–4533.

    Article  CAS  PubMed  Google Scholar 

  6. Cumano A, Furlonger C, Paige C. Differentiation and characterization of B-cell precursors detected in the yolk sac and embryo body of embryos beginning at the 10-to 12-somite stage. Proc Natl Acad Sci USA 1993; 90:6429–6433.

    Article  CAS  PubMed  Google Scholar 

  7. Rifkind R, Chui D, Epler H. An ultrastructural study of early morphogenetic events during the establishment of fetal hepatic erytrhopoiesis. J Cell Biol 1969; 40:343–365.

    Article  CAS  PubMed  Google Scholar 

  8. Johnson G, Moore M. Role of stem cell migration in initiation of mouse fetal liver hematopoiesis. Nature 1975; 258:726–728.

    Article  CAS  PubMed  Google Scholar 

  9. Kumaravelu P, Hook L, Morrison A et al. Quantitative developmental anatomy of definitive haematopoeitic stem cells/long-term repopulating units (HSC/RUs): Role of the aorta-gonad-mesonephros (AGM) region and the yolk sac in colonisation of the mouse embryonic liver. Development 2002; 129:4891–4899.

    CAS  PubMed  Google Scholar 

  10. Muller A, Medvinsky A, Strouboulis J et al. Development of hematopoietic stem cell activity in the mouse embryo. Immunity 1994; 1:291–301.

    Article  CAS  PubMed  Google Scholar 

  11. Ottersbach K, Dzierzak E. The murine placenta contains hematopoietic stem cells within the vascular labyrinth region. Dev Cell 2005; 8:377–387.

    Article  CAS  PubMed  Google Scholar 

  12. Gekas C, Dieterlen-Lievere F, Orkin S et al. The placenta is a niche for hematopoietic stem cells. Dev Cell 2005; 8:365–375.

    Article  CAS  PubMed  Google Scholar 

  13. Wolf NS, Bertoncello I, Jiang D et al. Developmental hematopoiesis from prenatal to young-adult life in the mouse model. Exper Hematol 1995; 23:142–146.

    CAS  Google Scholar 

  14. Harrison D, Zhong R, Jordan C et al. Relative to adult marrow, fetal liver repopulates nearly five times more effectively long-tem than short-term. Exper Hematol 1997; 25:293–297.

    CAS  Google Scholar 

  15. Kurata H, Mancini G, Alespeiti G et al. Stem cell factor induces proliferation and differentiation of fetal progenitor cells in the mouse. Br J Haematol 1998; 101:676–687.

    Article  CAS  PubMed  Google Scholar 

  16. Grossi C, Velardi A, Cooper M. Postnatal liver hemopoiesis in mice: Generation of preB cells, granulocytes, and erythrocytes in discrete colonies. J Immunol 1985; 135:2303–2311.

    CAS  PubMed  Google Scholar 

  17. Clapp D, Freie B, Lee W-H et al. Molecular evidence that in situ-transduced fetal liver hematopoietic stem/progenitor cells give rise to medullary hematopoiesis in adult rats. Blood 1995; 86:2113–2122.

    CAS  PubMed  Google Scholar 

  18. Gothert J, Gustin S, Hall M et al. In vivo fate-tracing studies using the SCI stem cell enhancer: Embryonic hematopoietic stem cells significantly contribute to adult hematopoiesis. Blood 2005; 105:2724–2732.

    Article  PubMed  Google Scholar 

  19. Zon L. Developmental biology of hematopoiesis. Blood 1995; 86:2876–2891.

    CAS  PubMed  Google Scholar 

  20. Moore M, Owen J. Stem-cell migration in developing myeloid and lymphoid systems. The Lancet 1967; 658–659.

    Google Scholar 

  21. Houssaint E. Differentiation of the mouse hepatic primordium. II. Extrinsic origin of the haemopoietic cell line. Cell Diff 1981; 10:243–247.

