Interplay between oncogene-induced DNA damage response and heterochromatin in senescence and cancer
Open accessAbstract
Two major mechanisms have been causally implicated in the establishment of cellular senescence: the activation of the DNA damage response (DDR) pathway and the formation of senescence-associated heterochromatic foci (SAHF). Here we show that in human fibroblasts resistant to premature p16(INK4a) induction, SAHF are preferentially formed following oncogene activation but are not detected during replicative cellular senescence or on exposure to a variety of senescence-inducing stimuli. Oncogene-induced SAHF formation depends on DNA replication and ATR (ataxia telangiectasia and Rad3-related). Inactivation of ATM (ataxia telangiectasia mutated) or p53 allows the proliferation of oncogene-expressing cells that retain increased heterochromatin induction. In human cancers, levels of heterochromatin markers are higher than in normal tissues, and are independent of the proliferative index or stage of the tumours. Pharmacological and genetic perturbation of heterochromatin in oncogene-expressing cells increase DDR signalling and lead to apoptosis. In vivo, a histone deacetylase inhibitor (HDACi) causes heterochromatin relaxation, increased DDR, apoptosis and tumour regression. These results indicate that heterochromatin induced by oncogenic stress restrains DDR and suggest that the use of chromatin-modifying drugs in cancer therapies may benefit from the study of chromatin and DDR status of tumours.
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HDAC inhibitor treatment induces chromatin relaxation, boosts DNA damage response signalling and causes apoptosis; this is probably the first reported successful senolytic approach, later supported by panobinostat's senolytic activity.
“treatment with histone deacetylase (HDAC) inhibitors, which induce chromatin relaxation, boosts DDR signalling with consequent cell death by apoptosis. This treatment is probably the first reported example of a successful senolytic approach52, which was later supported by the reported senolytic activity of the HDAC inhibitor panobinostat55”
From Cellular senescence in ageing: from mechanisms to therapeutic opportunities (2021) · cites this paper as [52]
The Results section ('Oncogene-induced heterochromatin restrains DDR signalling'; page unavailable) reports that HDAC inhibitors perturb heterochromatin, increase DDR signalling and induce apoptosis in oncogene-expressing cells. But the cells described as selectively eliminated were proliferating, and the paper does not establish this as a first successful senolytic approach that eliminates senescent cells. The later panobinostat finding is attached to a different citation in the citing sentence. (LLM, conf=0.88)
Experimental — accuracy not yet measuredElevated H4K20me3 and H3K9me3 contribute to proliferation arrest in senescence.
“Certain histone modifications are crucial for senescence, such as elevated H4K20me3 and H3K9me3, which contribute to the proliferation arrest (Cheng et al., 2017; Di Micco et al., 2011; Salama et al., 2014), whereas elevated H3K27ac at gene enhancers promotes a SASP (Hernandez-Segura et al., 2018).”
From Cellular Senescence: Defining a Path Forward (2019) · cites this paper as Di Micco et al., 2011
The Results section on proliferating oncogene-expressing cells reports that H3K9me3 accumulates at repressed proliferation-gene promoters during oncogene-induced senescence, supporting that part of the claim. Our copy does not report elevated H4K20me3 or establish that these two modifications together cause proliferation arrest across senescence generally. No page number is available in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measuredSenescence-associated heterochromatin foci enforce a DNA damage response-resistant heterochromatin structure that restrains DDR signalling.
“Rather, SAHF enforce a DDR-resistant heterochromatin structure that restrains DDR signalling52”
From Cellular senescence in ageing: from mechanisms to therapeutic opportunities (2021) · cites this paper as [52]
Experimental — accuracy not yet measuredSenescence-associated heterochromatin foci are not universal senescence markers; they are most robustly seen after oncogene activation and form in a DNA replication- and ATR-dependent manner.
“SAHF are not universal markers of senescence; they are most robustly observed upon oncogene activation and form in a DNA replication- and ATR-dependent manner52”
From Cellular senescence in ageing: from mechanisms to therapeutic opportunities (2021) · cites this paper as [52]
SAHFs seem to be cell type and stimulus dependent, as they are not seen in all senescent cells.
