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Corazonin neurons function in sexually dimorphic circuitry that shape behavioral responses to stress in Drosophila.

Zhao Y, Bretz CA, Hawksworth SA, Hirsh J, Johnson EC - PLoS ONE (2010)

Bottom Line: Silencing and activation of corazonin neurons lead to differential lifespan under stress, and these effects showed a strong dependence on sex.Additionally, altered corazonin neuron physiology leads to fundamental differences in locomotor activity, and these effects were also sex-dependent.These results underscore the importance of central peptidergic processing within the context of stress and place corazonin signaling as a critical feature of neuroendocrine events that shape stress responses and may underlie the inherent sexual dimorphic differences in stress responses.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Wake Forest University, Winston-Salem, North Carolina, United States of America.

ABSTRACT
All organisms are confronted with dynamic environmental changes that challenge homeostasis, which is the operational definition of stress. Stress produces adaptive behavioral and physiological responses, which, in the Metazoa, are mediated through the actions of various hormones. Based on its associated phenotypes and its expression profiles, a candidate stress hormone in Drosophila is the corazonin neuropeptide. We evaluated the potential roles of corazonin in mediating stress-related changes in target behaviors and physiologies through genetic alteration of corazonin neuronal excitability. Ablation of corazonin neurons confers resistance to metabolic, osmotic, and oxidative stress, as measured by survival. Silencing and activation of corazonin neurons lead to differential lifespan under stress, and these effects showed a strong dependence on sex. Additionally, altered corazonin neuron physiology leads to fundamental differences in locomotor activity, and these effects were also sex-dependent. The dynamics of altered locomotor behavior accompanying stress was likewise altered in flies with altered corazonin neuronal function. We report that corazonin transcript expression is altered under starvation and osmotic stress, and that triglyceride and dopamine levels are equally impacted in corazonin neuronal alterations and these phenotypes similarly show significant sexual dimorphisms. Notably, these sexual dimorphisms map to corazonin neurons. These results underscore the importance of central peptidergic processing within the context of stress and place corazonin signaling as a critical feature of neuroendocrine events that shape stress responses and may underlie the inherent sexual dimorphic differences in stress responses.

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Locomotor activity is differentially affected by corazonin neuron function and sex.A: Locomotion was monitored for three 12∶12 LD cycles on flies expressing different transgenes in corazonin neurons. Raw data are means +/− SEM from three replicate experiments. Records begin at lights on (ZT0). B: Quantification of total locomotion. Mean amount of locomotion per ten minute bins were estimated for the genotypes listed plotted with 95% confidence intervals are plotted from three independent experiments. Different letters denote statistical significance from each other (Tukey post-hoc test p<0.05). Locomotor values from females are designated in red, males in blue, and for animals with feminized corazonin neurons are indicated in yellow. Animals in the first group have wild-type corazonin neuronal function (w1118), the second grouping are expressing NaChBac in corazonin neurons (Activation) and the third grouping are expressing the ork channel in corazonin neurons (Silencing).
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pone-0009141-g003: Locomotor activity is differentially affected by corazonin neuron function and sex.A: Locomotion was monitored for three 12∶12 LD cycles on flies expressing different transgenes in corazonin neurons. Raw data are means +/− SEM from three replicate experiments. Records begin at lights on (ZT0). B: Quantification of total locomotion. Mean amount of locomotion per ten minute bins were estimated for the genotypes listed plotted with 95% confidence intervals are plotted from three independent experiments. Different letters denote statistical significance from each other (Tukey post-hoc test p<0.05). Locomotor values from females are designated in red, males in blue, and for animals with feminized corazonin neurons are indicated in yellow. Animals in the first group have wild-type corazonin neuronal function (w1118), the second grouping are expressing NaChBac in corazonin neurons (Activation) and the third grouping are expressing the ork channel in corazonin neurons (Silencing).

Mentions: We reasoned that the alterations in lifespan exhibited in flies differing in corazonin neuronal function may, in part, stem from changes in activity levels as activity may correlate with stress-sensitivity. We measured activity levels in flies that varied in corazonin neuronal function under a normal 12∶12 LD lighting regime. We found that the overall amount of activity levels of w1118 males and females were different from each other, consistent with previous observations [27]. However, there was a significant impact on activity levels that were influenced by sex and the specific alteration to corazonin neuronal function. Specifically, males expressing the Δork channel in corazonin neurons displayed greater activity levels than w1118 males. Furthermore, the opposite manipulation (NaChBac introduction) produced hypoactive males relative to w1118 (Figure 3A). Both of these phenotypes were not evident in females, where both manipulations produced activity levels indistinguishable from parental genotypes (Figure S3). Ablation of corazonin neurons produced activity levels slightly lower than w1118 levels for both males and females (Figure 3A). While we predicted that the ablation and silencing phenotypes would be similar for males, this inconsistent finding may be attributable to either differences in transgene impact (silencing is incomplete as compared to ablation) or developmental or physiological compensation in animals lacking corazonin neurons.


