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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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Corazonin neuronal manipulations differentially impact survival during different forms of stress.Median survival times for different genotypes subjected to three different physiological stresses. Three replicate vials of thirty individuals were assessed twice daily for survival and non-linear regression was used to estimate median survival per replicate (GraphPad Prism, San Diego). Data are mean +/− SEM from three replicates per genotype. Boxed asterisks indicate statistical difference between the background control (w1118) line (Blue bars) (ANOVA, p<0.05).
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pone-0009141-g002: Corazonin neuronal manipulations differentially impact survival during different forms of stress.Median survival times for different genotypes subjected to three different physiological stresses. Three replicate vials of thirty individuals were assessed twice daily for survival and non-linear regression was used to estimate median survival per replicate (GraphPad Prism, San Diego). Data are mean +/− SEM from three replicates per genotype. Boxed asterisks indicate statistical difference between the background control (w1118) line (Blue bars) (ANOVA, p<0.05).

Mentions: To evaluate the potential roles of corazonin neurons in mediating stress response, we first measured lifespan of these different genotypes under three different physiological stress conditions: starvation, osmotic, and oxidative. Corazonin cell ablation consistently extended lifespan during these stresses in males and females, as compared to the parental stocks or w1118 genetic background controls, although the degree to which lifespan was extended varied with both gender and the nature of the stress (Figure 2). Introduction of a modified ion channel construct (Δork) to electrically silence corazonin neurons, also resulted in a lengthened lifespan under these stresses, with these effects most pronounced in males and dependent upon the nature of the stress in females. In contrast, activation of these neurons produced differential stress sensitivities in males and females. Predictably, expression of the NaChBac channel in males, results to increased stress sensitivity for all three stresses tested, as measured by lifespan. However, in females there is a strong stress by gender interaction. Notably, both the introduction of a reporter gene (UAS-CD8-GFP) to corazonin cells and the ablation of a group of well-defined neurons that express a different neuropeptide, Pigment Dispersing Factor (PDF) [25], showed stress sensitivities that were generally comparable to the w1118 background controls under these heterotypic stresses (Figure 2). This indicates that changes in lifespan are likely the consequence of manipulations to corazonin neuronal populations and not solely caused by increased hybrid vigor or differences in genetic backgrounds. Although there are strong differences in quantitative traits such as lifespan [26], and some of the results we present here may be attributed to genetic background effects, our control genotypes neither showed the same large effects of the corazonin manipulations nor in many cases were background effect in the same direction. Additionally, evaluation of lifespan of genotypes with altered corazonin neuronal function indicates that the majority of these changes are a specific consequence of physiological stress, as for almost all genotypes, aging was not significantly impacted (Figure S2).


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)

Corazonin neuronal manipulations differentially impact survival during different forms of stress.Median survival times for different genotypes subjected to three different physiological stresses. Three replicate vials of thirty individuals were assessed twice daily for survival and non-linear regression was used to estimate median survival per replicate (GraphPad Prism, San Diego). Data are mean +/− SEM from three replicates per genotype. Boxed asterisks indicate statistical difference between the background control (w1118) line (Blue bars) (ANOVA, p<0.05).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2818717&req=5

pone-0009141-g002: Corazonin neuronal manipulations differentially impact survival during different forms of stress.Median survival times for different genotypes subjected to three different physiological stresses. Three replicate vials of thirty individuals were assessed twice daily for survival and non-linear regression was used to estimate median survival per replicate (GraphPad Prism, San Diego). Data are mean +/− SEM from three replicates per genotype. Boxed asterisks indicate statistical difference between the background control (w1118) line (Blue bars) (ANOVA, p<0.05).
Mentions: To evaluate the potential roles of corazonin neurons in mediating stress response, we first measured lifespan of these different genotypes under three different physiological stress conditions: starvation, osmotic, and oxidative. Corazonin cell ablation consistently extended lifespan during these stresses in males and females, as compared to the parental stocks or w1118 genetic background controls, although the degree to which lifespan was extended varied with both gender and the nature of the stress (Figure 2). Introduction of a modified ion channel construct (Δork) to electrically silence corazonin neurons, also resulted in a lengthened lifespan under these stresses, with these effects most pronounced in males and dependent upon the nature of the stress in females. In contrast, activation of these neurons produced differential stress sensitivities in males and females. Predictably, expression of the NaChBac channel in males, results to increased stress sensitivity for all three stresses tested, as measured by lifespan. However, in females there is a strong stress by gender interaction. Notably, both the introduction of a reporter gene (UAS-CD8-GFP) to corazonin cells and the ablation of a group of well-defined neurons that express a different neuropeptide, Pigment Dispersing Factor (PDF) [25], showed stress sensitivities that were generally comparable to the w1118 background controls under these heterotypic stresses (Figure 2). This indicates that changes in lifespan are likely the consequence of manipulations to corazonin neuronal populations and not solely caused by increased hybrid vigor or differences in genetic backgrounds. Although there are strong differences in quantitative traits such as lifespan [26], and some of the results we present here may be attributed to genetic background effects, our control genotypes neither showed the same large effects of the corazonin manipulations nor in many cases were background effect in the same direction. Additionally, evaluation of lifespan of genotypes with altered corazonin neuronal function indicates that the majority of these changes are a specific consequence of physiological stress, as for almost all genotypes, aging was not significantly impacted (Figure S2).

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