Identification of multipotent progenitors that emerge prior to hematopoietic stem cells in embryonic development

Stem Cell Reports

Volumn 2, Issue 4, 2014, Pages 457-472

  Inlay, Matthew A ^a   Serwold, Thomas ^b   Mosley, Adriane ^a   Fathman, John W ^a,c   Dimov, Ivan K ^a   Seita, Jun ^a   Weissman, Irving L ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c GENOMICS INSTITUTE OF THE NOVARTIS RESEARCH FOUNDATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; AORTA; ARTICLE; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; FETUS LIVER; GONAD; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; IN VITRO STUDY; MALE; MESONEPHROS; MOUSE; MULTIPOTENT STEM CELL; NONHUMAN; PRIORITY JOURNAL; YOLK SAC; ANIMAL; CELL DIFFERENTIATION; CELL LINEAGE; CFU COUNTING; CYTOLOGY; EMBRYOLOGY; GENETICS; IMMUNOPHENOTYPING; METABOLISM; PHENOTYPE; ASSAY; CONTROLLED STUDY; FETUS;

LEUKOSIALIN; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MEMBRANE ANTIGEN; STEM CELL FACTOR RECEPTOR;

ANIMALS; ANTIGENS, CD11A; ANTIGENS, CD43; ANTIGENS, SURFACE; CELL DIFFERENTIATION; CELL LINEAGE; COLONY-FORMING UNITS ASSAY; EMBRYONIC DEVELOPMENT; FEMALE; HEMATOPOIETIC STEM CELLS; IMMUNOPHENOTYPING; MICE; MULTIPOTENT STEM CELLS; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-KIT; YOLK SAC;

EID: 84898039580     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2014.02.001     Document Type: Article

References (47)

