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Juvenile hormone and insulin regulate trehalose homeostasis in the red flour beetle, Tribolium castaneum.

Xu J, Sheng Z, Palli SR - PLoS Genet. (2013)

Bottom Line: The Drosophila melanogaster insulin-like receptor (InR) mutant showed extended life span due to reduced juvenile hormone (JH) levels.Reduction in JH biosynthesis, JH action, or insulin-like peptide 2 (ILP2) syntheses by RNA interference (RNAi)-aided knockdown in the expression of genes coding for juvenile hormone acid methyltransferase (JHAMT), methoprene-tolerant (Met), or ILP2 respectively decreased lipid and carbohydrate metabolism and extended the survival of starved beetles.More importantly, JH regulates trehalose homeostasis, including trehalose transport and metabolism, and controls utilization of stored nutrients in starved adults.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, College of Agriculture, University of Kentucky, Lexington, KY, USA.

ABSTRACT
Insulin/IGF-1 signaling (IIS) has been well studied for its role in the control of life span extension and resistance to a variety of stresses. The Drosophila melanogaster insulin-like receptor (InR) mutant showed extended life span due to reduced juvenile hormone (JH) levels. However, little is known about the mechanism of cross talk between IIS and JH in regulation of life span extension and resistance to starvation. In the current study, we investigated the role of IIS and JH signaling in regulation of resistance to starvation. Reduction in JH biosynthesis, JH action, or insulin-like peptide 2 (ILP2) syntheses by RNA interference (RNAi)-aided knockdown in the expression of genes coding for juvenile hormone acid methyltransferase (JHAMT), methoprene-tolerant (Met), or ILP2 respectively decreased lipid and carbohydrate metabolism and extended the survival of starved beetles. Interestingly, the extension of life span could be restored by injection of bovine insulin into JHAMT RNAi beetles but not by application of JH III to ILP2 RNAi beetles. These data suggest that JH controls starvation resistance by regulating synthesis of ILP2. More importantly, JH regulates trehalose homeostasis, including trehalose transport and metabolism, and controls utilization of stored nutrients in starved adults.

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JH and ILP2 regulate carbohydrate, protein, and lipid metabolism during starvation.A. Total carbohydrate, protein, and lipid levels were determined by Anthrone reagent, Bradford, and vanillin reagent respectively in samples collected from day 3 to day 8 starved and fed male beetles. Three beetles were used for each time point and six biological replicate were used. The Means+S.D (n = 6) are shown. B. The nutrient levels including carbohydrate, protein, and lipid are regulated by JH and ILP2 during starvation. The male beetles injected with malE, ILP2, or JHAMT dsRNA were collected on day 8. The total carbohydrate, protein, and lipid were determined. Shown are the Means+S.D (n = 6). Asterisks show treatments that are significantly different (P<0.05) by one-way ANOVA.
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pgen-1003535-g002: JH and ILP2 regulate carbohydrate, protein, and lipid metabolism during starvation.A. Total carbohydrate, protein, and lipid levels were determined by Anthrone reagent, Bradford, and vanillin reagent respectively in samples collected from day 3 to day 8 starved and fed male beetles. Three beetles were used for each time point and six biological replicate were used. The Means+S.D (n = 6) are shown. B. The nutrient levels including carbohydrate, protein, and lipid are regulated by JH and ILP2 during starvation. The male beetles injected with malE, ILP2, or JHAMT dsRNA were collected on day 8. The total carbohydrate, protein, and lipid were determined. Shown are the Means+S.D (n = 6). Asterisks show treatments that are significantly different (P<0.05) by one-way ANOVA.

Mentions: To determine the major energy source for starved beetles, the total lipid, carbohydrate, and protein levels were measured in fed and starved beetles. In the fed beetles, the levels of all three nutrients did not change significantly during days 3–8 PAE (Fig. 2A). In contrast, in the starved animals, the levels of all three nutrients gradually decreased from day 3 to day 8 PAE (Fig. 2A). These data suggest that the beetles use all three sources of nutrients during starvation. To determine whether JH or IIS regulate metabolism of these macromolecules, the levels of these macromolecules were determined in JHAMT or ILP2 RNAi beetles. Strikingly, higher protein, carbohydrate, and lipid levels were detected in JHAMT and ILP2 RNAi beetles when compared to the levels in the control beetles injected with malE dsRNA (Fig. 2B). These data suggest that the life span extension during starvation in either JH or IIS deficient animals could be due to the reduced metabolism.


Juvenile hormone and insulin regulate trehalose homeostasis in the red flour beetle, Tribolium castaneum.

