Abstract
The maintenance of planar polarity in airway multiciliated cells (MCCs) has been poorly characterized. We recently reported that the direction of ciliary beating in a surgically inverted tracheal segment remained inverted beyond the time required for the turnover of cells, without adjustment to global distal-to-proximal polarity. We hypothesized that the local maintenance of tissue-level polarity occurs via locally reproduced cells. To provide further insight regarding this hypothetical property, we performed allotransplantation of an inverted tracheal segment between wild-type (donor) and tdTomato-expressing (host) rats, with and without scratching the mucosa of the transplants. The origin of cells in the transplants was assessed using tdTomato-specific immunostaining. Ciliary movement and structures were observed by high-speed video and electron microscopy to analyze MCC orientations. Variabilities in the orientations of closely and distantly located MCCs were analyzed to evaluate the local- and broad-scale coordination of polarity, respectively. The epithelium was maintained by donor-derived cells in the non-scratched inverted transplant over 6 months, beyond one cycle of turnover. The inverted orientation of MCCs was also maintained throughout the non-scratched transplant. MCCs regenerated in the scratched transplant were derived from the host and exhibited diverse orientations across the transplant. However, the orientations of adjacent regenerated MCCs were often coordinated, indicating that airway MCCs can locally coordinate their orientations. A steady-state airway may maintain MCC orientation by locally reproducing MCCs via the local coordination of polarity. This local coordination enables the formation and maintenance of tissue-level polarity in small regions after mucosal injury.
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Acknowledgements
We thank Keiko Okamoto-Furuta and Haruyasu Kohda from the Division of Electron Microscopic Study, Center for Anatomical Studies, Graduate School of Medicine, Kyoto University, for their technical support in electron microscopy.
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This study was supported by the Japan Society for the Promotion of Science (JSPS) KAKENHI (20K18251) and GSK Japan Research Grant 2020 (A-33).
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SO, RN, YK, YK, and KO designed the study; SO, RN, and TK performed the experiments; SO and RN analyzed the data; SO and RN wrote the manuscript; and TS, YK, YK, and KO supervised the project. All authors have read and approved the final manuscript.
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Oyagi, S., Nakamura, R., Katsuno, T. et al. Local coordination of epithelial planar polarity in the maintenance and regeneration of the adult rat airway. Cell Tissue Res 394, 163–175 (2023). https://doi.org/10.1007/s00441-023-03809-y
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DOI: https://doi.org/10.1007/s00441-023-03809-y