Cited by 52Genetics, Aging, and Longevity in Model OrganismsDNA Repair MechanismsTelomeres, Telomerase, and Senescence

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DNA damage in aging, the stem cell perspective

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McNeely, Taylor, Leone, Michael, Yanai, Hagai, Beerman, Isabel·2020·Human Genetics

DOI 10.1007/s00439-019-02047-zPMC PMC6980431

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Abstract

DNA damage is one of the most consistent cellular process proposed to contribute to aging. The maintenance of genomic and epigenomic integrity is critical for proper function of cells and tissues throughout life, and this homeostasis is under constant strain from both extrinsic and intrinsic insults. Considering the relationship between lifespan and genotoxic burden, it is plausible that the longest-lived cellular populations would face an accumulation of DNA damage over time. Tissue-specific stem cells are multipotent populations residing in localized niches and are responsible for maintaining all lineages of their resident tissue/system throughout life. However, many of these stem cells are impacted by genotoxic stress. Several factors may dictate the specific stem cell population response to DNA damage, including the niche location, life history, and fate decisions after damage accrual. This leads to differential handling of DNA damage in different stem cell compartments. Given the importance of adult stem cells in preserving normal tissue function during an individual's lifetime, DNA damage sensitivity and accumulation in these compartments could have crucial implications for aging. Despite this, more support for direct functional effects driven by accumulated DNA damage in adult stem cell compartments is needed. This review will present current evidence for the accumulation and potential influence of DNA damage in adult tissue-specific stem cells and propose inquiry directions that could benefit individual healthspan.

