The visceral yolk sac endoderm provides for absorption of nutrients to the embryo during neurulation

Abstract

Neural tube defects (NTDs) represent some of the most common congenital malformations in humans. The causes of NTDs are complex with both genetic and environmental contributing factors. Periconception nutrition is an important environmental factor influencing the penetrance of NTDs. NTDs arise from failure to close the neural tube completely during development, an event that occurs before establishment of the chorioallantoic placenta. During neurulation, nutrients are absorbed by histotrophic mechanisms and absorbed by endocytosis in the endoderm-derived cell layer of the visceral yolk sac (VYS). Here we review the histotrophic mechanisms by which nutrients are delivered to the human embryo during this critical time period. Because more detailed studies on the molecular mechanisms regulating uptake of nutrients have been performed using rodent models, most importantly mouse and rat models, we will also review nutrient uptake in these model organisms to set the stage for presentation of experimental data that have provided valuable information about how nutrients are delivered to the neurulating embryo.

A conserved role for non-neural ectoderm cells in early neural development

“…Previous literature did not report evidence that development outside the VYS can directly affect anterior neural patterning (Madabhushi and Lacy, 2011;Molkentin et al, 1997). Nevertheless, we cannot rule out the possibility that VYS deficiencies contribute, at least in part, to the head phenotype of PROX embryos (Mao et al, 2010;Zohn and Sarkar, 2010). In chick experiments, the anterior non-neural ectoderm is specifically removed without altering the subjacent endoderm layer at HH4, a developmental stage equivalent to mouse E7.5.…”

Mouse early extra-embryonic lineages activate compensatory endocytosis in response to poor maternal nutrition

“…Preimplantation embryos differentiate a polarised endocytic and lysosomal system within the outer TE lineage during cleavage that preferentially internalises fluid from the outer apical membrane domain (Fleming and Pickering, 1985), comprises megalin (Lrp2 -Mouse Genome Informatics) and cubilin LDL-family receptors (Gueth-Hallonet et al, 1994;Moestrup and Verroust, 2001;Assémat et al, 2005) and is sensitive to insulin . Endocytic, histiotrophic nutrition characterises the maternal-fetal nutrient pathway of the visceral yolk sac (VYS) placenta (Beckman et al, 1997;Zohn and Sarkar, 2010), and we have shown that megalin-mediated VYS endocytosis is enhanced in late gestation in response to maternal protein restriction (Watkins et al, 2008). This second extra-embryonic lineage derives from the primitive endoderm (PE) formed in the late blastocyst at the blastocoelic face of the ICM (Rossant and Tam, 2009).…”

Urea-based osmoregulation in the developing embryo of oviparous cartilaginous fish (Callorhinchus milii): contribution of the extraembryonic yolk sac during the early developmental period

“…Taken together, our findings indicate that urea is produced in the endodermal layer of the YSM, and is then excreted into nearby blood vessels, and subsequently transferred to the embryo in order to maintain a high concentration of urea in the body fluid. Yolk sacs are found in many vertebrates, and the extra-embryonic YSM has been considered to play a key role in the absorption of yolk nutrients (Lambson, 1970;Diez and Davenport, 1990;Lechenault et al, 1993;Zohn and Sarkar, 2010;Bauer et al, 2013). An intriguing finding on the role of the YSM in teleost fish is that it is involved in osmoregulation during early development .…”