    Article  CAS  Google Scholar 

  22. Moore M, Metcalf D. Ontogeny of the haemopoietic system: Yolk sac origin of in vivo and in vitro colony forming cells in the developing mouse embryo. Br J Haematol 1970; 18:279–296.

    Article  CAS  PubMed  Google Scholar 

  23. Orlic D, Bodine D. What defines a pluripotent hematopoietic stem cell (PHSC): Will the real PHSC please stand up! Blood 1994; 84:3991–3994.

    CAS  PubMed  Google Scholar 

  24. McGrath K, Koniski A, Malik J et al. Circulation is established in a stepwise pattern in the mammalian embryo. Blood 2003; 101:1669–1676.

    Article  CAS  PubMed  Google Scholar 

  25. Weissman I, Papaioannou V, Gardner D. Fetal hematopoietic origins of the adult hematolymphoid system. In: Clarkson B, Marks PA, Till JE, eds. Differentiation of Normal and Neoplastic Hematopoietic Cells. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 1978:33–47.

    Google Scholar 

  26. Toles JF, Chui DH, Belbeck LW et al. Hematopoietic stem cells in murine embryonic yolk sac and peripheral blood. Proc Natl Acad Sci USA 1990; 86:7456–7459.

    Article  Google Scholar 

  27. Harrison D, Astle C, DeLaittre J. Processing by the Thymus is not required for cells that cure and populate W/Wv recipients. Blood 1979; 54:1152–1157.

    CAS  PubMed  Google Scholar 

  28. Medvinsky A, Dzierzak E. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 1996; 86:897–906.

    Article  CAS  PubMed  Google Scholar 

  29. Cumano A, Ferraz JC, Klaine M et al. Intraembryonic, but not yolk sac hematopoietic precursors, isolated before circulation, provide long-term multilineage reconstitution. Immunity 2001; 15:477–485.

    Article  CAS  PubMed  Google Scholar 

  30. Yoder MC, Hiatt K, Dutt P et al. Characterization of definitive lymphohematopoietic stem cells in the day 9 murine yolk sac. Immunity 1997; 7:335–344.

    Article  CAS  PubMed  Google Scholar 

  31. Yoder M, Cumming J, Hiatt K et al. A novel method of myeloablation to enhance engraftment of adult bone marrow cells in newborn mice. Biol Blood Marrow Transplant 1996; 2:59–67.

    CAS  PubMed  Google Scholar 

  32. Yoder M, Hiatt K. Engraftment of embryonic hematopoietic cells in conditioned newborn recipients. Blood 1997; 89:2176–2183.

    CAS  PubMed  Google Scholar 

  33. Yoder M, Hiatt K, Mukherjee P. In vivo repopulating hematopoietic stem cells are present in the murine yolk sac at day 9.0 postcoitus. Proc Natl Acad Sci USA 1997; 94:6776–6780.

    Article  CAS  PubMed  Google Scholar 

  34. Sato T, Laver J, Ogawa M. Reversible expression of CD34 by murine hematopoietic stem cells. Blood 1999; 94:2548–2554.

    CAS  PubMed  Google Scholar 

  35. Ito T, Tajima F, Ogawa M. Developmental changes of CD34 expression by murine hematopoietic stem cells. Exp Hematol 2000; 28:1269–1273.

    Article  CAS  PubMed  Google Scholar 

  36. Zeigler F, Bennett B, Jordan C et al. Cellular and molecular characterization of the role of the flk-2/flt-3 receptor tyrosine kinase in hematopoietic stem cells. Blood 1994; 84:2422–2430.

    CAS  PubMed  Google Scholar 

  37. 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.

    Article  CAS  PubMed  Google Scholar 

  38. Matsuoka S, Tsuji K, Hisakawa H et al. Generation of definitive hematopoietic stem cells from murine early yolk sac and paraaortic splanchnopleura by aorta-gonad-mesonephros region-derived stromal cells. Blood 2001; 98:6–12.

