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Aggression is associated with aerobic glycolysis in the honey bee brain(1).

ABSTRACT: Aerobic glycolysis involves increased glycolysis and decreased oxidative catabolism of glucose even in the presence of an ample oxygen supply. Aerobic glycolysis, a common metabolic pattern in cancer cells, was recently discovered in both the healthy and diseased human brain, but its functional significance is not understood. This metabolic pattern in the brain is surprising because it results in decreased efficiency of adenosine triphosphate (ATP) production in a tissue with high energetic demands. We report that highly aggressive honey bees (Apis mellifera) show a brain transcriptomic and metabolic state consistent with aerobic glycolysis, i.e. increased glycolysis in combination with decreased oxidative phosphorylation. Furthermore, exposure to alarm pheromone, which provokes aggression, causes a metabolic shift to aerobic glycolysis in the bee brain. We hypothesize that this metabolic state, which is associated with altered neurotransmitter levels, increased glycolytically derived ATP and a reduced cellular redox state, may lead to increased neuronal excitability and oxidative stress in the brain. Our analysis provides evidence for a robust, distinct and persistent brain metabolic response to aggression-inducing social cues. This finding for the first time associates aerobic glycolysis with naturally occurring behavioral plasticity, which has important implications for understanding both healthy and diseased brain function.

SUBMITTER: Chandrasekaran S

PROVIDER: S-EPMC4449359 | biostudies-literature | 2015 Feb

REPOSITORIES: biostudies-literature

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Aggression is associated with aerobic glycolysis in the honey bee brain(1).

Chandrasekaran S S Rittschof C C CC Djukovic D D Gu H H Raftery D D Price N D ND Robinson G E GE

Genes, brain, and behavior 20150201 2

Aerobic glycolysis involves increased glycolysis and decreased oxidative catabolism of glucose even in the presence of an ample oxygen supply. Aerobic glycolysis, a common metabolic pattern in cancer cells, was recently discovered in both the healthy and diseased human brain, but its functional significance is not understood. This metabolic pattern in the brain is surprising because it results in decreased efficiency of adenosine triphosphate (ATP) production in a tissue with high energetic dema ...[more]

PMID: 25640316

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Project description:Background: Aggression is influenced by individual variation in temperament as well as behavioral plasticity in response to adversity. DNA methylation is stably maintained over time, but also reversible in response to specific environmental conditions, and may thus be a neuromolecular regulator of both of these processes. A previous study reported DNA methylation differences between aggressive Africanized and gentle European honey bees. We investigated whether threat-induced aggression altered DNA methylation profiles in the honey bee brain in response to a behavioral stimulus (aggression-provoking intruder bee or inert control). We sampled five minutes and two hours after stimulus exposure to examine the effect of time on epigenetic profiles of aggression. Results: There were DNA methylation differences between aggressive and control bees for individual cytosine-guanine dinucleotides (CpGs) across the genome. Eighteen individual CpG sites showed significant difference between aggressive and control bees 120 minutes post stimulus. For clusters of CpGs, we report four genomic regions differentially methylated between aggressive and control bees at the 5-minute time point, and 50 regions differentially methylated at the120-minute time point following intruder exposure. Differential methylation occurred at genes involved in neural plasticity, chromatin remodeling and hormone signaling. Additionally, there was a significant overlap of differential methylation with previously published epigenetic differences that distinguish aggressive Africanized and gentle European honey bees, suggesting an evolutionarily conserved use of brain DNA methylation in the regulation of aggression. Lastly, we identified individually statistically suggestive CpGs that as a group were significantly associated with differentially expressed genes underlying aggressive behavior and also co-localize with binding sites of transcription factors involved in neuroplasticity or neurodevelopment. Conclusions: There were DNA methylation differences in the brain associated with response to an intruder. These differences increased in number a few hours after the initial exposure and overlap with previously reported aggression-associated genes and neurobiologically relevant transcription factor binding sites. Many DNA methylation differences that occurred in association with the expression of aggression in real time also exist between Africanized bees and European bees, suggesting an evolutionarily conserved role for epigenetic regulation in aggressive behavior.

Project description:BackgroundAggression is influenced by individual variation in temperament as well as behavioral plasticity in response to adversity. DNA methylation is stably maintained over time, but also reversible in response to specific environmental conditions, and may thus be a neuromolecular regulator of both of these processes. A previous study reported DNA methylation differences between aggressive Africanized and gentle European honey bees. We investigated whether threat-induced aggression altered DNA methylation profiles in the honey bee brain in response to a behavioral stimulus (aggression-provoking intruder bee or inert control). We sampled five minutes and two hours after stimulus exposure to examine the effect of time on epigenetic profiles of aggression.ResultsThere were DNA methylation differences between aggressive and control bees for individual cytosine-guanine dinucleotides (CpGs) across the genome. Eighteen individual CpG sites showed significant difference between aggressive and control bees 120 min post stimulus. For clusters of CpGs, we report four genomic regions differentially methylated between aggressive and control bees at the 5-min time point, and 50 regions differentially methylated at the120-minute time point following intruder exposure. Differential methylation occurred at genes involved in neural plasticity, chromatin remodeling and hormone signaling. Additionally, there was a significant overlap of differential methylation with previously published epigenetic differences that distinguish aggressive Africanized and gentle European honey bees, suggesting an evolutionarily conserved use of brain DNA methylation in the regulation of aggression. Lastly, we identified individually statistically suggestive CpGs that as a group were significantly associated with differentially expressed genes underlying aggressive behavior and also co-localize with binding sites of transcription factors involved in neuroplasticity or neurodevelopment.ConclusionsThere were DNA methylation differences in the brain associated with response to an intruder. These differences increased in number a few hours after the initial exposure and overlap with previously reported aggression-associated genes and neurobiologically relevant transcription factor binding sites. Many DNA methylation differences that occurred in association with the expression of aggression in real time also exist between Africanized bees and European bees, suggesting an evolutionarily conserved role for epigenetic regulation in aggressive behavior.

Dataset Information

Aggression is associated with aerobic glycolysis in the honey bee brain(1).

Publications

Aggression is associated with aerobic glycolysis in the honey bee brain(1).

Similar Datasets

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