Jitterbug/Filamin and Myosin-II form a complex in tendon cells required to maintain epithelial shape and polarity during musculoskeletal system development.

During musculoskeletal system development, mechanical tension is generated between muscles and tendon-cells. This tension is required for muscle differentiation and is counterbalanced by tendon-cells avoiding tissue deformation. Both, Jbug/Filamin, an actin-meshwork organizing protein, and non-muscle Myosin-II (Myo-II) are required to maintain the shape and cell orientation of the Drosophila notum epithelium during flight muscle attachment to tendon cells. Here we show that halving the genetic dose of Rho kinase (Drok), the main activator of Myosin-II, enhances the epithelial deformation and bristle orientation defects associated with jbug/Filamin knockdown. Drok and activated Myo-II localize at the apical cell junctions, tendon processes and are associated to the myotendinous junction. Further, we found that Jbug/Filamin co-distribute at tendon cells with activated Myo-II. Finally, we found that Jbug/Filamin and Myo-II are in the same molecular complex and that the actin-binding domain of Jbug/Filamin is necessary for this interaction. These data together suggest that Jbug/Filamin and Myo-II proteins may act together in tendon cells to balance the tension generated during development of muscles-tendon interaction, maintaining the shape and polarity of the Drosophila notum epithelium.

• Publication year

  2018

• Venue

  Mechanisms of Development

• Publication date

  2018-09-10

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1016/j.mod.2018.09.002PMID 30213743
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Mechanical Control of Myotendinous Junction Formation and Tendon Differentiation during Development

  2017cited by this paper
• Establishment of the Muscle–Tendon Junction During Thorax Morphogenesis in Drosophila Requires the Rho-Kinase

  2016cited by this paper
• Hindsight regulates photoreceptor axon targeting through transcriptional control of jitterbug/Filamin and multiple genes involved in axon guidance in Drosophila

  2015cited by this paper
• Tension and force-resistant attachment are essential for myofibrillogenesis in Drosophila flight muscle.

  2014cited by this paper
• Molecular Mechanisms of Cellular Mechanosensing

  2013cited by this paper
• PTEN controls junction lengthening and stability during cell rearrangement in epithelial tissue.

  2013cited by this paper
• Distinct tissue distributions and subcellular localizations of differently phosphorylated forms of the myosin regulatory light chain in Drosophila.

  2011cited by this paper
• Intertissue mechanical stress affects Frizzled-mediated planar cell polarity in the Drosophila notum epidermis.

  2011cited by this paper
• Differential mechanical stability of filamin A rod segments.

  2011cited by this paper
• Mechanical strain in actin networks regulates FilGAP and integrin binding to Filamin A

  2011cited by this paper
• Mechanical control of tissue and organ development

  2010cited by this paper
• Mechanosensing through cooperative interactions between myosin II and the actin crosslinker cortexillin I.

  2009cited by this paper
• A tense situation: forcing tumour progression

  2009cited by this paper
• Prominent actin fiber arrays in Drosophila tendon cells represent architectural elements different from stress fibers.

  2008cited by this paper
• Cellular adaptation to mechanical stress: role of integrins, Rho, cytoskeletal tension and mechanosensitive ion channels

  2006cited by this paper
• A guided tour into subcellular colocalization analysis in light microscopy

  2006cited by this paper
• Filamins: promiscuous organizers of the cytoskeleton.

  2006cited by this paper
• The carboxy-terminal pleckstrin homology domain of ROCK interacts with filamin-A.

  2003cited by this paper
• Filamins as integrators of cell mechanics and signalling

  2001cited by this paper
• Retinal axon target selection in Drosophila is regulated by a receptor protein tyrosine phosphatase.

  1999cited by this paper
• Targeted gene expression as a means of altering cell fates and generating dominant phenotypes.

  1993cited by this paper
• The regulatory light chain of nonmuscle myosin is encoded by spaghetti-squash, a gene required for cytokinesis in Drosophila.

  1991cited by this paper
• Development of the indirect flight muscles of Drosophila.

  1991cited by this paper

• The typical and the atypical filamins of Drosophila.

  2025cites this paper
• Formin 3 stabilizes the cytoskeleton of Drosophila tendon cells, thus enabling them to resist muscle tensile forces

  2025cites this paper
• Single-cell RNA sequencing of mid-to-late stage spider embryos: new insights into spider development

  2024cites this paper
• Developmental origin of tendon diversity in Drosophila melanogaster

  2023cites this paper
• Isoform-specific roles of the Drosophila filamin-type protein Jitterbug (Jbug) during development

  2020cites this paper
• How the mechanobiome drives cell behavior, viewed through the lens of control theory

  2019cites this paper