Autophagy mediates the mitotic senescence transition
Open accessAbstract
As a stress response, senescence is a dynamic process involving multiple effector mechanisms whose combination determines the phenotypic quality. Here we identify autophagy as a new effector mechanism of senescence. Autophagy is activated during senescence and its activation is correlated with negative feedback in the PI3K–mammalian target of rapamycin (mTOR) pathway. A subset of autophagy-related genes are up-regulated during senescence: Overexpression of one of those genes, ULK3, induces autophagy and senescence. Furthermore, inhibition of autophagy delays the senescence phenotype, including senescence-associated secretion. Our data suggest that autophagy, and its consequent protein turnover, mediate the acquisition of the senescence phenotype.
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The functional relevance of autophagy in senescence varies depending on cell type and senescence triggers.
“Some studies have touched on the functional relevance of autophagy in senescence, where its role appears to vary depending on cell type and senescence triggers (Patschan et al. 2007; Young et al. 2009; Leidal et al. 2012; Mosieniak et al. 2012; Singh et al. 2012; Dörr et al. 2013).”
From Cellular senescence and its effector programs (2014) · cites this paper as Young et al. 2009
The introduction (page not provided) says the relative contribution of senescence effectors varies with trigger and cell type, and the Results and Discussion show that autophagy contributes to senescence establishment. The paper does not show that autophagy’s own role in senescence varies across cell types or triggers. (LLM, conf=0.86)
Experimental — accuracy not yet measuredIn preclinical models, proteotoxic stress not only drives entry into a senescent state, but also activates autophagy, which buffers toxicity from misfolded SASP factors.
“In preclinical models, proteotoxic stress not only drives entry into a senescent state, but also activates autophagy, which consequently buffers toxicity from misfolded SASP factors 44,45 .”
From Senescence and cancer — role and therapeutic opportunities (2022) · cites this paper as [44]
The Results and Discussion (page not provided) report that autophagy is activated during oncogene-induced senescence and that inhibiting it delays production of the secreted factors IL6 and IL8. The paper does not establish that proteotoxic stress drives senescence or activates autophagy, or that autophagy buffers toxicity from misfolded SASP factors. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe kinetics of these gene expression changes were similar to that of SASP components, implying some level of correlation between autophagy and the SASP.
“The kinetics of these gene expression changes were similar to that of SASP components, implying some level of correlation between autophagy and the SASP.”
From Cellular senescence and its effector programs (2014) · cites this paper as Young et al. 2009
Autophagy is activated during the dynamic phase of OIS in HDFs, accompanied by concerted up-regulation of genes involved in autophagy and lysosomal biogenesis.
“We recently showed that autophagy is activated during the dynamic phase of OIS in HDFs, which was accompanied by a concerted up-regulation of genes involved in both autophagy and lysosomal biogenesis (Young et al. 2009).”
From Cellular senescence and its effector programs (2014) · cites this paper as Young et al. 2009
Inhibition of autophagy suppressed production of both IL6 and IL8 and delayed establishment of senescence.
“Indeed, inhibition of autophagy suppressed the production of both IL6 and IL8 and delayed the establishment of senescence.”
From Cellular senescence and its effector programs (2014) · cites this paper as Young et al. 2009
Autophagy has been implicated in establishing the SASP through the TOR autophagy spatial coupling compartment (TASCC).
“macro-autophagy (hereafter referred to as autophagy)—a tightly regulated major lysosomal degradation pathway (27–30)—has been implicated in establishing the SASP through the target of rapamycin (TOR) autophagy spatial coupling compartment (TASCC).”
From The DNA damage response induces inflammation and senescence by inhibiting autophagy of GATA4. (2015) · cites this paper as [31]
Autophagy is both a negative and a positive regulator of senescence, resolving apparently contradictory reports in the literature.
“Our results indicate that autophagy is both a negative and a positive regulator of senescence, resolving apparently contradictory reports in the literature (31–33, 44).”
From The DNA damage response induces inflammation and senescence by inhibiting autophagy of GATA4. (2015) · cites this paper as [31]
Senescent cells use autophagy for their maintenance.
“These cells use autophagy for their maintenance”
From p21 maintains senescent cell viability under persistent DNA damage response by restraining JNK and caspase signaling (2017) · cites this paper as Young et al, 2009
Autophagy is activated during senescence.
“Autophagy is activated during senescence”
From Inside and out: the activities of senescence in cancer (2014) · cites this paper as [59]
Autophagy is dynamically activated during OIS and facilitates synthesis of IL-6 and IL-8, major SASP components.
