IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-40618-x.html
   My bibliography  Save this article

Early-adulthood spike in protein translation drives aging via juvenile hormone/germline signaling

Author

Listed:
  • Harper S. Kim

    (University of Alabama at Birmingham
    University of Alabama at Birmingham
    University of Texas Health San Antonio
    University of Texas Health San Antonio)

  • Danitra J. Parker

    (University of Alabama at Birmingham
    McGovern Medical School at UTHealth)

  • Madison M. Hardiman

    (University of Alabama at Birmingham)

  • Erin Munkácsy

    (University of Texas Health San Antonio)

  • Nisi Jiang

    (University of Texas Health San Antonio)

  • Aric N. Rogers

    (MDI Biological Laboratory)

  • Yidong Bai

    (University of Texas Health San Antonio
    University of Texas Health San Antonio)

  • Colin Brent

    (USDA-ARS Arid Land Agricultural Research Center)

  • James A. Mobley

    (University of Alabama at Birmingham)

  • Steven N. Austad

    (University of Alabama at Birmingham
    University of Alabama at Birmingham)

  • Andrew M. Pickering

    (University of Alabama at Birmingham
    University of Texas Health San Antonio
    McGovern Medical School at UTHealth
    University of Texas Health San Antonio)

Abstract

Protein translation (PT) declines with age in invertebrates, rodents, and humans. It has been assumed that elevated PT at young ages is beneficial to health and PT ends up dropping as a passive byproduct of aging. In Drosophila, we show that a transient elevation in PT during early-adulthood exerts long-lasting negative impacts on aging trajectories and proteostasis in later-life. Blocking the early-life PT elevation robustly improves life-/health-span and prevents age-related protein aggregation, whereas transiently inducing an early-life PT surge in long-lived fly strains abolishes their longevity/proteostasis benefits. The early-life PT elevation triggers proteostatic dysfunction, silences stress responses, and drives age-related functional decline via juvenile hormone-lipid transfer protein axis and germline signaling. Our findings suggest that PT is adaptively suppressed after early-adulthood, alleviating later-life proteostatic burden, slowing down age-related functional decline, and improving lifespan. Our work provides a theoretical framework for understanding how lifetime PT dynamics shape future aging trajectories.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40618-x
    DOI: 10.1038/s41467-023-40618-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-40618-x
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-40618-x?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. Cynthia J. Kenyon, 2010. "Erratum: The genetics of ageing," Nature, Nature, vol. 467(7315), pages 622-622, September.
    3. Popi Syntichaki & Kostoula Troulinaki & Nektarios Tavernarakis, 2007. "eIF4E function in somatic cells modulates ageing in Caenorhabditis elegans," Nature, Nature, vol. 445(7130), pages 922-926, February.
    Full references (including those not matched with items on IDEAS)

    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. 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.
    2. 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.
    3. 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.
    4. 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.
    5. Huiru Bai & Xiaoqin Liu & Meizhen Lin & Yuan Meng & Ruolan Tang & Yajing Guo & Nan Li & Michael F. Clarke & Shang Cai, 2024. "Progressive senescence programs induce intrinsic vulnerability to aging-related female breast cancer," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    6. Jiangbo Song & Zhiquan Li & Lei Zhou & Xin Chen & Wei Qi Guinevere Sew & Héctor Herranz & Zilu Ye & Jesper Velgaard Olsen & Yuan Li & Marianne Nygaard & Kaare Christensen & Xiaoling Tong & Vilhelm A. , 2024. "FOXO-regulated OSER1 reduces oxidative stress and extends lifespan in multiple species," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    7. 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.
    8. 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.
    9. Zhifei Zhang & Haiyan Yang & Lei Fang & Guangrong Zhao & Jun Xiang & Jialin C. Zheng & Zhao Qin, 2024. "DOS-3 mediates cell-non-autonomous DAF-16/FOXO activity in antagonizing age-related loss of C. elegans germline stem/progenitor cells," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    10. 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.
    11. 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.
    12. Mark G Sterken & L Basten Snoek & Kobus J Bosman & Jikke Daamen & Joost A G Riksen & Jaap Bakker & Gorben P Pijlman & Jan E Kammenga, 2014. "A Heritable Antiviral RNAi Response Limits Orsay Virus Infection in Caenorhabditis elegans N2," PLOS ONE, Public Library of Science, vol. 9(2), pages 1-8, February.
    13. 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.
    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. 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.
    16. Paul R. H. J. Timmers & James F. Wilson & Peter K. Joshi & Joris Deelen, 2020. "Multivariate genomic scan implicates novel loci and haem metabolism in human ageing," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    17. 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.
    18. Smith, Ken R. & Hanson, Heidi A. & Norton, Maria C. & Hollingshaus, Michael S. & Mineau, Geraldine P., 2014. "Survival of offspring who experience early parental death: Early life conditions and later-life mortality," Social Science & Medicine, Elsevier, vol. 119(C), pages 180-190.
    19. Daniele Campa & Francesco De Rango & Maura Carrai & Paolina Crocco & Alberto Montesanto & Federico Canzian & Giuseppina Rose & Cosmeri Rizzato & Giuseppe Passarino & Roberto Barale, 2012. "Bitter Taste Receptor Polymorphisms and Human Aging," PLOS ONE, Public Library of Science, vol. 7(11), pages 1-8, November.
    20. Denisa Margină & Anca Ungurianu & Carmen Purdel & Dimitris Tsoukalas & Evangelia Sarandi & Maria Thanasoula & Fotios Tekos & Robin Mesnage & Demetrios Kouretas & Aristidis Tsatsakis, 2020. "Chronic Inflammation in the Context of Everyday Life: Dietary Changes as Mitigating Factors," IJERPH, MDPI, vol. 17(11), pages 1-27, June.

    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_s41467-023-40618-x. 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.