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Experimental and theoretical model for the origin of coiling of cellular protrusions around fibers
ID Kumar Sadhu, Raj (Author), ID Hernandez-Padilla, Christian (Author), ID Eshed Eisenbach, Yael (Author), ID Penič, Samo (Author), ID Zhang, Lixia (Author), ID Vishwasrao, Harshad D. (Author), ID Behkam, Bahareh (Author), ID Konstantopoulos, Konstantinos (Author), ID Shroff, Hari (Author), ID Iglič, Aleš (Author), ID Peles, Elior (Author), ID Nain, Amrinder S. (Author), ID Gov, Nir S. (Author)

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Abstract
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 DualView light-sheet microscopy (diSPIM). Overall, we provide a theoretical framework, supported by experiments, which explains the physical origin of the coiling phenomenon.

Language:English
Keywords:cell motility, computer simulations, Monte Carlo method, physical protein model
Work type:Article
Typology:1.01 - Original Scientific Article
Organization:FE - Faculty of Electrical Engineering
Publication status:Published
Publication version:Version of Record
Year:2023
Number of pages:Str. 1-13
Numbering:Vol. 14, [article no.] 5612
PID:20.500.12556/RUL-155480 This link opens in a new window
UDC:577
ISSN on article:2041-1723
DOI:10.1038/s41467-023-41273-y This link opens in a new window
COBISS.SI-ID:166115587 This link opens in a new window
Publication date in RUL:04.04.2024
Views:529
Downloads:447
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Record is a part of a journal

Title:Nature communications
Shortened title:Nat. commun.
Publisher:Springer Nature
ISSN:2041-1723
COBISS.SI-ID:2315876 This link opens in a new window

Licences

License:CC BY 4.0, Creative Commons Attribution 4.0 International
Link:http://creativecommons.org/licenses/by/4.0/
Description:This is the standard Creative Commons license that gives others maximum freedom to do what they want with the work as long as they credit the author.

Secondary language

Language:Slovenian
Keywords:mobilnost celice, računalniške simulacije, metoda Monte Carlo, fizikalni model proteinov

Projects

Funder:NSF - National Science Foundation
Funding programme:National Science Foundation
Project number:1762634
Name:Collaborative Research: Mechanobiology of Fiber Geometry-RhoGTPase Crosstalk at the Leading Edge of Cells Crawling on Fibers

Funder:NSF - National Science Foundation
Funding programme:National Science Foundation
Project number:2119949
Name:Collaborative Research: Theory and experiment of contact inhibition of locomotion in nanofiber geometries

Funder:NSF - National Science Foundation
Funding programme:National Science Foundation
Project number:2107332
Name:III:Medium:Physics-guided Machine Learning for Predicting Cell Trajectories, Shapes, and Interactions in Complex Dynamic Environments

Funder:ARIS - Slovenian Research and Innovation Agency
Project number:P2-0232
Name:Analiza biomedicinskih slik in signalov

Funder:ARIS - Slovenian Research and Innovation Agency
Project number:J3-3066
Name:Optimizacija s trombociti in zunajceličnimi vezikli bogate avtologne krvne plazme za zdravljenje pooperativnih ran v otorinolaringologiji

Funder:ARIS - Slovenian Research and Innovation Agency
Project number:J2-4447
Name:Vpliv mehanike in topologije membrane na celično ujetje bakterij, virionov in anorganskih delcev

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