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Avian Lymphopoiesis and Transcriptional Control of Hematopoietic Stem Cell Differentiation

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Hematopoietic Stem Cell Development

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

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Abstract

Hematopoiesis starts in the yolk sac blood islands and in a region of dorsal aorta in the early embryo. Interest in the emergence of the hematopoietic stem cells in the embryo proper has increased in last years. In an avian model the primitive erythropoiesis derived from extraembryonic yolk sac is short lived and the evidence that adult hematopoiesis arises from intraembryonic sources has been extended from birds to mammals. Definitive lymphohematopoiesis initiates in the ventral wall of the dorsal aorta in all the vertebrate species.

Second major issue in early hematopoiesis is the existence of hemangioblast, a bipotential cell, able to differentiate into a hematopoietic stem cell or a vascular endothelial cell. It has become clear that the emergence of hematopoietic stem cells and hemangioblasts is tightly linked. The rapid commitment of hematopoietic and endothelial lineages in the developing embryo indicates that the distinction between mesoderm and hemangioblast maybe difficult to define. It is, however, possible that the hemangioblast stage is very short lived.

As the intraembryonic hemogenic sites start to seed the lymphoid organ rudiments, developmental programs of the homing progenitors are gradually restricted towards downstream lineages. Eventually, thymus, bone marrow, spleen and the avian bursa of Fabricius serve as permissive environments for further maturation, proliferative expansion and selection processes. During these complex events multiple both cell-intrinsic and -extrinsic mediators critically influence the emergence of lymphohemopoietic progeny.

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References

  1. Choi K, Kennedy M, Kazarov A et al. A common precursor for hematopoietic and endothelial cells. Development 1998; 125:725–732.

    CAS  PubMed  Google Scholar 

  2. Jaffredo T, Gautier R, Brajeul V et al. Tracing the progeny of the aortic hemangioblast in the avian embryo. Dev Biol 2000; 224:204–214.

    Article  CAS  PubMed  Google Scholar 

  3. Jaffredo T, Gautier R, Eichmann A et al. Intraaortic hemopoietic cells are derived from endothelial cells during ontogeny. Development 1998; 125:4575–4583.

    CAS  PubMed  Google Scholar 

  4. Pardanaud L, Dieterlen-Lièvre F. Manipulation of the angiopoietic/hemangiopoietic commitment in the avian embryo. Development 1999; 126:617–627.

    CAS  PubMed  Google Scholar 

  5. Pardanaud L, Luton D, Prigent M et al. Two distinct endothelial lineages in ontogeny, one of them related to hemopoiesis. Development 1996; 122:1363–1371.

    CAS  PubMed  Google Scholar 

  6. Caprioli A, Jaffredo T, Gautier R et al. Blood-borne seeding by hematopoietic and endothelial precursors from the allantois. Proc Natl Acad Sci USA 1998; 95:1641–1646.

    Article  CAS  PubMed  Google Scholar 

  7. Eichmann A, Corbel C, Pardanaud L et al. Hemangioblastic precursors in the avian embryo. Curr Top Microbiol Immunol 2000; 251:83–90.

    CAS  PubMed  Google Scholar 

  8. Lampisuo M, Karvinen J, Arstila TP et al. Intraembryonic haemopoietic cells and early T cell development. Scand J Immunol 1995; 41:65–69.

    Article  CAS  PubMed  Google Scholar 

  9. Wood HB, May G, Healy L et al. CD34 expression patterns during early mouse development are related to modes of blood vessel formation and reveal additional sites of hematopoiesis. Blood 1997; 90:2300–2311.

    CAS  PubMed  Google Scholar 

  10. Eichmann A, Corbel C, Nataf V et al. Ligand-dependent development of the endothelial and hemopoietic lineages from embryonic mesodermal cells expressing vascular endothelial growth factor receptor 2. Proc Natl Acad Sci USA 1997; 94:5141–5146.

    Article  CAS  PubMed  Google Scholar 

  11. Takakura N, Watanabe T, Suenobu S et al. A role for hematopoietic stem cells in promoting angiogenesis. Cell 2000; 102:199–209.

