Abstract
The relative contribution of yolk sac (YS)-derived cells to the circulating definitive hematopoietic progenitor cell (HPC) pool that seeds the fetal liver remains controversial due to the presence of systemic circulation and the onset of hematopoiesis within the embryo proper (EP) before liver seeding. Ncx1-/- embryos fail to initiate a heartbeat on embryonic day (E) 8.25, but continue to develop through E10. We detected normal numbers of primitive erythroid progenitors in Ncx1-/- versus wild type (WT) YS, but primitive erythroblasts did not circulate in the Ncx1-/- EP. While there was no significant difference in the number of definitive HPCs in Ncx1-/- versus WT YS through E9.5, the Ncx1-/- EP was nearly devoid of HPCs. Thus, primitive erythroblasts and essentially all definitive HPCs destined to initially seed the fetal liver after E9.5 are generated in the YS between E7.0-E9.5 and are redistributed into the EP via the systemic circulation.
MeSH Terms
Animals
Embryo, Mammalian/cytology,embryology
Erythroblasts/cytology,metabolism
Hematopoietic Stem Cells/cytology,metabolism
Liver/cytology,embryology
Mice
Mice, Knockout
Sodium-Calcium Exchanger/genetics,metabolism
Yolk Sac/cytology,embryology
Chemicals
NCX1 protein, mouse
Sodium-Calcium Exchanger
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Lux Christopher T
Department of Pediatrics, Herman B Wells Center for Pediatric Research, Indiana University School of Medicine, Indianapolis 46202-5254, USA.
Yoshimoto Momoko
McGrath Kathleen
Conway Simon J
Palis James
Yoder Mervin C
References (23)
23 references, click to expand
-
Sodium-calcium exchanger is initially expressed in a heart-restricted pattern within the early mouse embryo.
Mech Dev. 1999 Oct;88(1):119-22
PMID: 10525196
-
Cloning of a third mammalian Na+-Ca2+ exchanger, NCX3.
J Biol Chem. 1996 Oct 4;271(40):24914-21
PMID: 8798769
-
Cell tracing shows the contribution of the yolk sac to adult haematopoiesis.
Nature. 2007 Apr 26;446(7139):1056-61
PMID: 17377529
-
Circulation is established in a stepwise pattern in the mammalian embryo.
Blood. 2003 Mar 1;101(5):1669-76
PMID: 12406884
-
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
-
Qualitative and quantitative aspects of haematopoietic cell development in the mammalian embryo.
Immunol Today. 1998 May;19(5):228-36
PMID: 9613041
-
Hemoglobin switching during murine embryonic development: evidence for two populations of embryonic erythropoietic progenitor cells.
Blood. 1986 Mar;67(3):716-21
PMID: 3947744
-
Definitive hematopoiesis is autonomously initiated by the AGM region.
Cell. 1996 Sep 20;86(6):897-906
PMID: 8808625
-
AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis.
Cell. 1996 Jan 26;84(2):321-30
PMID: 8565077
-
Onset of cardiac function during early mouse embryogenesis coincides with entry of primitive erythroblasts into the embryo proper.
Circ Res. 2003 Feb 7;92(2):133-5
PMID: 12574139
-
Hematopoiesis in the yolk sac: more than meets the eye.
Exp Hematol. 2005 Sep;33(9):1021-8
PMID: 16140150
-
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 U S A. 1995 Jan 31;92(3):773-7
PMID: 7846049
-
The allantois and chorion, when isolated before circulation or chorio-allantoic fusion, have hematopoietic potential.
Development. 2006 Nov;133(21):4183-92
PMID: 17038514
-
Chromosome marker studies on the development of the haemopoietic system in the chick embryo.
Nature. 1965 Dec 4;208(5014):956 passim
PMID: 5868856
-
The placenta is a niche for hematopoietic stem cells.
Dev Cell. 2005 Mar;8(3):365-75
PMID: 15737932
-
Targeted inactivation of the sodium-calcium exchanger (Ncx1) results in the lack of a heartbeat and abnormal myofibrillar organization.
FASEB J. 2001 May;15(7):1209-11
PMID: 11344090
-
Ontogeny of the hematopoietic system.
Annu Rev Immunol. 2007;25:745-85
PMID: 17201678
-
Blood island formation: longstanding observations and modern interpretations.
Exp Hematol. 2005 Sep;33(9):1041-7
PMID: 16140152
-
Differentiation of the mouse hepatic primordium. II. Extrinsic origin of the haemopoietic cell line.
Cell Differ. 1981 Nov;10(5):243-52
PMID: 7307077
-
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
-
Erythropoiesis and lymphopoiesis in the chick yolk-sac-embryo chimeras: contribution of yolk sac and intraembryonic stem cells.
Blood. 1982 Feb;59(2):377-81
PMID: 7034816
-
Role of stem cell migration in initiation of mouse foetal liver haemopoiesis.
Nature. 1975 Dec 25;258(5537):726-8
PMID: 1207754
-
Spatial and temporal emergence of high proliferative potential hematopoietic precursors during murine embryogenesis.
Proc Natl Acad Sci U S A. 2001 Apr 10;98(8):4528-33
PMID: 11296291