1. K. Akashi, D. Traver, T. Miyamoto, and I.L. Weissman A clonogenic common myeloid progenitor that gives rise to all myeloid lineages Nature 404 2000 193 197
2. M. Alvarez-Silva, P. Belo-Diabangouaya, J. Salaün, and F. Dieterlen-Lièvre Mouse placenta is a major hematopoietic organ Development 130 2003 5437 5444
3. A.B. Balazs, A.J. Fabian, C.T. Esmon, and R.C. Mulligan Endothelial protein C receptor (CD201) explicitly identifies hematopoietic stem cells in murine bone marrow Blood 107 2006 2317 2321
4. J.C. Boisset, W. van Cappellen, C. Andrieu-Soler, N. Galjart, E. Dzierzak, and C. Robin In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium Nature 464 2010 116 120
5. A. Cumano, and I. Godin Ontogeny of the hematopoietic system Annu. Rev. Immunol. 25 2007 745 785
6. A. Cumano, F. Dieterlen-Lievre, and I. Godin Lymphoid potential, probed before circulation in mouse, is restricted to caudal intraembryonic splanchnopleura Cell 86 1996 907 916
7. A. Cumano, J.C. Ferraz, M. Klaine, J.P. Di Santo, and I. Godin Intraembryonic, but not yolk sac hematopoietic precursors, isolated before circulation, provide long-term multilineage reconstitution Immunity 15 2001 477 485
8. M.F. de Bruijn, N.A. Speck, M.C. Peeters, and E. Dzierzak Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo EMBO J. 19 2000 2465 2474
9. E. Dzierzak, and A. Medvinsky Mouse embryonic hematopoiesis Trends Genet. 11 1995 359 366
10. C. Gekas, F. Dieterlen-Lièvre, S.H. Orkin, and H.K. Mikkola The placenta is a niche for hematopoietic stem cells Dev. Cell 8 2005 365 375
11. I.E. Godin, J.A. Garcia-Porrero, A. Coutinho, F. Dieterlen-Lièvre, and M.A. Marcos Para-aortic splanchnopleura from early mouse embryos contains B1a cell progenitors Nature 364 1993 67 70
12. I. Godin, F. Dieterlen-Lièvre, and A. Cumano 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 1995 773 777
13. S. Gordon-Keylock, M. Sobiesiak, S. Rybtsov, K. Moore, and A. Medvinsky Mouse extraembryonic arterial vessels harbor precursors capable of maturing into definitive HSCs Blood 122 2013 2338 2345
14. E.S. Harris, and W.J. Nelson VE-cadherin: at the front, center, and sides of endothelial cell organization and function Curr. Opin. Cell Biol. 22 2010 651 658
15. M.L. Hibbs, H. Xu, S.A. Stacker, and T.A. Springer Regulation of adhesion of ICAM-1 by the cytoplasmic domain of LFA-1 integrin beta subunit Science 251 1991 1611 1613
16. N. Hogg, I. Patzak, and F. Willenbrock The insider's guide to leukocyte integrin signalling and function Nat. Rev. Immunol. 11 2011 416 426
17. H. Huang, and R. Auerbach Identification and characterization of hematopoietic stem cells from the yolk sac of the early mouse embryo Proc. Natl. Acad. Sci. USA 90 1993 10110 10114
18. M.A. Inlay, D. Bhattacharya, D. Sahoo, T. Serwold, J. Seita, H. Karsunky, S.K. Plevritis, D.L. Dill, and I.L. Weissman Ly6d marks the earliest stage of B-cell specification and identifies the branchpoint between B-cell and T-cell development Genes Dev. 23 2009 2376 2381
19. H. Iwasaki, F. Arai, Y. Kubota, M. Dahl, and T. Suda Endothelial protein C receptor-expressing hematopoietic stem cells reside in the perisinusoidal niche in fetal liver Blood 116 2010 544 553
20. H. Karsunky, M.A. Inlay, T. Serwold, D. Bhattacharya, and I.L. Weissman Flk2+ common lymphoid progenitors possess equivalent differentiation potential for the B and T lineages Blood 111 2008 5562 5570
21. Y.Y. Kisanuki, R.E. Hammer, J. Miyazaki, S.C. Williams, J.A. Richardson, and M. Yanagisawa Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo Dev. Biol. 230 2001 230 242
22. H. Kodama, M. Nose, S. Niida, S. Nishikawa, and S. Nishikawa Involvement of the c-kit receptor in the adhesion of hematopoietic stem cells to stromal cells Exp. Hematol. 22 1994 979 984
23. P. Kumaravelu, L. Hook, A.M. Morrison, J. Ure, S. Zhao, S. Zuyev, J. Ansell, and A. Medvinsky Quantitative developmental anatomy of definitive haematopoietic 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 129 2002 4891 4899
24. C.T. Lux, M. Yoshimoto, K. McGrath, S.J. Conway, J. Palis, and M.C. Yoder All primitive and definitive hematopoietic progenitor cells emerging before E10 in the mouse embryo are products of the yolk sac Blood 111 2008 3435 3438
