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Review
. 2022 Nov:131:117-123.
doi: 10.1016/j.semcdb.2022.05.009. Epub 2022 May 27.

Human epiblast lumenogenesis: From a cell aggregate to a lumenal cyst

Amber E Carleton  1 , Mara C Duncan  2 , Kenichiro Taniguchi  3
Affiliations
Review

Human epiblast lumenogenesis: From a cell aggregate to a lumenal cyst

Amber E Carleton et al. Semin Cell Dev Biol. 2022 Nov.

Abstract

The formation of a central lumen in the human epiblast is a critical step for development. However, because the lumen forms in the epiblast coincident with implantation, the molecular and cellular events of this early lumenogenesis process cannot be studied in vivo. Recent developments using new model systems have revealed insight into the underpinnings of epiblast formation. To provide an up-to-date comprehensive review of human epiblast lumenogenesis, we highlight recent findings from human and mouse models with an emphasis on new molecular understanding of a newly described apicosome compartment, a novel 'formative' state of pluripotency that coordinates with epiblast polarization, and new evidence about the physical and polarized trafficking mechanisms contributing to lumenogenesis.

Keywords: Epiblast lumenogenesis; Epithelial cell polarity; Human epiblast; Membrane trafficking; Pluripotent stem cells.

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Conflict of interest statement

Declaration of Competing Interest The authors declare no conflict of interest.

Figures

Figure 1.
Figure 1.. Mouse and human epiblast lumenogenesis.
(Top) As the human blastocyst implants, polar TE (pTE, yellow) attaches to the uterus, unpolarized epiblast cells (light teal) begin to polarize, initiate radial organization, and develop a central epiblast lumen (white space surrounded by epiblast cells (shown in teal or green depending on the pluripotency state)). A population of the epiblast cells adjacent to the pTE initiates squamous morphogenesis and adopts an amnion fate (squamous cells), forming an asymmetric amniotic sac structure. (Middle) In the mouse, mural TE cells (salmon color) initiate placentation. Polar TE cells give rise to the ectoplacental cone and ExE (yellow mushroom-shaped structure overlying the epiblast); ExE formation “pushes” the epiblast domain into the blastocoel cavity [38, 45, 46], enabling the formation of the cup-like epiblast structure encased by primitive endoderm (blue). (Botom) Illustration of the transition of the pluripotency states, from naïve to formative to primed (shown in the gradient of light teal, teal, light green and green), occurring in the epiblast cells in both mouse and human embryos.
Figure 2.
Figure 2.. Fluid transport facilitates epiblast lumen opening.
Schematic showing known fluid transport pathways that facilitate epiblast lumen opening in mouse embryos. A recent study by Kim et al. uncovered that fluid transport is mediated by transcytosis, pumps (Na+/K+-ATPases and aquaporins), as well as by the formation of leaky junctions during mitosis [21].
Figure 3.
Figure 3.. Polarized membrane trafficking and apical membrane morphogenesis discovered in the human epiblast.
A schematic summary of some of the polarized trafficking pathways that are supported by existing data in hPSC models (pink – early endosome; green – recycling endosome; blue – secretory vesicles, demarcated by distinct RAB proteins). Note that the overall trafficking machinery is much more complex and remains to be identified by further exploration in pluripotent cell types. Comprehensive reviews of various trafficking networks are found elsewhere (e.g., [63]).
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