    Article  CAS  PubMed  Google Scholar 

  12. Porcher C, Swat W, Rockwell K et al. The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages. Cell 1996; 86:47–57.

    Article  CAS  PubMed  Google Scholar 

  13. Gering M, Rodaway ARF, Göttgens B et al. The SCL gene specifies haemangioblast development from early mesoderm. EMBO J 1998; 17:4029–4045.

    Article  CAS  PubMed  Google Scholar 

  14. Olson EN. MyoD family: A paradigm for development? Genes Dev 1990; 4:1454–1461.

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  16. Dieterlen-Lièvre F. On the origin of haematopoietic stem cells in the avian embryo: An experimental approach. J Embryol Exp Morphol 1975; 33:607–619.

    PubMed  Google Scholar 

  17. Lassila O, Eskola J, Toivanen P et al. The origin of lymphoid stem cells studied in chick yolk sac-embryo chimaeras. Nature 1978; 272:353–354.

    Article  CAS  PubMed  Google Scholar 

  18. Cumano A, Dieterlen-Lièvre 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 

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

    Article  CAS  PubMed  Google Scholar 

  20. Lassila O, Martin C, Toivanen P et al. Erythropoiesis and lymphopoiesis in the chick yolk sac-embryo chimeras: Contribution of yolk sac and intraembryonic stem cells. Blood 1982; 59:377–381.

    CAS  PubMed  Google Scholar 

  21. Sieweke MH, Graf T. A transcription factor party during blood cell differentiation. Curr Opin Gen Dev 1998; 8:545–551.

    Article  CAS  Google Scholar 

  22. Glimcher LH, Singh H. Transcription factors in lymphocyte development — T and B cells get together. Cell 1999; 96:13–23.

    Article  CAS  PubMed  Google Scholar 

  23. Ohmura K, Kawamoto H, Fujimoto S et al. Emergence of T, B, and myeloid lineage-committed progenitors in the aorta-gonad-mesonephros region of day 10 fetuses of the mouse. J Immunol 1999; 163:4788–4795.

    CAS  PubMed  Google Scholar 

  24. Tsang AP, Fujiwara Y, Horn DB et al. Failure of megakaryopoiesis and arrested erythropoiesis in mice lacking the GATA-1 transcriptional cofactor FOG. Genes Dev 1998; 12:1176–1188.

    Article  CAS  PubMed  Google Scholar 

  25. Nerlov C, Querfurth E, Kulessa H et al. GATA-1 interacts with the myeloid PU.l transcription factor and represses PU.l-dependent transcription. Blood 2000; 95:2543–2551.

    CAS  PubMed  Google Scholar 

  26. Cortes M, Wong E, Koipally J et al. Control of lymphocyte development by the Ikaros gene family. Curr Opin Immunol 1999; 11:167–171.

    Article  CAS  PubMed  Google Scholar 

  27. Lassila O, Eskola J, Toivanen P. Prebursal stem cells in the intraembryonic mesenchyme of the chick embryo at 7 days of incubation. J Immunol 1979; 123:2091–2094.

    CAS  PubMed  Google Scholar 

  28. Delassus S, Titley I, Enver T. Functional and molecular analysis of hematopoietic progenitors derived from the aorta-gonad-mesonephros region of the mouse embryo. Blood 1999; 94:1495–1503.

    CAS  PubMed  Google Scholar 

  29. Lampisuo M, Liippo J, Vainio O et al. Characterization of prethymic progenitors within the chicken embryo. Int Immunol 1999; 11:63–69.

    Article  CAS  PubMed  Google Scholar 

  30. Nieminen P, Liippo J, Lassila O. Bursa of Fabricius. Encyclopedia of Life Sciences / ©. Macmillan Publishers Ltd, Nature Publishing Group, 2001.

    Google Scholar 

  31. Mansikka A, Sandberg M, Lassila O et al. Rearrangement of immunoglobulin light chain genes in the chicken occurs prior to colonization of the embryonic bursa of Fabricius. Proc Natl Acad Sci USA 1990; 87:9416–9420.

