Abstract
The question of how cell division orientation is determined is fundamentally important for understanding tissue and organ shape in both healthy or disease conditions. Here we provide evidence for cell contact-dependent orientation of planar cell division in the mammalian embryonic skin. We propose a model where the core planar polarity proteins Celsr1 and Frizzled-6 (Fz6) communicate the long axis orientation of interphase basal cells to neighbouring basal mitoses so that they align their horizontal division plane along the same axis. The underlying mechanism requires a direct, cell surface, planar polarised cue, which we posit depends upon variant post-translational forms of Celsr1 protein coupled to Fz6. Our hypothesis has parallels with contact-mediated division orientation in early C. elegans embryos suggesting functional conservation between the adhesion-GPCRs Celsr1 and Latrophilin-1. We propose that linking planar cell division plane with interphase neighbour long axis geometry reinforces axial bias in skin spreading around the mouse embryo body.
Highlights
Horizontal cell divisions that generate symmetric daughters contribute new cells to epithelia driving tissue shape and growth
The interphase cell long axis is linked to cell division orientation in a number of different cell and tissue contexts[2, 5, 32]
Studies of the insect wing reveal that planar polarity-dependent control over cell division orientation can be achieved by actively generating cell shape anisotropies in the mitotic cells themselves[12]
Summary
Horizontal (planar) cell divisions that generate symmetric daughters contribute new cells to epithelia driving tissue shape and growth. Compelling evidence suggests that as mitotic cells round up they retain a ‘memory’ of the spatial geometry of their previous interphase existence by using cellular landmarks derived from both extracellular matrix contacts[3] and tri-cellular junctions[4]. Another intriguing idea posits that local cell shape during interphase influences the cleavage plane of neighbouring mitotic cells[5]. In this study we provide evidence for a cell contact-dependent mechanism of cell division orientation in the mammalian skin epithelium, where planar polarity proteins align the cleavage plane of horizontal cell divisions with the planar cell shape of neighbouring interphase cells. We propose a model whereby cell surface asymmetry of planar polarity proteins communicates interphase long axis geometry to a neighbouring dividing cell to directly orient the mitotic spindle
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