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The Journal of Neuroscience, January 11, 2006, 26(2):573-584; doi:10.1523/JNEUROSCI.3916-05.2006

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Cellular/Molecular
Functional Dissection of a Neuronal Network Required for Cuticle Tanning and Wing Expansion in Drosophila

Haojiang Luan,^1 * William C. Lemon,^1 * Nathan C. Peabody,¹ Jascha B. Pohl,¹ Paul K. Zelensky,¹ Ding Wang,¹ Michael N. Nitabach,² Todd C. Holmes,³ and Benjamin H. White¹

¹Laboratory of Molecular Biology, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland 20892, ²Department of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, Connecticut 06520, and ³Department of Biology, New York University, New York, New York 10003

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 (N_CCAP) 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 N_CCAP-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 N_CCAP-R, consists of N_CCAP neurons outside the c929-Gal4 pattern. Because suppression of synaptic transmission and protein kinase A (PKA) activity throughout N_CCAP, but not in N_CCAP-c929, also blocks tanning and wing expansion, we conclude that neurotransmission and PKA are required in N_CCAP-R to regulate bursicon secretion from N_CCAP-c929. Enhancement of electrical activity in N_CCAP-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 N_CCAP-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 N_CCAP 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.

Key words: excitability; network; circuit; hormone; neuropeptide; Drosophila

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Received Sep 15, 2005; revised November 18, 2005; accepted November 22, 2005.

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