Sharp boundaries of Dpp signalling trigger local cell death required for Drosophila leg morphogenesis

Nat Cell Biol. 2007 Jan;9(1):57-63. doi: 10.1038/ncb1518. Epub 2006 Dec 3.

Abstract

Morphogens are secreted signalling molecules that govern many developmental processes. In the Drosophila wing disc, the transforming growth factor beta (TGFbeta) homologue Decapentaplegic (Dpp) forms a smooth gradient and specifies cell fate by conferring a defined value of morphogen activity. Thus, neighbouring cells have similar amounts of Dpp protein, and if a sharp discontinuity in Dpp activity is generated between these cells, Jun kinase (JNK)-dependent apoptosis is triggered to restore graded positional information. To date, it has been assumed that this apoptotic process is only activated when normal signalling is distorted. However, we now show that a similar process occurs during normal development: rupture in Dpp activity occurs during normal segmentation of the distal legs of Drosophila. This sharp boundary of Dpp signalling, independently of the absolute level of Dpp activity, induces a JNK-reaper-dependent apoptosis required for the morphogenesis of a particular structure of the leg, the joint. Our results show that Dpp could induce a developmental programme not only in a concentration dependent manner, but also by the creation of a sharp boundary of Dpp activity. Furthermore, the same process could be used either to restore a normal pattern in response to artificial disturbance or to direct a morphogenetic process.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila Proteins / physiology
  • Drosophila melanogaster / embryology*
  • Drosophila melanogaster / metabolism
  • Extremities / anatomy & histology
  • Extremities / embryology*
  • Extremities / physiology
  • Gene Expression Regulation, Developmental*
  • MAP Kinase Kinase 4 / metabolism
  • Models, Biological
  • Morphogenesis*
  • Signal Transduction*
  • Wings, Animal / physiology

Substances

  • Drosophila Proteins
  • dpp protein, Drosophila
  • MAP Kinase Kinase 4