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Correlating Cell Behavior with Tissue Topology in Embryonic Epithelia

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  • Sebastian A Sandersius
  • Manli Chuai
  • Cornelis J Weijer
  • Timothy J Newman

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.

Suggested Citation

  • Sebastian A Sandersius & Manli Chuai & Cornelis J Weijer & Timothy J Newman, 2011. "Correlating Cell Behavior with Tissue Topology in Embryonic Epithelia," PLOS ONE, Public Library of Science, vol. 6(4), pages 1-11, April.
  • Handle: RePEc:plo:pone00:0018081
    DOI: 10.1371/journal.pone.0018081
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    References listed on IDEAS

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    1. Matthew C. Gibson & Ankit B. Patel & Radhika Nagpal & Norbert Perrimon, 2006. "The emergence of geometric order in proliferating metazoan epithelia," Nature, Nature, vol. 442(7106), pages 1038-1041, August.
    2. Ying Gong & Chunhui Mo & Scott E. Fraser, 2004. "Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation," Nature, Nature, vol. 430(7000), pages 689-693, August.
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    Cited by:

    1. Nilay Kumar & Jennifer Rangel Ambriz & Kevin Tsai & Mayesha Sahir Mim & Marycruz Flores-Flores & Weitao Chen & Jeremiah J. Zartman & Mark Alber, 2024. "Balancing competing effects of tissue growth and cytoskeletal regulation during Drosophila wing disc development," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    2. Jordán, Ferenc, 2022. "The network perspective: Vertical connections linking organizational levels," Ecological Modelling, Elsevier, vol. 473(C).
    3. Ying Xin & Chathuri Madubhashini Karunarathna Mudiyanselage & Winfried Just, 2018. "Development of epithelial tissues: How are cleavage planes chosen?," PLOS ONE, Public Library of Science, vol. 13(11), pages 1-16, November.
    4. Nieves Atienza & Maria-Jose Jimenez & Manuel Soriano-Trigueros, 2021. "Stable Topological Summaries for Analyzing the Organization of Cells in a Packed Tissue," Mathematics, MDPI, vol. 9(15), pages 1-22, July.

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