Abstract
Human embryonic development involves transition from yolk sac (YS) to liver (L) hemopoiesis. We report the identification of pluripotent, erythroid, and granulo-macrophage progenitors in YS, L, and blood from human embryos. Furthermore, comprehensive studies are presented on the number of hemopoietic progenitors and precursors, as well as of other cell types, in YS, L, and blood at precisely sequential stages in embryos and early fetuses (i.e., at 4.5-8 wk and 9-10 wk postconception, respectively). Our results provide circumstantial support to a monoclonal hypothesis for human embryonic hemopoiesis, based on migration of stem and early progenitor cells from a generation site (YS) to a colonization site (L) via circulating blood. The YS----L transition is associated with development of the differentiation program in proliferating stem cells: their erythroid progeny shows, therefore, parallel switches of multiple parameters, e.g., morphology (megaloblasts----macrocytes) and globin expression (zeta----alpha, epsilon----gamma).
MeSH Terms
Colony-Forming Units Assay
Embryo, Mammalian/physiology
Erythroblasts/analysis
Female
Granulocytes/cytology
Hematopoiesis
Humans
Liver/embryology
Monocytes/cytology
Pregnancy
Stem Cells/physiology
Time Factors
Yolk Sac/physiology
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Migliaccio G
Migliaccio A R
Petti S
Mavilio F
Russo G
Lazzaro D
Testa U
Marinucci M
Peschle C
References (30)
30 references, click to expand
-
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
-
Surface phenotypes of human hemopoietic progenitor cells defined by monoclonal antibodies.
Blood. 1985 Sep;66(3):496-502
PMID: 4027376
-
In vitro production of erythropoietin by mouse fetal liver.
Blood. 1975 Jul;46(1):85-90
PMID: 1131429
-
Role of stem cell migration in initiation of mouse foetal liver haemopoiesis.
Nature. 1975 Dec 25;258(5537):726-8
PMID: 1207754
-
Human erythroid colony formation in vitro: evidence for clonal origin.
J Cell Physiol. 1976 NOV;89(3):489-92
PMID: 977665
-
Purification of human erythropoietin.
J Biol Chem. 1977 Aug 10;252(15):5558-64
PMID: 18467
-
Circulating erythropoietic precursors assessed in culture: characterization in normal men and patients with hemoglobinopathies.
Blood. 1977 Dec;50(6):1081-92
PMID: 922159
-
Developmental biology of human hemoglobins.
Prog Hematol. 1977;10:43-90
PMID: 337366
-
Erythroid colony formation from human fetal liver.
Proc Natl Acad Sci U S A. 1978 Feb;75(2):984-8
PMID: 273259
-
Identification of megakaryocytes, macrophages, and eosinophils in colonies of human bone marrow containing neurtophilic granulocytes and erythroblasts.
Blood. 1979 May;53(5):1023-7
PMID: 435638
-
Characterization of circulating erythroid progenitor cells in human newborn blood.
J Lab Clin Med. 1981 Mar;97(3):322-31
PMID: 7462770
-
Structural identity of the pluripotential hemopoietic stem cell.
Blood Cells. 1979 Jun 15;5(2):143-59
PMID: 122166
-
Identification and characterization of three classes of erythroid progenitors in human fetal liver.
Blood. 1981 Sep;58(3):565-72
PMID: 7259837
-
Studies of circulating hemopoietic progenitor cells in human fetal blood.
Blood. 1982 May;59(5):976-9
PMID: 7074222
-
Renewal and commitment to differentiation of hemopoietic stem cells (an interpretive review).
Blood. 1983 May;61(5):823-9
PMID: 6338973
-
Stem cells in normal and leukemic hemopoiesis (Henry Stratton Lecture, 1982).
Blood. 1983 Jul;62(1):1-13
PMID: 6407542
-
Development of pluripotent hematopoietic progenitor cells in the human fetus.
Blood. 1983 Jul;62(1):118-23
PMID: 6860790
-
Antigenically distinct subpopulations of myeloid progenitor cells (CFU-GM) in human peripheral blood and marrow.
Proc Natl Acad Sci U S A. 1983 Jul;80(13):4114-8
PMID: 6191330
-
Mouse yolk sac and intraembryonic tissues produce factors able to elicit differentiation of erythroid burst-forming units and colony-forming units, respectively.
Proc Natl Acad Sci U S A. 1984 Mar;81(5):1453-6
PMID: 6584891
-
Embryonic----Fetal Hb switch in humans: studies on erythroid bursts generated by embryonic progenitors from yolk sac and liver.
Proc Natl Acad Sci U S A. 1984 Apr;81(8):2416-20
PMID: 6201856
-
G6PD isoenzyme analysis of myeloid and lymphoid cells in human multilineage colonies.
Blood. 1984 Jun;63(6):1481-7
PMID: 6609730
-
Blood cell development. The message in the medium.
Nature. 1984 Jun 28-Jul 4;309(5971):746-7
PMID: 6738692
-
Cell migrations in embryos.
Cell. 1984 Sep;38(2):353-60
PMID: 6467371
-
Purification and characterization of human T-lymphocyte-derived erythroid-potentiating activity.
J Biol Chem. 1984 Aug 25;259(16):9992-6
PMID: 6332112
-
Haemoglobin switching in human embryos: asynchrony of zeta----alpha and epsilon----gamma-globin switches in primitive and definite erythropoietic lineage.
Nature. 1985 Jan 17-23;313(5999):235-8
PMID: 2578614
-
Isolation and characterization of genomic and cDNA clones of human erythropoietin.
Nature. 1985 Feb 28-Mar 6;313(6005):806-10
PMID: 3838366
-
Purification and biochemical characterization of human pluripotent hematopoietic colony-stimulating factor.
Proc Natl Acad Sci U S A. 1985 Mar;82(5):1526-30
PMID: 3871951
-
Erythroid progenitor cells and stimulating factors during murine embryonic and fetal development.
Exp Hematol. 1985 Mar;13(3):200-8
PMID: 3872223
-
Molecular characterization and expression of the gene encoding human erythroid-potentiating activity.
Nature. 1985 Jun 27-Jul 3;315(6022):768-71
PMID: 3839290
-
Erythropoietic progenitors capable of colony formation in culture: response of normal and genetically anemic W-W-V mice to manipulations of the erythron.
J Cell Physiol. 1974 Aug;84(1):1-12
PMID: 4602376