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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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MethodAge-related mechanisms in the context of rheumatic disease
Alsaleh, G., Richter, F. C., & Simon, A. K. (2022) · Nature Reviews Rheumatology · doi:10.1038/s41584-022-00863-8 · Cited by 20
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Mania, A., Mantzouratou, A., Delhanty, J. D. A., Baio, G., Serhal, P. F., & SenGupta, S. B. (2014) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2013.12.010 · Cited by 19
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Stock, A. J., Ayyar, S., Kashyap, A., Wang, Y., Yanai, H., Starost, M. F., Tanaka-Yano, M., Bodogai, M., Sun, C., Wang, Y., et al. (2023) · GeroScience · doi:10.1007/s11357-023-00752-2 · Cited by 25
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Ji, G., Liu, K., Okuka, M., Liu, N., & Liu, L. (2012) · BMC Cell Biology · doi:10.1186/1471-2121-13-36 · Cited by 18
“Telomere FISH and quantification were performed as described previously [22,23,41], except that a fluorescein isothiocyanate (FITC)-labeled (CCCTAA) peptide nucleic acid (PNA) probe was used in this study.”
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Yoshida, T., Kondo, N., Oka, S., Ahsan, M. K., Hara, T., Masutani, H., Nakamura, H., & Ab, J. Y. (2006) · BioFactors · doi:10.1002/biof.5520270105 · Cited by 18
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BackgroundAl-Ajmi, N., Saretzki, G. C., Miles, C. G., & Spyridopoulos, I. (2014) · Experimental Gerontology · doi:10.1016/j.exger.2014.07.010 · Cited by 17
Effectors of mammalian telomere dysfunction: a comparative transcriptome analysis using mouse models
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InfluentialThe telomere gestational clock: increasing short telomeres at term in the mouse
Phillippe, M., Sawyer, M. R., & Edelson, P. K. (2019) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2019.01.218 · Cited by 15
Generation of pluripotent stem cells from eggs of aging mice
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“Telomere FISH and quantification were performed based on method described previously (Herrera et al., 1999), except for that FITC-labeled (CCCTAA) peptide nucleic acid (PNA) probe was used in this study.”
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“It remains unclear whether the downregulation of hTERT gene expression which we observed is causally associated with the impairment of germ cell differentiation, as has been demonstrated for mice genetically deficient in murine telomerase RNA [41,42] or whether there is no correlation.”
Rampersaud, R., Wu, G. W. Y., Reus, V. I., Lin, J., Blackburn, E. H., Epel, E. S., Hough, C. M., Mellon, S. H., & Wolkowitz, O. M. (2023) · Scientific Reports · doi:10.1038/s41598-023-35912-z · Cited by 12
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“Within these cell compartments, telomerase may be important for preventing senescence by maintaining telomere-length integrity in highly proliferative cells, like spermatocytes or hematopoietic stem cells.(42,44,70,73) Some studies have detected telomerase activity, as well as shown age-related declines, in WBCs from…”
InfluentialP. berghei Telomerase Subunit TERT is Essential for Parasite Survival
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“conditional mutagenesis [5,6,47–50] to inactivate TERT, might”
Near‐to‐perfect homeostasis: Examples of universal aging rule which germline evades
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“…in which telomere shortening clearly contributes to aging phenotypes and losses of regenerative abilities in a majority of tissues, mice have longer telomeres, and knocking out telomerase leads to preliminary aging phenotype only after 3–4 generations [Herrera et al., 1999; Rudolph et al., 1999].”
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Varshney, A., Ramakrishnan, S. K., Sharma, A., Santosh, B., Bala, J., Yadava, P. K., & Jaiswal, R. K. (2014) · Gene · doi:10.1016/j.gene.2014.06.018 · Cited by 12
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“CR has been suggested to synergize with telomerase expression to result in significant lifespan extension [34], and telomere shortening is associated with aging [35]; thus, telomere dynamics may play a role in the systemic effects of CR.”
