The allantois and chorion, when isolated before circulation or chorio-allantoic fusion, have hematopoietic potential

Zeigler, Brandon M.; Sugiyama, Daisuke; Chen, Michael; Guo, Yue; Downs, Karen M.; Speck, Nancy A.

doi:10.1242/dev.02596

Cited by 157 publications

(151 citation statements)

References 59 publications

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“…Similar analysis of the E9.5-activated embryos (Fig. S3B) confirmed the expression of the MER-Cre-MER recombinase in Runx1 + embryonic territories (16).…”

Section: Resultssupporting

confidence: 71%

“…At the neural-plate stage (E7.5), Runx1 is expressed in extraembryonic mesoderm of the proximal yolk sac and chorion, as revealed by β-galactosidase reporter gene staining (16). The chorionic expression of Runx1 at the late neural-plate stage was detected by in situ hybridization with a radioactive probe corresponding to the upstream coding region (18).…”

Section: Resultsmentioning

confidence: 99%

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Early ontogenic origin of the hematopoietic stem cell lineage

Tanaka¹,

Hayashi²,

Kubota³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Several lines of evidence suggest that the adult hematopoietic system has multiple developmental origins, but the ontogenic relationship between nascent hematopoietic populations under this scheme is poorly understood. In an alternative theory, the earliest definitive blood precursors arise from a single anatomical location, which constitutes the cellular source for subsequent hematopoietic populations. To deconvolute hematopoietic ontogeny, we designed an embryo-rescue system in which the key hematopoietic factor Runx1 is reactivated in Runx1-null conceptuses at specific developmental stages. Using complementary in vivo and ex vivo approaches, we provide evidence that definitive hematopoiesis and adult-type hematopoietic stem cells originate predominantly in the nascent extraembryonic mesoderm. Our data also suggest that other anatomical sites that have been proposed to be sources of the definitive hematopoietic hierarchy are unlikely to play a substantial role in de novo blood generation.

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“…Similar analysis of the E9.5-activated embryos (Fig. S3B) confirmed the expression of the MER-Cre-MER recombinase in Runx1 + embryonic territories (16).…”

Section: Resultssupporting

confidence: 71%

Section: Resultsmentioning

confidence: 99%

Early ontogenic origin of the hematopoietic stem cell lineage

Tanaka¹,

Hayashi²,

Kubota³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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“…It has been well-documented that extraembryonic tissues, including the yolk sac and allantois in birds and mammals and the placenta in mammals, contribute to the generation of definitive erythrocytes during amniote development (Dantschakoff, 1908;Moore and Owen, 1965;Moore and Metcalf, 1970;Dieterlen-Lievre et al, 1976;Weissman et al, 1978;Beaupain et al, 1979;Caprioli et al, 1998;Palis and Yoder, 2001;McGrath and Palis, 2005;Mikkola et al, 2005;Ottersbach and Dzierzak, 2005;Zeigler et al, 2006;Corbel et al, 2007;Samokhvalov et al, 2007;Lux et al, 2008;Rhodes et al, 2008). What remain not well-understood are the precise cellular source and niche of definitive erythropoiesis and the relative contributions of intraembryonic-and extraembryonic-generated definitive erythrocytes in embryonic blood.…”

Section: Introductionmentioning

confidence: 99%

Definitive erythropoiesis in chicken yolk sac

Nagai¹,

Sheng²

2008

Developmental Dynamics

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The first wave of erythropoiesis in amniotic animals generates all primitive erythrocytes and takes place exclusively in yolk sac mesoderm. It is less clear, however, to what extend and for how long the yolk sac contributes to the second wave of erythropoiesis which gives rise to definitive erythrocytes for later embryonic and adult use. Here, we examine the initiation, duration, and site of definitive erythrocyte formation in chicken yolk sac. We show that the earliest definitive erythrocytes are generated in yolk sac venous vessels surrounding major arteries at embryonic day (E) 4 -4.5, and that mature definitive erythrocytes enter circulating at E4.5-E5. This takes place at a time when yolk sac vasculature remodels extensively to generate paired arterial/venous vessels. The yolk sac remains the predominant site for definitive erythropoiesis from E5 to E10, and continues to generate definitive erythrocytes at least until E15. Similar to primitive erythropoiesis, definitive erythropoiesis in the yolk sac is accompanied by the expression of transcriptional regulators gata1, scl, and lmo2. Furthermore, our data suggest that one main source of definitive erythropoietic cells is the pre-existing vascular endothelial cells. It remains unclear whether yolk sac derived hematopoietic progenitors that do not undergo erythropoiesis in the yolk sac may take up intraembryonic niches and contribute to erythropoietic stem cell population after hatching.

