STELLA-positive subregions of the primitive streak contribute to posterior tissues of the mouse gastrula

Abstract

The developmental relationship between the posterior embryonic and extraembryonic regions of the mammalian gastrula is poorly understood. Although many different cell types are deployed within this region, only the primordial germ cells (PGCs) have been closely studied. Recent evidence has suggested that the allantois, within which the PGCs temporarily take up residence, contains a pool of cells, called the Allantoic Core Domain (ACD), critical for allantoic elongation to the chorion. Here, we have asked whether the STELLA-positive cells found within this region, thought to be specified PGCs, are actually part of the ACD and to what extent they, and other ACD cells, contribute to the allantois and fetal tissues. To address these hypotheses, STELLA was immunolocalized to the mouse gastrula between Early Streak (ES) and 12-somite pair (-s) stages (~6.75 – 9.0 days post coitum, dpc) in histological sections. STELLA was found in both the nucleus and cytoplasm in a variety of cell types, both within and outside of the putative PGC trajectory. Fate-mapping the headfold-stage (~7.75 – 8.0 dpc) posterior region, by which time PGCs are thought to be segregated into a distinct lineage, revealed that the STELLA-positive proximal ACD and intraembryonic posterior primitive streak (IPS) contributed to a wide range of somatic tissues that encompassed derivatives of the three primary germ layers. This contribution included STELLA-positive cells localizing to tissues both within and outside of the putative PGC trajectory. Thus, while STELLA may identify a subpopulation of cells destined for the PGC lineage, our findings reveal that it may be part of a broader niche that encompasses the ACD and through which the STELLA population may contribute cells to a wide variety of posterior tissues of the mouse gastrula.

The hypoblast (visceral endoderm): an evo-devo perspective

“…However, there might also be a contribution from the posterior primitive streak for the cloacal region (Hassoun et al, 2010) and within the allantois (Mikedis and Downs, 2012). In addition, recent findings have raised the possibility that remnants of the AVE might remain in the final endodermal layer and contribute to the gut (Kwon et al, 2008) (Fig.…”

“…There, in collaboration with what appears to be a posterior extension of the primitive streak, a putative posterior node is established, whose cells direct allantoic elongation to the chorion and contribute to a variety of posterior structures, both embryonic and extra-embryonic (Mikedis and Downs, 2012). Characterization of 'allantoisassociated extra-embryonic visceral endoderm' (AX) is in its early stages and thus, its relation to the PVE and other types of VE is not yet clear.…”

Mouse Primordial Germ Cells

“…(C 2 ) The XPS then expands to form the ACD, a stem/progenitor cell pool. "PGCs" in the ACD and intraembryonic posterior primitive streak (IPS) are part of the anteroposterior body axis and contribute to multiple somatic lineages within the surrounding posterior embryo (Mikedis and Downs, 2012). (C 3 ) The posterior end of the primitive streak has regressed/differentiated and is confined to the embryo.…”

“…Some ACD descendants within the allantois form a midline file of cells (black line within allantois), similar to the anterior node-derived notochord (black line extending from the yellow circle representing the node) ). Scholer et al, 1990), PRDM1 (BLIMP1) (Mikedis and Downs, unpublished;Ohinata et al, 2005;Vincent et al, 2005), STELLA (DPPA3, PGC7) (Mikedis and Downs, 2012;Saitou et al, 2002), and IFITM3 (FRAGILIS, MIL1) (Mikedis and Downs, 2013;Saitou et al, 2002). Thus, in light of the existence of the ACD, we investigated the evidence for an extragonadal germ line within the allantois, and balanced this question by turning it on its head, asking whether PGCs might actually be part of a pluripotent stem cell pool that builds the understudied fetal-umbilical connection.…”

The Formation and Migration of Primordial Germ Cells in Mouse and Man

“…Although it is not exactly clear when PGCs undergo irreversible determination, PGCs formed in extraembryonic tissues are subsequently incorporated into the hindgut and move inside the embryo proper (Chiquoine 1954;Ginsburg et al 1990;Lawson and Hage 1994;Mikedis and Downs 2012). Several cell types migrate during development, the length and varied terrain that PGCs traverse is, however, unrivaled.…”