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Cell division in tissues enables macrophage infiltration

View ORCID ProfileMaria Akhmanova, View ORCID ProfileAttila Gyoergy, Mikhail Vlasov, Fedor Vlasov, View ORCID ProfileDaniel Krueger, Andrei Akopian, View ORCID ProfileShamsi Emtenani, View ORCID ProfileAparna Ratheesh, View ORCID ProfileStefano De Renzis, View ORCID ProfileDaria E. Siekhaus
doi: https://doi.org/10.1101/2021.04.19.438995
Maria Akhmanova
1Institute of Science and Technology Austria, Am Campus 1, 3400 Klosterneuburg, Austria
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  • For correspondence: maria.akhmanova@gmail.com daria.siekhaus@ist.ac.at
Attila Gyoergy
1Institute of Science and Technology Austria, Am Campus 1, 3400 Klosterneuburg, Austria
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Mikhail Vlasov
2Bundesgymnasium Klosterneuburg, Buchberggasse 31, 3400 Klosterneuburg, Austria
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Fedor Vlasov
2Bundesgymnasium Klosterneuburg, Buchberggasse 31, 3400 Klosterneuburg, Austria
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Daniel Krueger
3European Molecular Biology Laboratory, Developmental Biology Unit, Meyerhofstrasse 1, 69117 Heidelberg, Germany
4Hubrecht Institute, Royal Netherlands Academy of Arts and Sciences (KNAW), Utrecht, the Netherlands
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Andrei Akopian
2Bundesgymnasium Klosterneuburg, Buchberggasse 31, 3400 Klosterneuburg, Austria
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Shamsi Emtenani
1Institute of Science and Technology Austria, Am Campus 1, 3400 Klosterneuburg, Austria
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  • ORCID record for Shamsi Emtenani
Aparna Ratheesh
1Institute of Science and Technology Austria, Am Campus 1, 3400 Klosterneuburg, Austria
5Centre for Mechanochemical Cell Biology, Warwick Medical School, University of Warwick, Coventry CV4 7AL, UK
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Stefano De Renzis
3European Molecular Biology Laboratory, Developmental Biology Unit, Meyerhofstrasse 1, 69117 Heidelberg, Germany
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Daria E. Siekhaus
1Institute of Science and Technology Austria, Am Campus 1, 3400 Klosterneuburg, Austria
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  • ORCID record for Daria E. Siekhaus
  • For correspondence: maria.akhmanova@gmail.com daria.siekhaus@ist.ac.at
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Abstract

Migration of cells through diverse tissues is essential for development, immune response and cancer metastasis 1–3. To reach their destination, cells must overcome the resistance imposed by complex microenvironments, composed of neighboring cells and extracellular matrix (ECM)4–6. While migration through pores and tracks in ECM has been well studied 4,5,7, little is known about cellular traversal into confining cell-dense tissues. Here by combining quantitative live imaging with genetic and optogenetic perturbations we identify a crucial role for cell division during cell migration into tissues. We find that normal embryonic invasion by Drosophila macrophages between the ectoderm and mesoderm8,9 absolutely requires division of an epithelial ectodermal cell at the site of entry. Dividing ectodermal cells disassemble ECM attachment formed by Integrin-mediated focal adhesions next to mesodermal cells, allowing macrophages to move their nuclei ahead and invade. Decreasing or increasing the frequency of ectodermal division correspondingly either hinders or promotes macrophage invasion. Reducing the levels of focal adhesion components in the ectoderm allows macrophage entry even in the absence of division. Our study demonstrates the critical importance of division at the entry site to enable in vivo cell invasion by relieving the steric impediment caused by focal adhesions. We thus provide a new perspective on the regulation of cellular movement into tissues.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
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 April 20, 2021.
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Cell division in tissues enables macrophage infiltration
Maria Akhmanova, Attila Gyoergy, Mikhail Vlasov, Fedor Vlasov, Daniel Krueger, Andrei Akopian, Shamsi Emtenani, Aparna Ratheesh, Stefano De Renzis, Daria E. Siekhaus
bioRxiv 2021.04.19.438995; doi: https://doi.org/10.1101/2021.04.19.438995
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Cell division in tissues enables macrophage infiltration
Maria Akhmanova, Attila Gyoergy, Mikhail Vlasov, Fedor Vlasov, Daniel Krueger, Andrei Akopian, Shamsi Emtenani, Aparna Ratheesh, Stefano De Renzis, Daria E. Siekhaus
bioRxiv 2021.04.19.438995; doi: https://doi.org/10.1101/2021.04.19.438995

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