Senolytic therapy alleviates physiological human brain aging and COVID-19 neuropathology
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Abstract
Aging is a major risk factor for neurodegenerative diseases, and coronavirus disease 2019 (COVID-19) is linked to severe neurological manifestations. Senescent cells contribute to brain aging, but the impact of virus-induced senescence on neuropathologies is unknown. Here we show that senescent cells accumulate in aged human brain organoids and that senolytics reduce age-related inflammation and rejuvenate transcriptomic aging clocks. In postmortem brains of patients with severe COVID-19 we observed increased senescent cell accumulation compared with age-matched controls. Exposure of human brain organoids to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) induced cellular senescence, and transcriptomic analysis revealed a unique SARS-CoV-2 inflammatory signature. Senolytic treatment of infected brain organoids blocked viral replication and prevented senescence in distinct neuronal populations. In human-ACE2-overexpressing mice, senolytics improved COVID-19 clinical outcomes, promoted dopaminergic neuron survival and alleviated viral and proinflammatory gene expression. Collectively our results demonstrate an important role for cellular senescence in driving brain aging and SARS-CoV-2-induced neuropathology, and a therapeutic benefit of senolytic treatments.
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- Authors
- Aguado, J., Amarilla, A. A., Taherian Fard, A., Albornoz, E. A., Tyshkovskiy, A., Schwabenland, M., Chaggar, H. K., Modhiran, N., Gómez-Inclán, C., Javed, I., Baradar, A. A., Liang, B., Peng, L., Dharmaratne, M., Pietrogrande, G., Padmanabhan, P., Freney, M. E., Parry, R., Sng, J. D. J., Isaacs, A., Khromykh, A. A., Valenzuela Nieto, G., Rojas-Fernandez, A., Davis, T. P., Prinz, M., Bengsch, B., Gladyshev, V. N., Woodruff, T. M., Mar, J. C., Watterson, D., & Wolvetang, E. J.
- Affiliations
- The University of Queensland (AU)
- Brigham and Women's Hospital (US)
- University of Freiburg (DE)
- Broad Institute (US)
- Corresponding author
- Aguado, Julio
- ORCID
- Aguado, Julio
- Amarilla, Alberto A.
- Taherian Fard, Atefeh
- Albornoz, Eduardo A.
- Tyshkovskiy, Alexander
- Schwabenland, Marius
- Modhiran, Naphak
- Javed, Ibrahim
- Baradar, Alireza A.
- Liang, Benjamin
- Peng, Lianli
- Dharmaratne, Malindrie
- Pietrogrande, Giovanni
- Padmanabhan, Pranesh
- Freney, Morgan E.
- Parry, Rhys
- Sng, Julian D. J.
- Isaacs, Ariel
- Khromykh, Alexander A.
- Davis, Thomas P.
- Prinz, Marco
- Bengsch, Bertram
- Gladyshev, Vadim N.
- Woodruff, Trent M.
- Mar, Jessica C.
- Watterson, Daniel
- Wolvetang, Ernst J.
- Venue
- Nature Aging
- Published
- 2023-11-13
- Volume
- 3
- Issue
- 12
- Pages
- 1561-1575
- ISSN
- 2662-8465 (ISSN-L)
- PMC
- PMC10724067
- OpenAlex
- W4388626094
- Cited by
- 80
- References
- 69
- Citations by year
- 2026: 29 · 2025: 29 · 2024: 17 · 2023: 5
- FWCI
- 14.13
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Nature Aging (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nd)
- Research Square (acceptedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- UniSA Research Outputs Repository (University of South Australia) (submittedVersion, cc-by)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion, cc-by)
- Funders
- Brigham and Women's Hospital
- Children's Hospital Foundation
- Broad Institute
- University of Oxford
- Deutsche Forschungsgemeinschaft (413517907)
- Fondation Jérôme Lejeune
- University of South Australia
- University of Queensland (UQECR2058457)
- Albert-Ludwigs-Universität Freiburg
- Universidad Austral de Chile
- Lomonosov Moscow State University
- Agencia Nacional de Investigación y Desarrollo (3220635, 1200427)
- Medical Research Council
- Australian Research Council (DP210103401)
- National Health and Medical Research Council (2012883, 2001408, 2009957)
- Queensland Brain Institute
- Medizinische Fakultät der Albert-Ludwigs-Universität Freiburg
- Topics
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Keywords
- senolytic therapy, cellular senescence, brain aging, SARS-CoV-2, human brain organoids, age-related inflammation, dopaminergic neurons, neuroinflammation, viral replication, neurodegeneration
- MeSH terms
- COVID-19, SARS-CoV-2, Senotherapeutics, Aged, Aging, Animals, Brain, Humans, Mice
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