    Article  CAS  PubMed  Google Scholar 

  32. Weill JC, Reynaud CA. The chicken B cell compartment. Science 1987; 238:1094–1098.

    Article  CAS  PubMed  Google Scholar 

  33. Kondo M, Weissman IL, Akashi K. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 1997; 91:661–672.

    Article  CAS  PubMed  Google Scholar 

  34. Le Douarin NM, Houssaint E, Jotereau FV et al. Origin of hematopoietic stem cells in embryonic bursa of Fabricius and bone marrow studied through interspecific chimeras. Proc Natl Acad Sci USA 1975; 72:2701–2705.

    Article  PubMed  Google Scholar 

  35. Lassila O, Alanen A, Lefkovits I et al. Immunoglobulin diversification in embryonic chicken bursae and in individual bursal follicles. Eur J Immunol 1988; 18:943–949.

    Article  CAS  PubMed  Google Scholar 

  36. Mansikka A, Jalkanen S, Sandberg M et al. Bursectomy of chicken embryos at 60 hours of incubation leads to an oligoclonal B cell compartment and restricted Ig diversity. J Immunol 1990; 145:3601–3609.

    CAS  PubMed  Google Scholar 

  37. Liippo J, Koskela K, Lassila O. Prethymic progenitors from the avian para-aortic mesoderm express GATA-3 and distinct chTcf isoforms but still lack T-cell receptor-γ rearrangements. Scand J Immunol 2000; 52:502–509.

    Article  CAS  PubMed  Google Scholar 

  38. Pandolfi PP, Roth ME, Karis A et al. Targeted disruption of the GATA-3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis. Nat Genet 1995; 11:40–44.

    Article  CAS  PubMed  Google Scholar 

  39. Manaia A, Lemarchandel V, Klaine M et al. Lmo2 and GATA-3 associated expression in intraembryonic hemogenic sites. Development 2000; 127:643–653.

    CAS  PubMed  Google Scholar 

  40. Ting C, Olson MC, Barton KP et al. Transcription factor GATA-3 is required for development of the T-cell lineage. Nature 1996; 384:474–478.

    Article  CAS  PubMed  Google Scholar 

  41. Kuo CT, Leiden JM. Transcriptional regulation of T lymphocyte development and function. Annu Rev Immunol 1999; 17:149–187.

    Article  CAS  PubMed  Google Scholar 

  42. Clevers H, van de Wetering M. TCF/LEF factor earn their wings. Trends Genet 1997; 12:485–489.

    Article  Google Scholar 

  43. Okamura RM, Sigvardsson M, Galceran J et al. Redundant regulation of T cell differentiation and TCRα gene expression by the transcription factors LEF-1 and TCF-1. Immunity 1998; 8:11–20.

    Article  CAS  PubMed  Google Scholar 

  44. Castrop J, Hoevenagel R, Young JR et al. A common ancestor of the mammalian transcription factors TCF-1 and TCF-la/LEF-1 expressed in chicken T cells. Eur J Immunol 1992; 22:1327–1330.

    Article  Google Scholar 

  45. Reya T, Grosschedl R. Transcriptional regulation of B-cell differentiation. Curr Opin Immunol 2000; 10:158–165.

    Article  Google Scholar 

  46. Busslinger M, Nutt SL, Rolink AG. Lineage commitment in lymphopoiesis. Curr Opin Immunol 2000; 12:151–158.

    Article  CAS  PubMed  Google Scholar 

  47. Nutt SL, Heavey B, Rolink AG et al. Commitment to the B lymphoid lineage depends on the transcription factor Pax5. Nature 1999; 401:556–562.

    Article  CAS  PubMed  Google Scholar 

  48. Enver T, Greaves M. Loops, lineages, and leukemia. Cell 1998; 94:9–12.

    Article  CAS  PubMed  Google Scholar 

  49. Georgopoulos K, Winandy S, Avitahl N. The role of the Ikaros gene in lymphocyte development and homeostasis. Annu Rev Immunol 1997; 15:155–176.

