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Autophagy impairment with lysosomal and mitochondrial dysfunction is an important characteristic of oxidative stress-induced senescence
Open accessAbstract
Macroautophagy/autophagy has profound implications for aging. However, the true features of autophagy in the progression of aging remain to be clarified. In the present study, we explored the status of autophagic flux during the development of cell senescence induced by oxidative stress. In this system, although autophagic structures increased, the degradation of SQSTM1/p62 protein, the yellow puncta of mRFP-GFP-LC3 fluorescence and the activity of lysosomal proteolytic enzymes all decreased in senescent cells, indicating impaired autophagic flux with lysosomal dysfunction. The influence of autophagy activity on senescence development was confirmed by both positive and negative autophagy modulators; and MTOR-dependent autophagy activators, rapamycin and PP242, efficiently suppressed cellular senescence through a mechanism relevant to restoring autophagic flux. By time-phased treatment of cells with the antioxidant N-acetylcysteine (NAC), the mitochondria uncoupler carbonyl cyanide m-chlorophenyl hydrazone (CCCP) and ambroxol, a reagent with the effect of enhancing lysosomal enzyme maturation, we found that mitochondrial dysfunction plays an initiating role, while lysosomal dysfunction is more directly responsible for autophagy impairment and senescence. Interestingly, the effect of rapamycin on autophagy flux is linked to its role in functional revitalization of both mitochondrial and lysosomal functions. Together, this study demonstrates that autophagy impairment is crucial for oxidative stress-induced cell senescence, thus restoring autophagy activity could be a promising way to retard senescence.
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In the citing paper
“All aspects of mitochondrial function have been reported to be impaired in AD [237]”
From Ageing, Cellular Senescence and Neurodegenerative Disease (2018) · cites this paper as [237]
In the citing paper
“On the other hand, autophagy inhibition leads to toxic cell waste accumulation and elevated ROS levels that can induce senescence [261].”
From Mechanisms and Regulation of Cellular Senescence (2021) · cites this paper as [261]
In the citing paper
“Depletion of lysosomal-associated membrane protein 2 (LAMP2), which is critical for fusion between autophagosomes and lysosomes, can induce cellular senescence [57], [73], as can pharmacological inhibition of lysosomal activity (hydroxychloroquine & leupeptin treatment) [57].”
From Iron accumulation in senescent cells is coupled with impaired ferritinophagy and inhibition of ferroptosis (2018) · cites this paper as [57]
In the citing paper
“Additionally, lysosomal dysfunction can precede senescence development and drive the associated phenotypic changes [57], [73].”
From Iron accumulation in senescent cells is coupled with impaired ferritinophagy and inhibition of ferroptosis (2018) · cites this paper as [57]
In the citing paper
“Consistent with our findings (Fig. 5,Fig. S3), lysosomal dysfunction has been documented in replicative [74] and oxidative stress-induced senescence [57] and in both cases was associated with the buildup of autophagosomes and related markers (e.g. LC3-II, p62).”
From Iron accumulation in senescent cells is coupled with impaired ferritinophagy and inhibition of ferroptosis (2018) · cites this paper as [57]
In the citing paper
“Autophagy impairment incurred through lysosomal dysfunction has recently been described in cellular senescence and shown to regulate SASP [57], [72], [73], [74], [75].”
From Iron accumulation in senescent cells is coupled with impaired ferritinophagy and inhibition of ferroptosis (2018) · cites this paper as [57]
In the citing paper
“The mTOR inhibitor rapamycin has been shown to restore lysosomal function in senescent cells [57].”
From Iron accumulation in senescent cells is coupled with impaired ferritinophagy and inhibition of ferroptosis (2018) · cites this paper as [57]
In the citing paper
“Elevated p62 levels were previously observed in oxidative stress-induced senescent cells [57], and consistent with this study, we demonstrated that our senescent MEFs (MEF IR) likewise had markedly elevated levels of p62 when compared to primary MEFs (MEF PRI) (Fig. 5D).”
From Iron accumulation in senescent cells is coupled with impaired ferritinophagy and inhibition of ferroptosis (2018) · cites this paper as [57]
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Metadata
- Authors
- Tai, H., Wang, Z., Gong, H., Han, X., Zhou, J., Wang, X., Wei, X., Ding, Y., Huang, N., Qin, J., Zhang, J., Wang, S., Gao, F., Chrzanowska-Lightowlers, Z. M., Xiang, R., & Xiao, H.
- Affiliations
- Sichuan University (CN)
- Wellcome Centre for Mitochondrial Research (GB)
- Wellcome Trust Center for Mitochondrial Research, Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, UK
- Nankai University (CN)
- Corresponding author
- Xiao, Hengyi
- ORCID
- Venue
- Autophagy
- Publisher
- Informa UK Limited
- Published
- 2016-11-21
- Volume
- 13
- Issue
- 1
- Pages
- 99-113
- ISSN
- 1554-8627 (ISSN-L)
- 1554-8635
- PMC
- PMC5240829
- OpenAlex
- W2541855063
- Cited by
- 334
- References
- 51
- Citations by year
- 2026: 33 · 2025: 37 · 2024: 30 · 2023: 39 · 2022: 51 · 2021: 39 · 2020: 45 · 2019: 24 · 2018: 19 · 2017: 17
- FWCI
- 18.76
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Autophagy (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Newcastle University ePrints (Newcastle Univesity) (cc-by-nc-nd)
- Funders
- Wellcome Trust (096919, 096919/Z/11/Z, /Z/11/Z)
- National Natural Science Foundation of China (81273224, 2013CB911300)
- National Key Research and Development Program of China (2016YFC1200203, 2013CB911300)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Telomeres, Telomerase, and Senescence
- Keywords
- autophagy dysfunction, cellular senescence, oxidative stress, lysosomal dysfunction, mitochondrial dysfunction, autophagic flux, rapamycin, PP242, mTOR signaling, N-acetylcysteine, CCCP, ambroxol, aging
- MeSH terms
- Sequestosome-1 Protein, Acetylcysteine, Adenosine Triphosphate, Animals, Antioxidants, Autophagy, Humans, Hydrogen Peroxide, Lysosomes, Mitochondria, Signal Transduction, Cellular Senescence, Reactive Oxygen Species, Oxidative Stress, Microscopy, Confocal, NIH 3T3 Cells, Mice, TOR Serine-Threonine Kinases
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