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Forces drive basement membrane invasion in Caenorhabditis elegans
During invasion, cells breach basement membrane (BM) barriers with actin-rich protrusions. It remains unclear, however, whether actin polymerization applies pushing forces to help break through BM, or whether actin filaments play a passive role as scaffolding for targeting invasive machinery. Here,...
Autores principales: | , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
National Academy of Sciences
2018
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6233148/ https://www.ncbi.nlm.nih.gov/pubmed/30348801 http://dx.doi.org/10.1073/pnas.1808760115 |
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author | Cáceres, Rodrigo Bojanala, Nagagireesh Kelley, Laura C. Dreier, Jes Manzi, John Di Federico, Fahima Chi, Qiuyi Risler, Thomas Testa, Ilaria Sherwood, David R. Plastino, Julie |
author_facet | Cáceres, Rodrigo Bojanala, Nagagireesh Kelley, Laura C. Dreier, Jes Manzi, John Di Federico, Fahima Chi, Qiuyi Risler, Thomas Testa, Ilaria Sherwood, David R. Plastino, Julie |
author_sort | Cáceres, Rodrigo |
collection | PubMed |
description | During invasion, cells breach basement membrane (BM) barriers with actin-rich protrusions. It remains unclear, however, whether actin polymerization applies pushing forces to help break through BM, or whether actin filaments play a passive role as scaffolding for targeting invasive machinery. Here, using the developmental event of anchor cell (AC) invasion in Caenorhabditis elegans, we observe that the AC deforms the BM and underlying tissue just before invasion, exerting forces in the tens of nanonewtons range. Deformation is driven by actin polymerization nucleated by the Arp2/3 complex and its activators, whereas formins and cross-linkers are dispensable. Delays in invasion upon actin regulator loss are not caused by defects in AC polarity, trafficking, or secretion, as appropriate markers are correctly localized in the AC even when actin is reduced and invasion is disrupted. Overall force production emerges from this study as one of the main tools that invading cells use to promote BM disruption in C. elegans. |
format | Online Article Text |
id | pubmed-6233148 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
spelling | pubmed-62331482018-11-14 Forces drive basement membrane invasion in Caenorhabditis elegans Cáceres, Rodrigo Bojanala, Nagagireesh Kelley, Laura C. Dreier, Jes Manzi, John Di Federico, Fahima Chi, Qiuyi Risler, Thomas Testa, Ilaria Sherwood, David R. Plastino, Julie Proc Natl Acad Sci U S A Biological Sciences During invasion, cells breach basement membrane (BM) barriers with actin-rich protrusions. It remains unclear, however, whether actin polymerization applies pushing forces to help break through BM, or whether actin filaments play a passive role as scaffolding for targeting invasive machinery. Here, using the developmental event of anchor cell (AC) invasion in Caenorhabditis elegans, we observe that the AC deforms the BM and underlying tissue just before invasion, exerting forces in the tens of nanonewtons range. Deformation is driven by actin polymerization nucleated by the Arp2/3 complex and its activators, whereas formins and cross-linkers are dispensable. Delays in invasion upon actin regulator loss are not caused by defects in AC polarity, trafficking, or secretion, as appropriate markers are correctly localized in the AC even when actin is reduced and invasion is disrupted. Overall force production emerges from this study as one of the main tools that invading cells use to promote BM disruption in C. elegans. National Academy of Sciences 2018-11-06 2018-10-22 /pmc/articles/PMC6233148/ /pubmed/30348801 http://dx.doi.org/10.1073/pnas.1808760115 Text en Copyright © 2018 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) . |
spellingShingle | Biological Sciences Cáceres, Rodrigo Bojanala, Nagagireesh Kelley, Laura C. Dreier, Jes Manzi, John Di Federico, Fahima Chi, Qiuyi Risler, Thomas Testa, Ilaria Sherwood, David R. Plastino, Julie Forces drive basement membrane invasion in Caenorhabditis elegans |
title | Forces drive basement membrane invasion in Caenorhabditis elegans |
title_full | Forces drive basement membrane invasion in Caenorhabditis elegans |
title_fullStr | Forces drive basement membrane invasion in Caenorhabditis elegans |
title_full_unstemmed | Forces drive basement membrane invasion in Caenorhabditis elegans |
title_short | Forces drive basement membrane invasion in Caenorhabditis elegans |
title_sort | forces drive basement membrane invasion in caenorhabditis elegans |
topic | Biological Sciences |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6233148/ https://www.ncbi.nlm.nih.gov/pubmed/30348801 http://dx.doi.org/10.1073/pnas.1808760115 |
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