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  • 51.
    Nässel, Dick
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Enell, Lina
    Stockholm University, Faculty of Science, Department of Zoology.
    Santos, Jonathan
    Wegener, Christian
    Johard, Helena
    Stockholm University, Faculty of Science, Department of Zoology.
    A large population of diverse neurons in the Drosophila central nervous system expresses short neuropeptide F, suggesting multiple distributed peptide functions2008In: BMC neuroscience (Online), ISSN 1471-2202, E-ISSN 1471-2202, Vol. 9, no 1, p. 90-125Article in journal (Refereed)
    Abstract [en]

    Background

    Insect neuropeptides are distributed in stereotypic sets of neurons that commonly constitute a small fraction of the total number of neurons. However, some neuropeptide genes are expressed in larger numbers of neurons of diverse types suggesting that they are involved in a greater diversity of functions. One of these widely expressed genes, snpf, encodes the precursor of short neuropeptide F (sNPF). To unravel possible functional diversity we have mapped the distribution of transcript of the snpf gene and its peptide products in the central nervous system (CNS) of Drosophila in relation to other neuronal markers.

    Results

    There are several hundreds of neurons in the larval CNS and several thousands in the adult Drosophila brain expressing snpf transcript and sNPF peptide. Most of these neurons are intrinsic interneurons of the mushroom bodies. Additionally, sNPF is expressed in numerous small interneurons of the CNS, olfactory receptor neurons (ORNs) of the antennae, and in a small set of possibly neurosecretory cells innervating the corpora cardiaca and aorta. A sNPF-Gal4 line confirms most of the expression pattern. None of the sNPF immunoreactive neurons co-express a marker for the transcription factor DIMMED, suggesting that the majority are not neurosecretory cells or large interneurons involved in episodic bulk transmission. Instead a portion of the sNPF producing neurons co-express markers for classical neurotransmitters such as acetylcholine, GABA and glutamate, suggesting that sNPF is a co-transmitter or local neuromodulator in ORNs and many interneurons. Interestingly, sNPF is coexpressed both with presumed excitatory and inhibitory neurotransmitters. A few sNPF expressing neurons in the brain colocalize the peptide corazonin and a pair of dorsal neurons in the first abdominal neuromere coexpresses sNPF and insulin-like peptide 7 (ILP7).

    Conclusion

    It is likely that sNPF has multiple functions as neurohormone as well as local neuromodulator/co-transmitter in various CNS circuits, including olfactory circuits both at the level of the first synapse and at the mushroom body output level. Some of the sNPF immunoreactive axons terminate in close proximity to neurosecretory cells producing ILPs and adipokinetic hormone, indicating that sNPF also might regulate hormone production or release.

  • 52.
    Nässel, Dick
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Orchard, Ian
    Insect neuroendocrinology in the post-genomic era.2007In: Gen Comp Endocrinol, ISSN 0016-6480, Vol. 153, no 1-3, p. 57-8Article in journal (Other academic)
  • 53.
    Nässel, Dick R.
    Stockholm University, Faculty of Science, Department of Zoology.
    Insulin producing cells and their regulation in physiology and behavior of Drosophila2012In: Canadian Journal of Zoology, ISSN 0008-4301, E-ISSN 1480-3283, Vol. 90, no 4, p. 476-488Article, review/survey (Refereed)
    Abstract [en]

    Insulin-like peptide signaling regulates development, growth, reproduction, metabolism, stress resistance, and life span in a wide spectrum of animals. Not only the peptides, but also their tyrosine kinase receptors and the downstream signaling pathways are conserved over evolution. This review summarizes roles of insulin-like peptides (DILPs) in physiology and behavior of Drosophila melanogaster Meigen, 1830. Seven DILPs (DILP1-7) and one receptor (dInR) have been identified in Drosophila. These DILPs display cell and stage specific expression patterns. In the adult, DILP2, 3, and 5 are expressed in insulin-producing cells (IPCs) among the median neurosecretory cells of the brain, DILP7 in 20 neurons of the abdominal ganglion, and DILP6 in the fat body. The DILPs of the IPCs regulate starvation resistance, responses to oxidative and temperature stress, and carbohydrate and lipid metabolism. Furthermore, the IPCs seem to regulate feeding, locomotor activity, sleep and ethanol sensitivity, but the mechanisms are not elucidated. Insulin also alters the sensitivity in the olfactory system that affects food search behavior, and regulates peptidergic neurons that control aspects of feeding behavior. Finally, the control of insulin production and release by humoral and neuronal factors is discussed. This includes a fat body derived factor and the neurotransmitters GABA, serotonin, octopamine, and two neuropeptides.

