The Drosophila gene RanBPM functions in the mushroom body to regulate larval behavior

PLoS One. 2010 May 14;5(5):e10652. doi: 10.1371/journal.pone.0010652.

Abstract

Background: In vertebrates, Ran-Binding Protein in the Microtubule Organizing Center (RanBPM) appears to function as a scaffolding protein in a variety of signal transduction pathways. In Drosophila, RanBPM is implicated in the regulation of germ line stem cell (GSC) niche organization in the ovary. Here, we addressed the role of RanBPM in nervous system function in the context of Drosophila larval behavior.

Methodology/principal findings: We report that in Drosophila, RanBPM is required for larval feeding, light-induced changes in locomotion, and viability. RanBPM is highly expressed in the Kenyon cells of the larval mushroom body (MB), a structure well studied for its role in associative learning in Drosophila and other insects. RanBPM mutants do not display major disruption in nervous system morphology besides reduced proliferation. Expression of the RanBPM gene in the Kenyon cells is sufficient to rescue all behavioral phenotypes. Through genetic epistasis experiments, we demonstrate that RanBPM participates with the Drosophila orthologue of the Fragile X Mental Retardation Protein (FMRP) in the development of neuromuscular junction (NMJ).

Conclusions/significance: We demonstrate that the RanBPM gene functions in the MB neurons for larval behavior. Our results suggest a role for this gene in an FMRP-dependent process. Taken together our findings point to a novel role for the MB in larval behavior.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics*
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Behavior, Animal / physiology*
  • Behavior, Animal / radiation effects
  • Cell Differentiation / radiation effects
  • Cell Proliferation / radiation effects
  • Cytoskeletal Proteins / genetics*
  • Cytoskeletal Proteins / metabolism
  • Drosophila melanogaster / cytology
  • Drosophila melanogaster / genetics*
  • Drosophila melanogaster / radiation effects
  • Feeding Behavior / radiation effects
  • Fragile X Mental Retardation Protein / metabolism
  • Larva / radiation effects
  • Light
  • Locomotion / radiation effects
  • Mushroom Bodies / cytology
  • Mushroom Bodies / metabolism*
  • Mushroom Bodies / radiation effects
  • Mutation / genetics
  • Neuromuscular Junction / cytology
  • Neuromuscular Junction / metabolism
  • Neuromuscular Junction / radiation effects
  • Neurons / cytology
  • Neurons / metabolism
  • Neurons / radiation effects
  • Nuclear Proteins / genetics*
  • Nuclear Proteins / metabolism
  • Phenotype
  • Protein Isoforms / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • Cytoskeletal Proteins
  • Nuclear Proteins
  • Protein Isoforms
  • Ran binding protein 9
  • Fragile X Mental Retardation Protein