    Article  CAS  PubMed  Google Scholar 

  50. Georgopoulos K, Moore DD, Derfler B. Ikaros, an early lymphoid-specific transcription factor and a putative mediator for T cell commitment. Science 1992; 258:808–812.

    Article  CAS  PubMed  Google Scholar 

  51. Morgan B, Sun L, Avitahl N et al. Aiolos, a lymphoid restricted transcription factor that interacts with Ikaros to regulate lymphocyte differentiation. EMBO J 1997; 16:2004–2013.

    Article  CAS  PubMed  Google Scholar 

  52. Kelley CM, Ikeda T, Koipally J et al. Helios, a novel dimerization partner of Ikaros expressed in the earliest hematopoietic progenitors. Curr Biol 1998; 8:508–515.

    Article  CAS  PubMed  Google Scholar 

  53. Hahm K, Cobb BS, McCarty AS et al. Helios, a T cell-restricted Ikaros family member that quantitatively associates with Ikaros at centromeric heterochromatin. Genes Dev 1998; 12:782–796.

    Article  CAS  PubMed  Google Scholar 

  54. Nichogiannopoulou A, Trevisan M, Neben S et al. Defects in hemopoietic stem cell activity in Ikaros mutant mice. J Exp Med 1999; 190:1201–1213.

    Article  CAS  PubMed  Google Scholar 

  55. Winandy S, Wu L, Wang J-H et al. PreT cell receptor (TCR) and TCR-controlled checkpoints in T cell differentiation are set by Ikaros. J Exp Med 1999; 190:1039–1048.

    Article  CAS  PubMed  Google Scholar 

  56. Wang J-H, Avitahl N, Cariappa A et al. Aiolos regulates B cell activation and maturation to effector state. Immunity 1998; 9:543–553.

    Article  CAS  PubMed  Google Scholar 

  57. Brown KE, Guest SS, Smale ST et al. Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell 1997; 91:845–854.

    Article  CAS  PubMed  Google Scholar 

  58. Kim J, Sif S, Jones B et al. Ikaros DNA-binding proteins direct formation of chromatin remodeling complexes in lymphocytes. Immunity 1999; 10:345–355.

    Article  CAS  PubMed  Google Scholar 

  59. Workman JL, Kingston RE. Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu Rev Biochem 1998; 67:545–579.

    Article  CAS  PubMed  Google Scholar 

  60. Koipally J, Renold A, Kim J et al. Repression by Ikaros and Aiolos is mediated through histone deacetylase complexes. EMBO J 1999; 18:3090–3100.

    Article  CAS  PubMed  Google Scholar 

  61. Cobb BS, Morales-Alcelay S, Kleiger G et al. Targeting of Ikaros to pericentromeric heterochromatin by direct DNA-binding. Genes Dev 2000; 14:2146–2160.

    Article  CAS  PubMed  Google Scholar 

  62. Liippo J, Lassila O. Avian Ikaros gene is expressed early in embryogenesis. Eur J Immunol 1997; 27:1853–1857.

    Article  CAS  PubMed  Google Scholar 

  63. Liippo J, Nera K-P, Kohonen P et al. The Ikaros family and the development of early intraembryonic hematopoietic stem cells. Curr Topics Microbiol Immunol 2000; 251:51–58.

    CAS  Google Scholar 

  64. Liippo J, Mansikka A, Lassila O. The evolutionarily conserved avian Aiolos gene encodes alternative isoforms. Eur J Immunol 1999; 29:2651–2657.

    Article  CAS  PubMed  Google Scholar 

  65. Liippo J, Nera K-P, Lähdesmäki A et al. Both normal and leukemic B lymphocytes express multiple isoforms of the human Aiolos gene. Eur J Immunol 2001; 31:3469–3474.

    Article  CAS  PubMed  Google Scholar 

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Liippo, J., Lassila, O. (2006). Avian Lymphopoiesis and Transcriptional Control of Hematopoietic Stem Cell Differentiation. In: Hematopoietic Stem Cell Development. Medical Intelligence Unit. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-33535-3_4

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