Linking functional decline of telomeres, mitochondria and stem cells during ageing.
paper
Cited
Public
- Authors
- Sahin, Ergün; Depinho, Ronald A
- Year
- 2010
- Journal
- Nature
- PMID
- 20336134
- DOI
- 10.1038/nature08982
- PMCID
- PMC3733214
The study of human genetic disorders and mutant mouse models has provided evidence that genome maintenance mechanisms, DNA damage signalling and metabolic regulation cooperate to drive the ageing process. In particular, age-associated telomere damage, diminution of telomere 'capping' function and associated p53 activation have emerged as prime instigators of a functional decline of tissue stem cells and of mitochondrial dysfunction that adversely affect renewal and bioenergetic support in diverse tissues. Constructing a model of how telomeres, stem cells and mitochondria interact with key molecules governing genome integrity, 'stemness' and metabolism provides a framework for how diverse factors contribute to ageing and age-related disorders.
Haematopoietic stem cells experience functional decline with ageingMajor differences between young (left) and old (right) haematopoietic stem cells (HSCs) are shown, exemplifying general mechanisms that may occur with age in stem cells, including decreased regenerative potential and dysregulated differentiation. Cell-extrinsic and cell-intrinsic factors contribute to the overall functional decline of ageing HSCs. Although the self-renewal capacity might be increased in aged HSCs, there is decreased functional regenerative capacity, particularly under stress conditions. Importantly, aged HSCs have an altered differentiation programme with reduced output of common lymphoid progenitors (CLPs), whereas common myeloid progenitors (CMPs) are produced at the same rate as by young HSCs. The decrease in numbers of CLPs and mature B and T cells (‘immunosenescence’) is in contrast to the increased frequency of common granulocyte–macrophage progenitors (GMPs) and, consequently, granulocytes and macrophages. Numbers of megakaryocyte–erythrocyte progenitors (MEPs) are not altered. Possible cell-extrinsic alterations relevant for HSC function include altered stromal compositions and altered cytokine profiles that favour specific differentiation programmes such as decreased lymphopoiesis and increased myelopoiesis. Other age-related changes could affect osteoblast and endothelial cells that have been shown to modulate HSC function. The relevance of systemic factors in modulating stem-cell function has been shown in parabiosis studies: the regenerative capacity of muscle satellite cells in aged mice was increased by exposure to the circulatory system of young mice through the restoration of Delta–Notch signalling20. LRPs, lineage-restricted progenitors.
LLM interpretation
This diagram compares the functional characteristics and differentiation pathways of young (left) and old (right) haematopoietic stem cells (HSCs). The visualization shows that while common myeloid progenitor (CMP) and megakaryocyte-erythrocyte progenitor (MEP) outputs remain similar, aged HSCs exhibit a reduction in common lymphoid progenitors (CLPs), B cells, and T cells, alongside an increase in granulocyte-macrophage progenitors (GMPs) and their resulting mature cells. The figure also highlights that aged HSCs are influenced by altered systemic factors and microenvironments, leading to decreased regenerative potential.
Telomerase knockout mice with dysfunctional telomeres develop premature ageingTelomerase knockout mice (G1) are viable, with intact chromosomes, and have minor physiological abnormalities in the case of long telomeres (top image; arrow); however, with advanced age, they develop degenerative symptoms sooner than do age-matched mice with wild-type Terc . Continuous interbreeding of telomerase knockout mice leads to subsequent generations of mice (G2, G3 and so on) with telomeres of decreasing length. Mice with dysfunctional telomeres have chromosomal abnormalities (bottom image; arrows point to loss of telomere signal, resulting in fused chromosomes), and they develop multiple ageing-associated degenerative disorders in highly proliferative organs, as well as in post-mitotic tissues. Highly proliferative organs such as the intestine, skin and testes are characterized by atrophic changes indicating stem-cell-based failure. Functional decline in post-mitotic tissues (such as cardiomyopathy) and age-associated metabolic changes (such as insulin resistance) have been noted in mice with dysfunctional telomeres. Such mice have a shortened lifespan and a modest increase in cancer, in line with the role of telomeres in preventing illegitimate recombination events.
