4.1 Article

A population of neurons that produce hugin and express the diuretic hormone 44 receptor gene projects to the corpora allata in Drosophila melanogaster

Journal

DEVELOPMENT GROWTH & DIFFERENTIATION
Volume 63, Issue 4-5, Pages 249-261

Publisher

WILEY
DOI: 10.1111/dgd.12733

Keywords

corpora allata; diuretic hormone 44; Drosophila melanogaster; hugin; juvenile hormone

Funding

  1. Japan Society for the Promotion of Science [KAKENHI 17J00218, KAKENHI 26250001, KAKENHI A17H01378]
  2. Precursory Research for Embryonic Science and Technology [JPMJPR12M1]
  3. Tomizawa Jun-ichi & Keiko Fund of the Molecular Biology Society of Japan for Young Scientists

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The corpora allata (CA) are endocrine organs that synthesize juvenile hormone (JH) to regulate insect development. In insects like Drosophila melanogaster, neurons projecting to CA have been identified, but their role in JH biosynthesis remains unclear. This study on Drosophila found that hugin neurons projecting to CA have synaptic connections with upstream neurons, although inhibiting these neurons did not significantly impact JH-inducible gene expression.
The corpora allata (CA) are essential endocrine organs that biosynthesize and secrete the sesquiterpenoid hormone, namely juvenile hormone (JH), to regulate a wide variety of developmental and physiological events in insects. CA are directly innervated with neurons in many insect species, implying the innervations to be important for regulating JH biosynthesis. Although this is also true for the model organism Drosophila melanogaster, neurotransmitters produced in the CA-projecting neurons are yet to be identified. In this study on D. melanogaster, we aimed to demonstrate that a subset of neurons producing the neuropeptide hugin, the invertebrate counterpart of the vertebrate neuromedin U, directly projects to the adult CA. A synaptic vesicle marker in the hugin neurons was observed at their axon termini located on the CA, which were immunolabeled with a newly-generated antibody to the JH biosynthesis enzyme JH acid O-methyltransferase. We also found the CA-projecting hugin neurons to likely express a gene encoding the specific receptor for diuretic hormone 44 (Dh44). Moreover, our data suggest that the CA-projecting hugin neurons have synaptic connections with the upstream neurons producing Dh44. Unexpectedly, the inhibition of CA-projecting hugin neurons did not significantly alter the expression levels of the JH-inducible gene Kruppel-homolog 1, which implies that the CA-projecting neurons are not involved in JH biosynthesis but rather in other known biological processes. This is the first study to identify a specific neurotransmitter of the CA-projecting neurons in D. melanogaster, and to anatomically characterize a neuronal pathway of the CA-projecting neurons and their upstream neurons.

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