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Temkin, A. M., & Spyropoulos, D. D. (2014) · Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology · doi:10.1016/j.cbpc.2014.02.003 · Cited by 10
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“…on a mixed C57BL6/129Sv background were found to have significantly smaller litters than G1 mTR2/2 mice, whereas generation 6 intercrosses exhibited infertility due to a number of factors, including a possible compromise in uterine structure and function (Lee et al. 1998, Herrera et al. 1999a).”
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Zhang, F., Cheng, D., Porter, K. I., Heck, E. A., Wang, S., Zhang, H., Davis, C. J., Robertson, G. P., & Zhu, J. (2025) · Nature Communications · doi:10.1038/s41467-025-56559-6 · Cited by 11
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Tian, C., Heng, D., Zhao, N., Liu, L., Sheng, X., Chen, J., & Liu, L. (2022) · Science China Life Sciences · doi:10.1007/s11427-022-2151-0 · Cited by 9
“, 1998), phenotype resembling that of late generation Terc, short telomere mice (Figure S1 in Supporting Information) (Herrera et al., 1999; Rudolph et al., 1999).”
BackgroundPolonio, A. M., Medrano, M., Chico-Sordo, L., Córdova-Oriz, I., Cozzolino, M., Montáns, J., Herraiz, S., Seli, E. U., Pellicer, A., García-Velasco, J. A., et al. (2023) · Aging · doi:10.18632/aging.204731 · Cited by 10
Molecular Diagnosis and Precision Therapeutic Approaches for Telomere Biology Disorders
Perona, R., Iarriccio, L., Pintado‐Berninches, L., Rodríguez-Centeno, J., Manguán-García, C., Garcia, E., López‐Ayllón, B. D., & Sastre, L. (2016) · InTech eBooks · doi:10.5772/65353 · Cited by 9
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“already mentioned, previous studies have indicated that the sperm telomere length of fertile males is significantly higher compared to that of infertile males (5,31,33-35,39).”
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“However, studying aging and age-related disease in mammalian model systems has been difficult because species-specific features can limit the extrapolation of observations between an animal model and human aging time frames [73–76].”
Large defects of type I allergic response in telomerase reverse transcriptase knockout mice
Ujike, A., Okada, A., Du, Y., Maruyama, M., Yuan, X., Ishikawa, F., Motoo, Y., Isobe, K., & Nakajima, H. (2007) · Journal of Leukocyte Biology · doi:10.1189/jlb.1006638 · Cited by 7
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BackgroundInfluentialThe contribution of biogerontology to quality ageing
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“…begin to develop cancer and exhibit certain other pathologies associated with human aging such as hair graying, alopecia, skin lesions, impaired wound healing, cancer, and shortened lifespan (Blasco et al., 1997; Lee et al., 1998; Herrera et al., 1999; Rudolph et al., 1999; Artandi et al., 2000).”
BackgroundInfluentialChang, W., Wu, Y.-H., Xu, J., & Sung, L. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20051236 · Cited by 7
“The tail-tip fibroblast from wild-type C57BL/6, Terc+/− and Terc−/− generation 2 (G2) mice [3,32] was used as the donor cells for somatic cell nuclear transfer (SCNT) and generated for ntESCs in this study.”
MethodDifferential impact of a dyskeratosis congenita mutation in TPP1 on mouse hematopoiesis and germline
Graniel, J. V., Bisht, K. K., Friedman, A. D., White, J. S., Perkey, E., Vanderbeck, A., Moroz, A., Carrington, L. J., Brandstadter, J. D., Allen, F., et al. (2021) · Life Science Alliance · doi:10.26508/lsa.202101208 · Cited by 7
“We next turned our attention to fertility as a readout for germ cell function, as complete knockout of telomerase is known to cause infertility in late-generation mice (Blasco et al. 1997; Herrera et al. 1999).”
