Intertissue mechanical stress affects Frizzled-mediated planar cell polarity in the Drosophila notum epidermis

Curr Biol. 2011 Feb 8;21(3):236-42. doi: 10.1016/j.cub.2011.01.001. Epub 2011 Jan 27.

Abstract

Frizzled/planar cell polarity (Fz/PCP) signaling controls the orientation of sensory bristles and cellular hairs (trichomes) along the anteroposterior axis of the Drosophila thorax (notum). A subset of the trichome-producing notum cells differentiate as "tendon cells," serving as attachment sites for the indirect flight muscles (IFMs) to the exoskeleton. Through the analysis of chascon (chas), a gene identified by its ability to disrupt Fz/PCP signaling under overexpression conditions, and jitterbug (jbug)/filamin, we show that maintenance of anteroposterior planar polarization requires the notum epithelia to balance mechanical stress generated by the attachment of the IFMs. chas is expressed in notum tendon cells, and its loss of function disturbs cellular orientation at and near the regions where IFMs attach to the epidermis. This effect is independent of the Fz/PCP and fat/dachsous systems. The chas phenotype arises during normal shortening of the IFMs and is suppressed by genetic ablation of the IFMs. chas acts through jbug/filamin and cooperates with MyosinII to modulate the mechanoresponse of notum tendon cells. These observations support the notion that the ability of epithelia to respond to mechanical stress generated by one or more interactions with other tissues during development and organogenesis influences the maintenance of its shape and PCP features.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Polarity*
  • Contractile Proteins / metabolism
  • Drosophila / cytology*
  • Drosophila / metabolism
  • Drosophila Proteins / metabolism*
  • Filamins
  • Frizzled Receptors / metabolism*
  • Genes, Insect / physiology
  • Membrane Proteins / metabolism
  • Microfilament Proteins / metabolism
  • Myosin Heavy Chains / metabolism
  • Signal Transduction
  • Stress, Physiological*

Substances

  • Contractile Proteins
  • Drosophila Proteins
  • Filamins
  • Frizzled Receptors
  • Membrane Proteins
  • Microfilament Proteins
  • Zip protein, Drosophila
  • fz protein, Drosophila
  • Myosin Heavy Chains