Evolving topological order in the postnatal visceral pleura

Author:

Liu Betty S.1,Ali Ali B.1,Kwan Stacey P.1,Pan Jennifer M.1,Wagner Willi L.2,Khalil Hassan A.1,Chen Zi1,Ackermann Maximilian3,Mentzer Steven J.1ORCID

Affiliation:

1. Laboratory of Adaptive and Regenerative Biology Brigham & Women's Hospital, Harvard Medical School Boston Massachusetts USA

2. Translational Lung Research Center, Department of Diagnostic and Interventional Radiology University of Heidelberg Heidelberg Germany

3. Institute of Functional and Clinical Anatomy, University Medical Center of the Johannes Gutenberg‐University Mainz Germany

Abstract

AbstractBackgroundChanges in epithelial cell shape reflects optimal cell packing and the minimization of surface free energy, but also cell–cell interactions, cell proliferation, and cytoskeletal rearrangements.ResultsHere, we studied the structure of the rat pleura in the first 15 days after birth. After pleural isolation and image segmentation, the analysis demonstrated a progression of epithelial order from postnatal day 1 (P1) to P15. The cells with the largest surface area and greatest shape variability were observed at P1. In contrast, the cells with the smallest surface area and most shape consistency were observed at P15. A comparison of polygonal cell geometries demonstrated progressive optimization with an increase in the number of hexagons (six‐sided) as well as five‐sided and seven‐sided polygons. Analysis of the epithelial organization with Voronoi tessellations and graphlet motif frequencies demonstrated a developmental path strikingly distinct from mathematical and natural reference paths. Graph Theory analysis of cell connectivity demonstrated a progressive decrease in network heterogeneity and clustering coefficient from P1 to P15.ConclusionsWe conclude that the rat pleura undergoes a striking change in pleural structure from P1 to P15. Further, a geometric and network‐based approach can provide a quantitative characterization of these developmental changes.

Funder

National Institutes of Health

Deutsche Forschungsgemeinschaft

Publisher

Wiley

Subject

Developmental Biology

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