  • 54.
    Nässel, Dick R.
    Stockholm University, Faculty of Science, Department of Zoology.
    Neuropeptides regulating Drosophila behavior2014In: BEHAVIORAL GENETICS OF THE FLY (DROSOPHILA MELANOGASTER) / [ed] Dubnau, J, Cambridge: Cambridge University Press, 2014, p. 20-36Chapter in book (Refereed)
  • 55.
    Nässel, Dick R.
    Stockholm University, Faculty of Science, Department of Zoology.
    Substrates for Neuronal Cotransmission With Neuropeptides and Small Molecule Neurotransmitters in Drosophila2018In: Frontiers in Cellular Neuroscience, ISSN 1662-5102, E-ISSN 1662-5102, Vol. 12, article id 83Article, review/survey (Refereed)
    Abstract [en]

    It has been known for more than 40 years that individual neurons can produce more than one neurotransmitter and that neuropeptides often are colocalized with small molecule neurotransmitters (SMNs). Over the years much progress has been made in understanding the functional consequences of cotransmission in the nervous system of mammals. There are also some excellent invertebrate models that have revealed roles of coexpressed neuropeptides and SMNs in increasing complexity, flexibility, and dynamics in neuronal signaling. However, for the fly Drosophila there are surprisingly few functional studies on cotransmission, although there is ample evidence for colocalization of neuroactive compounds in neurons of the CNS, based both on traditional techniques and novel single cell transcriptome analysis. With the hope to trigger interest in initiating cotransmission studies, this review summarizes what is known about Drosophila neurons and neuronal circuits where different neuropeptides and SMNs are colocalized. Coexistence of neuroactive substances has been recorded in different neuron types such as neuroendocrine cells, interneurons, sensory cells and motor neurons. Some of the circuits highlighted here are well established in the analysis of learning and memory, circadian clock networks regulating rhythmic activity and sleep, as well as neurons and neuroendocrine cells regulating olfaction, nociception, feeding, metabolic homeostasis, diuretic functions, reproduction, and developmental processes. One emerging trait is the broad role of short neuropeptide F in cotransmission and presynaptic facilitation in a number of different neuronal circuits. This review also discusses the functional relevance of coexisting peptides in the intestine. Based on recent single cell transcriptomics data, it is likely that the neuronal systems discussed in this review are just a fraction of the total set of circuits where cotransmission occurs in Drosophila. Thus, a systematic search for colocalized neuroactive compounds in further neurons in anatomically defined circuits is of interest for the near future.

  • 56.
    Nässel, Dick R.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Kubrak, Olga I.
    Stockholm University, Faculty of Science, Department of Zoology.
    Liu, Yiting
    Stockholm University, Faculty of Science, Department of Zoology.
    Luo, Jiangnan
    Stockholm University, Faculty of Science, Department of Zoology.
    Lushchak, Oleh V.
    Stockholm University, Faculty of Science, Department of Zoology.
    Factors that regulate insulin producing cells and their output in Drosophila2013In: Frontiers in Physiology, ISSN 1664-042X, E-ISSN 1664-042X, Vol. 4, article id 252Article, review/survey (Refereed)
    Abstract [en]

    Insulin-like peptides (ILPs) and growth factors (IGFs) not only regulate development, growth, reproduction, metabolism, stress resistance, and lifespan, but also certain behaviors and cognitive functions. ILPs, IGFs, their tyrosine kinase receptors and downstream signaling components have been largely conserved over animal evolution. Eight ILPs have been identified in Drosophila (DILP1-8) and they display cell and stage-specific expression patterns. Only one insulin receptor, dInR, is known in Drosophila and most other invertebrates. Nevertheless, the different DILPs are independently regulated transcriptionally and appear to have distinct functions, although some functional redundancy has been revealed. This review summarizes what is known about regulation of production and release of DILPs in Drosophila with focus on insulin signaling in the daily life of the fly. Under what conditions are DILP-producing cells (IPCs) activated and which factors have been identified in control of IPC activity in larvae and adult flies? The brain IPCs that produce DILP2, 3 and 5 are indirectly targeted by DILP6 and a leptin-like factor from the fat body, as well as directly by a few neurotransmitters and neuropeptides. Serotonin, octopamine, GABA, short neuropeptide F (sNPF), corazonin and tachykinin-related peptide have been identified in Drosophila as regulators of IPCs. The GABAergic cells that inhibit IPCs and DILP release are in turn targeted by a leptin-like peptide (unpaired 2) from the fat body, and the IPC-stimulating corazonin/sNPF neurons may be targeted by gut-derived peptides. We also discuss physiological conditions under which IPC activity may be regulated, including nutritional states, stress and diapause induction.

