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Metabolic stress responses in Drosophila are modulated by brain neurosecretory cells that produce multiple neuropeptides
Stockholm University, Faculty of Science, Department of Zoology, Functional Morphology.
Stockholm University, Faculty of Science, Department of Zoology.
Stockholm University, Faculty of Science, Department of Zoology, Functional Morphology.ORCID iD: 0000-0001-7815-4868
Stockholm University, Faculty of Science, Department of Zoology.
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2010 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 5, no 7, e11480- p.Article in journal (Refereed) Published
Abstract [en]

In Drosophila, neurosecretory cells that release peptide hormones play a prominent role in the regulation of development, growth, metabolism, and reproduction. Several types of peptidergic neurosecretory cells have been identified in the brain of Drosophila with release sites in the corpora cardiaca and anterior aorta. We show here that in adult flies the products of three neuropeptide precursors are colocalized in five pairs of large protocerebral neurosecretory cells in two clusters (designated ipc-1 and ipc-2a): Drosophila tachykinin (DTK), short neuropeptide F (sNPF) and ion transport peptide (ITP). These peptides were detected by immunocytochemistry in combination with GFP expression driven by the enhancer trap Gal4 lines c929 and Kurs-6, both of which are expressed in ipc-1 and 2a cells. This mix of colocalized peptides with seemingly unrelated functions is intriguing and prompted us to initiate analysis of the function of the ten neurosecretory cells. We investigated the role of peptide signaling from large ipc-1 and 2a cells in stress responses by monitoring the effect of starvation and desiccation in flies with levels of DTK or sNPF diminished by RNA interference. Using the Gal4-UAS system we targeted the peptide knockdown specifically to ipc-1 and 2a cells with the c929 and Kurs-6 drivers. Flies with reduced DTK or sNPF levels in these cells displayed decreased survival time at desiccation and starvation, as well as increased water loss at desiccation. Our data suggest that homeostasis during metabolic stress requires intact peptide signaling by ipc-1 and 2a neurosecretory cells.

Place, publisher, year, edition, pages
2010. Vol. 5, no 7, e11480- p.
National Category
Biological Sciences
Identifiers
URN: urn:nbn:se:su:diva-41306DOI: 10.1371/journal.pone.0011480ISI: 000279637100010OAI: oai:DiVA.org:su-41306DiVA: diva2:329408
Available from: 2010-07-10 Created: 2010-07-10 Last updated: 2017-12-12Bibliographically approved
In thesis
1. Distribution and modulatory roles of neuropeptides and neurotransmitters in the Drosophila brain 
Open this publication in new window or tab >>Distribution and modulatory roles of neuropeptides and neurotransmitters in the Drosophila brain 
2010 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The central complex is a prominent neuropil found in the middle of the insect brain. It is considered as a higher center for motor control and information processing. Multiple neuropeptides and neurotransmitters are produced in neurons of the central complex, however, distribution patterns and functional roles of signaling substances in this brain region are poorly known. Thus, this thesis focuses on the distribution of signaling substances and on modulatory roles of neuropeptides in the central complex of Drosophila.

Immunocytochemistry in combination with GAL4/UAS technique was used to visualize various signaling substances in the central complex. We revealed different central-complex neurons expressing the neuropeptides; Drosophila tachykinin (DTK), short neuropeptide F (sNPF), myoinhibitory peptide (MIP), allatostatin A, proctolin, SIFamide, neuropeptide F and FMRFamide. Subpopulations of DTK, sNPF and MIP-expressing neurons were found to co-localize a marker for acetylcholine. In addition, five metabotropic neurotransmitter receptors were found to be expressed in distinct patterns. Comparison of receptor/ligand distributions revealed a close match in most of the structures studied.

By using a video-tracking assay, peptidergic modulation of locomotor behavior was studied. Different DTK and sNPF-expressing neurons innervating the central complex were revealed to modulate spatial distribution, number of activity-rest phases and activity levels, suggesting circuit dependent modulation.

Furthermore, neurosecretory cells in the Drosophila brain that co-express three types of neuropeptides were shown to modulate stress responses to desiccation and starvation.

