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Forces drive basement membrane invasion in Caenorhabditis elegans.

Publication ,  Journal Article
Cáceres, R; Bojanala, N; Kelley, LC; Dreier, J; Manzi, J; Di Federico, F; Chi, Q; Risler, T; Testa, I; Sherwood, DR; Plastino, J
Published in: Proceedings of the National Academy of Sciences of the United States of America
November 2018

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.

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Published In

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

DOI

EISSN

1091-6490

ISSN

0027-8424

Publication Date

November 2018

Volume

115

Issue

45

Start / End Page

11537 / 11542

Related Subject Headings

  • Red Fluorescent Protein
  • Polymerization
  • Nuclear Proteins
  • Morphogenesis
  • Microfilament Proteins
  • Mechanotransduction, Cellular
  • Luminescent Proteins
  • Laminin
  • Green Fluorescent Proteins
  • Genes, Reporter
 

Citation

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Cáceres, R., Bojanala, N., Kelley, L. C., Dreier, J., Manzi, J., Di Federico, F., … Plastino, J. (2018). Forces drive basement membrane invasion in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 115(45), 11537–11542. https://doi.org/10.1073/pnas.1808760115
Cáceres, Rodrigo, Nagagireesh Bojanala, Laura C. Kelley, Jes Dreier, John Manzi, Fahima Di Federico, Qiuyi Chi, et al. “Forces drive basement membrane invasion in Caenorhabditis elegans.Proceedings of the National Academy of Sciences of the United States of America 115, no. 45 (November 2018): 11537–42. https://doi.org/10.1073/pnas.1808760115.
Cáceres R, Bojanala N, Kelley LC, Dreier J, Manzi J, Di Federico F, et al. Forces drive basement membrane invasion in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America. 2018 Nov;115(45):11537–42.
Cáceres, Rodrigo, et al. “Forces drive basement membrane invasion in Caenorhabditis elegans.Proceedings of the National Academy of Sciences of the United States of America, vol. 115, no. 45, Nov. 2018, pp. 11537–42. Epmc, doi:10.1073/pnas.1808760115.
Cáceres R, Bojanala N, Kelley LC, Dreier J, Manzi J, Di Federico F, Chi Q, Risler T, Testa I, Sherwood DR, Plastino J. Forces drive basement membrane invasion in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America. 2018 Nov;115(45):11537–11542.
Journal cover image

Published In

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

DOI

EISSN

1091-6490

ISSN

0027-8424

Publication Date

November 2018

Volume

115

Issue

45

Start / End Page

11537 / 11542

Related Subject Headings

  • Red Fluorescent Protein
  • Polymerization
  • Nuclear Proteins
  • Morphogenesis
  • Microfilament Proteins
  • Mechanotransduction, Cellular
  • Luminescent Proteins
  • Laminin
  • Green Fluorescent Proteins
  • Genes, Reporter