Natural Variation in the Thermotolerance of Neural Function and Behavior due to a cGMP-Dependent Protein Kinase

Dawson‐Scully, Ken; Armstrong, Gary A. B.; Kent, Clement F.; Robertson, R. Meldrum; Sokolowski, Marla B.

doi:10.1371/journal.pone.0000773

Cited by 56 publications

(65 citation statements)

References 33 publications

(46 reference statements)

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“…In locusts, in addition to the high PKG activity reported here, the gregarious phase is characterized by high levels of lipid reserves, higher hiperlipaemic response to flight, and increased adipokinetic response (mediated by CC neurohormones; Pener, 1992, 1995;Ayali et al, 1996;Pener et al, 1997). PKG signaling also plays a role in modulating environmental stresses, such as thermal stress (in D. melanogaster, Dawson-Scully et al, 2007). Phase differences are also related to thermotolerance in locusts, including, for example, expression of heat shock proteins (Wang et al, 2007) and response to pathogens (Elliot et al, 2003(Elliot et al, , 2005.…”

Section: Discussionmentioning

confidence: 74%

The locust foraging gene

Lucas

Kornfein

Chakaborty-Chatterjee

et al. 2010

Arch Insect Biochem Physiol

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Our knowledge of how genes act on the nervous system in response to the environment to generate behavioral plasticity is limited. A number of recent advancements in this area concern food-related behaviors and a specific gene family called foraging (for), which encodes a cGMPdependent protein kinase (PKG). The desert locust (Schistocerca gregaria) is notorious for its destructive feeding and long-term migratory behavior. Locust phase polyphenism is an extreme example of environmentally induced behavioral plasticity. In response to changes in population density, locusts dramatically alter their behavior, from solitary and relatively sedentary behavior to active aggregation and swarming. Very little is known about the molecular and genetic basis of this striking behavioral phenomenon. Here we initiated studies into the locust for gene by identifying, cloning, and studying expression of the gene in the locust brain. We determined the phylogenetic relationships between the locust PKG and other known PKG proteins in insects. FOR expression was found to be confined to neurons of the anterior midline of the brain, the pars intercerebralis. Our results suggest that differences in PKG enzyme activity are correlated to well-established phase-related behavioral differences. These results lay the groundwork for functional studies of the locust for gene and its possible relations to locust phase polyphenism.

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Section: Discussionmentioning

confidence: 74%

The locust foraging gene

Lucas

Kornfein

Chakaborty-Chatterjee

et al. 2010

Arch Insect Biochem Physiol

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“…Pharmacologically or genetically reducing levels of PKG, or its downstream targets, increases thermotolerance of the larval Drosophila neuromuscular junction. Similar treatments also increase the locust vCPG's tolerance to heat stress (Dawson-Scully et al, 2007), suggesting evolutionary conservation of the mechanism. Hyperthermic arrest of vCPG operation in the locust CNS is associated with SDlike increases of [K ϩ ] o that occur before irreversible cellular collapse (Rodgers et al, 2007).…”

Section: Introductionmentioning

confidence: 80%

Suppression of Spreading Depression-Like Events in Locusts by Inhibition of the NO/cGMP/PKG Pathway

Armstrong¹,

Rodgers²,

Money³

et al. 2009

Journal of Neuroscience

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Despite considerable research attention focused on mechanisms underlying neural spreading depression (SD), because of its association with important human CNS pathologies, such as stroke and migraine, little attention has been given to explaining its occurrence and regulation in invertebrates. In the locust metathoracic ganglion (MTG), an SD-like event occurs during heat and anoxia stress, which results in cessation of neuronal output for the duration of the applied stress. SD-like events were characterized by an abrupt rise in extracellular potassium ion concentration ([K ϩ ] o ) from a baseline concentration of ϳ8 to Ͼ30 mM, which returned to near baseline concentrations after removal of the applied stress. After return to baseline [K ϩ ] o , neuronal output (ventilatory motor pattern activity) from the MTG recovered. Unlike mammalian neurons, which depolarize almost completely during SD, locust neurons only partially depolarized. SD-like events in the locust CNS were suppressed by pharmacological inhibition of the nitric oxide/cyclic guanosine monophosphate/protein kinase G (NO/cGMP/PKG) pathway and were exacerbated by its activation. Also, environmental stressors such as heat and anoxia increased production of nitric oxide in the locust CNS. Finally, for the intact animal, manipulation of the pathway affected the speed of recovery from suffocation by immersion under water. We propose that SD-like events in locusts provide an adaptive mechanism for surviving extreme environmental conditions. The highly conserved nature of the NO/cGMP/PKG signaling pathway suggests that it may be involved in modulating SD in other organisms, including mammals.

