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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1995 Nov 7;92(23):10713–10717. doi: 10.1073/pnas.92.23.10713

Intraembryonic hematopoietic cell migration during vertebrate development.

H W Detrich 3rd 1, M W Kieran 1, F Y Chan 1, L M Barone 1, K Yee 1, J A Rundstadler 1, S Pratt 1, D Ransom 1, L I Zon 1
PMCID: PMC40682  PMID: 7479870

Abstract

Vertebrate hematopoietic stem cells are derived from vental mesoderm, which is postulated to migrate to both extra- and intraembryonic positions during gastrula and neurula stages. Extraembryonic migration has previously been documented, but the origin and migration of intraembryonic hematopoietic cells have not been visualized. The zebrafish and most other teleosts do not form yolk sac blood islands during early embryogenesis, but instead hematopoiesis occurs solely in a dorsal location known as the intermediate cell mass (IM) or Oellacher. In this report, we have isolated cDNAs encoding zebrafish homologs of the hematopoietic transcription factors GATA-1 and GATA-2 and have used these markers to determine that the IM is formed from mesodermal cells in a posterior-lateral position on the yolk syncytial layer of the gastrula yolk sac. Surprisingly, cells of the IM then migrate anteriorly through most of the body length prior to the onset of active circulation and exit onto the yolk sac. These findings support a hypothesis in which the hematopoietic program of vertebrates is established by variations in homologous migration pathways of extra- and intraembryonic progenitors.

