Carbon Dioxide Sensing Modulates Lifespan and Physiology in Drosophila

Poon, Peter C.; Kuo, Tsung Han; Linford, Nancy J.; Roman, Gregg; Pletcher, Scott D.

doi:10.1371/journal.pbio.1000356

Cited by 53 publications

(62 citation statements)

References 41 publications

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“…For example, the insulin/IGF1 pathway regulates the physiology, and consequently the longevity, of worms, flies, and mice (9,10,(47)(48)(49). Similarly, the sensory influence on lifespan is conserved in both worms (1) and flies at the level of olfaction (3,5). This study, as well as that of Waterson et al (44), shows that the conserved sensory effects on lifespan can also be extended to gustation.…”

Section: Discussionsupporting

confidence: 69%

“…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)(2)(3)(4)(5)(6).…”

mentioning

confidence: 99%

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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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Section: Discussionsupporting

confidence: 69%

mentioning

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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“…S3 in the supplementary material). Since lifespan is influenced by many types of cues and sensory neurons (Alcedo and Kenyon, 2004;Apfeld and Kenyon, 1999;Lee and Kenyon, 2009;Libert et al, 2007;Poon et al, 2010), it is not surprising that many cueresponsive ILPs would be involved in regulating DAF-2 activity to affect longevity.…”

Section: Developmentmentioning

confidence: 99%

Specific insulin-like peptides encode sensory information to regulate distinct developmental processes

et al. 2011

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An insulin-like signaling pathway mediates the environmental influence on the switch between the C. elegans developmental programs of reproductive growth versus dauer arrest. However, the specific role of endogenous insulin-like peptide (ILP) ligands in mediating the switch between these programs remains unknown. C. elegans has 40 putative insulin-like genes, many of which are expressed in sensory neurons and interneurons, raising the intriguing possibility that ILPs encode different environmental information to regulate the entry into, and exit from, dauer arrest. These two developmental switches can have different regulatory requirements: here we show that the relative importance of three different ILPs varies between dauer entry and exit. Not only do we find that one ILP, ins-1, ensures dauer arrest under harsh environments and that two other ILPs, daf-28 and ins-6, ensure reproductive growth under good conditions, we also show that daf-28 and ins-6 have non-redundant functions in regulating these developmental switches. Notably, daf-28 plays a more primary role in inhibiting dauer entry, whereas ins-6 has a more significant role in promoting dauer exit. Moreover, the switch into dauer arrest surprisingly shifts ins-6 transcriptional expression from a set of dauer-inhibiting sensory neurons to a different set of neurons, where it promotes dauer exit. Together, our data suggest that specific ILPs generate precise responses to dauer-inducing cues, such as pheromones and low food levels, to control development through stimulus-regulated expression in different neurons.

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“…Fresh food was provided every 2 or 3days. Details on media recipes can be found elsewhere (Poon et al, 2010).…”

Section: Fly Stocks and Husbandrymentioning

confidence: 99%

Aging modulates cuticular hydrocarbons and sexual attractiveness inDrosophila melanogaster

Kuo

Yew

Fedina

et al. 2012

Journal of Experimental Biology

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SUMMARY Attractiveness is a major component of sexual selection that is dependent on sexual characteristics, such as pheromone production, which often reflect an individual’s fitness and reproductive potential. Aging is a process that results in a steady decline in survival and reproductive output, yet little is known about its effect on specific aspects of attractiveness. In this report we asked how aging impacts pheromone production and sexual attractiveness in Drosophila melanogaster. Evidence suggests that key pheromones in Drosophila are produced as cuticular hydrocarbons (CHC), whose functions in attracting mates and influencing behavior have been widely studied. We employed gas chromatography/mass spectrometry and laser desorption/ionization mass spectrometry to show that the composition of D. melanogaster CHC is significantly affected by aging in both sexes and that these changes are robust to different genetic backgrounds. Aging affected the relative levels of many individual CHC, and it shifted overall hydrocarbon profiles to favor compounds with longer chain lengths. We also show that the observed aging-related changes in CHC profiles are responsible for a significant reduction in sexual attractiveness. These studies illuminate causal links among pheromones, aging and attractiveness and suggest that CHC production may be an honest indicator of animal health and fertility.

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Carbon Dioxide Sensing Modulates Lifespan and Physiology in Drosophila

Abstract: Loss of an olfactory receptor that senses carbon dioxide increases longevity and fecundity and alters overall physiology in fruit flies.

Cited by 53 publications

References 41 publications

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

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

Specific insulin-like peptides encode sensory information to regulate distinct developmental processes

Aging modulates cuticular hydrocarbons and sexual attractiveness inDrosophila melanogaster

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