In summary, we have studied two different neuropeptides (DTK and sNPF) expressed in interneuronal circuits and neurosecretory cells of the Drosophila brain in more detail. We found that these neuropeptides display multiple actions as neuromodulators and circulating hormones, and that their actions depend on where they are released.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University, 2010. 44 p.
Keyword
central complex, locomotor behavior, co-transmitter, metabotropic receptor, metabolic stress
National Category
Neurosciences
Research subject
Zoology
Identifiers
urn:nbn:se:su:diva-42947 (URN)978-91-7447-150-2 (ISBN)
Public defence
2010-10-29, Nordenskiöldsalen, Geovetenskapenshus, Svante Arrhenius väg 12, Stockholm, 10:00 (English)
Opponent
Supervisors
Note
At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 2: In press. Paper 3: Manuscript.Available from: 2010-10-07 Created: 2010-09-20 Last updated: 2012-01-20Bibliographically approved
2. Regulation of insulin producing cells, stress responses and metabolism in Drosophila
Open this publication in new window or tab >>Regulation of insulin producing cells, stress responses and metabolism in Drosophila
2012 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

In Drosophila, neuropeptides have regulatory roles in development, growth, metabolism and reproduction. This study focused on GABA and the neuropeptides Drosophila tachykinin (DTK), short neuropeptide F (sNPF), adipokinetic hormone (AKH), corazonin (CRZ) and Drosophila insulin-like peptides (DILPs) as possible regulators of metabolic stress responses and homeostasis. We showed that metabotropic GABAB receptors (GBRs) are expressed on brain insulin producing cells (IPCs), suggesting an inhibitory regulation of these cells by GABA. Knockdown of GBR on IPCs shortened lifespan and stress resistance, altered carbohydrate and lipid metabolism at stress (paper I). We showed that three different neuropeptides; DTK, sNPF and ITP, are co-expressed in five pairs of adult neurosecretory cells (paper II). ITP-knock down was not studied yet, but sNPF- and DTK-knock down flies showed decreased stress resistance at desiccation and starvation and decreased water levels at desiccation, suggesting that these peptides are involved in water homeostasis during stress conditions. sNPF was previously shown to affect feeding, growth and DILP expression via the IPCs, but it was not known which sNPF-expressing neurons are responsible for these actions. We could identify a specific set of bilateral neurons (DLPs) that co-express sNPF and corazonin that target the IPCs. We showed that these peptides co-released from DLPs regulate DILP transcription and probably release in the adult Drosophila brain and thus have roles in regulation of stress resistance and metabolism (paper III). AKH signaling was previously shown to affect hemolymph carbohydrate levels and lipid stores in Drosophila. Insulin (DILP) signaling and AKH signaling are suggested to have opposing effects on lipid and sugar metabolism in Drosophila. We studied the possible functional relationship between these two systems; do they mutually regulate each other?  Our results suggest action of DILPs via the Insulin Receptor on the IPCs and the AKH producing cells, but we could not provide evidence for AKH action on IPCs or AKH cells (paper IV). 

Place, publisher, year, edition, pages
Stockholm, Sweden: Department of Zoology, Stockholm Univeristy, 2012. 33 p.
Keyword
Insulin signaling, Drosophila melanogaster, peptide hormones, neuropeptides, GABA
National Category
Cell Biology
Research subject
Functional Zoomorphology
Identifiers
urn:nbn:se:su:diva-80518 (URN)978-91-7447-582-1 (ISBN)
Public defence
2012-10-26, Nordenskiöldsalen, Geovetenskapens hus, Svante Arrhenius väg 12, Stockholm, 10:00 (English)
Opponent
Supervisors
Funder
Swedish Research Council
Note

At the time of the doctoral defense, the following paper was unpublished and had a status as follows: Paper 3: Epub ahead of print. Paper 4: Manuscript.

Available from: 2012-10-04 Created: 2012-09-24 Last updated: 2014-10-28Bibliographically approved
3. Peptide and GABA regulation of Peptide Hormone Release in the Drosophila Brain
Open this publication in new window or tab >>Peptide and GABA regulation of Peptide Hormone Release in the Drosophila Brain
2010 (English)Licentiate thesis, comprehensive summary (Other academic)
Place, publisher, year, edition, pages
Department of Zoology, Stockholm University, 2010. 39 p.
Series
Licentiatavhandling / Zoologiska institutionen, Stockholms universitet, ISSN 1403-5227
National Category
Zoology
Identifiers
urn:nbn:se:su:diva-65831 (URN)
Presentation
2010-12-07, 14:00 (English)
Opponent
Supervisors
Available from: 2013-01-25 Created: 2011-12-14 Last updated: 2014-10-28Bibliographically approved

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