Autophagic activity dictates the cellular response to oncogenic RAS

Wang, Yihua; Wang, Xiao Dan; Lapi, Eleonora; Sullivan, Alexandra; Jia, Wei; He, You-Wen; Ratnayaka, Indrika; Zhong, Shan; Goldin, Robert D.; Goemans, Christoph G.; Tolkovsky, Aviva M.; Lu, Xin

doi:10.1073/pnas.1120193109

Cited by 117Autophagy in Disease and TherapyTelomeres, Telomerase, and SenescenceProtein Kinase Regulation and GTPase Signaling

Autophagic activity dictates the cellular response to oncogenic RAS

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Wang, Yihua, Wang, Xiao Dan, Lapi, Eleonora, Sullivan, Alexandra, Jia, Wei, He, You-Wen, Ratnayaka, Indrika, Zhong, Shan +4 more·2012·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1120193109PMC PMC3421174

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Abstract

RAS is frequently mutated in human cancers and has opposing effects on autophagy and tumorigenesis. Identifying determinants of the cellular responses to RAS is therefore vital in cancer research. Here, we show that autophagic activity dictates the cellular response to oncogenic RAS. N-terminal Apoptosis-stimulating of p53 protein 2 (ASPP2) mediates RAS-induced senescence and inhibits autophagy. Oncogenic RAS-expressing ASPP2 (Δ3/Δ3) mouse embryonic fibroblasts that escape senescence express a high level of ATG5/ATG12. Consistent with the notion that autophagy levels control the cellular response to oncogenic RAS, overexpressing ATG5, but not autophagy-deficient ATG5 mutant K130R, bypasses RAS-induced senescence, whereas ATG5 or ATG3 deficiency predisposes to it. Mechanistically, ASPP2 inhibits RAS-induced autophagy by competing with ATG16 to bind ATG5/ATG12 and preventing ATG16/ATG5/ATG12 formation. Hence, ASPP2 modulates oncogenic RAS-induced autophagic activity to dictate the cellular response to RAS: to proliferate or senesce.

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Inhibition of autophagy facilitates senescence.
“Indeed, some studies have shown that inhibition of autophagy facilitates senescence (Kang et al. 2011a; Wang et al. 2012), but this might be due in part to the loss of cell-protective roles of autophagy, which facilitates senescence effectors under some stressful conditions, where cells are not prone to apoptosis.”
From Cellular senescence and its effector programs (2014) · cites this paper as Wang et al. 2012

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Authors: Wang, Y., Wang, X. D., Lapi, E., Sullivan, A., Jia, W., He, Y.-W., Ratnayaka, I., Zhong, S., Goldin, R. D., Goemans, C. G., Tolkovsky, A. M., & Lu, X.
Affiliations: University of Oxford (GB)
Duke Medical Center (US)
Imperial College London (GB)
University of Cambridge (GB)
Ludwig Institute for Cancer Research Ltd., Nuffield Department of Clinical Medicine, University of Oxford, Oxford OX3 7DQ, United Kingdom;
ORCID: Wang, Yihua
Lapi, Eleonora
Jia, Wei
He, You-Wen
Zhong, Shan
Goldin, Robert D.
Tolkovsky, Aviva M.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2012-07-30
Volume: 109
Issue: 33
Pages: 13325-13330
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.1120193109
PMC: PMC3421174
OpenAlex: W2074957956
Cited by: 117
References: 31
Citations by year: 2026: 2 · 2025: 2 · 2024: 3 · 2023: 6 · 2022: 13 · 2021: 9 · 2020: 4 · 2019: 7 · 2018: 12 · 2017: 11 · 2016: 9 · 2015: 9 · 2014: 18 · 2013: 8 · 2012: 3
FWCI: 9.10
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
ePrints Soton (University of Southampton) (submittedVersion)
UCL Discovery (University College London) (submittedVersion)
Funders: Wellcome Trust
National Institute of Allergy and Infectious Diseases (R01AI074944)
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 › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
Keywords: oncogenic Ras, autophagy, cellular senescence, ASPP2, ATG5, ATG12, Atg16, ATG3, mouse embryonic fibroblasts, Ras-induced senescence, carcinogenesis, p53
MeSH terms: Autophagy-Related Protein 5, Autophagy-Related Protein 12, Animals, Autophagy, Embryo, Nonmammalian, Fibroblasts, Humans, Microtubule-Associated Proteins, Oncogenes, Protein Binding, Proteins, Proto-Oncogene Proteins p21(ras), Cellular Senescence, Tumor Suppressor Proteins, Multiprotein Complexes, Mice, Protein Stability

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Autophagic activity dictates the cellular response to oncogenic RAS

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