Loss of Slug Compromises DNA Damage Repair and Accelerates Stem Cell Aging in Mammary Epithelium
Open accessAbstract
DNA damage activates checkpoints that limit the replicative potential of stem cells, including differentiation. These checkpoints protect against cancer development but also promote tissue aging. Because mice lacking Slug/Snai2 exhibit limited stem cell activity, including luminobasal differentiation, and are protected from mammary cancer, we reasoned that Slug might regulate DNA damage checkpoints in mammary epithelial cells. Here, we show that Slug facilitates efficient execution of RPA32-mediated DNA damage response (DDR) signaling. Slug deficiency leads to delayed phosphorylation of ataxia telangiectasia mutated and Rad3-related protein (ATR) and its effectors RPA32 and CHK1. This leads to impaired RAD51 recruitment to DNA damage sites and persistence of unresolved DNA damage. In vivo, Slug/Snai2 loss leads to increased DNA damage and premature aging of mammary epithelium. Collectively, our work demonstrates that the mammary stem cell regulator Slug controls DDR checkpoints by dually inhibiting differentiation and facilitating DDR repair, and its loss causes unresolved DNA damage and accelerated aging.
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The infiltration of clonally expanded T cells and B cells is also observed in the brain and other tissues with ageing in mice and humans, and it is accentuated in age-related diseases.
“The infiltration of clonally expanded T cells and B cells is also observed in the brain and other tissues with ageing in mice and humans69,71–73, and it is accentuated in age-related diseases74,75.”
From Ageing and rejuvenation of tissue stem cells and their niches (2023) · cites this paper as [71]
The zinc-finger transcription factor SLUG can activate a DNA damage response in epithelial stem cells during ageing.
“Moreover, the zinc-finger transcription factor SLUG can activate a DNA damage response in epithelial stem cells during ageing71.”
From Ageing and rejuvenation of tissue stem cells and their niches (2023) · cites this paper as [71]
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Ageing and rejuvenation of tissue stem cells and their niches
Brunet, A., Goodell, M. A., & Rando, T. A. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00510-w · Cited by 407 · see citing works
- Authors
- Gross, K. M., Zhou, W., Breindel, J. L., Ouyang, J., Jin, D. X., Sokol, E. S., Gupta, P. B., Huber, K., Zou, L., & Kuperwasser, C.
- Affiliations
- Tufts University (US)
- Quinnipiac University (US)
- Harvard University (US)
- Whitehead Institute for Biomedical Research (US)
- Tufts Medical Center (US)
- Corresponding author
- Kuperwasser, Charlotte
- ORCID
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2019-07
- Volume
- 28
- Issue
- 2
- Pages
- 394-407.e6
- ISSN
- 2211-1247 (ISSN-L)
- OpenAlex
- W2958605953
- Cited by
- 58
- References
- 69
- Citations by year
- 2026: 5 · 2025: 3 · 2024: 14 · 2023: 11 · 2022: 9 · 2021: 10 · 2020: 4 · 2019: 2
- FWCI
- 2.07
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Neuroendocrine Tumor Research Foundation
- National Institutes of Health
- Breast Cancer Research Foundation
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- Slug, SNAI2, mammary stem cells, DNA damage response, DNA repair, ATR signaling, RPA32, Chk1, RAD51, stem cell aging, tissue aging, mammary epithelium, stem cell differentiation
- MeSH terms
- Snail Family Transcription Factors, Animals, Cell Differentiation, Cell Line, DNA Damage, DNA Repair, Humans, Mammary Glands, Animal, Mice, SCID, Mice, Inbred NOD, Cellular Senescence, Mammary Glands, Human, Cell Line, Tumor, Mice, HEK293 Cells
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