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Selected References

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  1. Bianchi D. W., Wilkins-Haug L. E., Enders A. C., Hay E. D. Origin of extraembryonic mesoderm in experimental animals: relevance to chorionic mosaicism in humans. Am J Med Genet. 1993 Jun 15;46(5):542–550. doi: 10.1002/ajmg.1320460517. [DOI] [PubMed] [Google Scholar]
  2. COLLE-VANDEVELDE A. Blood anlage in teleostei. Nature. 1963 Jun 22;198:1223–1223. doi: 10.1038/1981223a0. [DOI] [PubMed] [Google Scholar]
  3. Dieterlen-Lièvre F., Martin C. Diffuse intraembryonic hemopoiesis in normal and chimeric avian development. Dev Biol. 1981 Nov;88(1):180–191. doi: 10.1016/0012-1606(81)90228-1. [DOI] [PubMed] [Google Scholar]
  4. Gardner R. L., Lyon M. F., Evans E. P., Burtenshaw M. D. Clonal analysis of X-chromosome inactivation and the origin of the germ line in the mouse embryo. J Embryol Exp Morphol. 1985 Aug;88:349–363. [PubMed] [Google Scholar]
  5. Godin I. E., Garcia-Porrero J. A., Coutinho A., Dieterlen-Lièvre F., Marcos M. A. Para-aortic splanchnopleura from early mouse embryos contains B1a cell progenitors. Nature. 1993 Jul 1;364(6432):67–70. doi: 10.1038/364067a0. [DOI] [PubMed] [Google Scholar]
  6. Harland R. M. In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 1991;36:685–695. doi: 10.1016/s0091-679x(08)60307-6. [DOI] [PubMed] [Google Scholar]
  7. Ingram V. M. Embryonic red blood cell formation. Nature. 1972 Feb 11;235(5337):338–339. doi: 10.1038/235338a0. [DOI] [PubMed] [Google Scholar]
  8. Iuchi I. The post-hatching transition of erythrocytes from larval to adult type in the rainbow trout, Salmo gairdnerii irideus. J Exp Zool. 1973 Jun;184(3):383–396. doi: 10.1002/jez.1401840312. [DOI] [PubMed] [Google Scholar]
  9. Iuchi I., Yamamoto M. Erythropoiesis in the developing rainbow trout, Salmo gairdneri irideus: histochemical and immunochemical detection of erythropoietic organs. J Exp Zool. 1983 Jun;226(3):409–417. doi: 10.1002/jez.1402260311. [DOI] [PubMed] [Google Scholar]
  10. Kelley C., Yee K., Harland R., Zon L. I. Ventral expression of GATA-1 and GATA-2 in the Xenopus embryo defines induction of hematopoietic mesoderm. Dev Biol. 1994 Sep;165(1):193–205. doi: 10.1006/dbio.1994.1246. [DOI] [PubMed] [Google Scholar]
  11. Kimmel C. B., Kane D. A., Walker C., Warga R. M., Rothman M. B. A mutation that changes cell movement and cell fate in the zebrafish embryo. Nature. 1989 Jan 26;337(6205):358–362. doi: 10.1038/337358a0. [DOI] [PubMed] [Google Scholar]
  12. Medvinsky A. L., Samoylina N. L., Müller A. M., Dzierzak E. A. An early pre-liver intraembryonic source of CFU-S in the developing mouse. Nature. 1993 Jul 1;364(6432):64–67. doi: 10.1038/364064a0. [DOI] [PubMed] [Google Scholar]
  13. Moore M. A., 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 Mar;18(3):279–296. doi: 10.1111/j.1365-2141.1970.tb01443.x. [DOI] [PubMed] [Google Scholar]
  14. Orkin S. H. GATA-binding transcription factors in hematopoietic cells. Blood. 1992 Aug 1;80(3):575–581. [PubMed] [Google Scholar]
  15. Orkin S. H. Globin gene regulation and switching: circa 1990. Cell. 1990 Nov 16;63(4):665–672. doi: 10.1016/0092-8674(90)90133-y. [DOI] [PubMed] [Google Scholar]
  16. Pevny L., Simon M. C., Robertson E., Klein W. H., Tsai S. F., D'Agati V., Orkin S. H., Costantini F. Erythroid differentiation in chimaeric mice blocked by a targeted mutation in the gene for transcription factor GATA-1. Nature. 1991 Jan 17;349(6306):257–260. doi: 10.1038/349257a0. [DOI] [PubMed] [Google Scholar]
  17. Sanger F., Coulson A. R. A rapid method for determining sequences in DNA by primed synthesis with DNA polymerase. J Mol Biol. 1975 May 25;94(3):441–448. doi: 10.1016/0022-2836(75)90213-2. [DOI] [PubMed] [Google Scholar]
  18. Tavassoli M. Embryonic and fetal hemopoiesis: an overview. Blood Cells. 1991;17(2):269–286. [PubMed] [Google Scholar]
  19. Toles J. F., Chui D. H., Belbeck L. W., Starr E., Barker J. E. Hemopoietic stem cells in murine embryonic yolk sac and peripheral blood. Proc Natl Acad Sci U S A. 1989 Oct;86(19):7456–7459. doi: 10.1073/pnas.86.19.7456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Trinkaus J. P. The yolk syncytial layer of Fundulus: its origin and history and its significance for early embryogenesis. J Exp Zool. 1993 Mar 1;265(3):258–284. doi: 10.1002/jez.1402650308. [DOI] [PubMed] [Google Scholar]
  21. Tsai F. Y., Keller G., Kuo F. C., Weiss M., Chen J., Rosenblatt M., Alt F. W., Orkin S. H. An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature. 1994 Sep 15;371(6494):221–226. doi: 10.1038/371221a0. [DOI] [PubMed] [Google Scholar]
  22. Turpen J. B., Knudson C. M. Ontogeny of hematopoietic cells in Rana pipiens: precursor cell migration during embryogenesis. Dev Biol. 1982 Jan;89(1):138–151. doi: 10.1016/0012-1606(82)90302-5. [DOI] [PubMed] [Google Scholar]
  23. Wenckebach K F. Development of the Blood Corpuscles in the Embryo of Perca Fluviatilis. J Anat Physiol. 1885 Apr;19(Pt 3):i2–236. [PMC free article] [PubMed] [Google Scholar]
  24. Zon L. I., Mather C., Burgess S., Bolce M. E., Harland R. M., Orkin S. H. Expression of GATA-binding proteins during embryonic development in Xenopus laevis. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10642–10646. doi: 10.1073/pnas.88.23.10642. [DOI] [PMC free article] [PubMed] [Google Scholar]

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