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Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity.
Open accessAbstract
Loss of telomeric DNA during cell proliferation may play a role in ageing and cancer. Since telomeres permit complete replication of eukaryotic chromosomes and protect their ends from recombination, we have measured telomere length, telomerase activity and chromosome rearrangements in human cells before and after transformation with SV40 or Ad5. In all mortal populations, telomeres shortened by approximately 65 bp/generation during the lifespan of the cultures. When transformed cells reached crisis, the length of the telomeric TTAGGG repeats was only approximately 1.5 kbp and many dicentric chromosomes were observed. In immortal cells, telomere length and frequency of dicentric chromosomes stabilized after crisis. Telomerase activity was not detectable in control or extended lifespan populations but was present in immortal populations. These results suggest that chromosomes with short (TTAGGG)n tracts are recombinogenic, critically shortened telomeres may be incompatible with cell proliferation and stabilization of telomere length by telomerase may be required for immortalization.
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“In primary cells deficient for Rb and p53, continued cellular growth beyond the Hayflick limit results in severe telomere shortening, marked genetic instability, and massive cell death—a period referred to as crisis (Counter et al. 1992”
From p53 Deficiency Rescues the Adverse Effects of Telomere Loss and Cooperates with Telomere Dysfunction to Accelerate Carcinogenesis (1999) · cites this paper as Counter et al. 1992
In the citing paper
“However, as these human fibroblasts undergo additional cell divisions, telomere erosion continues and the loss of telomere capping function produces rampant chromosomal instability and widespread apoptosis, a cellular state termed crisis (27).”
From Telomeres and telomerase in cancer (2010) · cites this paper as [27]
In the citing paper
“Crisis serves as the second checkpoint in tumor suppression and is characterized by multiple chromosomal fusions36.”
From Telomere dysfunction and tumour suppression: the senescence connection (2008) · cites this paper as [36]
In the citing paper
“Telomere maintenance is essential to the replicative potential of malignant cells and the inhibition of telomerase can lead to telomere shortening and cessation of unrestrained proliferation.”
From A highly selective telomerase inhibitor limiting human cancer cell proliferation (2001) · cites this paper as Counter et al., 1992
In the citing paper
“Eventually, telomeres shorten to a critical length and lose their ability to protect the ends of chromosomal DNA (Counter et al., 1992;Blasco et al., 1997).”
From A highly selective telomerase inhibitor limiting human cancer cell proliferation (2001) · cites this paper as Counter et al., 1992
In the citing paper
“Telomere maintenance is essential to the replicative potential of malignant cells and the inhibition of telomerase can lead to telomere shortening and cessation of unrestrained proliferation.”
From A highly selective telomerase inhibitor limiting human cancer cell proliferation (2001) · cites this paper as Counter et al., 1992
In the citing paper
“In cancer cells, the reactivation of telomerase is thought to stabilize telomere length, thereby compensating for the cell division-related telomere erosion and providing unlimited proliferative capacity to malignant cells (Counter et al., 1992;Kim et al., 1994).”
From A highly selective telomerase inhibitor limiting human cancer cell proliferation (2001) · cites this paper as Counter et al., 1992
In the citing paper
“In most normal human cells, telomerase activity is low or not detectable, and telomeric DNA is progressively lost at a rate of 30±120 bp with each replication cycle (Harley et al., 1990;Hastie et al., 1990;Counter et al., 1992).”
From A highly selective telomerase inhibitor limiting human cancer cell proliferation (2001) · cites this paper as Counter et al., 1992
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“Telomerase is suppressed in the majority of somatic cells leading to the continuing telomere attrition which leads to irreversible cell-cycle arrest and cell senescence [74].”
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Telomerase activity and its clinicopathological significance in gastric cancer
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SIRT6 participates in the quality control of aged oocytes via modulating telomere function
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“These structures are closely related to cellular apoptosis [25, 26].”
