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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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“At crisis, the mean telomere length is much shorter than that at senescence (Counter et al., 1992), suggesting that loss of p53 and pRb checkpoints compromises the ability of cells to detect short telomeres and initiate a DNA damage response and the onset of replicative senescence.”
BackgroundMyc-mediated transformation: the repression connection
Claassen, G. F., & Hann, S. (1999) · Oncogene · doi:10.1038/sj.onc.1202747 · Cited by 127
“Telomerase activity is associated with cellular immortalization and may also play a role in tumorigenesis (reviewed in Counter et al., 1992; Kim et al., 1994; Zakian, 1997).”
BackgroundThe illusion of cell immortality
Hayflick, L. (2000) · British Journal of Cancer · doi:10.1054/bjoc.2000.1296 · Cited by 124
“Telomerase was later found to occur in extracts of immo human cell lines (Morin, 1989; Counter et al, 1992) and in ab 90% of all human tumours studied (Chiu and Harley, 199 Subsequently, the telomerase RNA component (Feng et al, 1 and the catalytic portion of the enzyme were cloned (Nakamu al,…”
BackgroundTelomerase activity and alterations in telomere length in human brain tumors.
Hiraga, S., Ohnishi, T., Izumoto, S., Miyahara, E., Kanemura, Y., Matsumura, H., & Arita, N. (1998) · PubMed · Cited by 123
Telomere shortening associated with disease evolution patterns in myelodysplastic syndromes.
Ohyashiki, J. H., Ohyashiki, K., Fujimura, T., Kawakubo, K., Shimamoto, T., Iwabuchi, A., & Toyama, K. (1994) · PubMed · Cited by 124
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“…of senescence seems to be bimodal and with an increasing proportion of cells entering senescence at late passages (Smith & Whitney, 1980), while mean telomere length seems to shorten in an almost linear fashion (Counter et al., 1992; Levy et al., 1992; Vaziri et al., 1994; Henderson et al., 1996).”
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Self-citationUbcD1, a Drosophila ubiquitin-conjugating enzyme required for proper telomere behavior.Preprint
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Evolving views of telomerase and cancer
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Telomeres and telomerase in prostate cancer development and therapy
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Restoration of the Cellular Senescence Program and Repression of Telomerase by Human Chromosome 3
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Human hepatocyte carcinogenesis
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“Thus, the length of the telomere limits the lifespan of normal somatic cells (65).”
BackgroundTelomeres and telomerase: biological and clinical importance
Dahse, R., Fiedler, W., & Ernst, G. (1997) · Clinical Chemistry · doi:10.1093/clinchem/43.5.708 · Cited by 120
“[20] transfected normal human embryonic kidney cells with Simian Virus 40 tumor antigen (SV 40 T), forming a tumor virus protein that extended the lifespan of cultured cells.”
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Time, telomeres and tumours: is cellular senescence more than an anticancer mechanism?
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For Better or Worse? Telomerase Inhibition and Cancer
de Lange, T., & Jacks, T. (1999) · Cell · doi:10.1016/s0092-8674(00)81955-8 · Cited by 119
Telomere uncapping and alternative lengthening of telomeres
Cesare, A. J., & Reddel, R. R. (2007) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2007.11.006 · Cited by 125
Structure and function of the telomeric CST complex
Rice, C., & Skordalakes, E. (2016) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2016.04.002 · Cited by 128
Immortalizing Cells for Human Consumption
Soice, E., & Johnston, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222111660 · Cited by 119
Immortal Activated Human Hepatic Stellate Cells Generated by Ectopic Telomerase Expression
Schnabl, B., Choi, Y. H., Olsen, J. C., Hagedorn, C. H., & Brenner, D. A. (2002) · Laboratory Investigation · doi:10.1038/labinvest.3780426 · Cited by 123
Visual inspection with acetic acid in the early detection of cervical cancer and precursors
Sankaranarayanan, R., Shyamalakumary, B., Wesley, R., Amma, N. S., Parkin, D. M., & Nair, M. K. (1999) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(19990105)80:1 · Cited by 114
The effects of nucleoside analogs on telomerase and telomeres inTetrahymena
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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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