Calories Do Not Explain Extension of Life Span by Dietary Restriction in Drosophila

Mair, William; Piper, Matthew D. W.; Partridge, Linda

doi:10.1371/journal.pbio.0030223

Cited by 455 publications

(444 citation statements)

References 50 publications

(50 reference statements)

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“…In addition, the context-dependent effect of resveratrol is unlikely due to the difference in resveratrol uptake by flies under different dietary conditions. Our lab and others observed that food intake among females on the high sugar-low protein, low sugar-high protein and standard base diets differed by no more than 20% (Mair et al 2005; our unpublished observation). Thus, resveratrol uptake should not be much different among these three diets.…”

Section: Discussionmentioning

confidence: 49%

The effect of resveratrol on lifespan depends on both gender and dietary nutrient composition in Drosophila melanogaster

Wang

Wheeler

Alberico

et al. 2011

AGE

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Resveratrol, a polyphenolic compound, has been shown to extend lifespan in different organisms. Emerging evidence suggests that the prolongevity effect of resveratrol depends on dietary composition. However, the mechanisms underlying the interaction of resveratrol and dietary nutrients in modulating lifespan remain elusive. Here, we investigated the effect of resveratrol on lifespan of Drosophila melanogaster fed diets differing in the concentrations of sugar, yeast extract, and palmitic acid representing carbohydrate, protein, and fat, respectively. Resveratrol at up to 200 μM in diets did not affect lifespan of wild-type female flies fed a standard, restricted or high sugar-low protein diet, but extended lifespan of females fed a low sugar-high protein diet. Resveratrol at 400 μM extended lifespan of females fed a high-fat diet. Lifespan extension by resveratrol was associated with downregulation of genes in aging-related pathways, including antioxidant peroxiredoxins, insulin-like peptides involved in insulin-like signaling and several downstream genes in Jun-kinase signaling involved in oxidative stress response. Furthermore, resveratrol increased lifespan of superoxide dismutase 1 (sod1) knockdown mutant females fed a standard or high-fat diet. No lifespan extension by resveratrol was observed in wild-type and sod1 knockdown males under the culture conditions in this study. Our results suggest that the gender-specific prolongevity effect of resveratrol is influenced by dietary composition and resveratrol promotes the survival of flies by modulating genetic pathways that can reduce cellular damage. This study reveals the context-dependent effect of resveratrol on lifespan and suggests the importance of dietary nutrients in implementation of effective aging interventions using dietary supplements.

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Section: Discussionmentioning

confidence: 49%

The effect of resveratrol on lifespan depends on both gender and dietary nutrient composition in Drosophila melanogaster

Wang

Wheeler

Alberico

et al. 2011

AGE

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“…This is a higher ratio than that which is typical of other dietary restriction studies. For example, the mean lifespan of control Dahomey flies reported by Mair et al (2005) is only 47% of the maximum lifespan reached by the longest lived yeast and sugar restricted flies. Such extension of median lifespan towards maximum lifespan, which is sometimes referred to as "squaring" of the survivorship curve, indicates successful aging in which the onset of agerelated morbidity is delayed and its duration is shortened (Figure 1).…”

Section: Discussionmentioning

confidence: 97%

Lifespan modification by glucose and methionine in Drosophila melanogaster fed a chemically defined diet

Troen

French

Roberts

et al. 2006

AGE

103

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Experimentally restricting dietary calories, while maintaining adequate dietary nutrient content, extends lifespan in phylogenetically diverse species; thus suggesting the existence of conserved pathways which can modify lifespan in response to energy intake. However, in some cases the impact on longevity may depend on the quality of the energy source. In Drosophila, restriction of dietary yeast yields considerable lifespan extension whereas isocaloric restriction of dietary sugar yields only modest extension, indicating that other diet-responsive pathways can modify lifespan in this species. In rodents, restricting intake of a single amino acid -methionine -extends lifespan. Here we show that dietary methionine can modify lifespan in adult female, non-virgin Oregon-R strain Drosophila fed a chemically defined media. Compared to a diet containing 0.135% methionine and 15% glucose, high dietary methionine (0.405%) shortened maximum lifespan by 2.33% from 86 to 84 days and mean lifespan by 9.55% from 71.7 to 64.9 days. Further restriction of methionine to 0.045% did not extend maximum lifespan and shortened mean lifespan by 1.95% from 71.1 to 70.3 days. Restricting glucose from 15% to 5% while holding methionine at a concentration of 0.135%, modestly extended maximum lifespan by 5.8% from 86 to 91 days, without extending mean lifespan. All these diet-induced changes were highly significant (log-rank p<0.0001). Notably, all four diets resulted in considerably longer life spans than those typically reported for flies fed conventional yeast and sugar based diets. Such defined diets can be used to identify lifespan-modifying pathways and specific gene-nutrient interactions in Drosophila.

