Analysis of the Function of Apoptosis during Imaginal Wing Disc Regeneration in Drosophila melanogaster

PLoS One. 2016 Nov 28;11(11):e0165554. doi: 10.1371/journal.pone.0165554. eCollection 2016.

Abstract

Regeneration is the ability that allows organisms to replace missing organs or lost tissue after injuries. This ability requires the coordinated activity of different cellular processes, including programmed cell death. Apoptosis plays a key role as a source of signals necessary for regeneration in different organisms. The imaginal discs of Drosophila melanogaster provide a particularly well-characterised model system for studying the cellular and molecular mechanisms underlying regeneration. Although it has been shown that signals produced by apoptotic cells are needed for homeostasis and regeneration of some tissues of this organism, such as the adult midgut, the contribution of apoptosis to disc regeneration remains unclear. Using a new method for studying disc regeneration in physiological conditions, we have defined the pattern of cell death in regenerating discs. Our data indicate that during disc regeneration, cell death increases first at the wound edge, but as regeneration progresses dead cells can be observed in regions far away from the site of damage. This result indicates that apoptotic signals initiated in the wound spread throughout the disc. We also present results which suggest that the partial inhibition of apoptosis does not have a major effect on disc regeneration. Finally, our results suggest that during disc regeneration distinct apoptotic signals might be acting simultaneously.

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Apoptosis / physiology*
  • Cell Death
  • Drosophila Proteins / genetics
  • Drosophila melanogaster / cytology
  • Drosophila melanogaster / physiology*
  • Gene Expression Regulation, Developmental
  • Green Fluorescent Proteins / genetics
  • Imaginal Discs / cytology
  • Imaginal Discs / physiology*
  • Inhibitor of Apoptosis Proteins / genetics
  • Intracellular Signaling Peptides and Proteins
  • Larva
  • MAP Kinase Kinase 4 / metabolism
  • Membrane Proteins
  • Regeneration / physiology*
  • Signal Transduction
  • Wings, Animal / cytology
  • Wings, Animal / physiology*
  • Wnt1 Protein / genetics

Substances

  • DIAP1 protein, Drosophila
  • Drosophila Proteins
  • Inhibitor of Apoptosis Proteins
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • Wnt1 Protein
  • delta protein
  • wg protein, Drosophila
  • Green Fluorescent Proteins
  • MAP Kinase Kinase 4

Grants and funding

This work was supported by a grant obtained from the MEC (BFU2014-54153-P). SDG was supported by an FPI fellowship from the MICINN.