“Autophagy is dynamically activated during OIS and facilitates the synthesis of interleukin 6 (IL-6) and IL-8, major components of the SASP 58,59 .”
From Inside and out: the activities of senescence in cancer (2014) · cites this paper as [59]
Inhibition of autophagy delays onset of senescence and SASP.
“and that the inhibition of autophagy delays of onset of senescence and SASP.”
From Inside and out: the activities of senescence in cancer (2014) · cites this paper as [59]
Autophagy is required for execution of the senescence program because its inhibition delays senescence-related cell cycle arrest and SASP factor accumulation, at least in OIS.
“Autophagy is also required for the execution of the senescence program because its inhibition delays the senescence-related cell cycle arrest and SASP factor accumulation, at least in OIS [244].”
From Mechanisms and Regulation of Cellular Senescence (2021) · cites this paper as [244]
In oncogenic Ras-induced senescence, protein synthesis and autophagic degradation are simultaneously activated, and the same cell displays high autophagic activity and activated mTOR.
“In senescence induced by oncogenic Ras, protein synthesis and autophagic degradation are simultaneous activated, and the same cell displays high autophagic activity and activated mTOR, the autophagy inhibitor [244].”
From Mechanisms and Regulation of Cellular Senescence (2021) · cites this paper as [244]
Autophagy is required for some instances of cell-autonomous tumor suppression by senescence (e.g., oncogene-induced senescence caused by HRAS V12 and BRAF V600E) and cell death (e.g., ferroptosis).
“Moreover, autophagy is required for some instances of cell-autonomous tumor suppression by senescence (e.g., in oncogene-induced senescence caused by HRAS V12 and BRAF V600E ) 156,157 and cell death (e.g., in the context of ferroptosis) 158 (Figure 3A).”
From Meta-hallmarks of aging and cancer (2023) · cites this paper as [156]
Proficient autophagy is required for the successful establishment of oncogene-induced senescence.
“Of note, proficient autophagy is required for the successful establishment of OIS.156”
From Meta-hallmarks of aging and cancer (2023) · cites this paper as [156]
BNIP3L encodes BCL2 interacting protein 3 like, is typically thought pro-apoptotic, but anti-apoptotic roles have been discovered in reactive astrocytes during ALS, and it increases in senescent cells to direct mitochondria to autophagosomes for degradation.
“Although BNIP3L is typically thought of as pro-apoptotic [181], anti-apoptotic roles have been recently discovered, particularly in reactive astrocytes during ALS disease progression [35]. Similarly, BNIP3L has been shown to increase in senescent cells to direct mitochondria to autophagosomes for degradation [174].”
From Early onset senescence and cognitive impairment in a murine model of repeated mTBI (2021) · cites this paper as [174]
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- Authors
- Young, A. R. J., Narita, M., Ferreira, M., Kirschner, K., Sadaie, M., Darot, J. F. J., Tavaré, S., Arakawa, S., Shimizu, S., Watt, F. M., & Narita, M.
- Affiliations
- Cancer Research UK (GB)
- European Bioinformatics Institute (GB)
- Tokyo Medical and Dental University (JP)
- ORCID
- Venue
- Genes & Development
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2009-03-11
- Volume
- 23
- Issue
- 7
- Pages
- 798-803
- ISSN
- 0890-9369 (ISSN-L)
- 1549-5477
- PMC
- PMC2666340
- OpenAlex
- W2113995129
- Cited by
- 1,078
- References
- 39
- Citations by year
- 2026: 19 · 2025: 36 · 2024: 53 · 2023: 56 · 2022: 62 · 2021: 90 · 2020: 64 · 2019: 52 · 2018: 70 · 2017: 64 · 2016: 78 · 2015: 60 · 2014: 78 · 2013: 86 · 2012: 72
- Type
- posted content
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genes & Development (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Research Portal (King's College London) (submittedVersion)
- Funders
- Cancer Research UK (19556)
- University of Cambridge
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- autophagy, cellular senescence, PI3K/mTOR pathway, ULK3, protein turnover, negative feedback regulation, autophagy-related genes
- MeSH terms
- Aging, Autophagy, Gene Expression Regulation, Humans, Immunohistochemistry, Microtubule-Associated Proteins, Mitosis, Neoplasms, Protein Kinases, Protein Serine-Threonine Kinases, Feedback, Physiological, TOR Serine-Threonine Kinases
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