Cell packing influences planar cell polarity signaling

  1. Dali Maa,1,
  2. Keith Amonlirdvimanb,1,
  3. Robin L. Raffardb,1,
  4. Alessandro Abateb,c,
  5. Claire J. Tomlinb,c, and
  6. Jeffrey D. Axelroda,2
  1. aDepartment of Pathology, Stanford University School of Medicine, Stanford, CA 94305-5324;
  2. bDepartment of Electrical Engineering and Computer Sciences, University of California, Berkeley, CA 94720; and
  3. cDepartment of Aeronautics and Astronautics, Stanford University, Stanford, CA 94305-4035
  1. Communicated by A. Dale Kaiser, Stanford University School of Medicine, Stanford, CA, September 23, 2008

  2. 1D.M., K.A., and R.L.R. contributed equally to this work. (received for review August 2, 2008)

Abstract

Some epithelial cells display asymmetry along an axis orthogonal to the apical-basal axis, referred to as planar cell polarity (PCP). A Frizzled-mediated feedback loop coordinates PCP between neighboring cells, and the cadherin Fat transduces a global directional cue that orients PCP with respect to the tissue axes. The feedback loop can propagate polarity across clones of cells that lack the global directional signal, although this polarity propagation is error prone. Here, we show that, in the Drosophila wing, a combination of cell geometry and nonautonomous signaling at clone boundaries determines the correct or incorrect polarity propagation in clones that lack Fat mediated global directional information. Pattern elements, such as veins, and sporadic occurrences of irregular geometry are obstacles to polarity propagation. Hence, in the wild type, broad distribution of the global directional cue combines with a local feedback mechanism to overcome irregularities in cell packing geometry during PCP signaling.

Footnotes

  • 2To whom correspondence should be addressed. E-mail: jaxelrod{at}stanford.edu
  • Author contributions: D.M., K.A., R.L.R., C.J.T., and J.D.A. designed research; D.M., K.A., R.L.R., and A.A. performed research; D.M., K.A., R.L.R., and A.A. contributed new reagents/analytic tools; D.M., K.A., R.L.R., A.A., C.J.T., and J.D.A. analyzed data; and D.M., K.A., R.L.R., C.J.T., and J.D.A. wrote the paper.

  • The authors declare no conflict of interest.

  • This article contains supporting information online at www.pnas.org/cgi/content/full/0808868105/DCSupplemental.

  • Freely available online through the PNAS open access option.

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