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The TFEB orthologue HLH-30 regulates autophagy and modulates longevity in Caenorhabditis elegans

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  • Louis R. Lapierre

    (Program of Development and Aging, Del E Webb Neuroscience, Aging and Stem Cell Research Center, Sanford-Burnham Medical Research Institute)

  • C. Daniel De Magalhaes Filho

    (The Howard Hughes Medical Institute, The Glenn Center for Aging Research, The Salk Institute for Biological Studies)

  • Philip R. McQuary

    (Program of Development and Aging, Del E Webb Neuroscience, Aging and Stem Cell Research Center, Sanford-Burnham Medical Research Institute
    Graduate School of Biomedical Sciences, Sanford-Burnham Medical Research Institute)

  • Chu-Chiao Chu

    (Program of Development and Aging, Del E Webb Neuroscience, Aging and Stem Cell Research Center, Sanford-Burnham Medical Research Institute)

  • Orane Visvikis

    (Massachusetts General Hospital, Harvard Medical School)

  • Jessica T. Chang

    (Program of Development and Aging, Del E Webb Neuroscience, Aging and Stem Cell Research Center, Sanford-Burnham Medical Research Institute)

  • Sara Gelino

    (Program of Development and Aging, Del E Webb Neuroscience, Aging and Stem Cell Research Center, Sanford-Burnham Medical Research Institute
    Graduate School of Biomedical Sciences, Sanford-Burnham Medical Research Institute)

  • Binnan Ong

    (Program of Development and Aging, Del E Webb Neuroscience, Aging and Stem Cell Research Center, Sanford-Burnham Medical Research Institute)

  • Andrew E. Davis

    (Program of Development and Aging, Del E Webb Neuroscience, Aging and Stem Cell Research Center, Sanford-Burnham Medical Research Institute)

  • Javier E. Irazoqui

    (Massachusetts General Hospital, Harvard Medical School)

  • Andrew Dillin

    (The Howard Hughes Medical Institute, The Glenn Center for Aging Research, The Salk Institute for Biological Studies)

  • Malene Hansen

    (Program of Development and Aging, Del E Webb Neuroscience, Aging and Stem Cell Research Center, Sanford-Burnham Medical Research Institute)

Abstract

Autophagy is a cellular recycling process that has an important anti-aging role, but the underlying molecular mechanism is not well understood. The mammalian transcription factor EB (TFEB) was recently shown to regulate multiple genes in the autophagy process. Here we show that the predicted TFEB orthologue HLH-30 regulates autophagy in Caenorhabditis elegans and, in addition, has a key role in lifespan determination. We demonstrate that hlh-30 is essential for the extended lifespan of Caenorhabditis elegans in six mechanistically distinct longevity models, and overexpression of HLH-30 extends lifespan. Nuclear localization of HLH-30 is increased in all six Caenorhabditis elegans models and, notably, nuclear TFEB levels are augmented in the livers of mice subjected to dietary restriction, a known longevity-extending regimen. Collectively, our results demonstrate a conserved role for HLH-30 and TFEB in autophagy, and possibly longevity, and identify HLH-30 as a uniquely important transcription factor for lifespan modulation in Caenorhabditis elegans.

Suggested Citation

  • Louis R. Lapierre & C. Daniel De Magalhaes Filho & Philip R. McQuary & Chu-Chiao Chu & Orane Visvikis & Jessica T. Chang & Sara Gelino & Binnan Ong & Andrew E. Davis & Javier E. Irazoqui & Andrew Dill, 2013. "The TFEB orthologue HLH-30 regulates autophagy and modulates longevity in Caenorhabditis elegans," Nature Communications, Nature, vol. 4(1), pages 1-8, October.
    • Handle: RePEc:nat:natcom:v:4:y:2013:i:1:d:10.1038_ncomms3267
    DOI: 10.1038/ncomms3267
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    Cited by:

    1. Silvia Maglioni & Alfonso Schiavi & Marlen Melcher & Vanessa Brinkmann & Zhongrui Luo & Anna Laromaine & Nuno Raimundo & Joel N. Meyer & Felix Distelmaier & Natascia Ventura, 2022. "Neuroligin-mediated neurodevelopmental defects are induced by mitochondrial dysfunction and prevented by lutein in C. elegans," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    2. Yan-Ping Zhang & Wen-Hong Zhang & Pan Zhang & Qi Li & Yue Sun & Jia-Wen Wang & Shaobing O. Zhang & Tao Cai & Cheng Zhan & Meng-Qiu Dong, 2022. "Intestine-specific removal of DAF-2 nearly doubles lifespan in Caenorhabditis elegans with little fitness cost," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    3. Elite Possik & Laura-Lee Klein & Perla Sanjab & Ruyuan Zhu & Laurence Côté & Ying Bai & Dongwei Zhang & Howard Sun & Anfal Al-Mass & Abel Oppong & Rasheed Ahmad & Alex Parker & S.R. Murthy Madiraju & , 2023. "Glycerol 3-phosphate phosphatase/PGPH-2 counters metabolic stress and promotes healthy aging via a glycogen sensing-AMPK-HLH-30-autophagy axis in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. Nan Wu & Yi-Cheng Ma & Xin-Qian Gong & Pei-Ji Zhao & Yong-Jian Jia & Qiu Zhao & Jia-Hong Duan & Cheng-Gang Zou, 2023. "The metabolite alpha-ketobutyrate extends lifespan by promoting peroxisomal function in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    5. Ian F. Price & Jillian A. Wagner & Benjamin Pastore & Hannah L. Hertz & Wen Tang, 2023. "C. elegans germ granules sculpt both germline and somatic RNAome," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    6. Eleonora Khabirova & Aileen Moloney & Stefan J Marciniak & Julie Williams & David A Lomas & Stephen G Oliver & Giorgio Favrin & David B Sattelle & Damian C Crowther, 2014. "The TRiC/CCT Chaperone Is Implicated in Alzheimer's Disease Based on Patient GWAS and an RNAi Screen in Aβ-Expressing Caenorhabditis elegans," PLOS ONE, Public Library of Science, vol. 9(7), pages 1-13, July.

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