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Differential proliferation rates generate patterns of mechanical tension that orient tissue growth

Yanlan Mao, Alexander L Tournier, Andreas Hoppe, Lennart Kester, Barry J Thompson, Nicolas Tapon

Author Affiliations

  1. Yanlan Mao1,,
  2. Alexander L Tournier*,2,,
  3. Andreas Hoppe3,
  4. Lennart Kester1,
  5. Barry J Thompson4 and
  6. Nicolas Tapon*,1
  1. 1 Apoptosis and Proliferation Control Laboratory, Cancer Research UK, London Research Institute, London, UK
  2. 2 Mathematical Modelling Unit, Cancer Research UK, London Research Institute, London, UK
  3. 3 Digital Imaging Research Centre, Faculty of Science, Engineering and Computing, Kingston University, Kingston‐upon‐Thames, UK
  4. 4 Epithelial Biology Laboratory, Cancer Research UK, London Research Institute, London, UK
  1. *Corresponding authors. Mathematical Modelling Unit, Cancer Research UK, London Research Institute, 44 Lincoln's Inn Fields, London WC2A 3LY, UK. Tel.:+44 (0)207 269 3583; Fax:+44 (0)207 269 3094; E-mail: alexander.tournier{at}cancer.org.ukApoptosis and Proliferation Control Laboratory, Cancer Research UK, London Research Institute, 44 Lincoln's Inn Fields, London WC2A 3LY, UK. Tel.:+44 (0)207 269 3635; Fax:+44 (0)207 269 3094; E-mail: nic.tapon{at}cancer.org.uk
  1. These authors contributed equally to this work.

Abstract

Orientation of cell divisions is a key mechanism of tissue morphogenesis. In the growing Drosophila wing imaginal disc epithelium, most of the cell divisions in the central wing pouch are oriented along the proximal–distal (P–D) axis by the Dachsous‐Fat‐Dachs planar polarity pathway. However, cells at the periphery of the wing pouch instead tend to orient their divisions perpendicular to the P–D axis despite strong Dachs polarization. Here, we show that these circumferential divisions are oriented by circumferential mechanical forces that influence cell shapes and thus orient the mitotic spindle. We propose that this circumferential pattern of force is not generated locally by polarized constriction of individual epithelial cells. Instead, these forces emerge as a global tension pattern that appears to originate from differential rates of cell proliferation within the wing pouch. Accordingly, we show that localized overgrowth is sufficient to induce neighbouring cell stretching and reorientation of cell division. Our results suggest that patterned rates of cell proliferation can influence tissue mechanics and thus determine the orientation of cell divisions and tissue shape.

There is a Have you seen? (October 2013) associated with this Article.

  • Received November 22, 2012.
  • Accepted August 9, 2013.

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