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...

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Published inPLoS genetics Vol. 15; no. 6; p. e1008158
Main Authors Nagy, Dóra, Cusumano, Paola, Andreatta, Gabriele, Anduaga, Ane Martin, Hermann-Luibl, Christiane, Reinhard, Nils, Gesto, João, Wegener, Christian, Mazzotta, Gabriella, Rosato, Ezio, Kyriacou, Charalambos P, Helfrich-Förster, Charlotte, Costa, Rodolfo
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 13.06.2019
Public Library of Science (PLoS)
Subjects
Animals
Animals, Genetically Modified - genetics
Biology
Biology and Life Sciences
Brain - metabolism
Calcium
Cellular signal transduction
Circadian rhythm
Circadian Rhythm - genetics
CLOCK Proteins - genetics
Cyclic adenosine monophosphate
Cyclic AMP
Developmental stages
Diapause
Diapause - genetics
Diapause - physiology
Dormancy
Drosophila
Drosophila melanogaster
Drosophila melanogaster - genetics
Drosophila melanogaster - growth & development
Drosophila Proteins - genetics
Explants
Gene expression
Gene Expression Regulation - genetics
Genetic aspects
Genetic engineering
Genetic regulation
Genetic research
Genetics
Genomes
Hormones
Insects
Insulin
Insulin - genetics
Medicine and Health Sciences
Nervous system
Neurobiology
Neurons
Neurons - metabolism
Neuropeptide F
Neuropeptides
Neuropeptides - genetics
Neurosciences
Peptides
Physiological aspects
Proteins
Reproduction - genetics
Research and Analysis Methods
Signal Transduction - genetics
Supervision
Zoological research
Italy
United Kingdom > UK
Germany
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Abstract 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.
AbstractList 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.
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-LN.sub.v s), 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 Ca.sup.2+ levels in the IPCs. Our results indicate that PDF and sNPF inhibit reproductive dormancy by maintaining the IPCs in an active state.
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-LN v s), 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 Ca 2+ levels in the IPCs. Our results indicate that PDF and sNPF inhibit reproductive dormancy by maintaining the IPCs in an active state. Diapause is a hormonally mediated process that allows insects to predict and respond to unfavourable conditions by altering their metabolism and behavior to resist the oncoming environmental challenges. In Drosophila melanogaster females a protective state of reproductive dormancy is induced by lower temperatures and shorter photoperiods that mimic the approach of winter. By genetically manipulating the circadian pacemaker s-LN v s cells, which express two neuropeptides, Pigment dispersing factor (PDF) and short Neuropeptide F (sNPF), we were able to modulate levels of gonadal arrest. PDF and sNPF appear to act as antagonists to dormancy, as do the Drosophila insulin-like peptides (dILPs) that are expressed in the insulin producing cells (IPCs). Indeed, we observe that the axonal projections from the s-LNvs appear to overlap with those from the IPCs implying that the clock cells signal to the IPCs. We confirm this possible communication by applying the two synthetic peptides to the IPCs and detecting a response in the IPC signal transduction pathway. We conclude that the clock neurons activate the IPCs via PDF and sNPF, which in turn release the dILPs, antagonise dormancy and lead to reproductive growth, thereby uncovering a neurogenetic circadian-overwintering axis.
