Abstract
The first definitive/adult-type hematopoietic stem cells (HSCs) in the mouse aorta-gonad-mesonephros region emerge between embryonic days 10.5 and 11.5. The discovery of clusters of hematopoietic cells on the ventral luminal surface of the dorsal aorta in various vertebrate species has led to speculation that the floor of the dorsal aorta may play an essential role for the development of the definitive hematopoietic system. Here, we functionally show affiliation of definitive HSCs with the ventral floor of the dorsal aorta, whereas colony-forming hematopoietic activity is associated with both ventral and dorsal domains. We show that a rare population of PECAM1(high)CD45(+) cells, within which definitive HSCs reside, is predominantly localized to intraaortic clusters. Furthermore, using ex vivo culture analysis, we demonstrate that the ventral domain of the dorsal aorta has an exclusive functional capacity of inducing and expanding definitive HSCs.
MeSH Terms
Animals
Aorta/cytology,embryology,metabolism
Cell Polarity
Hematopoietic Stem Cells/cytology,metabolism
Leukocyte Common Antigens/metabolism
Mice
Mice, Inbred C57BL
Phenotype
Platelet Endothelial Cell Adhesion Molecule-1/metabolism
Chemicals
Platelet Endothelial Cell Adhesion Molecule-1
Leukocyte Common Antigens
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Taoudi Samir
Ontogeny of Haematopoietic Stem Cells Group, Medical Research Council/Juvenile Diabetes Research Foundation Centre for Development in Stem Cell Biology, Institute for Stem Cell Research, University of Edinburgh, West Mains Road, Edinburgh, UK.
Medvinsky Alexander
References (25)
25 references, click to expand
-
Aorta-associated CD34+ hematopoietic cells in the early human embryo.
Blood. 1996 Jan 1;87(1):67-72
PMID: 8547678
-
Development of hematopoietic stem cell activity in the mouse embryo.
Immunity. 1994 Jul;1(4):291-301
PMID: 7889417
-
Development of day-8 colony-forming unit-spleen hematopoietic progenitors during early murine embryogenesis: spatial and temporal mapping.
Blood. 1996 Jan 15;87(2):557-66
PMID: 8555477
-
Definitive hematopoiesis is autonomously initiated by the AGM region.
Cell. 1996 Sep 20;86(6):897-906
PMID: 8808625
-
Characterization of definitive lymphohematopoietic stem cells in the day 9 murine yolk sac.
Immunity. 1997 Sep;7(3):335-44
PMID: 9324354
-
In vitro generation of lymphohematopoietic cells from endothelial cells purified from murine embryos.
Immunity. 1998 Jun;8(6):761-9
PMID: 9655490
-
Intraaortic hemopoietic cells are derived from endothelial cells during ontogeny.
Development. 1998 Nov;125(22):4575-83
PMID: 9778515
-
Cbfa2 is required for the formation of intra-aortic hematopoietic clusters.
Development. 1999 Jun;126(11):2563-75
PMID: 10226014
-
Characterization of purified intraembryonic hematopoietic stem cells as a tool to define their site of origin.
Proc Natl Acad Sci U S A. 2005 Jan 4;102(1):134-9
PMID: 15623562
-
The placenta is a niche for hematopoietic stem cells.
Dev Cell. 2005 Mar;8(3):365-75
PMID: 15737932
-
CD144 (VE-cadherin) is transiently expressed by fetal liver hematopoietic stem cells.
Blood. 2005 Aug 1;106(3):903-5
PMID: 15831702
-
Progressive divergence of definitive haematopoietic stem cells from the endothelial compartment does not depend on contact with the foetal liver.
Development. 2005 Sep;132(18):4179-91
PMID: 16107475
-
Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse.
Development. 1999 Nov;126(22):5073-84
PMID: 10529424
-
Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo.
EMBO J. 2000 Jun 1;19(11):2465-74
PMID: 10835345
-
CFU-S(11) activity does not localize solely with the aorta in the aorta-gonad-mesonephros region.
Blood. 2000 Oct 15;96(8):2902-4
PMID: 11023528
-
Runx1 expression marks long-term repopulating hematopoietic stem cells in the midgestation mouse embryo.
Immunity. 2002 May;16(5):661-72
PMID: 12049718
-
Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta.
Immunity. 2002 May;16(5):673-83
PMID: 12049719
-
Blood-forming potential of vascular endothelium in the human embryo.
Development. 2002 Sep;129(17):4147-57
PMID: 12163416
-
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. 2002 Nov;129(21):4891-9
PMID: 12397098
-
Putative intermediate precursor between hematogenic endothelial cells and blood cells in the developing embryo.
Dev Growth Differ. 2003 Feb;45(1):63-75
PMID: 12630947
-
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):279-96
PMID: 5491581
-
Diffuse intraembryonic hemopoiesis in normal and chimeric avian development.
Dev Biol. 1981 Nov;88(1):180-91
PMID: 7286444
-
Properties of the earliest clonogenic hemopoietic precursors to appear in the developing murine yolk sac.
Proc Natl Acad Sci U S A. 1986 Jun;83(11):3851-4
PMID: 3012535
-
Hemopoietic stem cells in murine embryonic yolk sac and peripheral blood.
Proc Natl Acad Sci U S A. 1989 Oct;86(19):7456-9
PMID: 2571992
-
Potential intraembryonic hemogenic sites at pre-liver stages in the mouse.
Anat Embryol (Berl). 1995 Nov;192(5):425-35
PMID: 8546334