BackgroundCallén, E., Ramı́rez, M. J., Creus, A., Marcos, R., Ortega, J., Olivé, T., Badell, I., & Surrallés, J. (2002) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(02)00081-7 · Cited by 6
Fertility, IVF and reproductive genetics
Varela, E., Sánchez-de-Puerta, I., & García-Velasco, J. A. (2018) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0000000000000456 · Cited by 6
Correction: 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/annotation/f5e4554b-18cc-46ef-ac39-73ac4d6750ae · Cited by 6
Prescott, J. C., & Blackburn, E. H. (2002) · Wiley eBooks · doi:10.1002/0471203076.emm1023 · Cited by 6
Emerging roles for telomerase in neuronal development and apoptosis
Mattson, M. P., & Klapper, W. (2001) · Journal of Neuroscience Research · doi:10.1002/1097-4547(20010101)63:1 · Cited by 76
Roberts, A. R., Huang, E., Jones, L., Daxinger, L., Chong, S., & Whitelaw, E. (2013) · Chromosoma · doi:10.1007/s00412-013-0427-8 · Cited by 5
“Reduced levels of telomerase result in the progressive acquisition of shorter telomeres across generations in the mouse (Blasco et al. 1997; Herrera et al. 1999).”
BackgroundMethodInfluentialTelomeres and Telomerase as Promising Targets for Malaria Therapy: A Comprehensive ReviewPreprint
Wakai, T. N., Anzaku, D. O., & Afolabi, I. S. (2024) · Preprints.org · doi:10.20944/preprints202404.1000.v1 · Cited by 4
Loss of Ten1 in mice induces telomere shortening and models human dyskeratosis congenita
Sanz‐Moreno, A., Becker, L., Xie, K., da Silva‐Buttkus, P., Dragano, N. R. V., Aguilar‐Pimentel, J. A., Amarie, O. V., Calzada‐Wack, J., Kraiger, M., Leuchtenberger, S., et al. (2025) · Science Advances · doi:10.1126/sciadv.adp8093 · Cited by 5
“Z e n t r a l b i b li o t h e k on A p r il 14 , 2025 atrophy was also reported in mice with shorter telomeres or telomerase deficiency ( 47 – 49 ).”
Self-citationCell-cycle-dependent telomere elongation by telomerase in budding yeast
Li, S. (2011) · Bioscience Reports · doi:10.1042/bsr20100095 · Cited by 4
Oncostatin M Maintains Naïve Pluripotency of mESCs by Tetraploid Embryo Complementation (TEC) Assay
Ye, X., Tian, C., Liu, L., Feng, G., Jin, K., Wang, H., Chen, J., & Liu, L. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.675411 · Cited by 4
Sonoda, S., & Yamaza, T. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1151429 · Cited by 4
“Furthermore, telomerase knockout mice express several disorders (60, 61).”
BackgroundTelomeres and Reproductive Aging
Aydos, S. (2012) · InTech eBooks · doi:10.5772/38854 · Cited by 4
“As well as various pathologies, telomere dysfunction in late generations also leads to decline in fertility in female mice, eventually resulting in sterility (Lee et al., 1998; Herrera et al., 1999).”
BackgroundWhen Long Noncoding RNAs Meet Genome Editing in Pluripotent Stem Cells
Chen, F., Ji, J., Shen, J., & Lu, X. (2017) · Stem Cells International · doi:10.1155/2017/3250624 · Cited by 4
“Ablation of the Terc lncRNA gene resulted in telomere shortening, which subsequently affected chromosome stability and proliferation of mouse ESCs [70, 71].”
BackgroundSui, Y., & Peng, S. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.618113 · Cited by 4
“, 1998), this does not align with evidence showing that only in germ line cell and adult stem cell populations the activity of telomerase is sufficient to sustain the telomere length (TL) of homeostasis (Lee et al., 1998; Herrera et al., 1999; Dokal, 2000; Hao et al., 2005; Liu et al., 2007), and in most fully differe…”
BackgroundRobinson, M. O. (2000) · Springer eBooks · doi:10.1007/978-1-4615-4199-8_12 · Cited by 4
Blasco, M. A. (2001) · Advances in cell aging and gerontology · doi:10.1016/s1566-3124(01)08008-7 · Cited by 4
Self-citationTrubitsyn, A. G. (2013) · Advances in Gerontology · doi:10.1134/s2079057013030120 · Cited by 4
“Herrera [49].”