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“Thus, the ability to maintain telomeres is considered to be an important step in carcinogenesis, not only to avoid senescence, but also to avoid the extensive chromosome fusion during crisis [8,9].”
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“Although the biological signi®cance of this telomeric length reduction is unclear, it is possibly related to an increased frequency of chromosome abnormalities (Counter et al. 1992).”
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“[21] and Morin [22] and performed previously by us in the study of giant cell tumor of bone [15, 16].”
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“The rare cell capable of escaping crisis always activates a telomere maintenance mechanism, which typically involves the enzyme telomerase (6, 24).”
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Dewhurst, S. M., Yao, X., Rosiene, J. A., Tian, H., Behr, J. M., Bosco, N., Takai, K., de Lange, T., & Imielinski, M. B. (2021) · Nature Communications · doi:10.1038/s41467-021-21933-7 · Cited by 38
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A simple, fast and highly sensitive assay for the detection of telomerase activity
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“A small subpopulation of cells bypass cell crisis and become immortal because of the reactivation of telomerase [16].”
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Schaetzlein, S., & Rudolph, K. L. (2004) · Reproduction Fertility and Development · doi:10.1071/rd04112 · Cited by 38
“(Counter et al. 1992; Blasco et al. 1997a; Hande et al. 1999).”
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“An important step that is required for continued division of cancer cells is therefore that they possess the ability to maintain telomeres, not only to avoid senescence but also to avoid chromosome fusion brought on by crisis (11, 25).”
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“Human telomerase is a ribonucleoprotein enzyme complex that maintains the telomeric structures at the chromosome termini by adding 50-TTAGGG-30 repeats [1,2].”
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“Cancer’s biological capabilities are often listed as including unlimited cell proliferation [1], angiogenesis [2], telomere shortening [3], suppression of apoptosis [4], and invasion and metastasis [5].”
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“A (TTAGGG) probe was randomlabelled with [α-32P]d-CTP and hybridization of membrane was performed as previously described (Counter et al., 1992).”
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“Critically shortened telomeres may thus be incompatible with cell proliferation, and stabilization of telomere length by telomerase may be required for cell immortalization [31].”
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“The (very rare) spontaneous escape from crisis observed in human cells is associated with activation of telomerase (Counter et al., 1992) or alternative, recombinationbased, mechanisms for telomere stabilization (Dunham et al., 2000), consistent with cell death being the result of excessive…”
BackgroundDNA topoisomerase II cleavage of telomeres in vitro and in vivo
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“Apart from SV40 T-antigen, a few other viruses and viral proteins, such as E1A and E1b protein of adenovirus, E6 and E7 ORFs of human papillomavirus, and Epstein-Barr virus, have been employed to produce immortal cell lines through inactivation of cell cycle checkpoints (Shay et al., 1991; Counter et al., 1992; Klinge…”
BackgroundTelomerase and hallmarks of cancer: An intricate interplay governing cancer cell evolution
Kumar, N., & Sethi, G. (2023) · Cancer Letters · doi:10.1016/j.canlet.2023.216459 · Cited by 35
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“Cytogenet Genome Res 122:255–262 (2008) 256 mechanisms, telomeres of cells that have circumvented senescence keep on shortening at every cell cycle, leading to massive chromosomal instability and cell death (Counter et al., 1992).”
A mouse model of Werner Syndrome: what can it tell us about aging and cancer?
Chang, S. S. (2004) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2004.11.007 · Cited by 35
Peptide Nucleic Acids, Morpholinos and Related Antisense Biomolecules
Janson, C. G., & During, M. J. (2006) · Springer eBooks · doi:10.1007/0-387-32956-0 · Cited by 35
Cabuy, E., & Ridder, L. D. (2001) · Archiv für Pathologische Anatomie und Physiologie und für Klinische Medicin · doi:10.1007/s004280100466 · Cited by 37
“Telomeres shorten progressively with each round of cell division as a result of the inability of DNA polymerases to replicate the 5’ end of linear DNA, and erosion of these sequences beyond a critical point is thought to signal cell cycle arrest and entry into cellular senescence [9].”
