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Disease states associated with telomerase deficiency appear earlier in mice with short telomeres
Open accessAbstract
Mice deficient for the mouse telomerase RNA (mTR-/-) and lacking telomerase activity can only be bred for approximately six generations due to decreased male and female fertility and to an increased embryonic lethality associated with a neural tube closure defect. Although late generation mTR-/- mice show defects in the hematopoietic system, they are viable to adulthood, only showing a decrease in viability in old age. To assess the contribution of genetic background to the effect of telomerase deficiency on viability, we generated mTR-/- mutants on a C57BL6 background, which showed shorter telomeres than the original mixed genetic background C57BL6/129Sv. Interestingly, these mice could be bred for only four generations and the survival of late generation mTR-/- mice decreased dramatically with age as compared with their wild-type counterparts. Fifty percent of the generation 4 mice die at only 5 months of age. This decreased viability with age in the late generation mice is coincident with telomere shortening, sterility, splenic atrophy, reduced proliferative capacity of B and T cells, abnormal hematology and atrophy of the small intestine. These results indicate that telomere shortening in mTR-/- mice leads to progressive loss of organismal viability.
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“However, the cyclin-dependent kinase inhibitor p21 has been shown to participate in the p53-dependent telomere checkpoint response in both human fibroblasts and in TERCÀ/À mice (66,76).”
From Telomeres and telomerase in cancer (2010) · cites this paper as [76]
In the citing paper
“Although it was initially clear that high-turnover tissues are particularly sensitive to telomere length85,101,112”
From The telomere syndromes (2012) · cites this paper as [112]
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 [51]
In the citing paper
“the generation and characterization of the telomerase knockout mouse model has been instrumental in demonstrating that short telomeres result in multiple organismal defects caused by defective tissue regeneration 57, 58, 59”
From The common biology of cancer and ageing (2007) · cites this paper as [59]
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Self-citationTargeting Telomeres and Telomerase: Studies in Aging and Disease Utilizing CRISPR/Cas9 Technology
Brane, A. C., & Tollefsbol, T. O. (2019) · Cells · doi:10.3390/cells8020186 · Cited by 30
“Mice that were bred to be deficient in telomerase showed a marked decrease in health and, after several generations, lose the ability to breed completely [11].”
BackgroundÖngel, M. E., Yıldız, C., Akpınaroğlu, C., Yılmaz, B., & Özilgen, M. (2020) · Clinical Nutrition · doi:10.1016/j.clnu.2020.07.030 · Cited by 30
Telomere dysfunction in human diseases: the long and short of it!
Carroll, K. A., & Ly, H. (2009) · Europe PMC (PubMed Central) · Cited by 30
Richardson, G. D., Sage, A., Bennaceur, K., Zhrany, N. A., Coelho‐Lima, J., Dookun, E., Draganova, L., Saretzki, G. C., Breault, D. T., Mallat, Z., et al. (2018) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.117.309940 · Cited by 29
“Regarding its specific role in T-lymphocytes, telomerase levels control the lifespan of T lymphocytes(22) while telomere dysfunction in late-generation TERC mice reduces the number and function of T- and B- lymphocytes.(16,20,23,24) The end replication problem is not the only mechanism that can contribute to telomere…”
BackgroundDenham, J. (2023) · Aging Cell · doi:10.1111/acel.13836 · Cited by 28
ATRX driver mutation in a composite malignant pheochromocytoma
Comino‐Méndez, I., Tejera, Á. M., Currás-Freixes, M., Remacha, L., Gonzálvo, P., Tonda, R., Letón, R., Blasco, M. A., Robledo, M., & Cascón, A. (2016) · Cancer Genetics · doi:10.1016/j.cancergen.2016.04.058 · Cited by 29
Self-citationLiu, N., Yin, Y., Wang, H., Zhou, Z., Sheng, X., Fu, H., Guo, R., Wang, H., Yang, J., Gong, P., et al. (2019) · PLoS Genetics · doi:10.1371/journal.pgen.1008368 · Cited by 28
Kosebent, E. G., Uysal, F., & Öztürk, S. (2020) · Experimental Gerontology · doi:10.1016/j.exger.2020.110975 · Cited by 27
Telomere Reprogramming and Maintenance in Porcine iPS Cells
Ji, G., Ruan, W., Liu, K., Wang, F., Sakellariou, D., Chen, J., Yang, Y., Okuka, M., Han, J., Liu, Z., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074202 · Cited by 28
“Telomere FISH and quantification were performed as described previously [70,71], except for a fluorescein isothiocyanate (FITC)labeled (CCCTAA) peptide nucleic acid (PNA) probe used in this study [45].”
MethodTelomere Recombination Accelerates Cellular Aging in Saccharomyces cerevisiae
Chen, X., Meng, F., & Zhou, J. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000535 · Cited by 25
“Telomerase-deficient mice with critically short telomeres exhibit decreased viability associated with diminished proliferative capacity of B and T cells [57–59].”
The role of telomere-binding modulators in pluripotent stem cells
Li, F., Ge, Y., Liu, D., & Songyang, Z. (2019) · Protein & Cell · doi:10.1007/s13238-019-0651-y · Cited by 25
Genetic and environmental factors influencing human diseases with telomere dysfunction.
Ly, H. (2009) · PubMed · Cited by 25
Deficiency of Colonic Telomerase in Ulcerative Colitis
Usselmann, B., Newbold, M., Morris, A. G., & Nwokolo, C. U. (2001) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2001.03752.x · Cited by 25
“Absence of telomerase in these animals leads to intestinal atrophy and ulceration, as well as areas of increased epithelial cell proliferation (19).”
