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  • 1.
    Liao, Sifang
    Stockholm University, Faculty of Science, Department of Zoology.
    The role of insulin signaling during development, reproductive diapause and aging in Drosophila Melanogaster2018Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    The insulin/insulin-like growth factor signaling pathway exists from invertebrates to vertebrates and it can regulate various biological processes, including development, metabolism, stress resistance and lifespan. In Drosophila, eight insulin-like peptides (DILP1-8) have been found. The specific function of each DILP is not fully known, especially for DILP1. In paper I, we found that dilp1 is specifically expressed in the brain insulin producing cells (IPCs), and it is mainly expressed from early pupa until few days of adult life, which correspond to non-feeding stages. The expression of dilp1 can last for at least 9 weeks of adult life when newborn virgin flies are induced to enter reproductive diapause. In addition, we found that the expression of dilp1 is under regulation by other dilps. Also larva-derived fat body, short neuropeptide F (sNPF) and juvenile hormone can affect dilp1 expression. We found that mutation of dilp1 affects female reproduction and starvation resistance. In paper II, we found that reproductive diapause can extend Drosophila life span, and at the same time ameliorate behavioral senescence, including negative geotaxis, activity rhythms and exploratory walking. Age-related changes in neuromuscular junction (NMJ) in abdominal muscle cannot be found in diapause-induced aging flies. The levels of several neuromodulators in the brain, including pigment dispersion factor (PDF), tyrosine hydroxylase (TH) and short neuropeptide F (sNPF), decreased significantly in normally aging flies, but less so in diapausing flies. In paper III, we show that mutation of dilp1 leads to a reduced organismal bodyweight, whereas overexpression increases it during the nonfeeding pupal stage. Overexpression of dilp1 additionally increases body size of flies, but reduces stores of larval-derived energy. This results in decreased starvation tolerance and increased feeding in newborn flies. In paper IV, we found that dilp1 expression is needed to extend lifespan in dilp2 mutant flies. Single dilp1 mutation has no effect on female lifespan, whereas transgene expression of dilp1 in flies with dilp1-dilp2 double mutant genetic background increased the lifespan. Furthermore, dilp1 and dilp2 interact to control circulating sugar, starvation resistance in a redundant or synergistic way.

  • 2.
    Liao, Sifang
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Broughton, Susan
    Nässel, Dick R.
    Stockholm University, Faculty of Science, Department of Zoology.
    Behavioral Senescence and Aging-Related Changes in Motor Neurons and Brain Neuromodulator Levels Are Ameliorated by Lifespan-Extending Reproductive Dormancy in Drosophila2017In: Frontiers in Cellular Neuroscience, ISSN 1662-5102, E-ISSN 1662-5102, Vol. 11, article id 111Article in journal (Refereed)
    Abstract [en]

    The lifespan of Drosophila melanogaster can be extended substantially by inducing reproductive dormancy (also known as diapause) by lowered temperature and short days. This increase of longevity is accompanied by lowered metabolism and increased stress tolerance. We ask here whether behavioral senescence is ameliorated during adult dormancy. To study this we kept flies for seven or more weeks in normal rearing conditions or in diapause conditions and compared to 1-week-old flies in different behavioral assays of sleep, negative geotaxis and exploratory walking. We found that the senescence of geotaxis and locomotor behavior seen under normal rearing conditions was negligible in flies kept in dormancy. The normal senescence of rhythmic activity and sleep patterns during the daytime was also reduced by adult dormancy. Investigating the morphology of specific neuromuscular junctions (NMJs), we found that changes normally seen with aging do not take place in dormant flies. To monitor age-associated changes in neuronal circuits regulating activity rhythms, sleep and walking behavior we applied antisera to tyrosine hydroxylase (TH), serotonin and several neuropeptides to examine changes in expression levels and neuron morphology. In most neuron types the levels of stored neuromodulators decreased during normal aging, but not in diapause treated flies. No signs of neurodegeneration were seen in either condition. Our data suggest that age-related changes in motor neurons could be the cause of part of the behavioral senescence and that this is ameliorated by reproductive diapause. Earlier studies established a link between age-associated decreases in neuromodulator levels and behavioral decline that could be rescued by overexpression of neuromodulator. Thus, it is likely that the retained levels of neuromodulators in dormant flies alleviate behavioral senescence.

  • 3.
    Liao, Sifang
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Post, Stephanie
    A. Veenstra, Jan
    Tatar, Marc
    Nässel, Dick
    Stockholm University, Faculty of Science, Department of Zoology.
    Drosophila insulin-like peptide 1 (DILP1) promotes organismal growth during non-feeding stagesManuscript (preprint) (Other academic)
  • 4.
    Liu, Yiting
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Liao, Sifang
    Stockholm University, Faculty of Science, Department of Zoology.
    Veenstra, Jan A.
    Nässel, Dick R.
    Stockholm University, Faculty of Science, Department of Zoology.
    Drosophila insulin-like peptide 1 (DILP1) is transiently expressed during non-feeding stages and reproductive dormancy2016In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 6, article id 26620Article in journal (Refereed)
    Abstract [en]

    The insulin/insulin-like growth factor signaling pathway is evolutionarily conserved in animals, and is part of nutrient-sensing mechanisms that control growth, metabolism, reproduction, stress responses, and lifespan. In Drosophila, eight insulin-like peptides (DILP1-8) are known, six of which have been investigated in some detail, whereas expression and functions of DILP1 and DILP4 remain enigmatic. Here we demonstrate that dilp1/DILP1 is transiently expressed in brain insulin producing cells (IPCs) from early pupa until a few days of adult life. However, in adult female flies where diapause is triggered by low temperature and short days, within a time window 0-10h post-eclosion, the dilp1/DILP1 expression remains high for at least 9 weeks. The dilp1 mRNA level is increased in dilp2, 3, 5 and dilp6 mutant flies, indicating feedback regulation. Furthermore, the DILP1 expression in IPCs is regulated by short neuropeptide F, juvenile hormone and presence of larval adipocytes. Male dilp1 mutant flies display increased lifespan and reduced starvation resistance, whereas in female dilp1 mutants oviposition is reduced. Thus, DILP1 is expressed in non-feeding stages and in diapausing flies, is under feedback regulation and appears to play sex-specific functional roles.

  • 5. 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)
  • 6. 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.

  • 7.
    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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