IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v16y2025i1d10.1038_s41467-025-60542-6.html
   My bibliography  Save this article

Aging and diet alter the protein ubiquitylation landscape in the mouse brain

Author

Listed:
  • Antonio Marino

    (Leibniz Institute on Aging—Fritz Lipmann Institute (FLI)
    University of Copenhagen)

  • Domenico Fraia

    (Leibniz Institute on Aging—Fritz Lipmann Institute (FLI)
    University of Rochester)

  • Diana Panfilova

    (Leibniz Institute on Aging—Fritz Lipmann Institute (FLI)
    UNIL—Université de Lausanne)

  • Amit Kumar Sahu

    (Leibniz Institute on Aging—Fritz Lipmann Institute (FLI))

  • Alberto Minetti

    (Leibniz Institute on Aging—Fritz Lipmann Institute (FLI))

  • Omid Omrani

    (Leibniz Institute on Aging—Fritz Lipmann Institute (FLI))

  • Emilio Cirri

    (Leibniz Institute on Aging—Fritz Lipmann Institute (FLI))

  • Alessandro Ori

    (Leibniz Institute on Aging—Fritz Lipmann Institute (FLI)
    Genentech Inc.)

Abstract

Post-translational modifications (PTMs) regulate protein homeostasis, but how aging impacts PTMs remains unclear. Here, we used mass spectrometry to reveal changes in hundreds of protein ubiquitylation, acetylation, and phosphorylation sites in the mouse aging brain. We show that aging has a major impact on protein ubiquitylation. 29% of the quantified ubiquitylation sites were affected independently of protein abundance, indicating altered PTM stoichiometry. Using iPSC-derived neurons, we estimated that 35% of ubiquitylation changes observed in the aged brain can be attributed to reduced proteasome activity. Finally, we tested whether protein ubiquitylation in the brain can be influenced by dietary intervention. We found that one cycle of dietary restriction and re-feeding modifies the brain ubiquitylome, rescuing some but exacerbating other ubiquitylation changes observed in old brains. Our findings reveal an age-dependent ubiquitylation signature modifiable by dietary intervention, providing insights into mechanisms of protein homeostasis impairment and highlighting potential biomarkers of brain aging.