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Mitochondrial DNA mutations are established in human colonic stem cells, and mutated clones expand by crypt fission
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Hematopoietic stem cells count and remember self-renewal divisions
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“HSCs predominantly reside in the bone marrow, and despite the hematopoietic system’s demanding cell-production burden, due to the high turnover rate of blood cells, the limited HSC population is largely quiescent with few divisions throughout an organism’s lifetime (Bernitz et al. 2016; Wilson et al. 2008).”
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Chance, development, and aging
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Long Neural Genes Harbor Recurrent DNA Break Clusters in Neural Stem/Progenitor Cells
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Physical exercise increases adult hippocampal neurogenesis in male rats provided it is aerobic and sustained
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Mutational Heterogeneity in Human Cancers: Origin and Consequences
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Effects of Aging and Niche Microenvironment on Spermatogonial Stem Cell Self-Renewal
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p53 functions as a negative regulator of osteoblastogenesis, osteoblast-dependent osteoclastogenesis, and bone remodeling
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TAp63 Prevents Premature Aging by Promoting Adult Stem Cell Maintenance
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Accumulating Mitochondrial DNA Mutations Drive Premature Hematopoietic Aging Phenotypes Distinct from Physiological Stem Cell Aging
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Spontaneous mutation and parental age in humans.
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Distinct DNA-damage-dependent and -independent responses drive the loss of oocytes in recombination-defective mouse mutants
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Somatic Mutations Reveal Lineage Relationships and Age-Related Mutagenesis in Human Hematopoiesis
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Background
The cutaneous uptake of atmospheric oxygen contributes significantly to the oxygen supply of human dermis and epidermis
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Biased competition between Lgr5 intestinal stem cells driven by oncogenic mutation induces clonal expansion
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The effects of male age on sperm DNA damage in healthy non-smokers
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Aged Stem Cells Reprogram Their Daily Rhythmic Functions to Adapt to Stress
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“yH2AX foci, 8-oxo-dG Accumulate in epSCs in a circadian dependent manner Solanas et al. (2017)”
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Recombination and maternal age-dependent nondisjunction: molecular studies of trisomy 16.
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Muscle-derived stem/progenitor cell dysfunction limits healthspan and lifespan in a murine progeria model
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Neural Stem and Progenitor Cells Retain Their Potential for Proliferation and Differentiation into Functional Neurons Despite Lower Number in Aged Brain
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Characterization of susceptible chiasma configurations that increase the risk for maternal nondisjunction of chromosome 21
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Combinations of genetic mutations in the adult neural stem cell compartment determine brain tumour phenotypes
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Interaction between ROS dependent DNA damage, mitochondria and p38 MAPK underlies senescence of human adult stem cells
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Stem cells and the aging hematopoietic system
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In Osteoporosis, differentiation of mesenchymal stem cells (MSCs) improves bone marrow adipogenesis
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Prevention of maternal aging-associated oocyte aneuploidy and meiotic spindle defects in mice by dietary and genetic strategies
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Non-disjunction of chromosome 18
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Wnt/β-Catenin Signaling Induces the Aging of Mesenchymal Stem Cells through the DNA Damage Response and the p53/p21 Pathway
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An Overview of Testicular Germ Cell Tumors
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Maternal age-related differential global expression profiles observed in human oocytes
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New Insights into Human Nondisjunction of Chromosome 21 in Oocytes
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DNA damage and senescence in osteoprogenitors expressing Osx1 may cause their decrease with age
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Replication Stress Drives Constitutive Activation of the DNA Damage Response and Radioresistance in Glioblastoma Stem-like Cells
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An early‐senescence state in aged mesenchymal stromal cells contributes to hematopoietic stem and progenitor cell clonogenic impairment through the activation of a pro‐inflammatory program
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“Strand breaks Increased in old stromal cells Gnani et al. (2019)”
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Ultra-deep sequencing of mouse mitochondrial DNA: mutational patterns and their origins
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Nfatc1 orchestrates aging in hair follicle stem cells
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Epigenetic Control of Stem Cell Potential during Homeostasis, Aging, and Disease
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Oocyte ageing and epigenetics
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Clonal expansion of early to mid-life mitochondrial DNA point mutations drives mitochondrial dysfunction during human ageing
Greaves, L. C., Nooteboom, M., Elson, J. L., Tuppen, H. A. L., Taylor, G. A., Commane, D. M., Arasaradnam, R. P., Khrapko, K., Taylor, R. W., Kirkwood, T. B. L., et al. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004620 · Cited by 172
Oocyte DNA damage quality control requires consecutive interplay of CHK2 and CK1 to activate p63
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Autophagy prevents irradiation injury and maintains stemness through decreasing ROS generation in mesenchymal stem cells
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Ataxia telangiectasia mutated is essential during adult neurogenesisPreprint
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Impaired Notch Signaling Leads to a Decrease in p53 Activity and Mitotic Catastrophe in Aged Muscle Stem Cells
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“To the contrary, more recent evidence has shown increased levels of DNA damage in satellite cells isolated from aged mice (Liu et al. 2018; Sinha et al. 2014) (Table 1).”
Result
Effect of TERT over-expression on the long-term transplantation capacity of hematopoietic stem cells
Allsopp, R. C., Morin, G. B., Horner, J. W., DePinho, R., Harley, C. B., & Weissman, I. L. (2003) · Nature Medicine · doi:10.1038/nm0403-369 · Cited by 155
Wnt/β-catenin signaling induces the aging of mesenchymal stem cells through promoting the ROS production
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The telomere theory of reproductive senescence in women
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Gain-of-function amino acid substitutions drive positive selection of FGFR2 mutations in human spermatogonia
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Trisomy 18: studies of the parent and cell division of origin and the effect of aberrant recombination on nondisjunction.
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Reduced hematopoietic reserves in DNA interstrand crosslink repair‐deficient Ercc1−/− mice
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“Mice with deficient nucleotide excision repair, homologous recombination, and non-homologous recombination pathways showed various aging HSC phenotypes under transplant paradigms (Nijnik et al. 2007; Prasher et al. 2005; Rossi et al. 2007).”
Background
Long-term repopulating ability of telomerase-deficient murine hematopoietic stem cells
Samper, E., Fernández, P., Eguı́a, R., Martı́n-Rivera, L., Bernad, A., Blasco, M. A., & Aracil, M. (2002) · Blood · doi:10.1182/blood.v99.8.2767 · Cited by 140
NAD + supplementation rejuvenates aged gut adult stem cells
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Spatiotemporal Changes to the Subventricular Zone Stem Cell Pool through Aging
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Age-Associated Methylation Suppresses SPRY1, Leading to a Failure of Re-quiescence and Loss of the Reserve Stem Cell Pool in Elderly Muscle
Bigot, A., Duddy, W. J., Ouandaogo, Z. G., Négroni, E., Mariot, V., Ghimbovschi, S. D., Harmon, B. T., Wielgosik, A., Loiseau, C., Devaney, J., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.09.067 · Cited by 136 · cited 1×
“Epigenetic alterations, including histone modifications and DNA methylation, have been associated with satellite cell aging (Bigot et al. 2015; Liu et al. 2013; Schworer et al. 2016) and may also contribute to their age-associated dysfunction.”
Background
Age Changes in Stem Cells of Murine Small Intestinal Crypts
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DNA damage drives accelerated bone aging via an NF- κ B–dependent mechanism
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“NER (Ercc1−/−/Ercc1−/Δ) Accelerated osteoporosis accompanied by progenitor senescence and accumulation of DNA damage Chen et al. (2013), Niedernhofer et al. (2006)”
BackgroundInfluential
High Doses of Synthetic Antioxidants Induce Premature Senescence in Cultivated Mesenchymal Stem Cells
Kornienko, J. S., Smirnova, I. S., Pugovkina, N. A., Ivanova, J. S., Shilina, M. A., Grinchuk, T. M., Shatrova, A. N., Aksenov, N. D., Zenin, V. V., Nikolsky, N. N., et al. (2019) · Scientific Reports · doi:10.1038/s41598-018-37972-y · Cited by 135
Epigenetic stress responses induce muscle stem-cell ageing by Hoxa9 developmental signals
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Defining the clonal dynamics leading to mouse skin tumour initiation
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The DNA Damage Checkpoint Eliminates Mouse Oocytes with Chromosome Synapsis Failure
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“Human Mutations in progeny Increase with both parental and maternal age Risch et al. (1987), Kong et al.”
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Somatic mutagenesis in satellite cells associates with human skeletal muscle aging
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“175).”

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Authors: McNeely, T., Leone, M., Yanai, H., & Beerman, I.
Affiliations: National Institutes of Health (US)
Corresponding author: Beerman, Isabel
ORCID: McNeely, Taylor
Leone, Michael
Yanai, Hagai
Beerman, Isabel
Venue: Human Genetics
Publisher: Springer Science and Business Media LLC
Published: 2019-07-19
Volume: 139
Issue: 3
Pages: 309-331
ISSN: 0018-7348 (ISSN-L)
0340-6717
1432-1203
DOI: 10.1007/s00439-019-02047-z
PMC: PMC6980431
OpenAlex: W2962795074
Semantic Scholar: e941bddd222e771b8a09dabfd854113fc588a2ed
Cited by: 52
References: 274
Citations by year: 2026: 2 · 2025: 7 · 2024: 14 · 2023: 6 · 2022: 8 · 2021: 5 · 2020: 10
FWCI: 0.50
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Human Genetics (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: NIA / NIH Intramural Research
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Telomeres, Telomerase, and Senescence
Keywords: DNA damage, aging, adult stem cells, genotoxic stress, stem cell niche, genome stability, lifespan, healthspan, stem cell fate
MeSH terms: Aging, Animals, DNA Damage, Homeostasis, Humans, Stem Cells

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DNA damage in aging, the stem cell perspective

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