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“…Are sitters more plastic than rovers across environmental contexts, or does it depend on the type of adversity (e.g., nutritional, social) the individual experiences, and the timing of that adversity (chronic acute) during development? Previous studies have shown that sitters are more resistant to acute abiotic stressors, such as heat and hypoxia, than are rovers (69)(70)(71). The type of exposure used, chronic or acute, may explain which variant exhibits plasticity.…”

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confidence: 99%

Gene–environment interplay inDrosophila melanogaster: Chronic food deprivation in early life affects adult exploratory and fitness traits

Burns

Svetec

Rowe

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Early life adversity has known impacts on adult health and behavior, yet little is known about the gene-environment interactions (GEIs) that underlie these consequences. We used the fruit fly Drosophila melanogaster to show that chronic early nutritional adversity interacts with rover and sitter allelic variants of foraging (for) to affect adult exploratory behavior, a phenotype that is critical for foraging, and reproductive fitness. Chronic nutritional adversity during adulthood did not affect rover or sitter adult exploratory behavior; however, early nutritional adversity in the larval period increased sitter but not rover adult exploratory behavior. Increasing for gene expression in the mushroom bodies, an important center of integration in the fly brain, changed the amount of exploratory behavior exhibited by sitter adults when they did not experience early nutritional adversity but had no effect in sitters that experienced early nutritional adversity. Manipulation of the larval nutritional environment also affected adult reproductive output of sitters but not rovers, indicating GEIs on fitness itself. The natural for variants are an excellent model to examine how GEIs underlie the biological embedding of early experience.genotype-environment interaction | plasticity T he question of how individual differences arise is fundamental to biology, psychology, and precision medicine (1, 2). From studies on mammals, we know that early adversity places individuals on developmental trajectories for health and behavior that can last a lifetime (3, 4). However, for the most part, this idea has not been investigated in simple model genetic organisms, such as the worm Caenorhabditis elegans or the fruit fly Drosophila melanogaster, in which gene manipulation can be readily accomplished. Two biological mechanisms that can underlie individual differences, and that go beyond the obsolete notion of nature or nurture, are gene-environment interactions (GEIs) and epigenetics. Here, we explore GEIs in the context of early adversity. In particular, we address how early adversity interacts with natural variants of the foraging (for) gene to affect adult behavior and fitness in D. melanogaster.Within human populations, nutritional adversity can lead to substantive effects on cognitive and behavioral development (5, 6). The question of how early adversities perturb normal development is a difficult one, because both the strength and timing of adversity can matter. For example, in humans, detrimental effects are seen after chronic protein or carbohydrate deprivation, yet one or a few acute deprivations have little long-term effect (7). Similarly, in fruit flies, levels of hemolymph carbohydrate affected by 3 h of food deprivation return to normal levels after just 2 h of refeeding (8). Moreover, not all individuals are affected equally by early nutritional adversity (9, 10), and these individual differences arise from GEIs.In evolutionary biology, GEIs can be important for the maintenance and expression of both phenotypic plasticit...

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Natural Variation in the Thermotolerance of Neural Function and Behavior due to a cGMP-Dependent Protein Kinase

Cited by 56 publications

References 33 publications

The locust foraging gene

The locust foraging gene

Suppression of Spreading Depression-Like Events in Locusts by Inhibition of the NO/cGMP/PKG Pathway

Gene–environment interplay inDrosophila melanogaster: Chronic food deprivation in early life affects adult exploratory and fitness traits

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