Extracting Extra-Telomeric Phenotypes from Telomerase Mouse Models
Sung, Y. H., Ali, M., & Lee, H. (2013) · Yonsei Medical Journal · doi:10.3349/ymj.2014.55.1.1 · Cited by 4
Self-citationScalp bacterial species influence SIRT1 and TERT expression in keratinocytes
Yamada, A., Watanabe, K., Nishi, Y., Oshiro, M., Katakura, Y., Sakai, K., & Tashiro, Y. (2023) · Bioscience Biotechnology and Biochemistry · doi:10.1093/bbb/zbad122 · Cited by 3
Klinaki, E., & Ogrodnik, M. B. (2024) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2024.111929 · Cited by 3
Moderate stem-cell telomere shortening rate postpones cancer onset in a stochastic model
Holbek, S., Bendtsen, K. M., & Juul, J. (2013) · Physical Review E · doi:10.1103/physreve.88.042706 · Cited by 3
The role of telomere dysfunction in genomic instability and age-related diseases
Xu, L., Zhang, K., & Cong, Y. (2021) · Genome Instability & Disease · doi:10.1007/s42764-021-00052-z · Cited by 3
Culture conditions of mouse ESCs impact the tumor appearance in vivo
Tian, C., Wang, J., Ye, X., Chen, J., Zheng, R., Yu, H., Li, J., Yin, G., Liu, L., Zhao, N., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112645 · Cited by 4
Alexander, G. (2012) · InTech eBooks · doi:10.5772/31410 · Cited by 3
“These data were confirmed by another group of authors led by Herrera (Herrera et al., 1999).”
ResultTrubitsyn, A. G. (2011) · Advances in Gerontology · doi:10.1134/s2079057011020147 · Cited by 3
“These data were confirmed by another group of authors led by Herrera [15].”
ResultBiogerontology research in Spain
Solana, R. (2003) · Experimental Gerontology · doi:10.1016/s0531-5565(03)00094-9 · Cited by 3
Murine Models of Dysfunctional Telomeres and Telomerase
Liu, Y., & Harrington, L. A. (2012) · Wiley eBooks · doi:10.1002/9781118268667.ch9 · Cited by 3
Telomere-based treatment strategy of cardiovascular diseases: imagination comes to reality
Abdel‐Gabbar, M., & Kordy, M. G. M. (2024) · Genome Instability & Disease · doi:10.1007/s42764-024-00123-x · Cited by 2
“These mice had premature aging characteristics in many highly proliferating compartments such as the heart and brain (Blasco et al., 1997; Ferrón et al., 2004; Herrera et al., 1999; Lee et al., 1998; Leri et al., 2003).”
Leukocyte Telomere Dynamics, Human Aging, and Life Span
Aviv, A. (2010) · Elsevier eBooks · doi:10.1016/b978-0-12-378638-8.00007-5 · Cited by 3
Telomerase Mutations and Premature Ageing in Humans
Du, H., Bessler, M., & Mason, P. J. (2007) · Springer eBooks · doi:10.1007/978-3-540-73709-4_5 · Cited by 2
Variation of telomeric DNA content in gingiva and dental pulp
Kumei, Y., Akiyama, H., Onizuka, T., & Kobayashi, C. (2011) · Archives of Oral Biology · doi:10.1016/j.archoralbio.2011.07.009 · Cited by 2
The Stem Cell Hypothesis of Aging
Meiliana, A., & Wijaya, A. (2010) · The Indonesian Biomedical Journal · doi:10.18585/inabj.v2i1.108 · Cited by 2
George, A. L., Boulanger, C. A., & Smith, G. H. (2016) · Aging · doi:10.18632/aging.100985 · Cited by 2
“It was reported that no phenotype was observed in the renewing tissues, such as the intestinal, germinal or hematopoietic tissues, in mice null for the telomerase RNA template in early generations, and defects only emerged after four breeding generations [36-38].”
BackgroundPhylogeny of age-related fitness decline in the wild and of related phenomena
Libertini, G. (2011) · Cited by 2
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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