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Essential role of limiting telomeres in the pathogenesis of Werner syndrome
Abstract
Mutational inactivation of the gene WRN causes Werner syndrome, an autosomal recessive disease characterized by premature aging, elevated genomic instability and increased cancer incidence. The capacity of enforced telomerase expression to rescue premature senescence of cultured cells from individuals with Werner syndrome and the lack of a disease phenotype in Wrn-deficient mice with long telomeres implicate telomere attrition in the pathogenesis of Werner syndrome. Here, we show that the varied and complex cellular phenotypes of Werner syndrome are precipitated by exhaustion of telomere reserves in mice. In late-generation mice null with respect to both Wrn and Terc (encoding the telomerase RNA component), telomere dysfunction elicits a classical Werner-like premature aging syndrome typified by premature death, hair graying, alopecia, osteoporosis, type II diabetes and cataracts. This mouse model also showed accelerated replicative senescence and accumulation of DNA-damage foci in cultured cells, as well as increased chromosomal instability and cancer, particularly nonepithelial malignancies typical of Werner syndrome. These genetic data indicate that the delayed manifestation of the complex pleiotropic of Wrn deficiency relates to telomere shortening.
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“In support of this hypothesis, lack of a disease phenotype in mouse models of other human diseases, such as Werner and Ataxia-Telangiectasia syndromes, has been linked to species-specific differences in telomere length, as when these models were crossed with mice lacking telomerase activity, the disease became apparent (Chang et al., 2004; Wong et al., 2003).”
From Short Telomeres and Stem Cell Exhaustion Model Duchenne Muscular Dystrophy in mdx/mTR Mice (2010) · cites this paper as Chang et al., 2004
In the citing paper
“SFEs represent chromosome ends with the shortest telomeres and correlate with and increased incidence of chromosome fusions and tissue dysfunction in vivo in telomerase knockout mice (Chang et al., 2004).”
From Short Telomeres and Stem Cell Exhaustion Model Duchenne Muscular Dystrophy in mdx/mTR Mice (2010) · cites this paper as Chang et al., 2004
In the citing paper
“In the WRN/Terc double deficient animals, phenotypes reminiscent of human WS that are not observed in either single mutant are present: osteopenia, diabetes, and sarcomas.”
From DNA Repair, Genome Stability, and Aging (2005) · cites this paper as Chang et al., 2004
In the citing paper
“This hypothesis has been proven correct by the generation of mice deficient in both WRN and Terc (Chang et al., 2004; Du et al., 2004”
From DNA Repair, Genome Stability, and Aging (2005) · cites this paper as Chang et al., 2004
In the citing paper
“Inactivation of SIRT6 leads to H3K9 hyperacetylation at telomeric chromatin in both human and mouse cells, but the mouse cells do not display the downstream cellular defects observed in human cells, which is consistent with the large functional reserve of mouse telomeres (Supplementary Fig. 13d; data not shown)14,25.”
From SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin (2008) · cites this paper as [25]
In the citing paper
“In particular, mice carrying a homozygous germline deletion of the telomerase RNA component gene (Terc−/−) exhibit critically short telomeres and a premature development of age-related pathologies from the second or third generation [8, 18–20, 51, 70, 72, 101, 103]”
From Senescence-related impairment of autophagy induces toxic intraneuronal amyloid-β accumulation in a mouse model of amyloid pathology (2023) · cites this paper as [18]
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Metadata
- Authors
- Chang, S., Multani, A. S., Cabrera, N. G., Naylor, M. L., Laud, P., Lombard, D., Pathak, S., Guarente, L., & DePinho, R. A.
- Affiliations
- The University of Texas MD Anderson Cancer Center (US)
- Harvard University (US)
- Brigham and Women's Hospital (US)
- Massachusetts Institute of Technology (US)
- Corresponding author
- Chang, Sandy
- DePinho, Ronald A
- ORCID
- Venue
- Nature Genetics
- Published
- 2004-07-04
- Volume
- 36
- Issue
- 8
- Pages
- 877-882
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- OpenAlex
- W2050228381
- Cited by
- 462
- References
- 24
- Citations by year
- 2026: 4 · 2025: 8 · 2024: 12 · 2023: 15 · 2022: 12 · 2021: 19 · 2020: 10 · 2019: 25 · 2018: 16 · 2017: 11 · 2016: 21 · 2015: 14 · 2014: 17 · 2013: 18 · 2012: 21
- FWCI
- 25.35
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Genetics (publishedVersion)
- PubMed (publishedVersion)
- Funders
- American Cancer Society
- Ellison Medical Foundation
- National Institute on Aging (K08AG024873, K08AG001019)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Keywords
- Werner syndrome, WRN gene, telomere shortening, telomerase, TERC, premature aging, replicative senescence, genomic instability, chromosomal instability, cancer susceptibility, telomere dysfunction, DNA damage foci
- MeSH terms
- Animals, Cells, Cultured, Diabetes Mellitus, Type 2, DNA Damage, Female, Life Expectancy, Mice, Mutant Strains, Neoplasms, Experimental, Werner Syndrome, Wound Healing, Telomere, Cellular Senescence, Apoptosis, Aging, Premature, Chromosomal Instability, Mice
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