LLM interpretation
This figure is a schematic diagram illustrating the progressive effects of telomerase knockout across multiple generations of mice. It combines a pedigree chart showing the breeding of *Terc* or *Tert* mutants with two fluorescence microscopy images of chromosomes, contrasting intact telomeres (top) with telomere loss and end-to-end fusions (bottom). The diagram maps these genetic and chromosomal changes to physiological outcomes, showing that while G1 mice have a near-normal lifespan, subsequent generations (G3–G6) exhibit severe degenerative disorders in post-mitotic tissues and proliferative organs, leading to a markedly decreased lifespan.
A model of interaction between DNA damage, p53 activation and mitochondrial dysfunctionIn this model, genotoxic stress brought about by telomere attrition, impaired DNA repair, ultraviolet (UV) radiation, ionizing radiation (IR), chemicals, ROS and other mechanisms activates p53 and induces cellular growth arrest (in proliferating compartments), senescence or apoptosis. We also propose that p53 can impair mitochondrial function either directly or indirectly (through regulation of ROS-detoxifying enzymes). This p53-mediated mitochondrial dysfunction triggers a cycle of DNA damage, p53 activation, mitochondrial compromise and increased ROS levels leading to additional DNA damage, and so on. The mitochondrial compromise could contribute to organ dysfunction through decreased ATP generation, as well as changes in mitochondrial metabolism. The interplay between p53 and other pathways implicated in ageing is also indicated. Caloric restriction (CR) activates SIRT1, which decreases p53 activity. Also, SIRT1 (and possibly SIRT6) activates PGC-1α and boosts mitochondrial biogenesis2. PGC-1α increases antioxidant defence through upregulation of antioxidants89, whereas p53 has been shown to increase or decrease the expression of antioxidants depending on cellular ROS concentrations86. BMI1 loss has been shown to induce mitochondrial dysfunction directly and induce upregulation of p16/ARF (refs 30, 32). ARF increases p53 activity through interaction with MDM2, the negative regulator of p53.
LLM interpretation
This figure is a schematic diagram illustrating the molecular interactions between DNA damage, p53 activation, and mitochondrial dysfunction. It maps how genotoxic stressors (e.g., UV, IR, telomere dysfunction) activate p53, which in turn leads to gene target activation (apoptosis, senescence) and mitochondrial dysfunction. The model further depicts regulatory loops involving SIRT1/SIRT6, PGC-1$\alpha$, and BMI1, showing how these factors modulate ROS levels and mitochondrial health to ultimately influence tissue function and ageing.
| Name | Type |
|---|---|
| accelerated ageing local | phenotype |
| Accelerated ageing of the immune system local | phenotype |
| accelerated ageing phenotypes local | phenotype |
| accelerated tissue degeneration local | phenotype |
| age | phenotype |
| age-associated disease local | phenotype |
| age-associated physiological decline local | phenotype |
| Age-dependent functional decline of stem cells local | phenotype |
| Aged humans local | cohort |
| Aged human tissues local | cohort |
| aged mice | cohort |
| Aged mouse tissues local | cohort |
| ageing | phenotype |
| Ageing humans local | cohort |
| Ageing mice local | cohort |
| ageing mouse brain local | anatomy |
| ageing phenotype local | phenotype |
| ageing phenotypes local | phenotype |
| ageing_phenotypes local | phenotype |
| Age-related pathologies local | phenotype |
| age-related phenotypes local | phenotype |
| aging | phenotype |
| anaemia | phenotype |
| anaphase bridges local | phenotype |
| antioxidant genes local | gene |
| apoptosis | phenotype |
| apoptotic elimination local | phenotype |
| Arthropathies local | phenotype |
| ataxia telangiectasia local | phenotype |
| ATM | gene |
| ATR local | gene |
| Bmi1 local | gene |
| BMI1 local | gene |
| Bmi1 deficiency local | phenotype |
| bone marrow failure local | phenotype |
| bone_marrow_failure local | phenotype |
| Bone marrow failure local | phenotype |
| bone marrow failure syndromes local | phenotype |
| Bone marrow failure syndromes local | phenotype |
| Bone marrow transplant patients local | cohort |
| brain | anatomy |