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“…The endoderm of yolk sac was biotinylated by submerging the conceptus in HBS supplemented with 1 mg/ml EZ-Link Sulfo-NHS-LC-biotin (Pierce Chemical, Rockford, IL). The mesoderm of yolk sac and the embryo proper were biotinylated by injecting the same solution into the exocoelomic cavity using a mouth-held microcapillary pipette (Zeigler et al, 2006). After a 10-min incubation, embryos were washed with HBS, fixed with 4% formaldehyde in HBS for 10 min at RT, and processed for fluorescence microscopy with streptavidin-Texas Red (Calbiochem, San Diego, CA.…”

mentioning

confidence: 99%

Deficiency of Zonula Occludens-1 Causes Embryonic Lethal Phenotype Associated with Defected Yolk Sac Angiogenesis and Apoptosis of Embryonic Cells

Katsuno

Umeda

Matsui

et al. 2008

MBoC

245

219

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Zonula occludens (ZO)-1/2/3 are the members of the TJ-MAGUK family of membrane-associated guanylate kinases associated with tight junctions. To investigate the role of ZO-1 (encoded by Tjp1) in vivo, ZO-1 knockout (Tjp1 ؊/؊ ) mice were generated by gene targeting. Although heterozygous mice showed normal development and fertility, delayed growth and development were evident from E8.5 onward in Tjp1 ؊/؊ embryos, and no viable Tjp1 ؊/؊ embryos were observed beyond E11.5. Tjp1 ؊/؊ embryos exhibited massive apoptosis in the notochord, neural tube area, and allantois at embryonic day (E)9.5. In the yolk sac, the ZO-1 deficiency induced defects in vascular development, with impaired formation of vascular trees, along with defective chorioallantoic fusion. Immunostaining of wild-type embryos at E8.5 for ZO-1/2/3 revealed that ZO-1/2 were expressed in almost all embryonic cells, showing tight junction-localizing patterns, with or without ZO-3, which was confined to the epithelial cells. ZO-1 deficiency depleted ZO-1-expression without influence on ZO-2/3 expression. In Tjp1 ؉/؉ yolk sac extraembryonic mesoderm, ZO-1 was dominant without ZO-2/3 expression. Thus, ZO-1 deficiency resulted in mesoderms with no ZO-1/2/3, associated with mislocalization of endothelial junctional adhesion molecules. As a result, angiogenesis was defected in Tjp1 ؊/؊ yolk sac, although differentiation of endothelial cells seemed to be normal. In conclusion, ZO-1 may be functionally important for cell remodeling and tissue organization in both the embryonic and extraembryonic regions, thus playing an essential role in embryonic development. INTRODUCTIONIn multicellular organisms, cell-cell adhesion is critical for development and morphogenesis. Various types of cell-cell adhesion-related molecules have been identified, and evidence has accumulated that their expression and functions are critically regulated in a spatiotemporally highly organized way (Tsukita et al., 2001;Halbleib and Nelson, 2006). In general, cell-cell adhesion molecules are integral membrane proteins that associate with peripheral membrane proteins to regulate and integrate cell-cell adhesion-related phenomena. Zonula occludens (ZO)-1 is a founding member of membrane-associated guanylate kinase (MAGUK) family proteins of tight junctions (TJs), composed of three postsynaptic density 95/disc-large/ZO-1 (PDZ) domains, a Src homology 3 domain, a guanylate kinase (GUK) domain, an acidic domain, and an actin binding region (Itoh et al., 1993; Willott et al., 1993;Jesaitis and Goodenough, 1996;Haskins et al., 1998). It was first defined as an antigen for monoclonal antibodies that recognized TJs in epithelial cells, and it was subsequently revealed as a peripheral membrane protein with a molecular mass of 220 kDa, which underlied the cytoplasmic surface of plasma membranes of TJs (Stevenson et al., 1986). Evidence has accumulated that in epithelial cells, ZO-1 is exclusively located at TJs, but when TJs are not formed, it is concentrated in adherens junctions (AJs) (Itoh et al., 199...

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The allantois and chorion, when isolated before circulation or chorio-allantoic fusion, have hematopoietic potential

Cited by 157 publications

References 59 publications

Early ontogenic origin of the hematopoietic stem cell lineage

Early ontogenic origin of the hematopoietic stem cell lineage

Definitive erythropoiesis in chicken yolk sac

Deficiency of Zonula Occludens-1 Causes Embryonic Lethal Phenotype Associated with Defected Yolk Sac Angiogenesis and Apoptosis of Embryonic Cells

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