Myosin II isoforms play distinct roles in adherens junction biogenesis

Mélina L. Heuzé (Corresponding author), Gautham Hari Narayana Sankara Narayana, Joseph D'Alessandro, Victor Cellerin, Tien Dang, David S. Williams, Jan C.M. van Hest, Philippe Marcq, René Marc Mège (Corresponding author), Benoit Ladoux (Corresponding author)

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Abstract

Adherens junction (AJ) assembly under force is essential for many biological processes like epithelial monolayer bending, collective cell migration, cell extrusion and wound healing. The acto-myosin cytoskeleton acts as a major force-generator during the de novo formation and remodeling of AJ. Here, we investigated the role of non-muscle myosin II isoforms (NMIIA and NMIIB) in epithelial junction assembly. NMIIA and NMIIB differentially regulate biogenesis of AJ through association with distinct actin networks. Analysis of junction dynamics, actin organization, and mechanical forces of control and knockdown cells for myosins revealed that NMIIA provides the mechanical tugging force necessary for cell-cell junction reinforcement and maintenance. NMIIB is involved in E-cadherin clustering, maintenance of a branched actin layer connecting E-cadherin complexes and perijunctional actin fibres leading to the building-up of anisotropic stress. These data reveal unanticipated complementary functions of NMIIA and NMIIB in the biogenesis and integrity of AJ.

Original languageEnglish
Article numbere46599
Number of pages30
JournaleLife
Volume8
DOIs
Publication statusPublished - 5 Sep 2019

Fingerprint

Myosin Type II
Adherens Junctions
Actins
Protein Isoforms
pioglitazone
Cadherins
Myosins
Maintenance
Biological Phenomena
Intercellular Junctions
Cytoskeleton
Wound Healing
Cell Movement
Extrusion
Cluster Analysis
Monolayers
Reinforcement
Fibers

Keywords

  • adherens junctions
  • cell biology
  • cytoskeleton
  • epithelial cells
  • mechanobiology
  • myosin
  • physics of living systems

Cite this

Heuzé, M. L., Sankara Narayana, G. H. N., D'Alessandro, J., Cellerin, V., Dang, T., Williams, D. S., ... Ladoux, B. (2019). Myosin II isoforms play distinct roles in adherens junction biogenesis. eLife, 8, [e46599]. https://doi.org/10.7554/eLife.46599
Heuzé, Mélina L. ; Sankara Narayana, Gautham Hari Narayana ; D'Alessandro, Joseph ; Cellerin, Victor ; Dang, Tien ; Williams, David S. ; van Hest, Jan C.M. ; Marcq, Philippe ; Mège, René Marc ; Ladoux, Benoit. / Myosin II isoforms play distinct roles in adherens junction biogenesis. In: eLife. 2019 ; Vol. 8.
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abstract = "Adherens junction (AJ) assembly under force is essential for many biological processes like epithelial monolayer bending, collective cell migration, cell extrusion and wound healing. The acto-myosin cytoskeleton acts as a major force-generator during the de novo formation and remodeling of AJ. Here, we investigated the role of non-muscle myosin II isoforms (NMIIA and NMIIB) in epithelial junction assembly. NMIIA and NMIIB differentially regulate biogenesis of AJ through association with distinct actin networks. Analysis of junction dynamics, actin organization, and mechanical forces of control and knockdown cells for myosins revealed that NMIIA provides the mechanical tugging force necessary for cell-cell junction reinforcement and maintenance. NMIIB is involved in E-cadherin clustering, maintenance of a branched actin layer connecting E-cadherin complexes and perijunctional actin fibres leading to the building-up of anisotropic stress. These data reveal unanticipated complementary functions of NMIIA and NMIIB in the biogenesis and integrity of AJ.",
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Heuzé, ML, Sankara Narayana, GHN, D'Alessandro, J, Cellerin, V, Dang, T, Williams, DS, van Hest, JCM, Marcq, P, Mège, RM & Ladoux, B 2019, 'Myosin II isoforms play distinct roles in adherens junction biogenesis', eLife, vol. 8, e46599. https://doi.org/10.7554/eLife.46599

Myosin II isoforms play distinct roles in adherens junction biogenesis. / Heuzé, Mélina L. (Corresponding author); Sankara Narayana, Gautham Hari Narayana; D'Alessandro, Joseph; Cellerin, Victor; Dang, Tien; Williams, David S.; van Hest, Jan C.M.; Marcq, Philippe; Mège, René Marc (Corresponding author); Ladoux, Benoit (Corresponding author).

In: eLife, Vol. 8, e46599, 05.09.2019.

Research output: Contribution to journalArticleAcademicpeer-review

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AU - Heuzé, Mélina L.

AU - Sankara Narayana, Gautham Hari Narayana

AU - D'Alessandro, Joseph

AU - Cellerin, Victor

AU - Dang, Tien

AU - Williams, David S.

AU - van Hest, Jan C.M.

AU - Marcq, Philippe

AU - Mège, René Marc

AU - Ladoux, Benoit

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Heuzé ML, Sankara Narayana GHN, D'Alessandro J, Cellerin V, Dang T, Williams DS et al. Myosin II isoforms play distinct roles in adherens junction biogenesis. eLife. 2019 Sep 5;8. e46599. https://doi.org/10.7554/eLife.46599