A biphasic locomotor response to acute unsignaled high temperature exposure in Drosophila

Ostrowski, Daniela; Salari, Autoosa; Zars, Melissa; Zars, Troy

doi:10.1371/journal.pone.0198702

Cited by 7 publications

(3 citation statements)

References 31 publications

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“…In agreement with previous studies, this work shows that exposition of flies only to heat shock reduces the locomotor activity, but fasting and electric shock increases the motor behavior (Bell et al, 1985;Mohammad et al, 2016a;Ostrowski et al, 2018). However, this study contradicts previous reports which showed that isolation reduced the exploratory behavior of adult flies (Araujo et al, 2018;Neckameyer and Nieto-Romero, 2015).…”

Section: Discussionsupporting

confidence: 89%

Stress-mediated hyperactivity and anhedonia resistant to diazepam and fluoxetine in drosophila

Ramos-Hryb

Ramírez

Oliveira

et al. 2020

Stress

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Distresses may induce behavioral phenotypes constituting heuristic models for psychopharmacology studies. In several species, including Drosophila, antidepressants counteract stress-induced phenotypes allowing the use of these models to test new psychoactive drugs. Here, we developed a novel and time-efficient protocol to provoke stress-induced phenotypes in Drosophila for the study of psychopharmacological agents. In the first experiment, flies (n=12/groups) were exposed to a random-sequence of different types of stresses during nearly 24 h (including social isolation, fasting, heat, and electric shock), a protocol named short-term variable stress (SVS). Second, flies were exposed to a single stressful stimulus (social isolation, fasting, heat shock or electric shock, n=12/groups). Next, flies submitted to SVS protocol were treated with vehicle, diazepam or fluoxetine (n=12/groups). At the end of the stress protocols, behavioral phenotypes were evaluated in the open field (OF) and sucrose preference tests. In comparison to the unstressed group, flies exposed to SVS exhibited hyperactivity, as well as shorter times exploring the boundaries of the OF.In contrast to fasting stress, SVS reduced sucrose preference in flies. By analyzing the effects of individual stimuli on fly behavior, fasting and electric shock appear to be the predominant influences on the SVS-induced behaviors. Although fluoxetine or diazepam reduced the initial locomotor activity of flies, no treatment prevented the sequelae of SVS. Altogether, this study provides a timeefficient model system for the study of stress-mediated hyperactivity and anhedonia-like state resistant to fluoxetine and diazepam. The applications of SVS in Drosophila to preclinical psychopharmacology require further studies.

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Section: Discussionsupporting

confidence: 89%

Stress-mediated hyperactivity and anhedonia resistant to diazepam and fluoxetine in drosophila

Ramos-Hryb

Ramírez

Oliveira

et al. 2020

Stress

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“…There was a general increase in locomotor activity of all flies with increase in temperature and decrease in activity following the sudden decrease in temperature to 24°C. These phenomena have been observed previously and are well documented [152]. Additionally, the median number of approaches and hot side dwells of R58E02-GAL4>UAS-Gr28bD flies that were trained at 38 or 40°C were significantly lower than those trained at 36°C (Mann-Whitney U test, p<0.019).…”

Section: Activity Testsupporting

confidence: 84%

Identification, characterization and use of novel thermogenetic tools in drosophilia melanogaster