  • 57.
    Nässel, Dick R.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Liu, Yiting
    Stockholm University, Faculty of Science, Department of Zoology.
    Luo, Jiangnan
    Stockholm University, Faculty of Science, Department of Zoology.
    Insulin/IGF signaling and its regulation in Drosophila2015In: General and Comparative Endocrinology, ISSN 0016-6480, E-ISSN 1095-6840, Vol. 221, p. 255-266Article in journal (Refereed)
    Abstract [en]

    Taking advantage of Drosophila as a genetically tractable experimental animal much progress has been made in our understanding of how the insulin/IGF signaling (IS) pathway regulates development, growth, metabolism, stress responses and lifespan. The role of IIS in regulation of neuronal activity and behavior has also become apparent from experiments in Drosophila. This review briefly summarizes these functional roles of IIS, and also how the insulin producing cells (IPCs) are regulated in the fly. Furthermore, we discuss functional aspects of the spatio-temporal production of eight different insulin-like peptides (DILP1-8) that are thought to act on one known receptor (dInR) in Drosophila.

  • 58.
    Nässel, Dick R.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Vanden Broeck, Jozef
    Insulin/IGF signaling in Drosophila and other insects: factors that regulate production, release and post-release action of the insulin-like peptides2016In: Cellular and Molecular Life Sciences (CMLS), ISSN 1420-682X, E-ISSN 1420-9071, Vol. 73, no 2, p. 271-290Article, review/survey (Refereed)
    Abstract [en]

    Insulin, insulin-like growth factors (IGFs) and insulin-like peptides (ILPs) are important regulators of metabolism, growth, reproduction and lifespan, and mechanisms of insulin/IGF signaling (IIS) have been well conserved over evolution. In insects, between one and 38 ILPs have been identified in each species. Relatively few insect species have been investigated in depth with respect to ILP functions, and therefore we focus mainly on the well-studied fruitfly Drosophila melanogaster. In Drosophila eight ILPs (DILP1-8), but only two receptors (dInR and Lgr3) are known. DILP2, 3 and 5 are produced by a set of neurosecretory cells (IPCs) in the brain and their biosynthesis and release are controlled by a number of mechanisms differing between larvae and adults. Adult IPCs display cell-autonomous sensing of circulating glucose, coupled to evolutionarily conserved mechanisms for DILP release. The glucose-mediated DILP secretion is modulated by neurotransmitters and neuropeptides, as well as by factors released from the intestine and adipocytes. Larval IPCs, however, are indirectly regulated by glucose-sensing endocrine cells producing adipokinetic hormone, or by circulating factors from the intestine and fat body. Furthermore, IIS is situated within a complex physiological regulatory network that also encompasses the lipophilic hormones, 20-hydroxyecdysone and juvenile hormone. After release from IPCs, the ILP action can be modulated by circulating proteins that act either as protective carriers (binding proteins), or competitive inhibitors. Some of these proteins appear to have additional functions that are independent of ILPs. Taken together, the signaling with multiple ILPs is under complex control, ensuring tightly regulated IIS in the organism.

  • 59.
    Nässel, Dick R.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Wegener, Christian
    A comparative review of short and long neuropeptide F signaling in invertebrates: Any similarities to vertebrate neuropeptide Y signaling?2011In: Peptides, ISSN 0196-9781, E-ISSN 1873-5169, Vol. 32, no 6, p. 1335-1355Article, review/survey (Refereed)
    Abstract [en]

    Neuropeptides referred to as neuropeptide F (NPF) and short neuropeptide F (sNPF) have been identified in numerous invertebrate species. Sequence information has expanded tremendously due to recent genome sequencing and EST projects. Analysis of sequences of the peptides and prepropeptides strongly suggest that NPFs and sNPFs are not closely related. However, the NPFs are likely to be ancestrally related to the vertebrate family of neuropeptide Y (NPY) peptides. Peptide diversification may have been accomplished by different mechanisms in NPFs and sNPFs; in the former by gene duplications followed by diversification and in the sNPFs by internal duplications resulting in paracopies of peptides. We discuss the distribution and functions of NPFs and their receptors in several model invertebrates. Signaling with sNPF, however, has been investigated mainly in insects, especially in Drosophila. Both in invertebrates and in mammals NPF/NPY play roles in feeding, metabolism, reproduction and stress responses. Several other NPF functions have been studied in Drosophila that may be shared with mammals. In Drosophila sNPFs are widely distributed in numerous neurons of the CNS and some gut endocrines and their functions may be truly pleiotropic. Peptide distribution and experiments suggest roles of sNPF in feeding and growth, stress responses, modulation of locomotion and olfactory inputs, hormone release, as well as learning and memory. Available data indicate that NPF and sNPF signaling systems are distinct and not likely to play redundant roles.