BackgroundExpression of Telomerase RNA, Telomerase Activity, and Telomere Length in Human Gliomas
Morii, K., Tanaka, R., Onda, K., Tsumanuma, I., & Yoshimura, J. (1997) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1997.7562 · Cited by 35
Telomere length of in vivo expanded CD4+CD25+ regulatory T-cells is preserved in cancer patients
Wolf, D. G. F., Rumpold, H. F., Koppelstätter, C., Gastl, G. A., Steurer, M., Mayer, G. J., Gunsilius, E., Tilg, H., & Wolf, A. M. (2005) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-005-0107-5 · Cited by 35
“shortening or complete loss leads to the formation of unstable end-to-end fusions resulting in chromosomal instability and growth arrest [4, 8].”
BackgroundKang, M., & Park, M.-H. (2001) · Critical Reviews in Oral Biology & Medicine · doi:10.1177/10454411010120010301 · Cited by 34
Incles, C. M., Schultes, C. M., Kèlland, L. R., & Neidle, S. (2003) · Molecular Pharmacology · doi:10.1124/mol.64.5.1101 · Cited by 35
“Telomere length was determined using both Slot and Southern blotting techniques as described previously (Counter et al., 1992; Bryant et al., 1997).”
MethodFang, D.-C. (2001) · World Journal of Gastroenterology · doi:10.3748/wjg.v7.i4.522 · Cited by 35
Telomerase: A Target for Anticancer Therapy
Lichtsteiner, S., LEBKOWSKI, J. S., & Vasserot, A. P. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09395.x · Cited by 35
TRF1 is a critical trans-acting factor required for de novo telomere formation in human cells
Okabe, J. (2000) · Human Molecular Genetics · doi:10.1093/hmg/9.18.2639 · Cited by 35
“0 kb) (11,13), whereas immortal cells can circumvent the crisis by stabilization of their telomeres (14).”
BackgroundTelomere length and telomerase activity in canine mammary gland tumors
Yazawa, M., Okuda, M., Setoguchi, A., Iwabuchi, S., Nishimura, R., Sasaki, N., Masuda, K., Ohno, K., & Tsujimoto, H. (2001) · American Journal of Veterinary Research · doi:10.2460/ajvr.2001.62.1539 · Cited by 36
Dairkee, S. H., Nicolau, M. M., Sayeed, A., Champion, S., Ji, Y., Moore, D. H., Yong, B., Meng, Z., & Jeffrey, S. S. (2007) · Oncogene · doi:10.1038/sj.onc.1210452 · Cited by 34
“Reactivation of telomerase for maintaining the telomeric ends of chromosomes is an essential prerequisite towards the immortalization of proliferating tumor cells (Counter et al., 1992).”
BackgroundFEZF1-AS1: a novel vital oncogenic lncRNA in multiple human malignancies
Shi, C., Sun, L., & Song, Y. (2019) · Bioscience Reports · doi:10.1042/bsr20191202 · Cited by 34
Cancer and myeloid clonal evolution in the short telomere syndromes
Schratz, K. E., & Armanios, M. Y. (2020) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2020.02.019 · Cited by 33
He, S., Yu, S., Wei, J., Ding, L., Yang, X., & Wu, Y. (2022) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2022.114043 · Cited by 34
Telomere length in Hepatitis C
Kitay‐Cohen, Y., Goldberg-Bittman, L., Hadary, R., Fejgin, M. D., & Amiel, A. (2008) · Cancer Genetics and Cytogenetics · doi:10.1016/j.cancergencyto.2008.08.006 · Cited by 34
“According to the telomere theory of aging, based on studies on yeast and in vitro human fibroblast models [3-7], at a critical point in this process, human somatic cells enter a nonreplicative but viable state, known as senescence (cellular growth arrest; mortality stage 1).”