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“…In C. elegans, the sensory influence depends on the recognition of food types, which can have different effects on lifespan (30,(34)(35)(36)(37). In Drosophila, the foodtype effect on lifespan has been demonstrated through alterations in the protein composition of its food source.…”

Section: Discussionmentioning

confidence: 99%

“…Besides food levels, the nature of the food source has also been shown to influence an animal's lifespan (30,(34)(35)(36)(37). Because yeast is a component of fly food that can shorten fly lifespan (36) partly through an olfaction-mediated mechanism (3), we asked whether the effect of yeast on lifespan also acts via taste inputs.…”

Section: Significancementioning

confidence: 99%

Positive and negative gustatory inputs affect Drosophila lifespan partly in parallel to dFOXO signaling

Ostojić

Boll

Waterson³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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In Caenorhabditis elegans, a subset of gustatory neurons, as well as olfactory neurons, shortens lifespan, whereas a different subset of gustatory neurons lengthens it. Recently, the lifespan-shortening effect of olfactory neurons has been reported to be conserved in Drosophila. Here we show that the Drosophila gustatory system also affects lifespan in a bidirectional manner. We find that taste inputs shorten lifespan through inhibition of the insulin pathway effector dFOXO, whereas other taste inputs lengthen lifespan in parallel to this pathway. We also note that the gustatory influence on lifespan does not necessarily depend on food intake levels. Finally, we identify the nature of some of the taste inputs that could shorten versus lengthen lifespan. Together our data suggest that different gustatory cues can modulate the activities of distinct signaling pathways, including different insulin-like peptides, to promote physiological changes that ultimately affect lifespan.sensory system | insulin signaling | physiology | gustatory receptors | aging A ging is a universal process that causes deterioration in the biological functions of an organism over the progression of its lifetime. This process is affected by genetic and environmental factors, whose interaction could be mediated by the sensory system, which perceives and transmits environmental information to modulate the signaling activities of downstream target tissues. Accordingly, external sensory cues and sensory neuron activities have been shown to alter the lifespan of both Caenorhabditis elegans and Drosophila melanogaster (1-6).In C. elegans, the laser ablation of a specific subset of gustatory or olfactory neurons extends lifespan, whereas ablation of a different subset of gustatory neurons shortens it (1). Interestingly, at least part of this sensory influence on lifespan has also been observed in other animals. In Drosophila, impairment of olfaction through a mutation in Or83b, which encodes a broadly expressed atypical odorant receptor (7), increases lifespan (3). In addition, exposure of dietary-restricted flies to food odors, like live yeast, can partly suppress their long-life phenotype (3). The conservation of the olfactory influence on lifespan is thus consistent with the possibility that gustatory inputs will also bidirectionally alter the lifespan of both C. elegans and D. melanogaster.The effects of sensory neurons on C. elegans lifespan have been shown to be partly mediated by insulin/IGF signaling (1, 2, 8). The insulin/IGF pathway also affects fly lifespan: down-regulation of the activities of the insulin receptor InR and the receptor substrate, CHICO, extends lifespan (9, 10). Moreover, an increase in activity of the downstream transcription factor dFOXO, which is negatively regulated by both InR and CHICO, increases fly lifespan (11,12). Consistent with these observations, mutations in several of the Drosophila insulin-like peptide (dilp) genes (13), which are expressed in the median neurosecretory cells (mNSCs) in the fly brain (14-1...

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Calories Do Not Explain Extension of Life Span by Dietary Restriction in Drosophila

Cited by 455 publications

References 50 publications

The effect of resveratrol on lifespan depends on both gender and dietary nutrient composition in Drosophila melanogaster

The effect of resveratrol on lifespan depends on both gender and dietary nutrient composition in Drosophila melanogaster

Lifespan modification by glucose and methionine in Drosophila melanogaster fed a chemically defined diet

Positive and negative gustatory inputs affect Drosophila lifespan partly in parallel to dFOXO signaling

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