| BRCA1 | gene |
| cancer | phenotype |
| CancerIncidence local | phenotype |
| cancer resistance local | phenotype |
| cancer risk | phenotype |
| cardiomyopathy | phenotype |
| cardiovascular disease | phenotype |
| cartilage–hair hypoplasia syndrome local | phenotype |
| CDKN1A local | gene |
| CDKN2A | gene |
| CDKN2AARF local | gene |
| cell-cycle arrest local | phenotype |
| cell proliferation | phenotype |
| cellular senescence | phenotype |
| cellular_senescence local | phenotype |
| centenarians | cohort |
| centenarians' offspring local | cohort |
| chromosomal end-to-end fusions local | phenotype |
| chromosomal fusions local | phenotype |
| chromosomal instability | phenotype |
| cognition | phenotype |
| compromised HSC function local | phenotype |
| compromised NSC renewal local | phenotype |
| Decline in neurogenesis local | phenotype |
| decreased engraftment capacity local | phenotype |
| decreased fecundity local | phenotype |
| decreased HSC activity local | phenotype |
| Decreased lymphoid lineage differentiation local | phenotype |
| decreased mitochondrial function local | phenotype |
| Decreased naive B cell numbers local | phenotype |
| Decreased naive T cell numbers local | phenotype |
| Decreased natural-killer activity local | phenotype |
| Decreased phagocytic ability of neutrophils and macrophages local | phenotype |
| Decrease in functionally competent HSCs local | phenotype |
| degenerative ageing phenotypes local | phenotype |
| Degenerative disease | phenotype |
| DegenerativePhenotype local | phenotype |
| degenerative phenotypes local | phenotype |
| delayed onset of ageing phenotype local | phenotype |
| delayed wound healing local | phenotype |
| dementia | phenotype |
| dentate gyrus | anatomy |
| diminished energy production local | phenotype |
| diminished epithelial replenishment local | phenotype |
| diminished oxidative defence local | phenotype |
| disease progression | phenotype |
| DNA damage | phenotype |
| DNA_damage local | phenotype |
| DNA damage foci local | phenotype |
| DNA damage foci at telomeres local | phenotype |
| Donor age local | phenotype |
| dyskeratosis congenita local | phenotype |
| end-to-end chromosomal fusions local | phenotype |
| engineered mice with hyperactive mutant p53 local | cohort |
| engineered mouse models local | cohort |
| engineered_mouse_models local | cohort |
| Epidermal stem-cell numbers local | phenotype |
| EpithelialCancerBreast local | phenotype |
| EpithelialCancerGI local | phenotype |
| EpithelialCancerSkin local | phenotype |
| epithelial tumours local | phenotype |
| ERCC2 local | gene |
| Expansion of myeloid lineage local | phenotype |
| FANCD1 local | gene |
| Fancd1_knockout_mice local | cohort |
| feeble immune responses local | phenotype |
| Fibroblasts local | drug |
| FoxO | gene |
| frailty | phenotype |
| functional decline local | phenotype |
| functional impairment | phenotype |
| G1 Terc−/− mice local | cohort |
| G3+ Terc−/− mice local | cohort |
| Genotoxic stress local | phenotype |
| germline p53 hyperactivation mice local | cohort |
| glucocorticoid | drug |
| glucose intolerance | phenotype |
| granular layer | anatomy |
| hair greying local | phenotype |
| Hair growth local | phenotype |
| hair loss local | phenotype |
| Hayflick limit local | phenotype |
| healthy | phenotype |
| HSC failure local | phenotype |
| HSC–NSC depletion phenotype local | phenotype |
| human | cohort |
| hyperactive mutant p53 allele local | variant |
| hyperactive mutant TP53 local | variant |
| hyper-p53 mice local | cohort |
| hyper‑p53 mice local | cohort |
| Hyperproliferative HSC phenotype local | phenotype |
| hypoxia | phenotype |
| idiopathic pulmonary fibrosis | phenotype |
| impaired differentiation local | phenotype |
| impaired haematopoiesis local | phenotype |
| impaired organ function local | phenotype |
| Impaired regeneration after injury local | phenotype |
| impaired wound healing local | phenotype |
| increased apoptosis local | phenotype |
| increased_apoptosis local | phenotype |
| Increased memory B cell numbers local | phenotype |
| Increased memory T cell numbers local | phenotype |
| Ink4a/Arf deficiency local | phenotype |
| Ink4a/Arf−/− mice local | cohort |
| Ink4aArfMinusMinus_Mice local | cohort |