Corazonin neurons function in sexually dimorphic circuitry that shape behavioral responses to stress in Drosophila.

Zhao Y, Bretz CA, Hawksworth SA, Hirsh J, Johnson EC - PLoS ONE (2010)

Locomotor activity is differentially affected by corazonin neuron function and sex.A: Locomotion was monitored for three 12∶12 LD cycles on flies expressing different transgenes in corazonin neurons. Raw data are means +/− SEM from three replicate experiments. Records begin at lights on (ZT0). B: Quantification of total locomotion. Mean amount of locomotion per ten minute bins were estimated for the genotypes listed plotted with 95% confidence intervals are plotted from three independent experiments. Different letters denote statistical significance from each other (Tukey post-hoc test p<0.05). Locomotor values from females are designated in red, males in blue, and for animals with feminized corazonin neurons are indicated in yellow. Animals in the first group have wild-type corazonin neuronal function (w1118), the second grouping are expressing NaChBac in corazonin neurons (Activation) and the third grouping are expressing the ork channel in corazonin neurons (Silencing).
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2818717&req=5

pone-0009141-g003: Locomotor activity is differentially affected by corazonin neuron function and sex.A: Locomotion was monitored for three 12∶12 LD cycles on flies expressing different transgenes in corazonin neurons. Raw data are means +/− SEM from three replicate experiments. Records begin at lights on (ZT0). B: Quantification of total locomotion. Mean amount of locomotion per ten minute bins were estimated for the genotypes listed plotted with 95% confidence intervals are plotted from three independent experiments. Different letters denote statistical significance from each other (Tukey post-hoc test p<0.05). Locomotor values from females are designated in red, males in blue, and for animals with feminized corazonin neurons are indicated in yellow. Animals in the first group have wild-type corazonin neuronal function (w1118), the second grouping are expressing NaChBac in corazonin neurons (Activation) and the third grouping are expressing the ork channel in corazonin neurons (Silencing).
Mentions: We reasoned that the alterations in lifespan exhibited in flies differing in corazonin neuronal function may, in part, stem from changes in activity levels as activity may correlate with stress-sensitivity. We measured activity levels in flies that varied in corazonin neuronal function under a normal 12∶12 LD lighting regime. We found that the overall amount of activity levels of w1118 males and females were different from each other, consistent with previous observations [27]. However, there was a significant impact on activity levels that were influenced by sex and the specific alteration to corazonin neuronal function. Specifically, males expressing the Δork channel in corazonin neurons displayed greater activity levels than w1118 males. Furthermore, the opposite manipulation (NaChBac introduction) produced hypoactive males relative to w1118 (Figure 3A). Both of these phenotypes were not evident in females, where both manipulations produced activity levels indistinguishable from parental genotypes (Figure S3). Ablation of corazonin neurons produced activity levels slightly lower than w1118 levels for both males and females (Figure 3A). While we predicted that the ablation and silencing phenotypes would be similar for males, this inconsistent finding may be attributable to either differences in transgene impact (silencing is incomplete as compared to ablation) or developmental or physiological compensation in animals lacking corazonin neurons.

Bottom Line: Silencing and activation of corazonin neurons lead to differential lifespan under stress, and these effects showed a strong dependence on sex.Additionally, altered corazonin neuron physiology leads to fundamental differences in locomotor activity, and these effects were also sex-dependent.These results underscore the importance of central peptidergic processing within the context of stress and place corazonin signaling as a critical feature of neuroendocrine events that shape stress responses and may underlie the inherent sexual dimorphic differences in stress responses.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Wake Forest University, Winston-Salem, North Carolina, United States of America.

ABSTRACT
All organisms are confronted with dynamic environmental changes that challenge homeostasis, which is the operational definition of stress. Stress produces adaptive behavioral and physiological responses, which, in the Metazoa, are mediated through the actions of various hormones. Based on its associated phenotypes and its expression profiles, a candidate stress hormone in Drosophila is the corazonin neuropeptide. We evaluated the potential roles of corazonin in mediating stress-related changes in target behaviors and physiologies through genetic alteration of corazonin neuronal excitability. Ablation of corazonin neurons confers resistance to metabolic, osmotic, and oxidative stress, as measured by survival. Silencing and activation of corazonin neurons lead to differential lifespan under stress, and these effects showed a strong dependence on sex. Additionally, altered corazonin neuron physiology leads to fundamental differences in locomotor activity, and these effects were also sex-dependent. The dynamics of altered locomotor behavior accompanying stress was likewise altered in flies with altered corazonin neuronal function. We report that corazonin transcript expression is altered under starvation and osmotic stress, and that triglyceride and dopamine levels are equally impacted in corazonin neuronal alterations and these phenotypes similarly show significant sexual dimorphisms. Notably, these sexual dimorphisms map to corazonin neurons. These results underscore the importance of central peptidergic processing within the context of stress and place corazonin signaling as a critical feature of neuroendocrine events that shape stress responses and may underlie the inherent sexual dimorphic differences in stress responses.

Show MeSH
Related in: MedlinePlus