MacroH2A1 and ATM Play Opposing Roles in Paracrine Senescence and the Senescence-Associated Secretory Phenotype
Open accessAbstract
Oncogene-induced senescence (OIS) is a tumor-suppressive mechanism typified by stable proliferative arrest, a persistent DNA damage response, and the senescence-associated secretory phenotype (SASP), which helps to maintain the senescent state and triggers bystander senescence in a paracrine fashion. Here, we demonstrate that the tumor suppressive histone variant macroH2A1 is a critical component of the positive feedback loop that maintains SASP gene expression and triggers the induction of paracrine senescence. MacroH2A1 undergoes dramatic genome-wide relocalization during OIS, including its removal from SASP gene chromatin. The removal of macroH2A1 from SASP genes results from a negative feedback loop activated by SASP-mediated endoplasmic reticulum (ER) stress. ER stress leads to increased reactive oxygen species and persistent DNA damage response including activation of ATM, which mediates removal macroH2A1 from SASP genes. Together, our findings indicate that macroH2A1 is a critical control point for the regulation of SASP gene expression during senescence.
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ATM indirectly regulates SASP gene expression by mediating removal of macroH2A1.1 from SASP genes in response to DNA damage and oncogenic stress.
“ATM was found to regulate expression of SASP genes indirectly by mediating the removal of the histone variant macroH2A1.1 from SASP genes in response to DNA damage and oncogenic stress87”
From Cellular senescence in ageing: from mechanisms to therapeutic opportunities (2021) · cites this paper as [87]
The Results section on ATM-mediated SASP gene repression reports that ATM activity triggers removal of macroH2A1 from SASP genes during oncogene-induced senescence, through a pathway involving DNA-damage signaling. The paper separately shows that macroH2A1.1 can stimulate SASP expression, but the ATM-removal experiments identify macroH2A1 generally, not the macroH2A1.1 splice variant specifically; that specificity is unsupported. (LLM, conf=0.85)
Experimental — accuracy not yet measuredMacroH2A1, HMGB2, MLL1 and BRD4 regulate SASP factor gene expression in response to DNA damage.
“Other epigenetic regulators, such as macroH2A1, high mobility group box 2 (HMGB2), mixed‐lineage leukemia 1 (MLL1) and bromodomain‐containing protein 4 (BRD4), have been demonstrated as regulators of SASP factor gene expression in response to DNA damage.52, 53, 54, 55”
From Cellular senescence and senescence-associated secretory phenotype via the cGAS-STING signaling pathway in cancer (2020) · cites this paper as [52]
SASP factors are primarily proinflammatory and act in a paracrine and autocrine manner.
“These factors are primarily proinflammatory and act in a paracrine and autocrine manner [44,45], although immunosuppressive mediators have also been identified as part of SASP [46,47].”
From Ageing, Cellular Senescence and Neurodegenerative Disease (2018) · cites this paper as [45]
The senescence-associated secretory phenotype consists of pro-inflammatory cytokines, proteases, chemokines, and extracellular matrix degrading proteins.
“The SASP consists of a noxious secretome comprised of pro-inflammatory cytokines, proteases, chemokines, and extracellular matrix degrading proteins (24–27).”
From Senolytic Therapy to Modulate the Progression of Alzheimer's Disease (SToMP-AD): A Pilot Clinical Trial (2022) · cites this paper as [25]
Upregulation of SASP genes is balanced by a negative feedback loop whereby macroH2A1 activates DDR signaling that leads to macroH2A1 removal from the chromatin of SASP genes, reducing their expression.
“Upregulation of SASP genes is balanced by a negative feedback loop whereby macroH2A1 activates DDR signaling that leads to macroH2A1 removal from the chromatin of SASP genes, thus reducing their expression [168].”
From Mechanisms and Regulation of Cellular Senescence (2021) · cites this paper as [168]
Active ATM triggers removal from SASP genes of the histone variant macroH2A1, leading to inhibition of their transcription and reduction in ER stress.
“Active ATM triggers the removal from SASP genes of the histone variant macroH2A1, leading to inhibition of their transcription and reduction in ER stress [168].”
From Mechanisms and Regulation of Cellular Senescence (2021) · cites this paper as [168]
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Self-citation
- Authors
- Chen, H., Ruiz, P. D., McKimpson, W. M., Novikov, L., Kitsis, R. N., & Gamble, M. J.
- Affiliations
- Albert Einstein College of Medicine (US)
- Corresponding author
- Gamble, Matthew J.
- Venue
- Molecular Cell
- Publisher
- Elsevier BV
- Published
- 2015-09
- Volume
- 59
- Issue
- 5
- Pages
- 719-731
- ISSN
- 1097-2765 (ISSN-L)
- PMC
- PMC4548812
- OpenAlex
- W1647232018
- Cited by
- 205
- References
- 64
- Citations by year
- 2026: 8 · 2025: 7 · 2024: 24 · 2023: 19 · 2022: 19 · 2021: 30 · 2020: 23 · 2019: 17 · 2018: 23 · 2017: 18 · 2016: 16 · 2015: 1
- FWCI
- 14.24
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Molecular Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Cancer Institute (R01CA155232, P30CA013330)
- National Institute of General Medical Sciences (T32GM007491)
- Topics
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- macroH2A1, ATM, oncogene-induced senescence, senescence-associated secretory phenotype, paracrine senescence, histone variants, DNA damage response, endoplasmic reticulum stress, reactive oxygen species, positive feedback loop
- MeSH terms
- Cell Line, DNA Damage, Gene Expression Regulation, Histones, Humans, Models, Biological, Oncogenes, Phenotype, Cellular Senescence, Paracrine Communication, Feedback, Physiological, Endoplasmic Reticulum Stress, Ataxia Telangiectasia Mutated Proteins
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