| intestinal atrophy local | phenotype |
| ionizing_radiation local | drug |
| kyphosis local | phenotype |
| laboratory mice null for Terc local | cohort |
| laboratory mice null for Tert local | cohort |
| late-generation Terc−/− Ink4a/Arf−/− mice local | cohort |
| Late-generation Terc−/− Ink4a/Arf−/− mice local | cohort |
| late-generation Terc−/− mice local | cohort |
| Late-generation Terc−/− p53−/− mice local | cohort |
| LateGen_TercMinusMinus_Ink4aArfMinusMinus_Mice local | cohort |
| LateGen_TercMinusMinus_p53MinusMinus_Mice local | cohort |
| LateGen_TercMinusMinus_p53PlusPlus_Mice local | cohort |
| life expectancy | phenotype |
| lifespan | phenotype |
| life-threatening infections local | phenotype |
| LIG4 local | gene |
| lipid profiles local | phenotype |
| Liver cirrhosis | phenotype |
| longer latency local | phenotype |
| longevity | phenotype |
| loss of oxidative defence local | phenotype |
| lymphoma local | phenotype |
| Lymphoma local | phenotype |
| lymphopenia local | phenotype |
| malignancy local | phenotype |
| MDM2 local | gene |
| melanocyte_stem_cell_attrition local | phenotype |
| mice | cohort |
| mild glucose intolerance local | phenotype |
| mismatch repair defects | phenotype |
| Mitochondrial complex I local | drug |
| Mitochondrial complex III local | drug |
| mitochondrial DNA mutation mice local | cohort |
| mitochondrial DNA mutations local | phenotype |
| mitochondrial dysfunction | phenotype |
| Mobilization capacity local | phenotype |
| mortality rates local | phenotype |
| MSH2 | gene |
| Msh2_knockout_mice local | cohort |
| mTOR | gene |
| muscle atrophy local | phenotype |
| myeloid lineage differentiation local | phenotype |
| neuro-degeneration local | phenotype |
| neurogenesis decline local | phenotype |
| Normocytic anaemia local | phenotype |
| NSC quiescence local | phenotype |
| nucleotide excision repair defects local | phenotype |
| Old mice local | cohort |
| old mouse brain local | anatomy |
| olfactory bulb | anatomy |
| olfactory discrimination impairment local | phenotype |
| olfactory epithelium | anatomy |
| Oncogene activation local | phenotype |
| organ atrophy local | phenotype |
| organismal ageing local | phenotype |
| osteoporosis | phenotype |
| OverallLongevity local | phenotype |
| oxidative stress | phenotype |
| p16Ink4a | gene |
| p19ARF local | gene |
| p53-dependent apoptosis local | phenotype |
| Parabiotic mice local | cohort |
| PGC-1α deficient mice local | cohort |
| PGC-1β deficient mice local | cohort |
| phenotypically unaffected local | phenotype |
| PI3K | gene |
| POLG local | gene |
| PPARGC1A | gene |
| PPARGC1B | gene |
| Preferred differentiation towards myeloid lineages local | phenotype |
| premature ageing local | phenotype |
| premature ageing phenotypes local | phenotype |
| progeroid syndromes local | phenotype |
| Pro-inflammatory state local | phenotype |
| proliferative arrest local | phenotype |
| pro-oxidant genes local | gene |
| psychiatric disorders | phenotype |
| Psychological stress local | phenotype |
| PTEN | gene |
| Pulmonary disease | phenotype |
| RAD50 local | gene |
| RAD50_hypermorphic_allele local | variant |
| Rad50_hypermorphic_mice local | cohort |
| rapamycin | drug |
| reactive oxygen species | drug |
| reduced_life_expectancy local | phenotype |
| reduced NSC pool local | phenotype |
| Regenerative potential decline local | phenotype |
| replicative potential local | phenotype |
| Repopulation capacity local | phenotype |
| repopulation capacity impairment local | phenotype |
| RMRP local | gene |
| RNase MRP complex local | drug |
| ROS | drug |
| ROS-induced stem-cell depletion local | phenotype |
| Rostral migratory stream local | anatomy |
| RPS6KB1 local | gene |
| sarcoma local | phenotype |
| Sarcoma local | phenotype |
| Satellite cell differentiation capacity decrease local | phenotype |
| Satellite cell number decrease local | phenotype |
| Satellite cell proliferative capacity decrease local | phenotype |
| senescent cells local | phenotype |
| Senescent sequelae local | phenotype |
| shortened telomeres local | phenotype |
| short limiting telomeres local | phenotype |
| short telomeres local | phenotype |
| SIRT1 | gene |
| SIRT6 local | gene |
| Sirt6_deletion_mice local | cohort |
