Functional dissection of a neuronal network required for cuticle tanning and wing expansion in Drosophila.
A subset of Drosophila neurons that expresses crustacean cardioactive peptide (CCAP) has been shown previously to make the hormone bursicon, which is required for cuticle tanning and wing expansion after eclosion. Here we present evidence that CCAP-expressing neurons (NCCAP) consist of two functionally distinct groups, one of which releases bursicon into the hemolymph and the other of which regulates its release. The first group, which we call NCCAP-c929, includes 14 bursicon-expressing neurons of the abdominal ganglion that lie within the expression pattern of the enhancer-trap line c929-Gal4. We show that suppression of activity within this group blocks bursicon release into the hemolymph together with tanning and wing expansion. The second group, which we call NCCAP-R, consists of NCCAP neurons outside the c929-Gal4 pattern. Because suppression of synaptic transmission and protein kinase A (PKA) activity throughout NCCAP, but not in NCCAP-c929, also blocks tanning and wing expansion, we conclude that neurotransmission and PKA are required in NCCAP-R to regulate bursicon secretion from NCCAP-c929. Enhancement of electrical activity in NCCAP-R by expression of the bacterial sodium channel NaChBac also blocks tanning and wing expansion and leads to depletion of bursicon from central processes. NaChBac expression in NCCAP-c929 is without effect, suggesting that the abdominal bursicon-secreting neurons are likely to be silent until stimulated to release the hormone. Our results suggest that NCCAP form an interacting neuronal network responsible for the regulation and release of bursicon and suggest a model in which PKA-mediated stimulation of inputs to normally quiescent bursicon-expressing neurons activates release of the hormone.
Luan
Haojiang
H
Laboratory of Molecular Biology, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland 20892, USA.
Lemon
William C
WC
Peabody
Nathan C
NC
Pohl
Jascha B
JB
Zelensky
Paul K
PK
Wang
Ding
D
Nitabach
Michael N
MN
Holmes
Todd C
TC
White
Benjamin H
BH
D000818:Animals; D030801:Animals, Genetically Modified; D001426:Bacterial Proteins / Q000502:physiology; D017868:Cyclic AMP-Dependent Protein Kinases / Q000502:physiology; D029721:Drosophila Proteins / Q000235:genetics / Q000502:physiology; D004331:Drosophila melanogaster / Q000254:growth & development / Q000502:physiology*; D004596:Electroretinography; D017952:Ganglia, Invertebrate / Q000166:cytology; D018390:Gene Targeting; D007447:Invertebrate Hormones / Q000378:metabolism*; D009415:Nerve Net / Q000502:physiology*; D009474:Neurons / Q000378:metabolism / Q000502:physiology*; D009479:Neuropeptides / Q000032:analysis*; D010641:Phenotype; D010858:Pigmentation; D011993:Recombinant Fusion Proteins / Q000502:physiology; D051637:Shaker Superfamily of Potassium Channels / Q000235:genetics / Q000502:physiology; D015222:Sodium Channels / Q000502:physiology; D009435:Synaptic Transmission; D014921:Wings, Animal / Q000502:physiology*
D001426:Bacterial Proteins; D029721:Drosophila Proteins; D007447:Invertebrate Hormones; C443666:NaChBac protein, bacteria; D009479:Neuropeptides; D011993:Recombinant Fusion Proteins; C496929:Sh protein, Drosophila; D051637:Shaker Superfamily of Potassium Channels; D015222:Sodium Channels; C058620:crustacean cardioactive peptide; C002295:bursicon; D017868:Cyclic AMP-Dependent Protein Kinases