Peptidergic signaling from clock neurons regulates reproductive dormancy in Drosophila melanogaster.
With the approach of winter, many insects switch to an alternative protective developmental program called diapause. Drosophila melanogaster females overwinter as adults by inducing a reproductive arrest that is characterized by inhibition of ovarian development at previtellogenic stages. The insuli...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2019-06-01
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| Series: | PLoS Genetics |
| Online Access: | https://doi.org/10.1371/journal.pgen.1008158 |
| _version_ | 1831588430326267904 |
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| author | Dóra Nagy Paola Cusumano Gabriele Andreatta Ane Martin Anduaga Christiane Hermann-Luibl Nils Reinhard João Gesto Christian Wegener Gabriella Mazzotta Ezio Rosato Charalambos P Kyriacou Charlotte Helfrich-Förster Rodolfo Costa |
| author_facet | Dóra Nagy Paola Cusumano Gabriele Andreatta Ane Martin Anduaga Christiane Hermann-Luibl Nils Reinhard João Gesto Christian Wegener Gabriella Mazzotta Ezio Rosato Charalambos P Kyriacou Charlotte Helfrich-Förster Rodolfo Costa |
| author_sort | Dóra Nagy |
| collection | DOAJ |
| description | With the approach of winter, many insects switch to an alternative protective developmental program called diapause. Drosophila melanogaster females overwinter as adults by inducing a reproductive arrest that is characterized by inhibition of ovarian development at previtellogenic stages. The insulin producing cells (IPCs) are key regulators of this process, since they produce and release insulin-like peptides that act as diapause-antagonizing hormones. Here we show that in D. melanogaster two neuropeptides, Pigment Dispersing Factor (PDF) and short Neuropeptide F (sNPF) inhibit reproductive arrest, likely through modulation of the IPCs. In particular, genetic manipulations of the PDF-expressing neurons, which include the sNPF-producing small ventral Lateral Neurons (s-LNvs), modulated the levels of reproductive dormancy, suggesting the involvement of both neuropeptides. We expressed a genetically encoded cAMP sensor in the IPCs and challenged brain explants with synthetic PDF and sNPF. Bath applications of both neuropeptides increased cAMP levels in the IPCs, even more so when they were applied together, suggesting a synergistic effect. Bath application of sNPF additionally increased Ca2+ levels in the IPCs. Our results indicate that PDF and sNPF inhibit reproductive dormancy by maintaining the IPCs in an active state. |
| first_indexed | 2024-12-17T22:14:11Z |
| format | Article |
| id | doaj.art-183d3da93a15420a81196bf596a03f94 |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2024-12-17T22:14:11Z |
| publishDate | 2019-06-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-183d3da93a15420a81196bf596a03f942022-12-21T21:30:40ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042019-06-01156e100815810.1371/journal.pgen.1008158Peptidergic signaling from clock neurons regulates reproductive dormancy in Drosophila melanogaster.Dóra NagyPaola CusumanoGabriele AndreattaAne Martin AnduagaChristiane Hermann-LuiblNils ReinhardJoão GestoChristian WegenerGabriella MazzottaEzio RosatoCharalambos P KyriacouCharlotte Helfrich-FörsterRodolfo CostaWith the approach of winter, many insects switch to an alternative protective developmental program called diapause. Drosophila melanogaster females overwinter as adults by inducing a reproductive arrest that is characterized by inhibition of ovarian development at previtellogenic stages. The insulin producing cells (IPCs) are key regulators of this process, since they produce and release insulin-like peptides that act as diapause-antagonizing hormones. Here we show that in D. melanogaster two neuropeptides, Pigment Dispersing Factor (PDF) and short Neuropeptide F (sNPF) inhibit reproductive arrest, likely through modulation of the IPCs. In particular, genetic manipulations of the PDF-expressing neurons, which include the sNPF-producing small ventral Lateral Neurons (s-LNvs), modulated the levels of reproductive dormancy, suggesting the involvement of both neuropeptides. We expressed a genetically encoded cAMP sensor in the IPCs and challenged brain explants with synthetic PDF and sNPF. Bath applications of both neuropeptides increased cAMP levels in the IPCs, even more so when they were applied together, suggesting a synergistic effect. Bath application of sNPF additionally increased Ca2+ levels in the IPCs. Our results indicate that PDF and sNPF inhibit reproductive dormancy by maintaining the IPCs in an active state.https://doi.org/10.1371/journal.pgen.1008158 |
| spellingShingle | Dóra Nagy Paola Cusumano Gabriele Andreatta Ane Martin Anduaga Christiane Hermann-Luibl Nils Reinhard João Gesto Christian Wegener Gabriella Mazzotta Ezio Rosato Charalambos P Kyriacou Charlotte Helfrich-Förster Rodolfo Costa Peptidergic signaling from clock neurons regulates reproductive dormancy in Drosophila melanogaster. PLoS Genetics |
| title | Peptidergic signaling from clock neurons regulates reproductive dormancy in Drosophila melanogaster. |
| title_full | Peptidergic signaling from clock neurons regulates reproductive dormancy in Drosophila melanogaster. |
| title_fullStr | Peptidergic signaling from clock neurons regulates reproductive dormancy in Drosophila melanogaster. |
| title_full_unstemmed | Peptidergic signaling from clock neurons regulates reproductive dormancy in Drosophila melanogaster. |
| title_short | Peptidergic signaling from clock neurons regulates reproductive dormancy in Drosophila melanogaster. |
| title_sort | peptidergic signaling from clock neurons regulates reproductive dormancy in drosophila melanogaster |
| url | https://doi.org/10.1371/journal.pgen.1008158 |
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