SUMO promotes longevity and maintains mitochondrial homeostasis during ageing in Caenorhabditis elegans

Andrea Princz; Federico Pelisch; Nektarios Tavernarakis

doi:10.1038/s41598-020-72637-9

SUMO promotes longevity and maintains mitochondrial homeostasis during ageing in Caenorhabditis elegans

Andrea Princz, Federico Pelisch, Nektarios Tavernarakis (Lead / Corresponding author)

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13 Citations (Scopus)

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Abstract

The insulin/IGF signalling pathway impacts lifespan across distant taxa, by controlling the activity of nodal transcription factors. In the nematode Caenorhabditis elegans, the transcription regulators DAF-16/FOXO and SKN-1/Nrf function to promote longevity under conditions of low insulin/IGF signalling and stress. The activity and subcellular localization of both DAF-16 and SKN-1 is further modulated by specific posttranslational modifications, such as phosphorylation and ubiquitination. Here, we show that ageing elicits a marked increase of SUMO levels in C. elegans. In turn, SUMO fine-tunes DAF-16 and SKN-1 activity in specific C. elegans somatic tissues, to enhance stress resistance. SUMOylation of DAF-16 modulates mitochondrial homeostasis by interfering with mitochondrial dynamics and mitophagy. Our findings reveal that SUMO is an important determinant of lifespan, and provide novel insight, relevant to the complexity of the signalling mechanisms that influence gene expression to govern organismal survival in metazoans.

Original language	English
Article number	15513
Number of pages	16
Journal	Scientific Reports
Volume	10
DOIs	https://doi.org/10.1038/s41598-020-72637-9
Publication status	Published - 23 Sept 2020

Keywords

Ageing
Cell biology
Organelles
Post-translational modifications

ASJC Scopus subject areas

General

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10.1038/s41598-020-72637-9Licence: CC BY

Final Published VersionFinal published version, 4.52 MBLicence: CC BY

Cite this

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title = "SUMO promotes longevity and maintains mitochondrial homeostasis during ageing in Caenorhabditis elegans",

abstract = "The insulin/IGF signalling pathway impacts lifespan across distant taxa, by controlling the activity of nodal transcription factors. In the nematode Caenorhabditis elegans, the transcription regulators DAF-16/FOXO and SKN-1/Nrf function to promote longevity under conditions of low insulin/IGF signalling and stress. The activity and subcellular localization of both DAF-16 and SKN-1 is further modulated by specific posttranslational modifications, such as phosphorylation and ubiquitination. Here, we show that ageing elicits a marked increase of SUMO levels in C. elegans. In turn, SUMO fine-tunes DAF-16 and SKN-1 activity in specific C. elegans somatic tissues, to enhance stress resistance. SUMOylation of DAF-16 modulates mitochondrial homeostasis by interfering with mitochondrial dynamics and mitophagy. Our findings reveal that SUMO is an important determinant of lifespan, and provide novel insight, relevant to the complexity of the signalling mechanisms that influence gene expression to govern organismal survival in metazoans.",

keywords = "Ageing, Cell biology, Organelles, Post-translational modifications",

author = "Andrea Princz and Federico Pelisch and Nektarios Tavernarakis",

note = "Some nematode strains used in this work were provided by the Caenorhabditis Genetics Center, which is funded by the National Center for Research Resources (NCRR) of the National Institutes of Health (NIH). This work was funded by the European Commission 7th Framework Programme Marie Curie (FP7 ITN CodeAge 316354), an EMBO Short-Term Fellowship and Grants from the European Research Council (ERC GA695190, MANNA; ERC-GA737599, NeuronAgeScreen).",

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AU - Princz, Andrea

AU - Pelisch, Federico

AU - Tavernarakis, Nektarios

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N2 - The insulin/IGF signalling pathway impacts lifespan across distant taxa, by controlling the activity of nodal transcription factors. In the nematode Caenorhabditis elegans, the transcription regulators DAF-16/FOXO and SKN-1/Nrf function to promote longevity under conditions of low insulin/IGF signalling and stress. The activity and subcellular localization of both DAF-16 and SKN-1 is further modulated by specific posttranslational modifications, such as phosphorylation and ubiquitination. Here, we show that ageing elicits a marked increase of SUMO levels in C. elegans. In turn, SUMO fine-tunes DAF-16 and SKN-1 activity in specific C. elegans somatic tissues, to enhance stress resistance. SUMOylation of DAF-16 modulates mitochondrial homeostasis by interfering with mitochondrial dynamics and mitophagy. Our findings reveal that SUMO is an important determinant of lifespan, and provide novel insight, relevant to the complexity of the signalling mechanisms that influence gene expression to govern organismal survival in metazoans.

AB - The insulin/IGF signalling pathway impacts lifespan across distant taxa, by controlling the activity of nodal transcription factors. In the nematode Caenorhabditis elegans, the transcription regulators DAF-16/FOXO and SKN-1/Nrf function to promote longevity under conditions of low insulin/IGF signalling and stress. The activity and subcellular localization of both DAF-16 and SKN-1 is further modulated by specific posttranslational modifications, such as phosphorylation and ubiquitination. Here, we show that ageing elicits a marked increase of SUMO levels in C. elegans. In turn, SUMO fine-tunes DAF-16 and SKN-1 activity in specific C. elegans somatic tissues, to enhance stress resistance. SUMOylation of DAF-16 modulates mitochondrial homeostasis by interfering with mitochondrial dynamics and mitophagy. Our findings reveal that SUMO is an important determinant of lifespan, and provide novel insight, relevant to the complexity of the signalling mechanisms that influence gene expression to govern organismal survival in metazoans.

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KW - Organelles

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SUMO promotes longevity and maintains mitochondrial homeostasis during ageing in Caenorhabditis elegans

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Regulation of Meiotic Chromosome Segregation by Post-Translational Modifications

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SUMO promotes longevity and maintains mitochondrial homeostasis during ageing in Caenorhabditis elegans

Abstract

Keywords

ASJC Scopus subject areas

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Regulation of Meiotic Chromosome Segregation by Post-Translational Modifications

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