BackgroundSmith, S., Hoelzl, F., Zahn, S., & Criscuolo, F. (2021) · Molecular Ecology · doi:10.1111/mec.16233 · Cited by 22
“…with reduced cell turnover, bone marrow failure, and reproductive impairment only in the sixth generation of homozygous mutants ( TERT -/- mice presented similar phenotypes (Herrera et al., 1999; Strong et al., 2011) for consistent results in a mouse strain with a different genetic background).”
BackgroundRole of cellular senescence in hepatic wound healing and carcinogenesis
Ramakrishna, G., Anwar, T., Angara, R. K., Chatterjee, N., Kiran, S., & Singh, S. (2012) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2012.08.002 · Cited by 23
Getliffe, K. M., Dulaimi, D. A., Martin-Ruiz, C. M., Holder, R. L., von Zglinicki, T., Morris, A. G., & Nwokolo, C. U. (2005) · Alimentary Pharmacology & Therapeutics · doi:10.1111/j.1365-2036.2005.02311.x · Cited by 24
Mammalian meiotic telomeres: composition and ultrastructure in telomerase-deficient mice
Franco, S., Alsheimer, M., Herrera, E., Benavente, R., & Blasco, M. A. (2002) · European Journal of Cell Biology · doi:10.1078/0171-9335-00259 · Cited by 24
Self-citationWiemann, S. U., Ande, S., Buer, J., Kamino, K., Manns, M. P., & Rudolph, K. L. (2004) · Oncogene · doi:10.1038/sj.onc.1208308 · Cited by 24
Responses to Telomere Erosion in Plants
Amiard, S., Ines, O. D., Gallego, M. E., & White, C. I. (2014) · PLoS ONE · doi:10.1371/journal.pone.0086220 · Cited by 22
Makino, N., Oyama, J., Maeda, T., Koyanagi, M., Higuchi, Y., Shimokawa, I., Mori, N., & Furuyama, T. (2015) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-015-2615-8 · Cited by 23
“In this regard, the well-documented association between telomere shortening and aging [8] suggests a possible role of telomere dynamics in the systemic effects of caloric restriction.”
Güneş, Ç., Avila, A. I., & Rudolph, K. L. (2017) · Differentiation · doi:10.1016/j.diff.2017.12.004 · Cited by 29
Stauffer, J., Bruneaux, M., Panda, B., Visse, M., Vasemägi, A., & Ilmonen, P. (2017) · Oecologia · doi:10.1007/s00442-017-3953-x · Cited by 23
Telomerase and oligodendrocyte differentiation
Caporaso, G. L., & Chao, M. V. (2001) · Journal of Neurobiology · doi:10.1002/neu.1077 · Cited by 24
Montero‐Conde, C., Leandro-Garcia, L. J., Martínez‐Montes, Á. M., Martínez, P., Moya, F., Letón, R., Gil, E., Martínez‐Puente, N., Guadalix, S., Currás-Freixes, M., et al. (2022) · Clinical and Translational Medicine · doi:10.1002/ctm2.1001 · Cited by 22
Self-citationTelomere Dysfunction in Oocytes and Embryos From Obese Mice
Ge, J., Li, C., Sun, H., et al. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.617225 · Cited by 22
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González‐Suárez, E., Goytisolo, F. A., Flores, J. M., & Blasco, M. A. (2003) · PubMed · Cited by 23
Self-citationPudas, S., Josefsson, M., Adolfsson, A. N., Landfors, M., Kauppi, K., Veng-Taasti, L. M., Hultdin, M., Adolfsson, R., & Degerman, S. (2020) · The Journals of Gerontology Series A · doi:10.1093/gerona/glaa322 · Cited by 21
“Experimental evidence shows that telomere shortening is a determinant of tissue-specific and systemic aging (2–4).”
Stem cells and aging: a chicken-or-the-egg issue?
Smith, J. A., & Daniel, R. (2012) · Europe PMC (PubMed Central) · Cited by 23
Telomeres, aging and reproduction
Córdova-Oriz, I., Chico-Sordo, L., & Varela, E. (2022) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0000000000000779 · Cited by 21
Metadata
- Authors
- Herrera, E., Samper, E., Martín‐Caballero, J., Flores, J. M., Lee, H., & Blasco, M. A.
- Affiliations
- Consejo Superior de Investigaciones Científicas (ES)
- Universidad Complutense de Madrid (ES)
- Samsung Biomedical Research Institute (KR)
- Corresponding author
- Blasco, María A.
- Venue
- The EMBO Journal
- Published
- 1999-06-01
- Volume
- 18
- Issue
- 11
- Pages
- 2950-2960
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC1171377
- OpenAlex
- W2153094950
- Semantic Scholar
- 2fedd51810926e4acbca1ade7ab5eecd55623631
- Cited by
- 471
- References
- 45
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 8 · 2023: 15 · 2022: 14 · 2021: 13 · 2020: 11 · 2019: 15 · 2018: 15 · 2017: 15 · 2016: 14 · 2015: 9 · 2014: 18 · 2013: 20 · 2012: 20
- FWCI
- 14.72
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The EMBO Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- European Molecular Biology Organization
- 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
- telomerase deficiency, telomere shortening, genetic background effects, age-related mortality, fertility, embryonic lethality, neural tube defects, hematopoietic defects, splenic atrophy, hematological abnormalities
- MeSH terms
- Aging, Animals, Atrophy, Body Weight, Cells, Cultured, Crosses, Genetic, Female, Genes, Lethal, Hematopoietic System, Infertility, Intestine, Small, Leukocyte Count, Longevity, Lymphocytes, Male, Mice, Inbred C57BL, Spleen, Testis, Time Factors, Telomere, Mice, Knockout, Telomerase, Mice
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