BackgroundInfluentialPierce, S. E., Kieltyka, R. E., Sleiman, H. F., & Brodbelt, J. S. (2008) · Biopolymers · doi:10.1002/bip.21130 · Cited by 34
Role of Pin2/TRF1 in telomere maintenance and cell cycle control
Zhou, X. Z., Perrem, K., & Lu, K. P. (2003) · Journal of Cellular Biochemistry · doi:10.1002/jcb.10496 · Cited by 34
“Telomerase activity is readily detected in most human tumor tissues and immortalized and/or transformedcell lines [Counter et al., 1992;Kimetal., 1994; Broccoli et al., 1995; Taylor et al., 1996] and is sufficient in most cases to allow transformed cells to escape from crisis [Bodnar et al., 1998;…”
BackgroundTelomeres and telomerase in the clinical management of colorectal cancer
Piñol-Felis, C., Fernández-Marcelo, T., Viñas-Salas, J., & Valls-Bautista, C. (2017) · Clinical and Translational Oncology · doi:10.1007/s12094-016-1559-0 · Cited by 13
“This proliferation is followed by ulterior telomeric erosion until cells reach a second stage of mortality (M2), whereas the telomeres are critically short [49].”
BackgroundTian, X.-X., Pang, J. C.-S., Zheng, J., Chen, J., To, S. S. T., & Ng, H.-K. (2002) · British Journal of Cancer · doi:10.1038/sj.bjc.6600244 · Cited by 10
“Electrophoresis through a 1% agarose gel and Southern transfer to a nylon membrane were performed as previously described (Counter et al, 1992).”
MethodYan, Y., Ouellette, M. M., Shay, J. W., & Wright, W. E. (1996) · Molecular Biology of the Cell · doi:10.1091/mbc.7.6.975 · Cited by 9
Telomerase activity in human germline and embryonic tissues and cells
Wright, W. E., Piatyszek, M. A., Rainey, W. E., Byrd, W., & Shay, J. W. (1996) · Developmental Genetics · doi:10.1002/(sici)1520-6408(1996)18:2
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Rapid screening for psychologic distress in men with prostate carcinoma
Roth, A. J., Kornblith, A. B., Batel-Copel, L., Peabody, E., Scher, H. I., & Holland, J. C. (1998) · Cancer · doi:10.1002/(sici)1097-0142(19980515)82:10
Metadata
- Authors
- Counter, C. M., Avilion, A. A., LeFeuvre, C. E., Stewart, N. G., Greider, C. W., Harley, C. B., & Bacchetti, S.
- Affiliations
- McMaster University (CA)
- Venue
- The EMBO Journal
- Published
- 1992-05-01
- Volume
- 11
- Issue
- 5
- Pages
- 1921-1929
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC556651
- OpenAlex
- W1543500873
- Cited by
- 2,096
- References
- 53
- Citations by year
- 2026: 10 · 2025: 21 · 2024: 25 · 2023: 25 · 2022: 27 · 2021: 35 · 2020: 29 · 2019: 28 · 2018: 39 · 2017: 42 · 2016: 48 · 2015: 53 · 2014: 51 · 2013: 65 · 2012: 55
- FWCI
- 23.80
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- The EMBO Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- 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 › Genetics › Chromosomal and Genetic Variations
- Keywords
- telomere shortening, telomerase, chromosomal instability, cell immortalization, telomere length, dicentric chromosomes, telomeric DNA, SV40 transformation, adenovirus type 5, cell transformation, telomere recombination, cell proliferation, aging, cancer
- MeSH terms
- Cell Transformation, Neoplastic, Cell Transformation, Viral, Chromosomes, Human, DNA, DNA Nucleotidylexotransferase, Humans, Karyotyping, Kidney, Transfection, Telomere, Cellular Senescence
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