Mishra¹

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Extrinsic control of neural activity is necessary to decipher the neural mechanisms underlying behavior. Molecular tools that employ light (optogenetics) or temperature (thermogenetics) are primarily used for extrinsic manipulation of neurons. While the available tools offer precise temporal and spatial resolution, their caveats lie in the limited number of tools that can be used simultaneously to alter neuronal activity. The overlapping spectrum of activation of optogenetic tools prevents their simultaneous use in preparations. Similarly, the lack of thermogenetic tools that can function in the physiological range of organisms has restricted their use. The use of thermogenetic tools is limited to two members from the Transient receptor family of proteins, TrpA1 and TrpM8 to activate neurons, and one protein that reduces synaptic output, Shibirets. A major drawback to the Trp channels is their response to both temperature and voltage changes. Hence, the discovery of a new temperature sensitive Gustatory Receptor protein provided an opportunity to mine for other temperature sensitive proteins and develop novel thermogenetic tools. In this thesis we report the identification of several thermosensitive proteins, their characterization, and use in studying the learning and memory of freely moving flies. In the first chapter, we probed several Gustatory receptors for their temperature sensitivity using the heat box. The heat box is a high throughput system that enables us to test and track the behavior of single flies in response to temperature. The top and bottom of heat box chamber has Peltier elements that allow for control of temperature with a resolution of 1[degrees]C. We overexpressed several Gustatory receptors one at a time pan neuronally in Drosophila melanogaster and exposed them to various assays. Our initials results imply that at least 2 Drosophila melanogaster Gustatory receptors other than Gr28bD are temperature sensitive. To increase the repertoire of thermosensitive proteins, we assayed for temperature response properties of Gr28bD orthologs from 5 other Drosophila species that occupy different habitats in the world. We rationalized that flies in different habitats will have Gr28bD orthologs with unique temperature response properties designed to sustain in that habitat. Of the 5 proteins we tested, we found that 4 proteins are temperature sensitive at different temperatures. While pan-neuronal overexpression is a robust method to determine the temperature responsiveness of a protein, it does not recapitulate the natural environment the protein is present in. In D. melanogaster, Gr28bD is present in specialized heat sensing cells in the antenna, called Hot Cells. There are 3 Hot cells on each of the two antennae. There is however no physiological information on the where the orthologs are expressed. Since Gr28bD is used for rapid heat avoidance in flies, we rationalized that its orthologs too sever a similar function in their host species and are expressed in the peripheral regions. Hence, in the second chapter, we tested for the avoidance behavior of flies using two choice assays. We made mutant flies that lacked Gr28b proteins, including Gr28bD in the antennae. We then examined the ability of the orthologs to rescue the heat avoidance behavior in these mutants. We found that all the orthologs respond to temperature differences albeit, at different temperatures. Above a threshold temperature, flies rescued with some orthologs could not differentiate between small temperature differences, suggesting that the activity of the orthologs might saturate beyond certain temperatures. Some homologs responded to temperature only when expressed in Hot Cells, thus leading us to examine the presence of accessory proteins it the hot cells that might be enhancing the thermosensitive properties of these homologs. We found several candidate proteins that can studied further to determine their role in the temperature sensing in the hot cells. When used as thermogenetic tools, thermosensitive proteins are in localized environments in small cluster of cells. In the third chapter, we expressed Gr28bD in small clusters of dopaminergic neurons in the fly brain with an aim to understand the role of activation of dopaminergic neurons in operant place learning and memory paradigm. In addition to examining their learning scores at different temperatures, we investigated other behaviors of the flies during the training. Contrary to previous results from our lab that showed that dopaminergic neurons are not important for place learning and memory, we found that activation of a specific subset of dopaminergic neurons does alter place learning and memory. Our findings new laid the groundwork for more experiments to investigate dopaminergic modulation of place learning and memory.

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“…There is also evidence that thermal stress has a significant negative impact on organismal energy reserves in D . melanogaster 53 , and that exposure to acute high temperatures increases both locomotor activity and metabolic rate, whereas starvation and cold exposure lead to reductions in both 54–56 . Combined with the notable observation from the current study that mtDNA CN is reduced with age in males but not in females this suggests that differences in metabolic demand and efficiency in male and female flies is key to understand sexual dimorphism in lifespan and trait specific and sex dependent responses to aging.…”

Section: Discussionmentioning

confidence: 99%

Sex and age specific reduction in stress resistance and mitochondrial DNA copy number in Drosophila melanogaster

Kristensen

Loeschcke

Tan

et al. 2019

Sci Rep

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Environmental stresses such as extreme temperatures, dehydration and food deprivation may have distinct consequences for different age-classes and for males and females across species. Here we investigate a natural population of the model organism Drosophila melanogaster . Males and females at ages 3, 19 and 35 days were tested for stress resistance; i.e. the ability of flies to cope with starvation and both cold and hot temperatures. Further, we tested a measure of metabolic efficiency, namely mitochondrial DNA copy number (mtDNA CN) in both sexes at all three age-classes. We hypothesize that stress resistance is reduced at old age and more so in males, and that mtDNA CN is a biomarker for sex- and age-dependent reductions in the ability to cope with harsh environments. We show that: (1) males exhibit reduced starvation tolerance at old age, whereas older females are better in coping with periods without food compared to younger females, (2) heat tolerance decreases with increasing age in males but not in females, (3) cold tolerance is reduced at old age in both sexes, and (4) old males have reduced mtDNA CN whereas mtDNA CN slightly increases with age in females. In conclusion, our data provide strong evidence for trait and sex specific consequences of aging with females generally being better at coping with environmental stress at old age. The reduced mtDNA CN in old males suggests reduced metabolic efficiency and this may partly explain why males are less stress tolerant at old age than females. We suggest that mtDNA CN might be a suitable biomarker for physiological robustness. Our findings likely extend to other taxa than Drosophila and therefore we discuss the observations in relation to aging and sex specific lifespan across species.

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A biphasic locomotor response to acute unsignaled high temperature exposure in Drosophila

Cited by 7 publications

References 31 publications

Stress-mediated hyperactivity and anhedonia resistant to diazepam and fluoxetine in drosophila

Stress-mediated hyperactivity and anhedonia resistant to diazepam and fluoxetine in drosophila

Identification, characterization and use of novel thermogenetic tools in drosophilia melanogaster

Sex and age specific reduction in stress resistance and mitochondrial DNA copy number in Drosophila melanogaster

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