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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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Trehalose metabolism plays an important role in extending life span during starvation.A. Starvation survival after feeding 10% trehalose plus cellulose, 10% glucose plus cellulose, or cellulose alone to the 8-day-old starved male beetles. The survival was recorded from day 9 to day 12. B. The ratio between hemolymph glucose and trehalose on days 4, 5, and 6 after injection of malE, ILP2, JHAMT, Met, TRET, or TPS dsRNA into the newly emerged adults. The hemolymph was extracted from three beetles for each treatment. The trehalose concentrations were determined using the glucose reagent and trehalase. The data shown are the Mean+S.D. (n = 6). C. Starvation survival after manipulation of endogenous trehalose level by injecting TRET, TPS, or trehalase dsRNA on day 0. The beetles were starved until 14 days. The survival was recorded from day 9 to day 14. D. The relative mRNA level of TPS, TRET, and trehalase after injecting malE, JHAMT, or ILP2 dsRNA. Total RNA was isolated on day 5 from beetles injected with control malE, JHAMT, or ILP2 dsRNA and starved. The RNA was converted to cDNA, and the relative levels of TPS, TRET, and trehalase mRNA were determined by qRT-PCR using RP49 as a control. The data shown are the Mean+S.D. (n = 3). Asterisks show treatments that are significantly different from the control (P<0.05) in one-way ANOVA.
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pgen-1003535-g003: Trehalose metabolism plays an important role in extending life span during starvation.A. Starvation survival after feeding 10% trehalose plus cellulose, 10% glucose plus cellulose, or cellulose alone to the 8-day-old starved male beetles. The survival was recorded from day 9 to day 12. B. The ratio between hemolymph glucose and trehalose on days 4, 5, and 6 after injection of malE, ILP2, JHAMT, Met, TRET, or TPS dsRNA into the newly emerged adults. The hemolymph was extracted from three beetles for each treatment. The trehalose concentrations were determined using the glucose reagent and trehalase. The data shown are the Mean+S.D. (n = 6). C. Starvation survival after manipulation of endogenous trehalose level by injecting TRET, TPS, or trehalase dsRNA on day 0. The beetles were starved until 14 days. The survival was recorded from day 9 to day 14. D. The relative mRNA level of TPS, TRET, and trehalase after injecting malE, JHAMT, or ILP2 dsRNA. Total RNA was isolated on day 5 from beetles injected with control malE, JHAMT, or ILP2 dsRNA and starved. The RNA was converted to cDNA, and the relative levels of TPS, TRET, and trehalase mRNA were determined by qRT-PCR using RP49 as a control. The data shown are the Mean+S.D. (n = 3). Asterisks show treatments that are significantly different from the control (P<0.05) in one-way ANOVA.

Mentions: To determine whether the trehalose, a major sugar in most insects, or the glucose, a major sugar in most animals, is utilized during starvation, trehalose or glucose were fed to the starved beetles. When beetles were fed on non-nutritional cellulose diet or cellulose diet supplemented with 10% trehalose or 10% glucose, the beetles fed on a trehalose-supplemented diet lived significantly longer when compared to the other two groups (P = 0.001, Fig. 3A). There was no significant difference in the survival of cellulose-fed or cellulose+10% glucose-fed beetles (Fig. 3A). These data suggest that major insect sugar trehalose is important for survival of starved beetles. Moreover, the ratio of glucose and trehalose in the hemolymph increased in the control beetles upon starvation from day 4 to day 6, suggesting more glucose is needed during starvation for the energy supply. However, this ratio decreased by 77–81%, 37–93%, and 70–89% in starved ILP2, JHAMT, or Met RNAi beetles respectively, when compared to the levels in control beetles (Fig. 3B). These data suggest that JH and ILP2 regulate trehalose levels in starved beetles.


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

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

Trehalose metabolism plays an important role in extending life span during starvation.A. Starvation survival after feeding 10% trehalose plus cellulose, 10% glucose plus cellulose, or cellulose alone to the 8-day-old starved male beetles. The survival was recorded from day 9 to day 12. B. The ratio between hemolymph glucose and trehalose on days 4, 5, and 6 after injection of malE, ILP2, JHAMT, Met, TRET, or TPS dsRNA into the newly emerged adults. The hemolymph was extracted from three beetles for each treatment. The trehalose concentrations were determined using the glucose reagent and trehalase. The data shown are the Mean+S.D. (n = 6). C. Starvation survival after manipulation of endogenous trehalose level by injecting TRET, TPS, or trehalase dsRNA on day 0. The beetles were starved until 14 days. The survival was recorded from day 9 to day 14. D. The relative mRNA level of TPS, TRET, and trehalase after injecting malE, JHAMT, or ILP2 dsRNA. Total RNA was isolated on day 5 from beetles injected with control malE, JHAMT, or ILP2 dsRNA and starved. The RNA was converted to cDNA, and the relative levels of TPS, TRET, and trehalase mRNA were determined by qRT-PCR using RP49 as a control. The data shown are the Mean+S.D. (n = 3). Asterisks show treatments that are significantly different from the control (P<0.05) in one-way ANOVA.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1003535-g003: Trehalose metabolism plays an important role in extending life span during starvation.A. Starvation survival after feeding 10% trehalose plus cellulose, 10% glucose plus cellulose, or cellulose alone to the 8-day-old starved male beetles. The survival was recorded from day 9 to day 12. B. The ratio between hemolymph glucose and trehalose on days 4, 5, and 6 after injection of malE, ILP2, JHAMT, Met, TRET, or TPS dsRNA into the newly emerged adults. The hemolymph was extracted from three beetles for each treatment. The trehalose concentrations were determined using the glucose reagent and trehalase. The data shown are the Mean+S.D. (n = 6). C. Starvation survival after manipulation of endogenous trehalose level by injecting TRET, TPS, or trehalase dsRNA on day 0. The beetles were starved until 14 days. The survival was recorded from day 9 to day 14. D. The relative mRNA level of TPS, TRET, and trehalase after injecting malE, JHAMT, or ILP2 dsRNA. Total RNA was isolated on day 5 from beetles injected with control malE, JHAMT, or ILP2 dsRNA and starved. The RNA was converted to cDNA, and the relative levels of TPS, TRET, and trehalase mRNA were determined by qRT-PCR using RP49 as a control. The data shown are the Mean+S.D. (n = 3). Asterisks show treatments that are significantly different from the control (P<0.05) in one-way ANOVA.
Mentions: To determine whether the trehalose, a major sugar in most insects, or the glucose, a major sugar in most animals, is utilized during starvation, trehalose or glucose were fed to the starved beetles. When beetles were fed on non-nutritional cellulose diet or cellulose diet supplemented with 10% trehalose or 10% glucose, the beetles fed on a trehalose-supplemented diet lived significantly longer when compared to the other two groups (P = 0.001, Fig. 3A). There was no significant difference in the survival of cellulose-fed or cellulose+10% glucose-fed beetles (Fig. 3A). These data suggest that major insect sugar trehalose is important for survival of starved beetles. Moreover, the ratio of glucose and trehalose in the hemolymph increased in the control beetles upon starvation from day 4 to day 6, suggesting more glucose is needed during starvation for the energy supply. However, this ratio decreased by 77–81%, 37–93%, and 70–89% in starved ILP2, JHAMT, or Met RNAi beetles respectively, when compared to the levels in control beetles (Fig. 3B). These data suggest that JH and ILP2 regulate trehalose levels in starved beetles.

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