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Skin-resident immune cells actively coordinate their distribution with epidermal cells during homeostasis

View ORCID ProfileSangbum Park, Catherine Matte-Martone, David G. Gonzalez, Elizabeth A. Lathrop, Dennis P. May, Cristiana M. Pineda, Jessica L. Moore, Jonathan D. Boucher, Edward D. Marsh, Axel Schmitter, Katie Cockburn, Yohanns Bellaïche, View ORCID ProfileValentina Greco
doi: https://doi.org/10.1101/2021.01.08.425932
Sangbum Park
1Department of Genetics, Yale School of Medicine, New Haven, CT 06510, USA
3Institute for Quantitative Health Science & Engineering (IQ), Michigan State University, East Lansing, MI 48824, USA
4Department of Medicine, Michigan State University, East Lansing, MI 48824, USA
5Department of Pharmacology and Toxicology, Michigan State University, East Lansing, MI 48824, USA
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Catherine Matte-Martone
1Department of Genetics, Yale School of Medicine, New Haven, CT 06510, USA
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David G. Gonzalez
1Department of Genetics, Yale School of Medicine, New Haven, CT 06510, USA
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Elizabeth A. Lathrop
1Department of Genetics, Yale School of Medicine, New Haven, CT 06510, USA
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Dennis P. May
1Department of Genetics, Yale School of Medicine, New Haven, CT 06510, USA
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Cristiana M. Pineda
6School of Medicine, Georgetown University, Washington, DC 20007, USA
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Jessica L. Moore
1Department of Genetics, Yale School of Medicine, New Haven, CT 06510, USA
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Jonathan D. Boucher
1Department of Genetics, Yale School of Medicine, New Haven, CT 06510, USA
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Edward D. Marsh
1Department of Genetics, Yale School of Medicine, New Haven, CT 06510, USA
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Axel Schmitter
3Institute for Quantitative Health Science & Engineering (IQ), Michigan State University, East Lansing, MI 48824, USA
4Department of Medicine, Michigan State University, East Lansing, MI 48824, USA
5Department of Pharmacology and Toxicology, Michigan State University, East Lansing, MI 48824, USA
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Katie Cockburn
1Department of Genetics, Yale School of Medicine, New Haven, CT 06510, USA
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Yohanns Bellaïche
7Institut Curie, Université PSL, CNRS UMR3215, INSERM U934, Génétique et Biologie du Développement, 75005 Paris, France
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Valentina Greco
1Department of Genetics, Yale School of Medicine, New Haven, CT 06510, USA
2Departments of Cell Biology and Dermatology, Yale Stem Cell Center, Yale Cancer Center, Yale School of Medicine, New Haven, CT 06510, USA
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  • ORCID record for Valentina Greco
  • For correspondence: Valentina.Greco@yale.edu
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Abstract

Our organs consist of multiple cell types that ensure proper architecture and function. How different cell types coexist and interact to maintain their homeostasis in vivo remain elusive. The skin epidermis comprises mostly epithelial cells, but also harbors Langerhans cells (LCs) and Dendritic Epidermal T cells (DETCs). In response to injury or infection, LCs and DETCs become activated and play critical immunological roles. During homeostasis, they coexist with epithelial cells in the basal layer of the epidermis. Whether, and how, distributions of LCs and DETCs are regulated during homeostasis is unclear. Here, we addressed this question by tracking LCs, DETCs and epithelial basal cells over time within the skin of live adult mice. We show that LCs and DETCs maintain their overall position despite continuous turnover of neighboring basal epithelial stem cells. Moreover, LCs and DETCs rapidly and maximally explore basal epithelial cell junctions through their dendritic extensions. Altering the epithelial cell density triggers corresponding changes in the immune cell density, but not vice versa, suggesting that epithelial cells determine immune tissue composition in the epidermis. Moreover, LCs and DETCs are organized in a tiling pattern that is actively maintained. When LCs or DETCs are ectopically removed, neighboring epidermal LCs or DETCs, respectively, move into the emptied spaces and re-establish the tiling pattern. Finally, LCs require the GTPase Rac1 to maintain their positional stability, density and tiling pattern. Overall, we discovered that epidermal cells regulate the density of immune cells during homeostasis, and that immune cells actively maintain a non-random spatial distribution, reminiscent of neuronal self-avoidance. We propose that these cellular mechanisms provide the epidermis with an optimal response to environmental insults.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 09, 2021.
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Skin-resident immune cells actively coordinate their distribution with epidermal cells during homeostasis
Sangbum Park, Catherine Matte-Martone, David G. Gonzalez, Elizabeth A. Lathrop, Dennis P. May, Cristiana M. Pineda, Jessica L. Moore, Jonathan D. Boucher, Edward D. Marsh, Axel Schmitter, Katie Cockburn, Yohanns Bellaïche, Valentina Greco
bioRxiv 2021.01.08.425932; doi: https://doi.org/10.1101/2021.01.08.425932
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Skin-resident immune cells actively coordinate their distribution with epidermal cells during homeostasis
Sangbum Park, Catherine Matte-Martone, David G. Gonzalez, Elizabeth A. Lathrop, Dennis P. May, Cristiana M. Pineda, Jessica L. Moore, Jonathan D. Boucher, Edward D. Marsh, Axel Schmitter, Katie Cockburn, Yohanns Bellaïche, Valentina Greco
bioRxiv 2021.01.08.425932; doi: https://doi.org/10.1101/2021.01.08.425932

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