Abstract
Measurements on embryonic epithelial tissues in a diverse range of organisms have shown that the statistics of cell neighbor numbers are universal in tissues where cell proliferation is the primary cell activity. Highly simplified non-spatial models of proliferation are claimed to accurately reproduce these statistics. Using a systematic critical analysis, we show that non-spatial models are not capable of robustly describing the universal statistics observed in proliferating epithelia, indicating strong spatial correlations between cells. Furthermore we show that spatial simulations using the Subcellular Element Model are able to robustly reproduce the universal histogram. In addition these simulations are able to unify ostensibly divergent experimental data in the literature. We also analyze cell neighbor statistics in early stages of chick embryo development in which cell behaviors other than proliferation are important. We find from experimental observation that cell neighbor statistics in the primitive streak region, where cell motility and ingression are also important, show a much broader distribution. A non-spatial Markov process model provides excellent agreement with this broader histogram indicating that cells in the primitive streak may have significantly weaker spatial correlations. These findings show that cell neighbor statistics provide a potentially useful signature of collective cell behavior.
Highlights
Development of higher organisms is dependent on extensive division and movement of cells arranged in well-organized, densely packed epithelial sheets, in many instances only one cell layer thick
The histogram obtained for Pre-S is narrow, and agrees well with the universal histogram measured by GPNP
Experimental histograms We have measured the distribution of neighbors in the epiblast of the early chick embryo at stage EGXII of development [15], which is pre-streak (Pre-S), as well as at stage HH2 where there is already a significant amount of cell movement occurring associated with the formation of the primitive streak [16]
Summary
Development of higher organisms is dependent on extensive division and movement of cells arranged in well-organized, densely packed epithelial sheets, in many instances only one cell layer thick. Major questions concern how tissue structure and dynamics are driven by individual cell behaviors; for example, whether the axes of cell divisions are organized on a tissue-wide scale, possibly resulting in directional tissue elongation, and whether there is any logic as to which cells become neighbors after division [1]. Cells in these embryonic epithelial sheets often have approximately polygonal cross-sections in the plane of the sheet. The statistics describing this diversity of cell neighbor numbers (CNN) have recently been observed to be strikingly universal across diverse taxa [2]
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