Definitive erythropoiesis in chicken yolk sac

Abstract

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.

Primitive and definitive erythropoiesis in the yolk sac: a birds eye view

“…Chick/quail and chick/chick chimera studies (Beaupain et al, 1979;Dieterlen-Lievre, 1975;Dieterlen-Lievre et al, 1976;Lassila et al, 1978;Lassila et al, 1982;Martin et al, 1978) and chick/chick parabiotic studies (Metcalf and Moore, 1971;Moore and Owen, 1965; indicated that, at least during the first few days of definitive erythrocyte generation, the source of cells is mainly yolk sac-derived. At about the same time, if not earlier, intraembryonic hematopoietic cells have been observed in association with the dorsal aorta (DieterlenLievre and Martin, 1981;Jaffredo et al, 2003;Jaffredo et al, 2005;Jaffredo et al, 2000;Jaffredo et al, 1998;Jordan, 1916;Nagai and Sheng, 2008;Olah et al, 1988;Pardanaud et al, 1996). A number of questions can be asked, for instance, about whether dorsal aorta-derived hematopoietic cells undergo definitive erythropoiesis either in circulation or in the yolk sac niche; whether yolk sac-derived hematopoietic cells can find their way to the dorsal aorta; and what is the exact type of cells from the yolk sac that contribute to early definitive erythropoiesis.…”

“…From E2 to E5, yolk sac vasculature undergoes at least two phases of remodeling. Hemodynamic changes initiated by heart pulsation remodels early vascular plexus into arterial and venous trees between E2 and E3, followed by the remodeling from two-dimensional apposing arterial/venous trees to a three-dimensional paired arterial/venous network between E3 and E5 (Eichmann et al, 2005;Gonzalez-Crussi, 1971;le Noble et al, 2004;Nagai and Sheng, 2008;Van Mierop and Bertuch, 1967) (Fig. 4).…”

“…Erythropoietic cells in the bone marrow are seeded exogenously. Hematopoietic stem/progenitor cells that do not undergoing erythropoiesis, derived from both the dorsal aorta intraembryonically and the yolk sac extraembryonically, are in circulation at least from late E4 Nagai and Sheng, 2008). It is unclear whether they remain as dormant stem/ progenitor cells in circulation or in a transitory niche before the bone marrow niche starts to form at about E9 and becomes receptive for seeding by circulatory stem cells at about E12 (Bruns and Ingram, 1973;Metcalf and Moore, 1971;.…”

Early ontogenic origin of the hematopoietic stem cell lineage

“…Finally, our findings must be compared with classical data on avian hematopoietic ontogenesis (28). It remains to be determined whether mammalian and avian de novo hematopoiesis differ significantly or whether a closer look at the presumed sites of blood-cell generation in chicken would reveal a more prominent role for the avian yolk sac (29).…”

Developmental regulation of hemoglobin synthesis in the green anole lizard Anolis carolinensis

“…Weber et al, 2000;Storz et al, 2008;Runck et al, 2009), the isoHb differentiation is not associated with any discrete differences in the developmental timing of expression. The two lizard-specific -globin paralogs exhibit subtle changes in expression during the course of prenatal development, but the pattern appears to be qualitatively different from the more discrete gene switching that characterizes the ontogenetic regulation of Hb synthesis in other tetrapod vertebrates (Banville and Williams, 1985a;Banville and Williams, 1985b;Hardison, 2001;Nagel and Steinberg, 2001;Fuchs et al, 2006;Nakazawa et al, 2006;Alev et al, 2008;McIntyre et al, 2008;Nagai and Sheng, 2008;Alev et al, 2009). …”