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Experimental and theoretical model for the origin of coiling of cellular protrusions around fibers

Protrusions at the leading-edge of a cell play an important role in sensing the extracellular cues during cellular spreading and motility. Recent studies provided indications that these protrusions wrap (coil) around the extracellular fibers. However, the physics of this coiling process, and the mec...

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Autores principales: Sadhu, Raj Kumar, Hernandez-Padilla, Christian, Eisenbach, Yael Eshed, Penič, Samo, Zhang, Lixia, Vishwasrao, Harshad D., Behkam, Bahareh, Konstantopoulos, Konstantinos, Shroff, Hari, Iglič, Aleš, Peles, Elior, Nain, Amrinder S., Gov, Nir S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10497540/
https://www.ncbi.nlm.nih.gov/pubmed/37699891
http://dx.doi.org/10.1038/s41467-023-41273-y
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author Sadhu, Raj Kumar
Hernandez-Padilla, Christian
Eisenbach, Yael Eshed
Penič, Samo
Zhang, Lixia
Vishwasrao, Harshad D.
Behkam, Bahareh
Konstantopoulos, Konstantinos
Shroff, Hari
Iglič, Aleš
Peles, Elior
Nain, Amrinder S.
Gov, Nir S.
author_facet Sadhu, Raj Kumar
Hernandez-Padilla, Christian
Eisenbach, Yael Eshed
Penič, Samo
Zhang, Lixia
Vishwasrao, Harshad D.
Behkam, Bahareh
Konstantopoulos, Konstantinos
Shroff, Hari
Iglič, Aleš
Peles, Elior
Nain, Amrinder S.
Gov, Nir S.
author_sort Sadhu, Raj Kumar
collection PubMed
description Protrusions at the leading-edge of a cell play an important role in sensing the extracellular cues during cellular spreading and motility. Recent studies provided indications that these protrusions wrap (coil) around the extracellular fibers. However, the physics of this coiling process, and the mechanisms that drive it, are not well understood. We present a combined theoretical and experimental study of the coiling of cellular protrusions on fibers of different geometry. Our theoretical model describes membrane protrusions that are produced by curved membrane proteins that recruit the protrusive forces of actin polymerization, and identifies the role of bending and adhesion energies in orienting the leading-edges of the protrusions along the azimuthal (coiling) direction. Our model predicts that the cell’s leading-edge coils on fibers with circular cross-section (above some critical radius), but the coiling ceases for flattened fibers of highly elliptical cross-section. These predictions are verified by 3D visualization and quantitation of coiling on suspended fibers using Dual-View light-sheet microscopy (diSPIM). Overall, we provide a theoretical framework, supported by experiments, which explains the physical origin of the coiling phenomenon.
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spelling pubmed-104975402023-09-14 Experimental and theoretical model for the origin of coiling of cellular protrusions around fibers Sadhu, Raj Kumar Hernandez-Padilla, Christian Eisenbach, Yael Eshed Penič, Samo Zhang, Lixia Vishwasrao, Harshad D. Behkam, Bahareh Konstantopoulos, Konstantinos Shroff, Hari Iglič, Aleš Peles, Elior Nain, Amrinder S. Gov, Nir S. Nat Commun Article Protrusions at the leading-edge of a cell play an important role in sensing the extracellular cues during cellular spreading and motility. Recent studies provided indications that these protrusions wrap (coil) around the extracellular fibers. However, the physics of this coiling process, and the mechanisms that drive it, are not well understood. We present a combined theoretical and experimental study of the coiling of cellular protrusions on fibers of different geometry. Our theoretical model describes membrane protrusions that are produced by curved membrane proteins that recruit the protrusive forces of actin polymerization, and identifies the role of bending and adhesion energies in orienting the leading-edges of the protrusions along the azimuthal (coiling) direction. Our model predicts that the cell’s leading-edge coils on fibers with circular cross-section (above some critical radius), but the coiling ceases for flattened fibers of highly elliptical cross-section. These predictions are verified by 3D visualization and quantitation of coiling on suspended fibers using Dual-View light-sheet microscopy (diSPIM). Overall, we provide a theoretical framework, supported by experiments, which explains the physical origin of the coiling phenomenon. Nature Publishing Group UK 2023-09-12 /pmc/articles/PMC10497540/ /pubmed/37699891 http://dx.doi.org/10.1038/s41467-023-41273-y Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Sadhu, Raj Kumar
Hernandez-Padilla, Christian
Eisenbach, Yael Eshed
Penič, Samo
Zhang, Lixia
Vishwasrao, Harshad D.
Behkam, Bahareh
Konstantopoulos, Konstantinos
Shroff, Hari
Iglič, Aleš
Peles, Elior
Nain, Amrinder S.
Gov, Nir S.
Experimental and theoretical model for the origin of coiling of cellular protrusions around fibers
title Experimental and theoretical model for the origin of coiling of cellular protrusions around fibers
title_full Experimental and theoretical model for the origin of coiling of cellular protrusions around fibers
title_fullStr Experimental and theoretical model for the origin of coiling of cellular protrusions around fibers
title_full_unstemmed Experimental and theoretical model for the origin of coiling of cellular protrusions around fibers
title_short Experimental and theoretical model for the origin of coiling of cellular protrusions around fibers
title_sort experimental and theoretical model for the origin of coiling of cellular protrusions around fibers
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10497540/
https://www.ncbi.nlm.nih.gov/pubmed/37699891
http://dx.doi.org/10.1038/s41467-023-41273-y
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