25. A. Medvinsky, and E. Dzierzak Definitive hematopoiesis is autonomously initiated by the AGM region Cell 86 1996 897 906
26. A.L. Medvinsky, N.L. Samoylina, A.M. Müller, and E.A. Dzierzak An early pre-liver intraembryonic source of CFU-S in the developing mouse Nature 364 1993 64 67
27. A. Monvoisin, J.A. Alva, J.J. Hofmann, A.C. Zovein, T.F. Lane, and M.L. Iruela-Arispe VE-cadherin-CreERT2 transgenic mouse: a model for inducible recombination in the endothelium Dev. Dyn. 235 2006 3413 3422
28. M.A. Moore, and D. Metcalf 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. 18 1970 279 296
29. S.J. Morrison, H.D. Hemmati, A.M. Wandycz, and I.L. Weissman The purification and characterization of fetal liver hematopoietic stem cells Proc. Natl. Acad. Sci. USA 92 1995 10302 10306
30. A.M. Müller, A. Medvinsky, J. Strouboulis, F. Grosveld, and E. Dzierzak Development of hematopoietic stem cell activity in the mouse embryo Immunity 1 1994 291 301
31. M.D. Muzumdar, B. Tasic, K. Miyamichi, L. Li, and L. Luo A global double-fluorescent Cre reporter mouse Genesis 45 2007 593 605
32. S.I. Nishikawa, S. Nishikawa, H. Kawamoto, H. Yoshida, M. Kizumoto, H. Kataoka, and Y. Katsura In vitro generation of lymphohematopoietic cells from endothelial cells purified from murine embryos Immunity 8 1998 761 769
33. K. Ottersbach, and E. Dzierzak The murine placenta contains hematopoietic stem cells within the vascular labyrinth region Dev. Cell 8 2005 377 387
34. J. Palis, S. Robertson, M. Kennedy, C. Wall, and G. Keller Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse Development 126 1999 5073 5084
35. K.E. Rhodes, C. Gekas, Y. Wang, C.T. Lux, C.S. Francis, D.N. Chan, S. Conway, S.H. Orkin, M.C. Yoder, and H.K. Mikkola The emergence of hematopoietic stem cells is initiated in the placental vasculature in the absence of circulation Cell Stem Cell 2 2008 252 263
36. S. Rybtsov, M. Sobiesiak, S. Taoudi, C. Souilhol, J. Senserrich, A. Liakhovitskaia, A. Ivanovs, J. Frampton, S. Zhao, and A. Medvinsky Hierarchical organization and early hematopoietic specification of the developing HSC lineage in the AGM region J. Exp. Med. 208 2011 1305 1315
37. I.M. Samokhvalov, N.I. Samokhvalova, and S. Nishikawa Cell tracing shows the contribution of the yolk sac to adult haematopoiesis Nature 446 2007 1056 1061
38. T.M. Schmitt, and J.C. Zúñiga-Pflücker Induction of T cell development from hematopoietic progenitor cells by delta-like-1 in vitro Immunity 17 2002 749 756
39. Y. Tanaka, M. Hayashi, Y. Kubota, H. Nagai, G. Sheng, S. Nishikawa, and I.M. Samokhvalov Early ontogenic origin of the hematopoietic stem cell lineage Proc. Natl. Acad. Sci. USA 109 2012 4515 4520
40. S. Taoudi, C. Gonneau, K. Moore, J.M. Sheridan, C.C. Blackburn, E. Taylor, and A. Medvinsky Extensive hematopoietic stem cell generation in the AGM region via maturation of VE-cadherin+CD45+ pre-definitive HSCs Cell Stem Cell 3 2008 99 108
41. M.A. Vodyanik, and I.I. Slukvin Hematoendothelial differentiation of human embryonic stem cells Curr. Protoc. Cell Biol. Chapter 23 2007 6
42. I.L. Weissman, S. Baird, R.L. Gardner, V.E. Papaioannou, and W. Raschke Normal and neoplastic maturation of T-lineage lymphocytes Cold Spring Harb. Symp. Quant. Biol. 41 1977 9 21
43. I. Weissman, V. Papaioannou, and R. Gardner Fetal hematopoietic origin of the adult hematolymphoid system B. Clarkson, P.A. Marks, J.E. Till, Differentiation of Normal and Neoplastic Hematopoietic Cells 1978 Cold Spring Harbor Laboratory Press Cold Spring Harbor 33 47
44. M.C. Yoder, and K. Hiatt Engraftment of embryonic hematopoietic cells in conditioned newborn recipients Blood 89 1997 2176 2183
45. M.C. Yoder, K. Hiatt, P. Dutt, P. Mukherjee, D.M. Bodine, and D. Orlic Characterization of definitive lymphohematopoietic stem cells in the day 9 murine yolk sac Immunity 7 1997 335 344
46. M.C. Yoder, K. Hiatt, and P. Mukherjee In vivo repopulating hematopoietic stem cells are present in the murine yolk sac at day 9.0 postcoitus Proc. Natl. Acad. Sci. USA 94 1997 6776 6780
47. A.C. Zovein, J.J. Hofmann, M. Lynch, W.J. French, K.A. Turlo, Y. Yang, M.S. Becker, L. Zanetta, E. Dejana, and J.C. Gasson et al. Fate tracing reveals the endothelial origin of hematopoietic stem cells Cell Stem Cell 3 2008 625 636