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The unfolded protein response reverses the effects of glucose on lifespan in chemically-sterilized C. elegans

Author

Listed:
  • Caroline Beaudoin-Chabot

    (Nanyang Technological University)

  • Lei Wang

    (Nanyang Technological University
    University of Miami Miller School of Medicine)

  • Cenk Celik

    (Nanyang Technological University)

  • Aishah Tul-Firdaus Abdul Khalid

    (Nanyang Technological University)

  • Subhash Thalappilly

    (Nanyang Technological University)

  • Shiyi Xu

    (Nanyang Technological University)

  • Jhee Hong Koh

    (Nanyang Technological University)

  • Venus Wen Xuan Lim

    (Nanyang Technological University)

  • Ann Don Low

    (Nanyang Technological University)

  • Guillaume Thibault

    (Nanyang Technological University
    National University of Singapore
    Institute of Molecular and Cell Biology, A*STAR)

Abstract

Metabolic diseases often share common traits, including accumulation of unfolded proteins in the endoplasmic reticulum (ER). Upon ER stress, the unfolded protein response (UPR) is activated to limit cellular damage which weakens with age. Here, we show that Caenorhabditis elegans fed a bacterial diet supplemented high glucose at day 5 of adulthood (HGD-5) extends their lifespan, whereas exposed at day 1 (HGD-1) experience shortened longevity. We observed a metabolic shift only in HGD-1, while glucose and infertility synergistically prolonged the lifespan of HGD-5, independently of DAF-16. Notably, we identified that UPR stress sensors ATF-6 and PEK-1 contributed to the longevity of HGD-5 worms, while ire-1 ablation drastically increased HGD-1 lifespan. Together, we postulate that HGD activates the otherwise quiescent UPR in aged worms to overcome ageing-related stress and restore ER homeostasis. In contrast, young animals subjected to HGD provokes unresolved ER stress, conversely leading to a detrimental stress response.

Suggested Citation

  • Caroline Beaudoin-Chabot & Lei Wang & Cenk Celik & Aishah Tul-Firdaus Abdul Khalid & Subhash Thalappilly & Shiyi Xu & Jhee Hong Koh & Venus Wen Xuan Lim & Ann Don Low & Guillaume Thibault, 2022. "The unfolded protein response reverses the effects of glucose on lifespan in chemically-sterilized C. elegans," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33630-0
    DOI: 10.1038/s41467-022-33630-0
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    References listed on IDEAS

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    1. Cynthia J. Kenyon, 2010. "The genetics of ageing," Nature, Nature, vol. 464(7288), pages 504-512, March.
    2. Cynthia J. Kenyon, 2010. "Erratum: The genetics of ageing," Nature, Nature, vol. 467(7315), pages 622-622, September.
    3. Patrick Narbonne & Richard Roy, 2009. "Caenorhabditis elegans dauers need LKB1/AMPK to ration lipid reserves and ensure long-term survival," Nature, Nature, vol. 457(7226), pages 210-214, January.
    4. Scott B. Vafai & Vamsi K. Mootha, 2012. "Mitochondrial disorders as windows into an ancient organelle," Nature, Nature, vol. 491(7424), pages 374-383, November.
    5. Javier Apfeld & Cynthia Kenyon, 1999. "Regulation of lifespan by sensory perception in Caenorhabditis elegans," Nature, Nature, vol. 402(6763), pages 804-809, December.
    6. Caspersen, C.J. & Thomas, G.D. & Boseman, L.A. & Beckles, G.L.A. & Albright, A.L., 2012. "Aging, diabetes, and the public health system in the United States," American Journal of Public Health, American Public Health Association, vol. 102(8), pages 1482-1497.
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