IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-35952-z.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-35952-z
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-35952-z?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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. Cynthia J. Kenyon, 2010. "Erratum: The genetics of ageing," Nature, Nature, vol. 467(7315), pages 622-622, September.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
    10. 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.
    11. 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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    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.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. 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.
    3. Arles Urrutia & Víctor A García-Angulo & Andrés Fuentes & Mauricio Caneo & Marcela Legüe & Sebastián Urquiza & Scarlett E Delgado & Juan Ugalde & Paula Burdisso & Andrea Calixto, 2020. "Bacterially produced metabolites protect C. elegans neurons from degeneration," PLOS Biology, Public Library of Science, vol. 18(3), pages 1-31, March.
    4. Eirini Lionaki & Ilias Gkikas & Ioanna Daskalaki & Maria-Konstantina Ioannidi & Maria I. Klapa & Nektarios Tavernarakis, 2022. "Mitochondrial protein import determines lifespan through metabolic reprogramming and de novo serine biosynthesis," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    5. Qucheng Deng & Yongping Wei & Lijuan Chen & Wei Liang & Jijun Du & Yuling Tan & Yinjun Zhao, 2019. "Relationship between Air Pollution and Regional Longevity in Guangxi, China," IJERPH, MDPI, vol. 16(19), pages 1-12, October.
    6. Cyril Statzer & Jin Meng & Richard Venz & Monet Bland & Stacey Robida-Stubbs & Krina Patel & Dunja Petrovic & Raffaella Emsley & Pengpeng Liu & Ianessa Morantte & Cole Haynes & William B. Mair & Alban, 2022. "ATF-4 and hydrogen sulfide signalling mediate longevity in response to inhibition of translation or mTORC1," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    7. Xueqing Wang & Quanlong Jiang & Hongdao Zhang & Zhidong He & Yuanyuan Song & Yifan Chen & Na Tang & Yifei Zhou & Yiping Li & Adam Antebi & Ligang Wu & Jing-Dong J. Han & Yidong Shen, 2024. "Tissue-specific profiling of age-dependent miRNAomic changes in Caenorhabditis elegans," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    8. Harper S. Kim & Danitra J. Parker & Madison M. Hardiman & Erin Munkácsy & Nisi Jiang & Aric N. Rogers & Yidong Bai & Colin Brent & James A. Mobley & Steven N. Austad & Andrew M. Pickering, 2023. "Early-adulthood spike in protein translation drives aging via juvenile hormone/germline signaling," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    9. Carlos A. Vergani-Junior & Raíssa De P. Moro & Silas Pinto & Evandro A. De-Souza & Henrique Camara & Deisi L. Braga & Guilherme Tonon-da-Silva & Thiago L. Knittel & Gabriel P. Ruiz & Raissa G. Ludwig , 2024. "An Intricate Network Involving the Argonaute ALG-1 Modulates Organismal Resistance to Oxidative Stress," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    10. 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.
    11. Edouard Debonneuil & Anne Eyraud-Loisel & Frédéric Planchet, 2018. "Can Pension Funds Partially Manage Longevity Risk by Investing in a Longevity Megafund?," Risks, MDPI, vol. 6(3), pages 1-27, July.
    12. Ichiro Kawasaki & Kenta Sugiura & Taeko Sasaki & Noriyuki Matsuda & Miyuki Sato & Ken Sato, 2024. "MARC-3, a membrane-associated ubiquitin ligase, is required for fast polyspermy block in Caenorhabditis elegans," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    13. Hope Dang & Raul Castro-Portuguez & Luis Espejo & Grant Backer & Samuel Freitas & Erica Spence & Jeremy Meyers & Karissa Shuck & Emily A. Gardea & Leah M. Chang & Jonah Balsa & Niall Thorns & Caroline, 2023. "On the benefits of the tryptophan metabolite 3-hydroxyanthranilic acid in Caenorhabditis elegans and mouse aging," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    14. Qucheng Deng & Lijuan Chen & Yongping Wei & Yonghua Li & Xuerong Han & Wei Liang & Yinjun Zhao & Xiaofei Wang & Juan Yin, 2018. "Understanding the Association between Environmental Factors and Longevity in Hechi, China: A Drinking Water and Soil Quality Perspective," IJERPH, MDPI, vol. 15(10), pages 1-17, October.
    15. Klement Stojanovski & Ioana Gheorghe & Peter Lenart & Anne Lanjuin & William B. Mair & Benjamin D. Towbin, 2023. "Maintenance of appropriate size scaling of the C. elegans pharynx by YAP-1," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    16. Maria Thürmer & André Gollowitzer & Helmut Pein & Konstantin Neukirch & Elif Gelmez & Lorenz Waltl & Natalie Wielsch & René Winkler & Konstantin Löser & Julia Grander & Madlen Hotze & Sönke Harder & A, 2022. "PI(18:1/18:1) is a SCD1-derived lipokine that limits stress signaling," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    17. Justin G. Boyer & Jiuzhou Huo & Sarah Han & Julian R. Havens & Vikram Prasad & Brian L. Lin & David A. Kass & Taejeong Song & Sakthivel Sadayappan & Ramzi J. Khairallah & Christopher W. Ward & Jeffery, 2022. "Depletion of skeletal muscle satellite cells attenuates pathology in muscular dystrophy," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    18. Malaguti, Giulia & Singh, Param Priya & Isambert, Hervé, 2014. "On the retention of gene duplicates prone to dominant deleterious mutations," Theoretical Population Biology, Elsevier, vol. 93(C), pages 38-51.
    19. Mustafa C. Camur & Thomas Sharkey & Chrysafis Vogiatzis, 2022. "The Star Degree Centrality Problem: A Decomposition Approach," INFORMS Journal on Computing, INFORMS, vol. 34(1), pages 93-112, January.
    20. Samim Sharifi & Prerana Chaudhari & Asya Martirosyan & Alexander Otto Eberhardt & Finja Witt & André Gollowitzer & Lisa Lange & Yvonne Woitzat & Eberechukwu Maryann Okoli & Huahui Li & Norman Rahnis &, 2024. "Reducing the metabolic burden of rRNA synthesis promotes healthy longevity in Caenorhabditis elegans," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-35952-z. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.