Regulation of insect steroid hormone biosynthesis by innervating peptidergic neurons
- Naoki Yamanaka*,
- Dušan Žitňan†,
- Young-Joon Kim‡,
- Michael E. Adams‡,
- Yue-Jin Hua§,
- Yusuke Suzuki¶,
- Minoru Suzuki¶,
- Akemi Suzuki¶,
- Honoo Satake‖,
- Akira Mizoguchi**,
- Kiyoshi Asaoka††,
- Yoshiaki Tanaka‡‡, and
- Hiroshi Kataoka*,§§
- *Department of Integrated Biosciences, Graduate School of Frontier Sciences, University of Tokyo, Chiba 277-8562, Japan;
- †Institute of Zoology, Slovak Academy of Sciences, Dúbravská cesta 9, 84206 Bratislava, Slovakia;
- ‡Departments of Entomology and Cell Biology and Neuroscience, University of California, 5429 Boyce Hall, Riverside, CA 92521;
- §Institute of Nuclear-Agricultural Science, Zhejiang University, Zhejiang 310029, China;
- ¶Frontier Research System, RIKEN, Saitama 351-0198, Japan;
- ‖Suntory Institute for Bioorganic Research, Osaka 618-8503, Japan;
- **Division of Biological Science, Graduate School of Science, Nagoya University, Nagoya 464-8602, Japan; and Laboratories of
- ††Insect Neurobiology and
- ‡‡Insect Growth Regulation, National Institute of Agrobiological Science, Ibaraki 305-8634, Japan
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Edited by Bruce D. Hammock, University of California, Davis, CA, and approved March 31, 2006 (received for review December 27, 2005)
Abstract
In insects, steroid hormones named ecdysteroids elicit molting and metamorphosis. The prothoracic gland (PG) is a predominant source of ecdysteroids, where their biosynthesis (ecdysteroidogenesis) is regulated by several neuropeptides. Here, we report that FMRFamide-related peptides (FaRPs) regulate ecdysteroidogenesis through direct innervation of the PG in the silkworm Bombyx mori. We purified a previously uncharacterized Bombyx FaRP, DPSFIRFamide, and identified the corresponding Bombyx FMRFamide gene (Bommo-FMRFamide, BRFa), which encodes three additional FaRPs. All BRFa peptides suppressed ecdysteroidogenesis in the PG by reducing cAMP production by means of the receptor for Bommo-myosuppressin, another FaRP we have previously shown to act as a prothoracicostatic factor. BRFa is predominantly expressed in neurosecretory cells of thoracic ganglia, and the neurons in the prothoracic ganglion innervate the PG to supply all four peptides to the gland surface. Electrophysiological recordings during development confirmed the increased firing activity of BRFa neurons in stages with low PG activity and decreased ecdysteroid levels in the hemolymph. To our knowledge, this study provides the first report of peptides controlling ecdysteroidogenesis by direct innervation.
Footnotes
- §§To whom correspondence should be addressed. E-mail: kataoka{at}k.u-tokyo.ac.jp
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Author contributions: N.Y., K.A., Y.T., and H.K. designed research; N.Y., D.Ž., Y.-J.K., Y.-J.H., Y.S., M.S., A.S., H.S., and A.M. performed research; N.Y. analyzed data; and N.Y., D.Ž., and M.E.A. wrote the paper.
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Conflict of interest statement: No conflicts declared.
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Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. AB234100 and AB253536).
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This paper was submitted directly (Track II) to the PNAS office.
- Abbreviations:
- FaRP,
- FMRFamide-related peptide;
- PG,
- prothoracic gland;
- PTTH,
- prothoracicotropic hormone;
- BMS,
- Bommo-myosuppressin;
- BMSR,
- BMS receptor;
- BRFa,
- Bommo-FMRFamide;
- BRFaR,
- BRFa receptor;
- NS-VTL1,2,
- ventrolateral neurosecretory cells 1 and 2;
- PBST,
- PBS containing 0.05% (vol/vol) Tween 20.
Abbreviations:
- © 2006 by The National Academy of Sciences of the USA
