The influence of pioneer neurons on a growing motor nerve in Drosophila requires the neural cell adhesion molecule homolog FasciclinII.
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.
Sánchez-Soriano
Natalia
N
Wellcome Trust Centre for Cell Matrix Research, Faculty of Life Sciences, The University of Manchester, Manchester M13 9PT, United Kingdom. NSanchez@manchester.ac.uk
Prokop
Andreas
A
D000818:Animals; D001369:Axons / Q000502:physiology*; D015816:Cell Adhesion Molecules, Neuronal / Q000502:physiology*; D002450:Cell Communication / Q000502:physiology; D004330:Drosophila / Q000033:anatomy & histology / Q000196:embryology; D029721:Drosophila Proteins / Q000502:physiology; D020439:Growth Cones / Q000502:physiology; D023421:Models, Animal; D008959:Models, Neurological; D009046:Motor Neurons / Q000502:physiology* / Q000648:ultrastructure; D009420:Nervous System / Q000166:cytology / Q000196:embryology; D009434:Neural Pathways / Q000196:embryology
D015816:Cell Adhesion Molecules, Neuronal; D029721:Drosophila Proteins; C051642:fasciclin II