    Article  CAS  PubMed  Google Scholar 

  39. Kyba M, Perlingeiro R, Daley GQ. HoxB4 confers definitive lymphoid-myeloid engraftment potential on embryonic stem cell and yolk sac hematopoietic progenitors. Cell 2002; 109:29–37.

    Article  CAS  PubMed  Google Scholar 

  40. Xu M, Tsuji K, Ueda T. Stimulation of mouse and human primitive hematopoiesis by murine embryonic aorta-gonad-mesonephros-derived stromal cell lines. Blood 1998; 92:2032–2040.

    CAS  PubMed  Google Scholar 

  41. Godin I, Garcia-Porrero J, Coutinho A et al. Para-aortic splanchnopleura from early mouse embryos contains Bla cell progenitors. Nature 1993; 364:67–70.

    Article  CAS  PubMed  Google Scholar 

  42. Godin I, Dieterlen-Lievre F, Cumano A. 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 1995; 92:773–777.

    Article  CAS  PubMed  Google Scholar 

  43. Cumano A, Godin I. Pluripotent hematopoietic stem cell development during embryogenesis. Curr Opin Immunol 2001; 13:166–171.

    Article  CAS  PubMed  Google Scholar 

  44. North T, Gu T, Stacy T et al. Cbfa2 is required for the formation of intra-aortic hematopoietic clusters. Development 1999; 126:2563–2575.

    CAS  PubMed  Google Scholar 

  45. de Bruijn M, Speck N, Peeters M et al. Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo. EMBO J 2000; 19:2465–2474.

    Article  PubMed  Google Scholar 

  46. Godin I, Garcia-Porrero JA, Dieterlen-Lievre F et al. Stem cell emergence and hemopoietic activity are incompatible in mouse intraembryonic sites. J Exp Med 1999; 190:43–52.

    Article  CAS  PubMed  Google Scholar 

  47. North T, de Bruijn M, Stacy T et al. Runxl expression marks long-term repopulating hematopoietic stem cells in the midgestation mouse embryo. Immunity 2002; 16:661–672.

    Article  CAS  PubMed  Google Scholar 

  48. Nishikawa S, Nishikawa S, Hirashima M et al. Progressive lineage analysis by cell sorting and culture identifies FLK 1+ VE-cadherin+ cells at a diverging point of endothelial and hematopoietic lineages. Development 1998; 125:1747–1757.

    CAS  PubMed  Google Scholar 

  49. Nishikawa S-I, Nishikawa S, Kawamoto H et al. In vitro generation of lymphohematopoietic cells from endothelial cells purified from murine embryos. Immunity 1998; 8:761–769.

    Article  CAS  PubMed  Google Scholar 

  50. Hara T, Nakano Y-K, Tanaka M et al. Identification of podocalyxin-like protein 1 as a novel cell surface marker for hemangioblasts in the murine aorta-gonad-mesonephros region. Immunity 1999; 11:567–578.

    Article  CAS  PubMed  Google Scholar 

  51. de Bruijn M, Ma X, Robin C et al. Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta. Immunity 2002; 16:673–683.

    Article  PubMed  Google Scholar 

  52. Palis J, Robertson S, Kennedy M et al. Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development 1999; 126:5073–5081.

    CAS  PubMed  Google Scholar 

  53. Palis J, Yoder M. Yolk Sac Hematopoiesis-The first blood cells of mouse and man. Exp Hematol 2001; 29:927–936.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Herman B. Wells Center for Pediatric Research, Indiana University School of Medicine, Indianapolis, Indiana, USA

    Mervin C. Yoder

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Yoder, M.C. (2006). Long-Term Reconstituting Hematopoietic Stem Cell Capacity in the Embryo. In: Hematopoietic Stem Cell Development. Medical Intelligence Unit. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-33535-3_6

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