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      The R148.3 Gene Modulates Caenorhabditis elegans Lifespan and Fat Metabolism

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          Abstract

          Despite many advances, the molecular links between energy metabolism and longevity are not well understood. Here, we have used the nematode model Caenorhabditis elegans to study the role of the yet-uncharacterized gene R148.3 in fat accumulation and lifespan. In wild-type worms, a R148.3 p::GFP reporter showed enhanced expression throughout life in the pharynx, in neurons, and in muscles. Functionally, a protein fusing a predicted 22 amino acid N-terminal signal sequence (SS) of R148.3 to mCherry displayed robust accumulation in coelomyocytes, indicating that R148.3 is a secreted protein. Systematic depletion of R148.3 by RNA interference (RNAi) at L1 but not at young-adult stage enhanced triglyceride accumulation, which was associated with increased food uptake and lower expression of genes involved in lipid oxidation. However, RNAi of R148.3 at both L1 and young-adult stages robustly diminished mean and maximal lifespan of wild-type worms, and also abolished the long-lived phenotypes of eat-2 and daf-2/InsR mutants. Based on these data, we propose that R148.3 is an SS that modulates fat mass and longevity in an independent manner.

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          Most cited references 40

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          The genetics of Caenorhabditis elegans.

          Methods are described for the isolation, complementation and mapping of mutants of Caenorhabditis elegans, a small free-living nematode worm. About 300 EMS-induced mutants affecting behavior and morphology have been characterized and about one hundred genes have been defined. Mutations in 77 of these alter the movement of the animal. Estimates of the induced mutation frequency of both the visible mutants and X chromosome lethals suggests that, just as in Drosophila, the genetic units in C. elegans are large.
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            A C. elegans mutant that lives twice as long as wild type.

            We have found that mutations in the gene daf-2 can cause fertile, active, adult Caenorhabditis elegans hermaphrodites to live more than twice as long as wild type. This lifespan extension, the largest yet reported in any organism, requires the activity of a second gene, daf-16. Both genes also regulate formation of the dauer larva, a developmentally arrested larval form that is induced by crowding and starvation and is very long-lived. Our findings raise the possibility that the longevity of the dauer is not simply a consequence of its arrested growth, but instead results from a regulated lifespan extension mechanism that can be uncoupled from other aspects of dauer formation. daf-2 and daf-16 provide entry points into understanding how lifespan can be extended.
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              The genetics of ageing.

              The nematode Caenorhabditis elegans ages and dies in a few weeks, but humans can live for 100 years or more. Assuming that the ancestor we share with nematodes aged rapidly, this means that over evolutionary time mutations have increased lifespan more than 2,000-fold. Which genes can extend lifespan? Can we augment their activities and live even longer? After centuries of wistful poetry and wild imagination, we are now getting answers, often unexpected ones, to these fundamental questions.
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                Author and article information

                Journal
                G3 (Bethesda)
                Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes|Genomes|Genetics
                Genetics Society of America
                2160-1836
                15 June 2017
                August 2017
                : 7
                : 8
                : 2739-2747
                Affiliations
                [* ]Quebec Heart and Lung Research Institute, G1V 4G5, Canada
                []Faculty of Pharmacy, Laval University, Québec, G1V 0A6, Canada
                []Centre for Molecular Medicine and Therapeutics, University of British Columbia, Vancouver, V5Z 4H4, Canada
                [§ ]British Columbia Children’s Hospital, Vancouver, V6H 3N1, Canada
                [** ]Department of Medical Genetics, University of British Columbia, Vancouver, V6H 3N1, Canada
                [†† ]Centre Hospitalier de l’Université Laval (CHU) de Québec Research Center, G1V 4G2, Canada
                [‡‡ ]Faculty of Medicine, Laval University, Québec, G1V 0A6, Canada
                Author notes
                [1 ]Corresponding authors: Rm. 2024, Centre for Molecular Medicine and Therapeutics, 950 West 28th Ave., Vancouver, BC V5Z 4H4, Canada. E-mail: taubert@ 123456cmmt.ubc.ca ; and Institut Universitaire de Cardiologie et de Pneumologie de Québec, Y4255.3 Pavillon Marguerite-d’Youville, 2725 Chemin Ste-Foy, Québec, QC G1V 4G5, Canada. E-mail: Frederic.Picard@ 123456criucpq.ulaval.ca
                Article
                GGG_041681
                10.1534/g3.117.041681
                5555478
                28620088
                Copyright © 2017 Roy-Bellavance et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                Page count
                Figures: 5, Tables: 0, Equations: 0, References: 40, Pages: 9
                Product
                Categories
                Investigations

                Genetics

                fat metabolism, lifespan, insulin signaling, r148.3, daf-2

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