“Notably, SAHFs seem to be cell type andstimulus dependent, as they are not seen in all senescent cells (Di Micco et al., 2011; Kennedy et al., 2010; Sharpless and Sherr, 2015), rendering them useful for senescence identification, while the functional significance remains to be elucidated.”
From Cellular Senescence: Defining a Path Forward (2019) · cites this paper as Di Micco et al., 2011
SAHFs are not seen in all senescent cells; they are cell type and stimulus dependent.
“Since SAHFs are not seen in all senescent cells, it seems that they are cell type and stimulus dependent (Kennedy et al., 2010; Di Micco et al., 2011; Aird and Zhang, 2013; Criscione et al., 2016; Zirkel et al., 2018).”
From Mechanisms of Cellular Senescence: Cell Cycle Arrest and Senescence Associated Secretory Phenotype (2021) · cites this paper as Di Micco et al., 2011
SAHF formation promotes cell survival by protecting senescent cells against excessive DNA damage signaling during oncogenic stress.
“Senescence-associated heterochromatic focus (SAHF) formation (discussed below) also promotes cell survival by protecting senescent cells against excessive DNA damage signaling during oncogenic stress [259].”
From Mechanisms and Regulation of Cellular Senescence (2021) · cites this paper as [259]
SAHF formation is not a universal feature of senescence.
“However, SAHF formation is not a universal feature of senescence.”
From Mechanisms and Regulation of Cellular Senescence (2021) · cites this paper as [259]
Formation of SAHF may be spontaneously stochastic and programmed; it can be induced in senescent cells by oncogenes, toxic agents, or telomere shortening.
“Formation of SAHF may be spontaneously stochastic and program-med; it can be induced in senescent cells by oncogenes, toxic agents, or telomere shortening [74, 76, 79-81].”
From Markers of cellular senescence. Telomere shortening as a marker of cellular senescence (2016) · cites this paper as [81]
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- Authors
- Di Micco, R., Sulli, G., Dobreva, M., Liontos, M., Botrugno, O. A., Gargiulo, G., dal Zuffo, R., Matti, V., d'Ario, G., Montani, E., Mercurio, C., Hahn, W. C., Gorgoulis, V., Minucci, S., & d'Adda di Fagagna, F.
- Affiliations
- IFOM (IT)
- National and Kapodistrian University of Athens (GR)
- European Institute of Oncology (IT)
- The Netherlands Cancer Institute (NL)
- Dana-Farber Cancer Institute (US)
- University of Milan (IT)
- ORCID
- Venue
- Nature Cell Biology
- Published
- 2011-02-20
- Volume
- 13
- Issue
- 3
- Pages
- 292-302
- ISSN
- 1465-7392 (ISSN-L)
- 1476-4679
- PMC
- PMC3918344
- OpenAlex
- W2025772032
- Cited by
- 382
- References
- 64
- Citations by year
- 2026: 15 · 2025: 20 · 2024: 29 · 2023: 29 · 2022: 21 · 2021: 29 · 2020: 18 · 2019: 13 · 2018: 13 · 2017: 28 · 2016: 28 · 2015: 19 · 2014: 32 · 2013: 30 · 2012: 39
- FWCI
- 26.39
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Aging (R01AG023145)
- Topics
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
- Keywords
- oncogene-induced senescence, DNA damage response, heterochromatin, ATR, ATM, p53, p16INK4a, DNA replication, apoptosis, histone deacetylase inhibitors, tumor regression, fibroblasts, cancer therapy
- MeSH terms
- Animals, Chromatin, DNA Damage, DNA Replication, Heterochromatin, Humans, Microscopy, Fluorescence, Neoplasm Transplantation, Neoplasms, Oncogenes, Plasmids, Cellular Senescence, Apoptosis, Cyclin-Dependent Kinase Inhibitor p16, RNA, Small Interfering, Cell Line, Tumor, Mice, Histone Deacetylase Inhibitors
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