Audience Academic
Author Cusumano, Paola
Costa, Rodolfo
Kyriacou, Charalambos P
Nagy, Dóra
Anduaga, Ane Martin
Hermann-Luibl, Christiane
Rosato, Ezio
Wegener, Christian
Gesto, João
Andreatta, Gabriele
Reinhard, Nils
Helfrich-Förster, Charlotte
Mazzotta, Gabriella
AuthorAffiliation 3 Neurobiology and Genetics, Theodor-Boveri-Institute, Biocenter, University of Würzburg, Würzburg, Germany
Washington University in Saint Louis School of Medicine, UNITED STATES
1 Department of Biology, University of Padova, Padova, Italy
2 Department of Genetics and Genome Biology, University of Leicester, Leicester, United Kingdom
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– name: 1 Department of Biology, University of Padova, Padova, Italy
– name: 2 Department of Genetics and Genome Biology, University of Leicester, Leicester, United Kingdom
– name: Washington University in Saint Louis School of Medicine, UNITED STATES
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  surname: Nagy
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  surname: Anduaga
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  surname: Hermann-Luibl
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  surname: Reinhard
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  organization: Neurobiology and Genetics, Theodor-Boveri-Institute, Biocenter, University of Würzburg, Würzburg, Germany
– sequence: 7
  givenname: João
  orcidid: 0000-0002-4390-2034
  surname: Gesto
  fullname: Gesto, João
  organization: Department of Genetics and Genome Biology, University of Leicester, Leicester, United Kingdom
– sequence: 8
  givenname: Christian
  orcidid: 0000-0003-4481-3567
  surname: Wegener
  fullname: Wegener, Christian
  organization: Neurobiology and Genetics, Theodor-Boveri-Institute, Biocenter, University of Würzburg, Würzburg, Germany
– sequence: 9
  givenname: Gabriella
  surname: Mazzotta
  fullname: Mazzotta, Gabriella
  organization: Department of Biology, University of Padova, Padova, Italy
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  givenname: Ezio
  surname: Rosato
  fullname: Rosato, Ezio
  organization: Department of Genetics and Genome Biology, University of Leicester, Leicester, United Kingdom
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  givenname: Charalambos P
  orcidid: 0000-0003-4889-7606
  surname: Kyriacou
  fullname: Kyriacou, Charalambos P
  organization: Department of Genetics and Genome Biology, University of Leicester, Leicester, United Kingdom
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  givenname: Charlotte
  orcidid: 0000-0002-0859-9092
  surname: Helfrich-Förster
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  givenname: Rodolfo
  orcidid: 0000-0002-2489-9116
  surname: Costa
  fullname: Costa, Rodolfo
  organization: Department of Biology, University of Padova, Padova, Italy
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31194738$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2019 Public Library of Science
2019 Nagy et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2019 Nagy et al 2019 Nagy et al
Copyright_xml – notice: COPYRIGHT 2019 Public Library of Science
– notice: 2019 Nagy et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: 2019 Nagy et al 2019 Nagy et al
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OK1
P2P
PIMPY
PQQKQ
PROAC
PSQYO
PV9
QF4
QN7
RIG
RNS
RPM
RZL
SV3
TR2
TUS
UKHRP
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7QR
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7TK
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FR3
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H94
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P64
PQEST
PQUKI
PRINS
RC3
7X8
5PM
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AAPBV
ABPTK
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Current address: Mosquitos Vetores: Endossimbiontes e Interação Patógeno-Vetor, Instituto René Rachou, Fiocruz, Belo Horizonte, MG, Brazil.
The authors have declared that no competing interests exist.
ORCID 0000-0003-4481-3567
0000-0002-7989-7150
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0000-0002-2489-9116
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6592559/
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SSID ssj0035897
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Snippet With the approach of winter, many insects switch to an alternative protective developmental program called diapause. Drosophila melanogaster females overwinter...
With the approach of winter, many insects switch to an alternative protective developmental program called diapause. Drosophila melanogaster females overwinter...
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StartPage e1008158
SubjectTerms Animals
Animals, Genetically Modified - genetics
Biology
Biology and Life Sciences
Brain - metabolism
Calcium
Cellular signal transduction
Circadian rhythm
Circadian Rhythm - genetics
CLOCK Proteins - genetics
Cyclic adenosine monophosphate
Cyclic AMP
Developmental stages
Diapause
Diapause - genetics
Diapause - physiology
Dormancy
Drosophila
Drosophila melanogaster
Drosophila melanogaster - genetics
Drosophila melanogaster - growth & development
Drosophila Proteins - genetics
Explants
Gene expression
Gene Expression Regulation - genetics
Genetic aspects
Genetic engineering
Genetic regulation
Genetic research
Genetics
Genomes
Hormones
Insects
Insulin
Insulin - genetics
Medicine and Health Sciences
Nervous system
Neurobiology
Neurons
Neurons - metabolism
Neuropeptide F
Neuropeptides
Neuropeptides - genetics
Neurosciences
Peptides
Physiological aspects
Proteins
Reproduction - genetics
Research and Analysis Methods
Signal Transduction - genetics
Supervision
Zoological research
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Title Peptidergic signaling from clock neurons regulates reproductive dormancy in Drosophila melanogaster
URI https://www.ncbi.nlm.nih.gov/pubmed/31194738
https://www.proquest.com/docview/2258819209/abstract/
https://search.proquest.com/docview/2253276108
https://pubmed.ncbi.nlm.nih.gov/PMC6592559
https://doaj.org/article/183d3da93a15420a81196bf596a03f94
http://dx.doi.org/10.1371/journal.pgen.1008158
Volume 15
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