Paper Info
Title
Quantification Of Nematic Cell Polarity In Three-Dimensional Tissues
Abstract
Author summaryCell polarity enables cells to carry out specific functions. Cell polarity is characterized by the formation of different plasma membrane domains, each with specific composition of proteins, phospholipids and cytoskeletal components. In simple epithelial sheets, or tube-like tissues such as kidney, epithelial cells are known to display a single apical domain, facing a lumenal cavity, and a single basal domain on the opposite side of the cell, facing a basal layer of extracellular matrix. This apico-basal polarity defines a vector of cell polarity, which provides a direction of fluid transport, e.g., from the basal side of the sheet to the lumen-facing side. In more complex, three-dimensional epithelial tissues, such as liver tissue with its complex network of blood-transporting sinusoids, the membrane domains of hepatocyte cells display more intricate patterns, including rings and antipodal pairs of apical membrane. Here, we develop a mathematical framework to precisely characterize and quantify complex polarity patterns. Thereby, we reveal ordered patterns of cell polarity that span across a liver lobule. Our new method builds on physical concepts originally developed for ordered phases of liquid crystals. It provides a versatile tool to characterize the spatial organization of a complex three-dimensional tissue.How epithelial cells coordinate their polarity to form functional tissues is an open question in cell biology. Here, we characterize a unique type of polarity found in liver tissue, nematic cell polarity, which is different from vectorial cell polarity in simple, sheet-like epithelia. We propose a conceptual and algorithmic framework to characterize complex patterns of polarity proteins on the surface of a cell in terms of a multipole expansion. To rigorously quantify previously observed tissue-level patterns of nematic cell polarity (Morales-Navarette et al., eLife 2019), we introduce the concept of co-orientational order parameters, which generalize the known biaxial order parameters of the theory of liquid crystals. Applying these concepts to three-dimensional reconstructions of single cells from high-resolution imaging data of mouse liver tissue, we show that the axes of nematic cell polarity of hepatocytes exhibit local coordination and are aligned with the biaxially anisotropic sinusoidal network for blood transport. Our study characterizes liver tissue as a biological example of a biaxial liquid crystal. The general methodology developed here could be applied to other tissues and in-vitro organoids.
Year
DOI
Venue
2020
10.1371/journal.pcbi.1008412
PLOS COMPUTATIONAL BIOLOGY
DocType
Volume
Issue
Journal
16
12
ISSN
Citations 
PageRank 
1553-734X
0
0.34
References 
Authors
0
12
Name
Order
Citations
PageRank
André Scholich100.68
Simon Syga200.68
Hernán Morales-Navarrete300.34
Fabián Segovia-Miranda400.34
Hidenori Nonaka501.01
Kirstin Meyer600.34
Walter de Back7204.90
Lutz Brusch8263.46
Yannis Kalaidzidis9304.20
Marino Zerial10263.06
Frank Jülicher1102.03
Benjamin M. Friedrich1232.67