Axon and dendrite pruning in Drosophila

Abstract

Pruning, a process by which neurons selectively remove exuberant or unnecessary processes without causing cell death, is crucial for the establishment of mature neural circuits during animal development. Yet relatively little is known about molecular and cellular mechanisms that govern neuronal pruning. Holometabolous insects, such as Drosophila, undergo complete metamorphosis and their larval nervous systems are replaced with adult-specific ones, thus providing attractive models for studying neuronal pruning. Drosophila mushroom body and dendritic arborization neurons have been utilized as two appealing systems to elucidate the underlying mechanisms of axon and dendrite pruning, respectively. In this review we highlight recent developments and discuss some similarities and differences in the mechanisms that regulate these two distinct modes of neuronal pruning in Drosophila.

Figure 1

A schematic representation of axon pruning in MB γ neurons. At larval stage, MB γ neurons project a single axon that branches to form dendrites (den), a tightly fasciculated axon peduncle (p) that bifurcates to the dorsal (d) and medial (m) lobe. Cortex glia (yellow) instruct MB axon pruning by secreting the TGF-β ligand Myoglianin. At 6 h after puparium formation (APF), MB γ dendrites are mostly eliminated, axons begin to undergo disassembly and astrocytes (magenta) infiltrate the dorsal and medial lobes. The role of the remaining unidentified glia or cortex glia during these time points is not known (gray). At 18 h APF fragmentation is complete and axonal fragments are being engulfed by astrocytes. Subsequently, γ neurons project new, adult specific axons, that project only to the medial lobe.

Figure 2

A schematic representation of dendrite pruning in ddaC neurons during metamorphosis. At the white prepupal stage (0 h APF), ddaC neurons extend highly-branched dendrites (green) as well as a single axon projecting ventrally to the ventral nerve cord. Peripheral glia (red) wrap the soma, axon and also the proximal dendritic area in ddaC neurons. Dendrites undergo blebbing, thinning, subsequently detachment starting from approximately 5 h APF, followed by fragmentation and debris clearance via phagocytes. By 16-18 h APF, all dendritic debris is eliminated. Open arrowheads point to proximal severing of the dorsal dendrite branches of ddaC neurons. Red arrowheads point to ddaC somas. An asterisk indicates a phagocyte.

Figure 3

Ecdysone signaling and its regulators govern axon and dendrite pruning in Drosophila. A table summarizes the conserved and differential mechanisms between MB axon pruning and ddaC dendrite pruning. Green circles indicate ‘required’, red circles indicate ‘not required’, and grey circle indicates ‘unknown’. Asterisks highlight the unpublished observations.