The Drosophila Gene RanBPM Functions in the Mushroom Body to Regulate Larval Behavior

Abstract

BackgroundIn 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 FindingsWe 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/SignificanceWe 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.

Insulin signalling in mushroom body neurons regulates feeding behaviour inDrosophilalarvae

“…Insulin signalling regulates starvationdependent food intake behaviour in the Drosophila larva (Britton et al, 2002;Wu et al, 2005a;Wu et al, 2005b). Our previous work indicated that the mushroom body plays a role in larval feeding behaviour (Scantlebury et al, 2010). Therefore, we asked whether proper insulin signalling is required in mushroom body neurons for feeding behaviour during larval development.…”

“…RanBPM is highly expressed in the cytoplasm of the mushroom body neurons and is also expressed to a lesser degree in a large number of central nervous system neurons (Scantlebury et al, 2010). Targeted expression of RanBPM in the mushroom body rescues the feeding behaviour and growth phenotypes of RanBPM mutant larvae.…”

Development of larval motor circuits in Drosophila

“…Other sensory projections are ipsilateral. While a majority of sensory neurons extend their axons through a ventral nerve root, the dorsal bd (dbd) neurons send their axons through a dorsal nerve root (Schrader & Merritt ; Grueber et al . ).…”

“…Each class of sensory neurons, representing different modalities, projects axons to distinct areas within the CNS to make connections to second‐order neurons (Fig. B) (Merritt & Whitington ; Schrader & Merritt ; Zlatic et al . ; Grueber et al .…”

“…). In contrast to the ventral projection of the cho and class II–IV da neurons, the bd and class I da neurons, which convey major sensory feedback information, project to a dorso‐medial region near the dendrites of motor neurons (Merritt & Whitington ; Schrader & Merritt ; Grueber et al . ).…”