  • 60.
    Nässel, Dick R.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Williams, Michael J.
    Cholecystokinin-like peptide (DSK) in Drosophila, not only for satiety signaling2014In: Frontiers in Endocrinology, ISSN 1664-2392, E-ISSN 1664-2392, Vol. 5, article id 219Article, review/survey (Refereed)
    Abstract [en]

    Cholecystokinin (CCK) signaling appears well conserved over evolution. In Drosophila, the CCK-like sulfakinins (DSKs) regulate aspects of gut function, satiety and food ingestion, hyperactivity and aggression, as well as escape-related locomotion and synaptic plasticity during neuromuscular junction development. Activity in the DSK-producing neurons is regulated by octopamine. We discuss mechanisms behind CCK function in satiety, aggression, and locomotion in some detail and highlight similarities to mammalian CCK signaling.

  • 61.
    Nässel, Dick R.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Winther, Åsa M. E.
    Stockholm University, Faculty of Science, Department of Zoology.
    Drosophila neuropeptides in regulation of physiology and behavior2010In: Progress in Neurobiology, ISSN 0301-0082, E-ISSN 1873-5118, Vol. 92, p. 42-104Article in journal (Refereed)
    Abstract [en]

    Studies of neuropeptide and peptide hormone signaling are coming of age in Drosophila due to rapid developments in molecular genetics approaches that overcome the difficulties caused by the small size of the fly. In addition we have genome-wide information on genes involved in peptide signaling, and growing pools of peptidomics data. A large number of different neuropeptides has been identified in a huge variety of neuron types in different parts of the Drosophila nervous system and cells in other locations. This review addresses questions related to peptidergic signaling in the Drosophila nervous system, especially how peptides regulate physiology and behavior during development and in the mature fly. We first summarize novel findings on neuropeptide precursor genes, processed bioactive peptides and their cognate receptors. Thereafter we provide an overview of the physiological and behavioral roles of peptide signaling in Drosophila. These roles include regulation of development, growth, feeding, metabolism, reproduction, homeostasis, and longevity, as well as neuromodulation in learning and memory, olfaction and locomotor control. The substrate of this signaling is the peptide products of about 42 precursor genes expressed in different combinations in a variety of neuronal circuits or that act as circulating hormones. Approximately 45 G-protein-coupled peptide receptors are known in Drosophila and for most of these the ligands have been identified. Functions of some peptides are better understood than others, and much work remains to reveal the spectrum of roles neuropeptides and peptide hormones play in the daily life of a fly

  • 62.
    Nässel, Dick R.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Zandawala, Meet
    Stockholm University, Faculty of Science, Department of Zoology. Brown University, USA.
    Recent advances in neuropeptide signaling in Drosophila, from genes to physiology and behavior2019In: Progress in Neurobiology, ISSN 0301-0082, E-ISSN 1873-5118, Vol. 179, article id UNSP 101607Article, review/survey (Refereed)
    Abstract [en]

    This review focuses on neuropeptides and peptide hormones, the largest and most diverse class of neuroactive substances, known in Drosophila and other animals to play roles in almost all aspects of daily life, as w;1;ell as in developmental processes. We provide an update on novel neuropeptides and receptors identified in the last decade, and highlight progress in analysis of neuropeptide signaling in Drosophila. Especially exciting is the huge amount of work published on novel functions of neuropeptides and peptide hormones in Drosophila, largely due to the rapid developments of powerful genetic methods, imaging techniques and innovative assays. We critically discuss the roles of peptides in olfaction, taste, foraging, feeding, clock function/sleep, aggression, mating/reproduction, learning and other behaviors, as well as in regulation of development, growth, metabolic and water homeostasis, stress responses, fecundity, and lifespan. We furthermore provide novel information on neuropeptide distribution and organization of peptidergic systems, as well as the phylogenetic relations between Drosophila neuropeptides and those of other phyla, including mammals. As will be shown, neuropeptide signaling is phylogenetically ancient, and not only are the structures of the peptides, precursors and receptors conserved over evolution, but also many functions of neuropeptide signaling in physiology and behavior.

  • 63. Poels, Jeroen
    et al.
    Birse, Ryan T
    Nachman, Ronald J
    Fichna, Jakub
    Janecka, Anna
    Vanden Broeck, Jozef
    Nässel, Dick R
    Stockholm University, Faculty of Science, Department of Zoology, Functional Morphology.
    Characterization and distribution of NKD, a receptor for Drosophila tachykinin-related peptide 6.2009In: Peptides, ISSN 0196-9781, E-ISSN 1873-5169, Vol. 30, no 3, p. 545-56Article in journal (Refereed)
    Abstract [en]

