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The Journal of Neuroscience, January 5, 2005, 25(1):78-87; doi:10.1523/JNEUROSCI.2377-04.2005

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DEVELOPMENT/PLASTICITY/REPAIR
The Influence of Pioneer Neurons on a Growing Motor Nerve in Drosophila Requires the Neural Cell Adhesion Molecule Homolog FasciclinII

Natalia Sánchez-Soriano and Andreas Prokop

Wellcome Trust Centre for Cell Matrix Research, Faculty of Life Sciences, The University of Manchester, Manchester M13 9PT, United Kingdom

The phenomenon of pioneer neurons has been known for almost a century, but so far we have little insights into mechanisms and molecules involved. Here, we study the formation of the Drosophila intersegmental motor nerve (ISN). We show that aCC/RP2 and U motor neurons grow together at the leading front of the ISN. Nevertheless, aCC/RP2 neurons are the pioneers, and U neurons are the followers, because only aCC/RP2 neurons effectively influence growth of the ISN. We also show that this influence depends on the neural cell adhesion molecule homolog FasciclinII. First, ablation of aCC/RP2 has a stronger impact on ISN growth than U ablation. Second, strong growth-influencing capabilities of aCC/RP2 are revealed with a stalling approach we used: when aCC/RP2 motor axons are stalled specifically, the entire ISN (including the U neurons) coarrests, demonstrating that aCC/RP2 neurons influence the behavior of U growth cones. In contrast, stalled U neurons do not have the same influence on other ISN motor neurons. The influence on ISN growth requires FasciclinII: targeted expression of FasciclinII in U neurons increases their influence on the ISN, whereas a FasciclinII loss-of-function background reduces ISN coarrest with stalled aCC/RP2 axons. The qualitative differences of both neuron groups are confirmed through our findings that aCC/RP2 growth cones are wider and more complex than those of U neurons. However, U growth cones adopt aCC/RP2-like wider shapes in a FasciclinII loss-of-function background. Therefore, FasciclinII is to a degree required and sufficient for pioneer-follower interactions, but its mode of action cannot be explained merely through an equally bidirectional adhesive interaction.

Key words: pathfinding; growth cone; motor neuron; axon; ablation; filopodia

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Received June 16, 2004; revised November 8, 2004; accepted November 10, 2004.

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