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Institute of Healthy Ageing, United Kingdom; email: i.bjedov@ucl.ac.uk\nInstitute of Healthy Ageing, Research Department of Genetics, Evolution and Environment, University College London, London, United Kingdom \n UCL Cancer Institute, Paul O'Gorman Building, London, United Kingdom \n Max Planck Institute for Biology of Ageing, Cologne, Germany \n MRC London Institute of Medical Sciences, Imperial College London, Du Cane Road, London, United Kingdom \n EMBL European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, United Kingdom \n Section on Islet Cell and Regenerative Biology, Research Division, Joslin Diabetes Center, Boston, MA, United States \n Department of Genetics, Harvard Stem Cell Institute, Harvard Medical School, Boston, MA, United States \n Institute of Structural and Molecular Biology, University College London, London, United Kingdom \n LAGENBIO, Facultad de Veterinaria-IIS, IA2-CITA, CIBERNED, Universidad de Zaragoza, Zaragoza, Spain \n MRC Mitochondrial Biology Unit, Keith Peters Building, University of Cambridge, Cambridge, United Kingdom \n Department of Genetics, Cell Biology and Development, University of Minnesota, 321 Church St. SE, Minneapolis, MN, United States \n Institute of Immunology and Infection Research, University of Edinburgh, Charlotte, Edinburgh, United Kingdom \n Export Date: 14 February 2021 \n Correspondence Address: Bjedov, I.; Institute of Healthy Ageing, United Kingdom; email: i.bjedov@ucl.ac.uk\nInstitute of Healthy Ageing, Research Department of Genetics, Evolution and Environment, University College London, London, United Kingdom \n UCL Cancer Institute, Paul O'Gorman Building, London, United Kingdom \n Max Planck Institute for Biology of Ageing, Cologne, Germany \n MRC London Institute of Medical Sciences, Imperial College London, Du Cane Road, London, United Kingdom \n EMBL European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, United Kingdom \n Section on Islet Cell and Regenerative Biology, Research Division, Joslin Diabetes Center, Boston, MA, United States \n Department of Genetics, Harvard Stem Cell Institute, Harvard Medical School, Boston, MA, United States \n Institute of Structural and Molecular Biology, University College London, London, United Kingdom \n LAGENBIO, Facultad de Veterinaria-IIS, IA2-CITA, CIBERNED, Universidad de Zaragoza, Zaragoza, Spain \n MRC Mitochondrial Biology Unit, Keith Peters Building, University of Cambridge, Cambridge, United Kingdom \n Department of Genetics, Cell Biology and Development, University of Minnesota, 321 Church St. SE, Minneapolis, MN, United States \n Institute of Immunology and Infection Research, University of Edinburgh, Charlotte, Edinburgh, United Kingdom \n Cited By :1 \n Export Date: 10 May 2021 \n Correspondence Address: Bjedov, I.; Institute of Healthy Ageing, United Kingdom; email: i.bjedov@ucl.ac.uk\nInstitute of Healthy Ageing, Research Department of Genetics, Evolution and Environment, University College London, London, United Kingdom \n UCL Cancer Institute, Paul O'Gorman Building, London, United Kingdom \n Max Planck Institute for Biology of Ageing, Cologne, Germany \n MRC London Institute of Medical Sciences, Imperial College London, Du Cane Road, London, United Kingdom \n EMBL European Bioinformatics Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, United Kingdom \n Section on Islet Cell and Regenerative Biology, Research Division, Joslin Diabetes Center, Boston, MA, United States \n Department of Genetics, Harvard Stem Cell Institute, Harvard Medical School, Boston, MA, United States \n Institute of Structural and Molecular Biology, University College London, London, United Kingdom \n LAGENBIO, Facultad de Veterinaria-IIS, IA2-CITA, CIBERNED, Universidad de Zaragoza, Zaragoza, Spain \n MRC Mitochondrial Biology Unit, Keith Peters Building, University of Cambridge, Cambridge, United Kingdom \n Department of Genetics, Cell Biology and Development, University of Minnesota, 321 Church St. SE, Minneapolis, MN, United States \n Institute of Immunology and Infection Research, University of Edinburgh, Charlotte, Edinburgh, United Kingdom \n Cited By :1 \n Export Date: 11 May 2021 \n Correspondence Address: Bjedov, I.; Institute of Healthy Ageing, United Kingdom; email: i.bjedov@ucl.ac.uk\nFunding Agency and Grant Number: Research into Ageing (Age UK); Wellcome TrustWellcome TrustEuropean Commission; Max Planck SocietyMax Planck SocietyFoundation CELLEX; European Research Council Starting GrantEuropean Research Council (ERC); Cancer Research UKCancer Research UK; Bill Lyons foundation\n Funding text: This work was supported by Research into Ageing (Age UK), the Wellcome Trust and the Max Planck Society (L.P.). The work was also funded by European Research Council Starting Grant, Cancer Research UK and The Bill Lyons foundation (I.B.). 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We report here that increased autophagy is necessary for reduced insulin-like signalling (IIS) to extend lifespan in Drosophila and is sufficient on its own to increase lifespan. We first established that the well-characterised lifespan extension associated with deletion of the insulin receptor substrate chico was completely abrogated by downregulation of the essential autophagy gene Atg5. We next directly induced autophagy by over-expressing the major autophagy kinase Atg1 and found that a mild increase in autophagy extended lifespan. Interestingly, strong Atg1 up-regulation was detrimental to lifespan. Transcriptomic and metabolomic approaches identified specific signatures mediated by varying levels of autophagy in flies. Transcriptional upregulation of mitochondrial-related genes was the signature most specifically associated with mild Atg1 upregulation and extended lifespan, whereas short-lived flies, possessing strong Atg1 overexpression, showed reduced mitochondrial metabolism and up-regulated immune system pathways. Increased proteasomal activity and reduced triacylglycerol levels were features shared by both moderate and high Atg1 overexpression conditions. These contrasting effects of autophagy on ageing and differential metabolic profiles highlight the importance of fine-tuning autophagy levels to achieve optimal healthspan and disease prevention. © 2020 Bjedov et al. 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