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Forces drive basement membrane invasion in Caenorhabditis elegans.


ABSTRACT: 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.

SUBMITTER: Caceres R 

PROVIDER: S-EPMC6233148 | biostudies-literature | 2018 Nov

REPOSITORIES: biostudies-literature

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Forces drive basement membrane invasion in <i>Caenorhabditis elegans</i>.

Cáceres Rodrigo R   Bojanala Nagagireesh N   Kelley Laura C LC   Dreier Jes J   Manzi John J   Di Federico Fahima F   Chi Qiuyi Q   Risler Thomas T   Testa Ilaria I   Sherwood David R DR   Plastino Julie J  

Proceedings of the National Academy of Sciences of the United States of America 20181022 45


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 <i>Caenorhabditis elegans</i>, we observe that the AC deforms the BM and underlying tissue just before invasion, exerting forces in the te  ...[more]

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