    Neuropeptides related to vertebrate tachykinins have been identified in Drosophila and are referred to as drosotachykinins, or DTKs. Two Drosophila G protein-coupled receptors, designated NKD (neurokinin receptor from Drosophila; CG6515) and DTKR (Drosophila tachykinin receptor; CG7887), display sequence similarities to mammalian tachykinin receptors. Whereas DTKR was shown to be activated by DTKs [Birse RT, Johnson EC, Taghert PH, Nässel DR. Widely distributed Drosophila G-protein-coupled receptor (CG7887) is activated by endogenous tachykinin-related peptides. J Neurobiol 2006;66:33-46; Poels J, Verlinden H, Fichna J, Van Loy T, Franssens V, Studzian K, et al. Functional comparison of two evolutionary conserved insect neurokinin-like receptors. Peptides 2007;28:103-8] and was localized by immunocytochemistry in Drosophila central nervous system (CNS), agonist-dependent activation and distribution of NKD have not yet been investigated in depth. In the present study, we have challenged NKD-expressing mammalian and insect cells with a library of Drosophila neuropeptides and discovered DTK-6 as a specific agonist that can induce a calcium response in these cells. In addition, we have produced antisera to sequences from NKD protein to analyze receptor distribution. We found that NKD is less abundantly distributed in the central nervous system than DTKR, and only NKD was found in the intestine. In fact, the two receptors are distributed in mutually exclusive patterns in the CNS. The combined distribution of the receptors in brain neuropils corresponds well with the distribution of DTKs. Most interestingly, NKD appears to be activated only by DTK-6, known to possess an Ala-substitution in an otherwise conserved C-terminal core motif. Our findings suggest that NKD and DTKR provide substrates for two functionally and spatially separated peptide signaling systems.

  • 64. Post, Stephanie
    et al.
    Liao, Sifang
    Stockholm University, Faculty of Science, Department of Zoology.
    Yamamoto, Rochele
    Veenstra, Jan A.
    Nässel, Dick R.
    Stockholm University, Faculty of Science, Department of Zoology.
    Tatar, Marc
    Drosophila insulin-like peptide dilp1 increases lifespan and glucagon-like Akh expression epistatic to dilp2In: Aging Cell, ISSN 1474-9718, E-ISSN 1474-9726Article in journal (Refereed)
  • 65. Post, Stephanie
    et al.
    Liao, Sifang
    Stockholm University, Faculty of Science, Department of Zoology.
    Yamamoto, Rochele
    Veenstra, Jan A.
    Nässel, Dick R.
    Stockholm University, Faculty of Science, Department of Zoology.
    Tatar, Marc
    Drosophila insulin-like peptide dilp1 increases lifespan and glucagon-like Akh expression epistatic to dilp22019In: Aging Cell, ISSN 1474-9718, E-ISSN 1474-9726, Vol. 18, no 1, article id e12863Article in journal (Refereed)
    Abstract [en]

    Insulin/IGF signaling (IIS) regulates essential processes including development, metabolism, and aging. The Drosophila genome encodes eight insulin/IGF-like peptide (dilp) paralogs, including tandem-encoded dilp1 and dilp2. Many reports show that longevity is increased by manipulations that decrease DILP2 levels. It has been shown that dilp1 is expressed primarily in pupal stages, but also during adult reproductive diapause. Here, we find that dilp1 is also highly expressed in adult dilp2 mutants under nondiapause conditions. The inverse expression of dilp1 and dilp2 suggests these genes interact to regulate aging. Here, we study dilp1 and dilp2 single and double mutants to describe epistatic and synergistic interactions affecting longevity, metabolism, and adipokinetic hormone (AKH), the functional homolog of glucagon. Mutants of dilp2 extend lifespan and increase Akh mRNA and protein in a dilp1-dependent manner. Loss of dilp1 alone has no impact on these traits, whereas transgene expression of dilp1 increases lifespan in dilp1-dilp2 double mutants. On the other hand, dilp1 and dilp2 redundantly or synergistically interact to control circulating sugar, starvation resistance, and compensatory dilp5 expression. These interactions do not correlate with patterns for how dilp1 and dilp2 affect longevity and AKH. Thus, repression or loss of dilp2 slows aging because its depletion induces dilp1, which acts as a pro-longevity factor. Likewise, dilp2 regulates Akh through epistatic interaction with dilp1. Akh and glycogen affect aging in Caenorhabditis elegans and Drosophila. Our data suggest that dilp2 modulates lifespan in part by regulating Akh, and by repressing dilp1, which acts as a pro-longevity insulin-like peptide.