| Skin renewal local | phenotype |
| stem_cell_attrition local | phenotype |
| stem-cell compromise local | phenotype |
| stem-cell decline local | phenotype |
| stem_cell_decline local | phenotype |
| stem‑cell defects local | phenotype |
| stem cell depletion local | phenotype |
| Stem-cell depletion phenotype local | phenotype |
| StemCellFunction local | phenotype |
| stem-cell loss local | phenotype |
| stroke | phenotype |
| Subgranular zone | anatomy |
| subventricular zone | anatomy |
| telomerase local | drug |
| Telomerase local | drug |
| Telomerase activity local | drug |
| telomerase knockout mice local | cohort |
| telomerase knockout mouse local | cohort |
| telomere capping status local | phenotype |
| Telomere damage and erosion local | phenotype |
| telomere dysfunction local | phenotype |
| telomere_dysfunction local | phenotype |
| Telomere dysfunction local | phenotype |
| telomere-dysfunctional mice local | cohort |
| telomere erosion local | phenotype |
| telomere length | phenotype |
| Telomere length maintenance defects local | phenotype |
| telomere_maintenance local | phenotype |
| telomere reserves local | phenotype |
| Telomeres | drug |
| telomere shortening local | phenotype |
| Terc local | gene |
| TERC local | gene |
| TERC−/− mice local | cohort |
| Terc−/− mouse model local | cohort |
| TERT | gene |
| testicular atrophy local | phenotype |
| tissue atrophy local | phenotype |
| tissue degeneration local | phenotype |
| tissue stem-cell defects local | phenotype |
| Tissue stem cell depletion local | phenotype |
| TP53 | gene |
| TP53 deficiency local | variant |
| transgenic mice | cohort |
| Transplant recipient survival local | phenotype |
| Trp53 | gene |
| TSC1 local | gene |
| TumourSpectrum local | phenotype |
| type 2 diabetes | phenotype |
| Werner syndrome local | phenotype |
| wild-type mice | cohort |
| wild‑type TP53 extra‑copy mice local | cohort |
| Wound healing | phenotype |
| WRN local | gene |
| XRCC5 | gene |
| XRCC6 | gene |
| years of healthy life local | phenotype |
| young mice | cohort |
| young mouse brain local | anatomy |
| ZMPSTE24 local | gene |
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In this knowledge base
| Title | Year | PMID |
|---|---|---|
| Detectable clonal mosaicism and its relationship to aging and cancer. | 2012 | 22561519 |
| Detectable clonal mosaicism from birth to old age and its relationship to cancer. | 2012 | 22561516 |
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| Changes of Wnt/β-catenin signalling, BMP2, and BMP4 in the jejunum during ageing in rats. | Dun Y et al. | — | 2020 | → |
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| Environmentally relevant concentrations of di(2-ethylhexyl)phthalate exposure alter larval growth and locomotion in medaka fish via multiple pathways. | Yang WK et al. | — | 2018 | → |
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| Increased risk of dementia in patients with Schizophrenia: A population-based cohort study in Taiwan. | Lin CE et al. | — | 2018 | → |
| Long-term Persistent Organic Pollutants Exposure Induced Telomere Dysfunction and Senescence-Associated Secretary Phenotype. | Yuan J et al. | — | 2018 | → |
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| Resveratrol counteracts bone loss via mitofilin-mediated osteogenic improvement of mesenchymal stem cells in senescence-accelerated mice. | Lv YJ et al. | — | 2018 | → |
| Telomerase Mediates Lymphocyte Proliferation but Not the Atherosclerosis-Suppressive Potential of Regulatory T-Cells. | Richardson GD et al. | — | 2018 | → |
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| Adipose-Derived Mesenchymal Stem Cells from the Elderly Exhibit Decreased Migration and Differentiation Abilities with Senescent Properties. | Liu M et al. | — | 2017 | → |
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| Ultraviolet Radiation-Induced Skin Aging: The Role of DNA Damage and Oxidative Stress in Epidermal Stem Cell Damage Mediated Skin Aging. | Panich U et al. | — | 2016 | → |
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| Concise review: hematopoietic stem cell aging and the prospects for rejuvenation. | Wahlestedt M et al. | — | 2015 | → |
