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New skin cells are continuously produced in the lowest cell layers of the epidermis, and move upwards to integrate into the stratum granulosum layer to replace old cells (which also move upwards to leave the layer). How stratum granulosum cells are replaced without disrupting the tight junction barrier was not well understood.

Further experiments revealed that the tight junctions move from cell to cell in a spatiotemporally-coordinated manner in order to maintain a continuous barrier throughout the stratum granulosum as cells are replaced. A newly formed stratum granulosum cell appears beneath the cell that it will replace. The shape of these cells enables a new barrier of three-way tight junction contacts to form between them and the neighboring cells in the stratum granulosum. After this barrier has formed, the upper cell leaves the stratum granulosum.

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A representative image of a ZO-1-positive double-edged polygon surrounded by six single-edged polygons evaluated in Figure 1E. The Z-axis position of each polygon was defined by an average of the Z-axis positions (numbers) of its vertices, analyzed by Imaris software (purple arrowheads, external polygon; yellow arrowheads, internal polygon; green arrowheads, adjacent single-edged polygons). Scale bar, 10 µm. TJ, tight junction.

(A) Colocalization of occludin, a transmembrane protein located at the TJs, with Venus in whole-mounted epidermal sheet from the ear skin of a ZO-1-Venus transgenic mouse. No morphological changes were observed in the TJ honeycomb in ZO-1-Venus transgenic mice. (B) Skin section staining of ZO-1-Venus transgenic mice after intradermal injection of Sulfo-NHS-LC-biotin as a tracer (Furuse et al., 2002; Yokouchi et al., 2015). Venus-positive junctions were observed to limit the inside-out permeation of the tracer (yellow arrows), indicating that Venus successfully labeled the TJs without any apparent change in their occlusive function. Scale bars, 10 µm. TJ, tight junction.

In our f-TKD model, the cell columns exist only in the SG and SC layers, rather than extending from the basal layer through to the SC. The cells originate from stem cells in the basal layer and are randomly supplied to a spinous layer. Once the cells enter the SG layer, cell turnover in adjacent columns is tightly coordinated in a spatiotemporal manner, leading to the regular interdigitation pattern (Figure 6C). Epidermal homeostasis is maintained by balancing cell proliferation in the basal layer, cell translocation (differentiation) from the basal to the spinous layer, cell integration to the SC/SG layer, and cell shedding from the top of the SC as squames. Future studies are needed to explore how this balance among critical processes in the epidermal layers is regulated to maintain a constant thickness of the epidermis.

Yokouchi and colleagues employs state of the art imaging technologies to reveal novel information regarding the structure and turnover of epidermal cells with tight junctions in the skin. The authors show that tight junctions appear with upper and lower polygons in the stratum granulosum (SG). Using observations on TJ shape and function, the present manuscript adapts Kelvin's tetrakaidecahedron to provide a very original, attractive and interesting mathematical and physical model that explains how the continuously renewing epidermal barrier can retain TJ barrier function in a single layer, the SG2, while individual cells move upward. Overall, this manuscript changes the paradigm for our understanding of how stratified cells with tight junctions continually regeneration and yet maintain barrier function. The work is logically presented and the data are reasonably thorough and convincing in support of these impactful conclusions.

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