  • 66. Root, Cory M.
    et al.
    Masuyama, Kaoru
    Green, David S.
    Enell, Lina
    Stockholm University, Faculty of Science, Department of Zoology. Funktionell zoomorfologi.
    Nässel, Dick
    Stockholm University, Faculty of Science, Department of Zoology. Funktionell zoomorfologi.
    Lee, Chi-Hon
    Wang, Jing W.
    A presynaptic gain control mechanism fine-tunes olfactory behavior2008In: Neuron, ISSN 0896-6273, Vol. 59, no 2, p. 311-21Article in journal (Refereed)
    Abstract [en]

    Early sensory processing can play a critical role in sensing environmental cues. We have investigated the physiological and behavioral function of gain control at the first synapse of olfactory processing in Drosophila. Olfactory receptor neurons (ORNs) express the GABA(B) receptor (GABA(B)R), and its expression expands the dynamic range of ORN synaptic transmission that is preserved in projection neuron responses. Strikingly, each ORN channel has a unique baseline level of GABA(B)R expression. ORNs that sense the aversive odorant CO(2) do not express GABA(B)Rs and do not have significant presynaptic inhibition. In contrast, pheromone-sensing ORNs express a high level of GABA(B)Rs and exhibit strong presynaptic inhibition. Furthermore, pheromone-dependent mate localization is impaired in flies that lack GABA(B)Rs in specific ORNs. These findings indicate that different olfactory receptor channels employ heterogeneous presynaptic gain control as a mechanism to allow an animal's innate behavioral responses to match its ecological needs.

  • 67. Santos, Jonathan G
    et al.
    Vömel, Matthias
    Struck, Rafael
    Homberg, Uwe
    Nässel, Dick R
    Stockholm University, Faculty of Science, Department of Zoology. Stockholm University, Faculty of Science, Department of Zoology, Department of Functional Morphology.
    Wegener, Christian
    Neuroarchitecture of peptidergic systems in the larval ventral ganglion of Drosophila melanogaster.2007In: PLoS ONE, ISSN 1932-6203, Vol. 2, no 1, p. e695-Article in journal (Refereed)
  • 68.
    Söderberg, Jeannette A. E.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Carlsson, Mikael A.
    Stockholm University, Faculty of Science, Department of Zoology.
    Nässel, Dick R.
    Stockholm University, Faculty of Science, Department of Zoology.
    Insulin-producing cells in the Drosophila brain also express satiety-inducing cholecystokinin-like peptide, drosulfakinin2012In: Frontiers in Endocrinology, ISSN 1664-2392, E-ISSN 1664-2392, Vol. 3, article id 109Article in journal (Refereed)
    Abstract [en]

    Regulation of meal size and assessing the nutritional value of food are two important aspects of feeding behavior. The mechanisms that regulate these two aspects have not been fully elucidated in Drosophila. Diminished signaling with insulin-like peptides Drosophila insulin-like peptides (DILPs) affects food intake in flies, but it is not clear what signal(s) mediates satiety. Here we investigate the role of DILPs and drosulfakinins (DSKs), cholecystokinin-like peptides, as satiety signals in Drosophila. We show that DSKs and DILPs are co-expressed in insulin-producing cells (IPCs) of the brain. Next we analyzed the effects of diminishing DSKs or DILPs employing the Gal4-UAS system by (1) diminishing DSK-levels without directly affecting DILP levels by targeted Dsk-RNAi, either in all DSK-producing cells (DPCs) or only in the IPCs or (2) expressing a hyperpolarizing potassium channel to inactivate either all the DPCs or only the IPCs, affecting release of both peptides. The transgenic flies were assayed for feeding and food choice, resistance to starvation, and for levels of Dilp and Dsk transcripts in brains of fed and starved animals. Diminishment of DSK in the IPCs alone is sufficient to cause defective regulation of food intake and food choice, indicating that DSK functions as a hormonal satiety signal in Drosophila. Quantification of Dsk and Dilp transcript levels reveals that knockdown of either peptide type affects the transcript levels of the other, suggesting a possible feedback regulation between the two signaling pathways. In summary, DSK and DILPs released from the IPCs regulate feeding, food choice and metabolic homeostasis in Drosophila in a coordinated fashion.

  • 69.
    Söderberg, Jeannette A.E.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology, Functional Morphology.
    Birse, Ryan T.
    The Burnham Institute for Medical Research.
    Nässel, Dick R.
    Stockholm University, Faculty of Science, Department of Zoology, Functional Morphology.
    Insulin Production and Signaling in Renal Tubules of Drosophila is under Control of Tachykinin-related Peptide and Regulates Stress Resistance2011In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 6, no 5, p. e19866-Article in journal (Refereed)
    Abstract [en]

    The insulin-signaling pathway is evolutionarily conserved in animals and regulates growth, reproduction, metabolichomeostasis, stress resistance and life span. In Drosophila seven insulin-like peptides (DILP1-7) are known, some of whichare produced in the brain, others in fat body or intestine. Here we show that DILP5 is expressed in principal cells of the renaltubules of Drosophila and affects survival at stress. Renal (Malpighian) tubules regulate water and ion homeostasis, but alsoplay roles in immune responses and oxidative stress. We investigated the control of DILP5 signaling in the renal tubules byDrosophila tachykinin peptide (DTK) and its receptor DTKR during desiccative, nutritional and oxidative stress. The DILP5levels in principal cells of the tubules are affected by stress and manipulations of DTKR expression in the same cells.Targeted knockdown of DTKR, DILP5 and the insulin receptor dInR in principal cells or mutation of Dilp5 resulted inincreased survival at either stress, whereas over-expression of these components produced the opposite phenotype. Thus,stress seems to induce hormonal release of DTK that acts on the renal tubules to regulate DILP5 signaling. Manipulations ofS6 kinase and superoxide dismutase (SOD2) in principal cells also affect survival at stress, suggesting that DILP5 acts locallyon tubules, possibly in oxidative stress regulation. Our findings are the first to demonstrate DILP signaling originating in therenal tubules and that this signaling is under control of stress-induced release of peptide hormone.

