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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
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    1. 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.
    2. 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.
    3. 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.
    4. 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.
    5. 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.
    6. 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.
    7. 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.
    8. 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.
    9. 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.
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