| Dissecting tumor metabolic heterogeneity: Telomerase and large cell size metabolically define a sub-population of stem-like, mitochondrial-rich, cancer cells. | Lamb R et al. | — | 2015 | → |
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| Effects of PTEN on the longevity of cultured human umbilical vein endothelial cells: the role of antioxidants. | Tait IS et al. | — | 2015 | → |
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| Exploration of the nicotinamide-binding site of the tankyrases, identifying 3-arylisoquinolin-1-ones as potent and selective inhibitors in vitro. | Paine HA et al. | — | 2015 | → |
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| Pharmacogenomic analysis indicates potential of 1,5-isoquinolinediol as a universal anti-aging agent for different tissues. | Park MS et al. | — | 2015 | → |
| Synchronized age-related gene expression changes across multiple tissues in human and the link to complex diseases. | Yang J et al. | — | 2015 | → |
| Telomere dynamics in parasitic great spotted cuckoos and their magpie hosts. | Soler JJ et al. | — | 2015 | → |
| Telomere Length in Peripheral Blood Mononuclear Cells of Patients on Chronic Hemodialysis Is Related With Telomerase Activity and Treatment Duration. | Stefanidis I et al. | — | 2015 | → |
| Telopodes of telocytes are influenced in vitro by redox conditions and ageing. | Enciu AM et al. | — | 2015 | → |
| The association between leukocyte telomere lengths and sleep instability based on cardiopulmonary coupling analysis. | Kwon AM et al. | — | 2015 | → |
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| Transgenic mice overexpressing glia maturation factor-β, an oxidative stress inducible gene, show premature aging due to Zmpste24 down-regulation. | Imai R et al. | — | 2015 | → |
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| The convergence of fracture repair and stem cells: interplay of genes, aging, environmental factors and disease. | Hadjiargyrou M et al. | — | 2014 | → |
| The emergence of the mitochondrial genome as a partial regulator of nuclear function is providing new insights into the genetic mechanisms underlying age-related complex disease. | Horan MP et al. | — | 2014 | → |
| The history of sleep apnea is associated with shorter leukocyte telomere length: the Helsinki Birth Cohort Study. | Savolainen K et al. | — | 2014 | → |
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| Chronic restraint stress in rats causes sustained increase in urinary corticosterone excretion without affecting cerebral or systemic oxidatively generated DNA/RNA damage. | Jorgensen A et al. | — | 2013 | → |
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| Diminished response to in vivo mechanical loading in trabecular and not cortical bone in adulthood of female C57Bl/6 mice coincides with a reduction in deformation to load. | Willie BM et al. | — | 2013 | → |
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| mRNA decay factor AUF1 maintains normal aging, telomere maintenance, and suppression of senescence by activation of telomerase transcription. | Pont AR et al. | — | 2012 | → |
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| RPE cell senescence: a key contributor to age-related macular degeneration. | Kozlowski MR | — | 2012 | → |
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| Telomere length in early life predicts lifespan. | Heidinger BJ et al. | — | 2012 | → |
| Telomere length, telomerase activity and osteogenic differentiation are maintained in adipose-derived stromal cells from senile osteoporotic SAMP6 mice. | Mirsaidi A et al. | — | 2012 | → |
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| Telomeres, atherosclerosis, and the hemothelium: the longer view. | Aviv A et al. | — | 2012 | → |
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| The role of DNA exonucleases in protecting genome stability and their impact on ageing. | Mason PA et al. | — | 2012 | → |
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| Differences in disease severity but similar telomere lengths in genetic subgroups of patients with telomerase and shelterin mutations. | Vulliamy TJ et al. | — | 2011 | → |
| Disruption of telomerase trafficking by TCAB1 mutation causes dyskeratosis congenita. | Zhong F et al. | — | 2011 | → |
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