  • 70. Wegener, Christian
    et al.
    Hamasaka, Yasutaka
    Stockholm University, Faculty of Science, Department of Zoology.
    Nässel, Dick
    Acetylcholine increases intracellular Ca2+ via nicotinic receptors in cultured PDF-containing clock neurons of Drosophila2004In: Journal of neurophysiology, ISSN 0022-3077, Vol. 91, no 2, p. 912-923Article in journal (Refereed)
  • 71. Yeoh, Joseph G. C.
    et al.
    Pandit, Aniruddha A.
    Zandawala, Meet
    Stockholm University, Faculty of Science, Department of Zoology.
    Nässel, Dick R.
    Stockholm University, Faculty of Science, Department of Zoology.
    Davies, Shireen-Anne
    Dow, Julian A. T.
    DINeR: Database for Insect Neuropeptide Research2017In: Insect Biochemistry and Molecular Biology, ISSN 0965-1748, E-ISSN 1879-0240, Vol. 86, p. 9-19Article in journal (Refereed)
    Abstract [en]

    Neuropeptides are responsible for regulating a variety of functions, including development, metabolism, water and ion homeostasis, and as neuromodulators in circuits of the central nervous system. Numerous neuropeptides have been identified and characterized. However, both discovery and functional characterization of neuropeptides across the massive Class Insecta has been sporadic. To leverage advances in post-genomic technologies for this rapidly growing field, insect neuroendocrinology requires a consolidated, comprehensive and standardised resource for managing neuropeptide information. The Database for Insect Neuropeptide Research (DINeR) is a web-based database-application used for search and retrieval of neuropeptide information of various insect species detailing their isoform sequences, physiological functionality and images of their receptor-binding sites, in an intuitive, accessible and user-friendly format. The curated data includes representatives of 50 well described neuropeptide families from over 400 different insect species. Approximately 4700 FASTA formatted, neuropeptide isoform amino acid sequences and over 200 records of physiological functionality have been recorded based on published literature. Also available are images of neuropeptide receptor locations. In addition, the data include comprehensive summaries for each neuropeptide family, including their function, location, known functionality, as well as cladograms, sequence alignments and logos covering most insect orders. Moreover, we have adopted a standardised nomenclature to address inconsistent classification of neuropeptides. As part of the H2020 nEUROSTRESSPEP project, the data will be actively maintained and curated, ensuring a comprehensive and standardised resource for the scientific community. DINeR is publicly available at the project website: http://www.neurostresspep.eu/diner/.

  • 72. Yurgel, Maria E.
    et al.
    Kakad, Priyanka
    Zandawala, Meet
    Stockholm University, Faculty of Science, Department of Zoology.
    Nässel, Dick R.
    Stockholm University, Faculty of Science, Department of Zoology.
    Godenschwege, Tanja A.
    Keene, Alex C.
    A single pair of leucokinin neurons are modulated by feeding state and regulate sleep-metabolism interactions2019In: PLoS biology, ISSN 1544-9173, E-ISSN 1545-7885, Vol. 17, no 2, article id e2006409Article in journal (Refereed)
    Abstract [en]

    Dysregulation of sleep and feeding has widespread health consequences. Despite extensive epidemiological evidence for interactions between sleep and metabolic function, little is known about the neural or molecular basis underlying the integration of these processes. D. melanogaster potently suppress sleep in response to starvation, and powerful genetic tools allow for mechanistic investigation of sleep-metabolism interactions. We have previously identified neurons expressing the neuropeptide leucokinin (Lk) as being required for starvation-mediated changes in sleep. Here, we demonstrate an essential role for Lk neuropeptide in metabolic regulation of sleep. The activity of Lk neurons is modulated by feeding, with reduced activity in response to glucose and increased activity under starvation conditions. Both genetic silencing and laser-mediated microablation localize Lk-dependent sleep regulation to a single pair of Lk neurons within the Lateral Horn (LHLK neurons). A targeted screen identified a role for 50 adenosine monophosphate-activated protein kinase (AMPK) in starvation-modulated changes in sleep. Knockdown of AMPK in Lk neurons suppresses sleep and increases LHLK neuron activity in fed flies, phenocopying the starvation state. Further, we find a requirement for the Lk receptor in the insulin-producing cells (IPCs), suggesting LHLK-IPC connectivity is critical for sleep regulation under starved conditions. Taken together, these findings localize feeding-state-dependent regulation of sleep to a single pair of neurons within the fruit fly brain and provide a system for investigating the cellular basis of sleep-metabolism interactions.

