Wnt5 and drl/ryk gradients pattern the Drosophila olfactory dendritic map.
During development, dendrites migrate to their correct locations in response to environmental cues. The mechanisms of dendritic guidance are poorly understood. Recent work has shown that the Drosophila olfactory map is initially formed by the spatial segregation of the projection neuron (PN) dendrites in the developing antennal lobe (AL). We report here that between 16 and 30 h after puparium formation, the PN dendrites undergo dramatic rotational reordering to achieve their final glomerular positions. During this period, a novel set of AL-extrinsic neurons express high levels of the Wnt5 protein and are tightly associated with the dorsolateral edge of the AL. Wnt5 forms a dorsolateral-high to ventromedial-low pattern in the antennal lobe neuropil. Loss of Wnt5 prevents the ventral targeting of the dendrites, whereas Wnt5 overexpression disrupts dendritic patterning. We find that Drl/Ryk, a known Wnt5 receptor, is expressed in a dorsolateral-to-ventromedial (DL > VM) gradient by the PN dendrites. Loss of Drl in the PNs results in the aberrant ventromedial targeting of the dendrites, a defect that is suppressed by reduction in Wnt5 gene dosage. Conversely, overexpression of Drl in the PNs results in the dorsolateral targeting of their dendrites, an effect that requires Drl's cytoplasmic domain. We propose that Wnt5 acts as a repulsive guidance cue for the PN dendrites, whereas Drl signaling in the dendrites inhibits Wnt5 signaling. In this way, the precise expression patterns of Wnt5 and Drl orient the PN dendrites allowing them to target their final glomerular positions.
Department of Cell and Developmental Biology, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801.
Yuping
Y
Wu
Department of Biology, The College at Brockport, SUNY, Brockport, New York 14420, and.
Jay-Christian
JC
Helt
Department of Biology, The College at Brockport, SUNY, Brockport, New York 14420, and.
Emily
E
Wexler
Laboratory of Developmental Neurobiology, Department of Molecular Cell Biology, Leiden University Medical Center, 2300 RC Leiden, The Netherlands.
Iveta M
IM
Petrova
Laboratory of Developmental Neurobiology, Department of Molecular Cell Biology, Leiden University Medical Center, 2300 RC Leiden, The Netherlands.
Jasprina N
JN
Noordermeer
Laboratory of Developmental Neurobiology, Department of Molecular Cell Biology, Leiden University Medical Center, 2300 RC Leiden, The Netherlands.
Lee G
LG
Fradkin
Department of Biology, The College at Brockport, SUNY, Brockport, New York 14420, and hhing@brockport.edu.
Huey
H
Hing
D000818:Animals; D057506:Arthropod Antennae / Q000254:growth & development / Q000294:innervation; D003712:Dendrites / Q000378:metabolism* / Q000502:physiology; D004330:Drosophila / Q000378:metabolism / Q000502:physiology*; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism*; D055495:Neurogenesis; D019581:Neuropil / Q000378:metabolism; D018034:Olfactory Receptor Neurons / Q000166:cytology / Q000378:metabolism* / Q000502:physiology; D011518:Proto-Oncogene Proteins / Q000235:genetics / Q000378:metabolism*; D020794:Receptor Protein-Tyrosine Kinases / Q000235:genetics / Q000378:metabolism*; D051153:Wnt Proteins / Q000235:genetics / Q000378:metabolism*; D060449:Wnt Signaling Pathway
D029721:Drosophila Proteins; D011518:Proto-Oncogene Proteins; D051153:Wnt Proteins; C491438:Wnt5 protein, Drosophila; C094492:DRL protein, Drosophila; D020794:Receptor Protein-Tyrosine Kinases
Drl; RYK; Wnt; dendrite; signaling; targeting