Suggested Citation

  • Antonio Marino & Domenico Fraia & Diana Panfilova & Amit Kumar Sahu & Alberto Minetti & Omid Omrani & Emilio Cirri & Alessandro Ori, 2025. "Aging and diet alter the protein ubiquitylation landscape in the mouse brain," Nature Communications, Nature, vol. 16(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-60542-6
    DOI: 10.1038/s41467-025-60542-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-025-60542-6
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-025-60542-6?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. Matt Ulgherait & Adil M. Midoun & Scarlet J. Park & Jared A. Gatto & Samantha J. Tener & Julia Siewert & Naomi Klickstein & Julie C. Canman & William W. Ja & Mimi Shirasu-Hiza, 2021. "Circadian autophagy drives iTRF-mediated longevity," Nature, Nature, vol. 598(7880), pages 353-358, October.
    2. Shinya Imada & Saleh Khawaled & Heaji Shin & Sven W. Meckelmann & Charles A. Whittaker & Renan Oliveira Corrêa & Chiara Alquati & Yixin Lu & Guodong Tie & Dikshant Pradhan & Gizem Calibasi-Kocal & Lui, 2024. "Short-term post-fast refeeding enhances intestinal stemness via polyamines," Nature, Nature, vol. 633(8031), pages 895-904, September.
    3. John D. Storey, 2002. "A direct approach to false discovery rates," Journal of the Royal Statistical Society Series B, Royal Statistical Society, vol. 64(3), pages 479-498, August.
    4. Fredrik Trulsson & Vyacheslav Akimov & Mihaela Robu & Nila Overbeek & David Aureliano Pérez Berrocal & Rashmi G. Shah & Jürgen Cox & Girish M. Shah & Blagoy Blagoev & Alfred C. O. Vertegaal, 2022. "Deubiquitinating enzymes and the proteasome regulate preferential sets of ubiquitin substrates," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    5. David Vilchez & Isabel Saez & Andrew Dillin, 2014. "The role of protein clearance mechanisms in organismal ageing and age-related diseases," Nature Communications, Nature, vol. 5(1), pages 1-13, December.
    6. Simone Sanzo & Katrin Spengler & Anja Leheis & Joanna M. Kirkpatrick & Theresa L. Rändler & Tim Baldensperger & Therese Dau & Christian Henning & Luca Parca & Christian Marx & Zhao-Qi Wang & Marcus A., 2021. "Mapping protein carboxymethylation sites provides insights into their role in proteostasis and cell proliferation," Nature Communications, Nature, vol. 12(1), pages 1-22, December.
    7. Hansruedi Mathys & Carles A. Boix & Leyla Anne Akay & Ziting Xia & Jose Davila-Velderrain & Ayesha P. Ng & Xueqiao Jiang & Ghada Abdelhady & Kyriaki Galani & Julio Mantero & Neil Band & Benjamin T. Ja, 2024. "Single-cell multiregion dissection of Alzheimer’s disease," Nature, Nature, vol. 632(8026), pages 858-868, August.
    8. Seda Koyuncu & Rute Loureiro & Hyun Ju Lee & Prerana Wagle & Marcus Krueger & David Vilchez, 2021. "Rewiring of the ubiquitinated proteome determines ageing in C. elegans," Nature, Nature, vol. 596(7871), pages 285-290, August.
    9. Eugenio F. Fornasiero & Sunit Mandad & Hanna Wildhagen & Mihai Alevra & Burkhard Rammner & Sarva Keihani & Felipe Opazo & Inga Urban & Till Ischebeck & M. Sadman Sakib & Maryam K. Fard & Koray Kirli &, 2018. "Precisely measured protein lifetimes in the mouse brain reveal differences across tissues and subcellular fractions," Nature Communications, Nature, vol. 9(1), pages 1-17, December.
    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. Wenjing Yan & Yongwang Zhong & Xin Hu & Tuan Xu & Yinghua Zhang & Stephen Kales & Yanyan Qu & Daniel C. Talley & Bolormaa Baljinnyam & Christopher A. LeClair & Anton Simeonov & Brian M. Polster & Ruil, 2023. "Auranofin targets UBA1 and enhances UBA1 activity by facilitating ubiquitin trans-thioesterification to E2 ubiquitin-conjugating enzymes," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Wen Shi & Xi Chen & Jennifer Shang, 2019. "An Efficient Morris Method-Based Framework for Simulation Factor Screening," INFORMS Journal on Computing, INFORMS, vol. 31(4), pages 745-770, October.
    3. Jianqing Fan & Xu Han, 2017. "Estimation of the false discovery proportion with unknown dependence," Journal of the Royal Statistical Society Series B, Royal Statistical Society, vol. 79(4), pages 1143-1164, September.
    4. Shigeyuki Matsui & Hisashi Noma, 2011. "Estimating Effect Sizes of Differentially Expressed Genes for Power and Sample-Size Assessments in Microarray Experiments," Biometrics, The International Biometric Society, vol. 67(4), pages 1225-1235, December.
    5. Lianming Wang & David B. Dunson, 2010. "Semiparametric Bayes Multiple Testing: Applications to Tumor Data," Biometrics, The International Biometric Society, vol. 66(2), pages 493-501, June.
    6. B. Moerkerke & E. Goetghebeur & J. De Riek & I. Roldán‐Ruiz, 2006. "Significance and impotence: towards a balanced view of the null and the alternative hypotheses in marker selection for plant breeding," Journal of the Royal Statistical Society Series A, Royal Statistical Society, vol. 169(1), pages 61-79, January.
    7. Zaili Fang & Inyoung Kim & Jeesun Jung, 2018. "Semiparametric Kernel-Based Regression for Evaluating Interaction Between Pathway Effect and Covariate," Journal of Agricultural, Biological and Environmental Statistics, Springer;The International Biometric Society;American Statistical Association, vol. 23(1), pages 129-152, March.
    8. Timothy B. Armstrong, 2014. "Adaptive Testing on a Regression Function at a Point," Cowles Foundation Discussion Papers 1957R, Cowles Foundation for Research in Economics, Yale University, revised Feb 2015.
    9. Nucera, Federico & Valente, Giorgio, 2013. "Carry trades and the performance of currency hedge funds," Journal of International Money and Finance, Elsevier, vol. 33(C), pages 407-425.
    10. Nickole Moon & Christopher P. Morgan & Ruth Marx-Rattner & Alyssa Jeng & Rachel L. Johnson & Ijeoma Chikezie & Carmen Mannella & Mary D. Sammel & C. Neill Epperson & Tracy L. Bale, 2024. "Stress increases sperm respiration and motility in mice and men," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    11. Iain Melvin & Jason Weston & William Stafford Noble & Christina Leslie, 2011. "Detecting Remote Evolutionary Relationships among Proteins by Large-Scale Semantic Embedding," PLOS Computational Biology, Public Library of Science, vol. 7(1), pages 1-8, January.
    12. Chen, Song Xi & Guo, Bin & Qiu, Yumou, 2023. "Testing and signal identification for two-sample high-dimensional covariances via multi-level thresholding," Journal of Econometrics, Elsevier, vol. 235(2), pages 1337-1354.
    13. West, Kenneth D., 2006. "Forecast Evaluation," Handbook of Economic Forecasting, in: G. Elliott & C. Granger & A. Timmermann (ed.), Handbook of Economic Forecasting, edition 1, volume 1, chapter 3, pages 99-134, Elsevier.
    14. Psaradellis, Ioannis & Laws, Jason & Pantelous, Athanasios A. & Sermpinis, Georgios, 2023. "Technical analysis, spread trading, and data snooping control," International Journal of Forecasting, Elsevier, vol. 39(1), pages 178-191.
    15. Dvorkin Daniel & Biehs Brian & Kechris Katerina, 2013. "A graphical model method for integrating multiple sources of genome-scale data," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 12(4), pages 469-487, August.
    16. Robert A. Connolly & Richard J. Rendleman, 2012. "What It Takes to Win on the PGA TOUR (If Your Name Is “Tiger” or If It Isn't)," Interfaces, INFORMS, vol. 42(6), pages 554-576, December.
    17. Alina C. Teuscher & Cyril Statzer & Anita Goyala & Seraina A. Domenig & Ingmar Schoen & Max Hess & Alexander M. Hofer & Andrea Fossati & Viola Vogel & Orcun Goksel & Ruedi Aebersold & Collin Y. Ewald, 2024. "Longevity interventions modulate mechanotransduction and extracellular matrix homeostasis in C. elegans," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    18. Yi Guo & Ge Yang & Haijiao Liu & Jin Chai & Jie Chen & John Shanklin & Qun Liu & Bin Liu & Min Lu, 2025. "Structure and mechanism of human vesicular polyamine transporter," Nature Communications, Nature, vol. 16(1), pages 1-16, December.
    19. Yuan Zhao, 2014. "Cross-sector fund performance comparison: the role of real estate mutual funds," ERES eres2014_213, European Real Estate Society (ERES).
    20. Wang Chamont & Gevertz Jana L., 2016. "Finding causative genes from high-dimensional data: an appraisal of statistical and machine learning approaches," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 15(4), pages 321-347, August.

    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:16:y:2025:i:1:d:10.1038_s41467-025-60542-6. 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.