  • 73.
    Zandawala, Meet
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Marley, Richard
    Davies, Shireen A.
    Nässel, Dick R.
    Stockholm University, Faculty of Science, Department of Zoology.
    Characterization of a set of abdominal neuroendocrine cells that regulate stress physiology using colocalized diuretic peptides in Drosophila2018In: Cellular and Molecular Life Sciences (CMLS), ISSN 1420-682X, E-ISSN 1420-9071, Vol. 75, no 6, p. 1099-1115Article in journal (Refereed)
    Abstract [en]

    Multiple neuropeptides are known to regulate water and ion balance in Drosophila melanogaster. Several of these peptides also have other functions in physiology and behavior. Examples are corticotropin-releasing factor-like diuretic hormone (diuretic hormone 44; DH44) and leucokinin (LK), both of which induce fluid secretion by Malpighian tubules (MTs), but also regulate stress responses, feeding, circadian activity and other behaviors. Here, we investigated the functional relations between the LK and DH44 signaling systems. DH44 and LK peptides are only colocalized in a set of abdominal neurosecretory cells (ABLKs). Targeted knockdown of each of these peptides in ABLKs leads to increased resistance to desiccation, starvation and ionic stress. Food ingestion is diminished by knockdown of DH44, but not LK, and water retention is increased by LK knockdown only. Thus, the two colocalized peptides display similar systemic actions, but differ with respect to regulation of feeding and body water retention. We also demonstrated that DH44 and LK have additive effects on fluid secretion by MTs. It is likely that the colocalized peptides are coreleased from ABLKs into the circulation and act on the tubules where they target different cell types and signaling systems to regulate diuresis and stress tolerance. Additional targets seem to be specific for each of the two peptides and subserve regulation of feeding and water retention. Our data suggest that the ABLKs and hormonal actions are sufficient for many of the known DH44 and LK functions, and that the remaining neurons in the CNS play other functional roles.

  • 74.
    Zandawala, Meet
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Yurgel, Maria E.
    Texada, Michael J.
    Liao, Sifang
    Stockholm University, Faculty of Science, Department of Zoology.
    Rewitz, Kim F.
    Keene, Alex C.
    Nässel, Dick R.
    Stockholm University, Faculty of Science, Department of Zoology.
    Modulation of Drosophila post-feeding physiology and behavior by the neuropeptide leucokinin2018In: PLoS Genetics, ISSN 1553-7390, E-ISSN 1553-7404, Vol. 14, no 11, article id e1007767Article in journal (Refereed)
    Abstract [en]

    Behavior and physiology are orchestrated by neuropeptides acting as central neuromodulators and circulating hormones. An outstanding question is how these neuropeptides function to coordinate complex and competing behaviors. In Drosophila, the neuropeptide leucokinin (LK) modulates diverse functions, but mechanisms underlying these complex interactions remain poorly understood. As a first step towards understanding these mechanisms, we delineated LK circuitry that governs various aspects of post-feeding physiology and behavior. We found that impaired LK signaling in Lk and Lk receptor (Lkr) mutants affects diverse but coordinated processes, including regulation of stress, water homeostasis, feeding, locomotor activity, and metabolic rate. Next, we sought to define the populations of LK neurons that contribute to the different aspects of this physiology. We find that the calcium activity in abdominal ganglia LK neurons (ABLKs), but not in the two sets of brain neurons, increases specifically following water consumption, suggesting that ABLKs regulate water homeostasis and its associated physiology. To identify targets of LK peptide, we mapped the distribution of Lkr expression, mined a brain single-cell transcriptome dataset for genes coexpressed with Lkr, and identified synaptic partners of LK neurons. Lkrexpression in the brain insulin-producing cells (IPCs), gut, renal tubules and chemosensory cells, correlates well with regulatory roles detected in the Lkand Lkr mutants. Furthermore, these mutants and flies with targeted knockdown of Lkr in IPCs displayed altered expression of insulin-like peptides (DILPs) and transcripts in IPCs and increased starvation resistance. Thus, some effects of LK signaling appear to occur via DILP action. Collectively, our data suggest that the three sets of LK neurons have different targets, but modulate the establishment of postprandial homeostasis by regulating distinct physiological processes and behaviors such as diuresis, metabolism, organismal activity and insulin signaling. These findings provide a platform for investigating feeding-related neuroendocrine regulation of vital behavior and physiology.

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