Xu J, Sheng Z, Palli SR - PLoS Genet. (2013)

JH and ILP2 regulate carbohydrate, protein, and lipid metabolism during starvation.A. Total carbohydrate, protein, and lipid levels were determined by Anthrone reagent, Bradford, and vanillin reagent respectively in samples collected from day 3 to day 8 starved and fed male beetles. Three beetles were used for each time point and six biological replicate were used. The Means+S.D (n = 6) are shown. B. The nutrient levels including carbohydrate, protein, and lipid are regulated by JH and ILP2 during starvation. The male beetles injected with malE, ILP2, or JHAMT dsRNA were collected on day 8. The total carbohydrate, protein, and lipid were determined. Shown are the Means+S.D (n = 6). Asterisks show treatments that are significantly different (P<0.05) by one-way ANOVA.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3675034&req=5

pgen-1003535-g002: JH and ILP2 regulate carbohydrate, protein, and lipid metabolism during starvation.A. Total carbohydrate, protein, and lipid levels were determined by Anthrone reagent, Bradford, and vanillin reagent respectively in samples collected from day 3 to day 8 starved and fed male beetles. Three beetles were used for each time point and six biological replicate were used. The Means+S.D (n = 6) are shown. B. The nutrient levels including carbohydrate, protein, and lipid are regulated by JH and ILP2 during starvation. The male beetles injected with malE, ILP2, or JHAMT dsRNA were collected on day 8. The total carbohydrate, protein, and lipid were determined. Shown are the Means+S.D (n = 6). Asterisks show treatments that are significantly different (P<0.05) by one-way ANOVA.
Mentions: To determine the major energy source for starved beetles, the total lipid, carbohydrate, and protein levels were measured in fed and starved beetles. In the fed beetles, the levels of all three nutrients did not change significantly during days 3–8 PAE (Fig. 2A). In contrast, in the starved animals, the levels of all three nutrients gradually decreased from day 3 to day 8 PAE (Fig. 2A). These data suggest that the beetles use all three sources of nutrients during starvation. To determine whether JH or IIS regulate metabolism of these macromolecules, the levels of these macromolecules were determined in JHAMT or ILP2 RNAi beetles. Strikingly, higher protein, carbohydrate, and lipid levels were detected in JHAMT and ILP2 RNAi beetles when compared to the levels in the control beetles injected with malE dsRNA (Fig. 2B). These data suggest that the life span extension during starvation in either JH or IIS deficient animals could be due to the reduced metabolism.

Bottom Line: The Drosophila melanogaster insulin-like receptor (InR) mutant showed extended life span due to reduced juvenile hormone (JH) levels.Reduction in JH biosynthesis, JH action, or insulin-like peptide 2 (ILP2) syntheses by RNA interference (RNAi)-aided knockdown in the expression of genes coding for juvenile hormone acid methyltransferase (JHAMT), methoprene-tolerant (Met), or ILP2 respectively decreased lipid and carbohydrate metabolism and extended the survival of starved beetles.More importantly, JH regulates trehalose homeostasis, including trehalose transport and metabolism, and controls utilization of stored nutrients in starved adults.

View Article: PubMed Central - PubMed

Affiliation: Department of Entomology, College of Agriculture, University of Kentucky, Lexington, KY, USA.

ABSTRACT
Insulin/IGF-1 signaling (IIS) has been well studied for its role in the control of life span extension and resistance to a variety of stresses. The Drosophila melanogaster insulin-like receptor (InR) mutant showed extended life span due to reduced juvenile hormone (JH) levels. However, little is known about the mechanism of cross talk between IIS and JH in regulation of life span extension and resistance to starvation. In the current study, we investigated the role of IIS and JH signaling in regulation of resistance to starvation. Reduction in JH biosynthesis, JH action, or insulin-like peptide 2 (ILP2) syntheses by RNA interference (RNAi)-aided knockdown in the expression of genes coding for juvenile hormone acid methyltransferase (JHAMT), methoprene-tolerant (Met), or ILP2 respectively decreased lipid and carbohydrate metabolism and extended the survival of starved beetles. Interestingly, the extension of life span could be restored by injection of bovine insulin into JHAMT RNAi beetles but not by application of JH III to ILP2 RNAi beetles. These data suggest that JH controls starvation resistance by regulating synthesis of ILP2. More importantly, JH regulates trehalose homeostasis, including trehalose transport and metabolism, and controls utilization of stored nutrients in starved adults.

Show MeSH
Related in: MedlinePlus