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A new AMPK isoform mediates glucose-restriction induced longevity non-cell autonomously by promoting membrane fluidity

Author

Listed:
  • Jin-Hyuck Jeong

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB)
    Korea University of Science and Technology (UST))

  • Jun-Seok Han

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB))

  • Youngae Jung

    (Korea Basic Science Institute)

  • Seung-Min Lee

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB))

  • So-Hyun Park

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB)
    Korea University of Science and Technology (UST))

  • Mooncheol Park

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB))

  • Min-Gi Shin

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB))

  • Nami Kim

    (Korea Basic Science Institute)

  • Mi Sun Kang

    (Korea Basic Science Institute)

  • Seokho Kim

    (Dong-A University)

  • Kwang-Pyo Lee

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB)
    Korea University of Science and Technology (UST))

  • Ki-Sun Kwon

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB)
    Korea University of Science and Technology (UST))

  • Chun-A. Kim

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB))

  • Yong Ryoul Yang

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB))

  • Geum-Sook Hwang

    (Korea Basic Science Institute
    Ewha Womans University)

  • Eun-Soo Kwon

    (Korea Research Institute of Bioscience and Biotechnology (KRIBB))

Abstract

Dietary restriction (DR) delays aging and the onset of age-associated diseases. However, it is yet to be determined whether and how restriction of specific nutrients promote longevity. Previous genome-wide screens isolated several Escherichia coli mutants that extended lifespan of Caenorhabditis elegans. Here, using 1H-NMR metabolite analyses and inter-species genetics, we demonstrate that E. coli mutants depleted of intracellular glucose extend C. elegans lifespans, serving as bona fide glucose-restricted (GR) diets. Unlike general DR, GR diets don’t reduce the fecundity of animals, while still improving stress resistance and ameliorating neuro-degenerative pathologies of Aβ42. Interestingly, AAK-2a, a new AMPK isoform, is necessary and sufficient for GR-induced longevity. AAK-2a functions exclusively in neurons to modulate GR-mediated longevity via neuropeptide signaling. Last, we find that GR/AAK-2a prolongs longevity through PAQR-2/NHR-49/Δ9 desaturases by promoting membrane fluidity in peripheral tissues. Together, our studies identify the molecular mechanisms underlying prolonged longevity by glucose specific restriction in the context of whole animals.

Suggested Citation

  • Jin-Hyuck Jeong & Jun-Seok Han & Youngae Jung & Seung-Min Lee & So-Hyun Park & Mooncheol Park & Min-Gi Shin & Nami Kim & Mi Sun Kang & Seokho Kim & Kwang-Pyo Lee & Ki-Sun Kwon & Chun-A. Kim & Yong Ryo, 2023. "A new AMPK isoform mediates glucose-restriction induced longevity non-cell autonomously by promoting membrane fluidity," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-35952-z
    DOI: 10.1038/s41467-023-35952-z
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    1. Cynthia J. Kenyon, 2010. "The genetics of ageing," Nature, Nature, vol. 464(7288), pages 504-512, March.
    2. Seung-Min Lee & Seol Hee Lee & Youngae Jung & Younglang Lee & Jong Hyun Yoon & Jeong Yi Choi & Chae Young Hwang & Young Hoon Son & Sung Sup Park & Geum-Sook Hwang & Kwang-Pyo Lee & Ki-Sun Kwon, 2020. "FABP3-mediated membrane lipid saturation alters fluidity and induces ER stress in skeletal muscle with aging," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    3. Xin Wang & Kang Xia & Xiaojing Yang & Chao Tang, 2019. "Growth strategy of microbes on mixed carbon sources," Nature Communications, Nature, vol. 10(1), pages 1-7, December.
    4. Fajun Yang & Bryan W. Vought & John S. Satterlee & Amy K. Walker & Z.-Y. Jim Sun & Jennifer L. Watts & Rosalie DeBeaumont & R. Mako Saito & Sven G. Hyberts & Shaosong Yang & Christine Macol & Lakshman, 2006. "An ARC/Mediator subunit required for SREBP control of cholesterol and lipid homeostasis," Nature, Nature, vol. 442(7103), pages 700-704, August.
    5. Richard C. Grandison & Matthew D. W. Piper & Linda Partridge, 2009. "Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila," Nature, Nature, vol. 462(7276), pages 1061-1064, December.
    6. Cynthia J. Kenyon, 2010. "Erratum: The genetics of ageing," Nature, Nature, vol. 467(7315), pages 622-622, September.
    7. Toshimasa Yamauchi & Junji Kamon & Yusuke Ito & Atsushi Tsuchida & Takehiko Yokomizo & Shunbun Kita & Takuya Sugiyama & Makoto Miyagishi & Kazuo Hara & Masaki Tsunoda & Koji Murakami & Toshiaki Ohteki, 2003. "Cloning of adiponectin receptors that mediate antidiabetic metabolic effects," Nature, Nature, vol. 423(6941), pages 762-769, June.
    8. Ravi S. Kamath & Andrew G. Fraser & Yan Dong & Gino Poulin & Richard Durbin & Monica Gotta & Alexander Kanapin & Nathalie Le Bot & Sergio Moreno & Marc Sohrmann & David P. Welchman & Peder Zipperlen &, 2003. "Systematic functional analysis of the Caenorhabditis elegans genome using RNAi," Nature, Nature, vol. 421(6920), pages 231-237, January.
    9. 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.
    10. Eun-Soo Kwon & Sri Devi Narasimhan & Kelvin Yen & Heidi A. Tissenbaum, 2010. "A new DAF-16 isoform regulates longevity," Nature, Nature, vol. 466(7305), pages 498-502, July.
    11. Manish Chamoli & Anita Goyala & Syed Shamsh Tabrez & Atif Ahmed Siddiqui & Anupama Singh & Adam Antebi & Gordon J. Lithgow & Jennifer L. Watts & Arnab Mukhopadhyay, 2020. "Polyunsaturated fatty acids and p38-MAPK link metabolic reprogramming to cytoprotective gene expression during dietary restriction," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
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    1. 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.

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