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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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“A major determinant of cellular mortality is the telomere shortening that accompanies normal proliferation [4], so a key event in acquisition of cellular immortality is the up-regulation of a telomere length maintenance mechanism (TMM) [5].”
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BackgroundCharacterization of Interactions between PinX1 and Human Telomerase Subunits hTERT and hTR
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“Telomerase, a ribonucleic acid-protein complex, adds hexameric repeats of 5'-TTAGGG-3' to the ends of telomeres to compensate for the progressive loss (Blackburn, 1991; Counter et al., 1992; de Lange, 1994).”
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BackgroundSenescence: does it all happen at the ends?
Stewart, S. A., & Weinberg, R. A. (2002) · Oncogene · doi:10.1038/sj.onc.1205062 · Cited by 77
“Rare variants, appearing at a frequency of less than one cell in 107, emerge from a population of cells in crisis (Counter et al., 1992; Wright et al., 1989).”
BackgroundTelomerase-independent Regulation of ATR by Human Telomerase RNA
Kedde, M., le Sage, C., Duursma, A. M., Zlotorynski, E., van Leeuwen, B., Nijkamp, W., Beijersbergen, R. L., & Agami, R. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m607676200 · Cited by 78
Akiyama, M., Yamada, O., Kanda, N., Akita, S., Kawano, T., Ohno, T., Mizoguchi, H., Eto, Y., Anderson, K. C., & Yamada, H. (2002) · Cancer Letters · doi:10.1016/s0304-3835(01)00838-2 · Cited by 74
Detection of telomerase activity by the TRAP assay and its variants and alternatives
Fajkus, J. (2006) · Clinica Chimica Acta · doi:10.1016/j.cca.2006.02.039 · Cited by 76
Human herpesvirus-8 and Kaposi's sarcoma: Relationship with the multistep concept of tumorigenesis
Stürzl, M., Zietz, C., Monini, P., & Ensoli, B. (2001) · Advances in cancer research · doi:10.1016/s0065-230x(01)81004-6 · Cited by 76
Telomerase and Cancer Stem CellsPreprint
Armanios, M. Y., & Greider, C. W. (2005) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2005.70.030 · Cited by 76
Self-citationSensing telomerase: From in vitro detection to in vivo imaging
Wang, L., Ma, F., Tang, B., & Zhang, C. (2016) · Chemical Science · doi:10.1039/c6sc04801c · Cited by 75
Induction of Telomerase Activity in Fibroblasts from Bleomycin-Injured Lungs
Nozaki, Y., Liu, T., Hatano, K., Gharaee‐Kermani, M., & Phan, S. H. (2000) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/ajrcmb.23.4.3958 · Cited by 75
Griffith, J. K., Bryant, J. E., Fordyce, C., Gilliland, F. D., Joste, N. E., & Moyzis, R. K. (1999) · Breast Cancer Research and Treatment · doi:10.1023/a:1006128228761 · Cited by 75
Telomerase is activated in the prostate and seminal vesicles of the castrated rat
Meeker, A. K., Sommerfeld, H. J., & Coffey, D. S. (1996) · Endocrinology · doi:10.1210/endo.137.12.8940411 · Cited by 75
Potent Inhibition of Human Telomerase by Nitrostyrene Derivatives
Kim, J., Kim, J. H., Lee, G. E., Lee, J. E., & Chung, I. K. (2003) · Molecular Pharmacology · doi:10.1124/mol.63.5.1117 · Cited by 75
“In immortal cells, telomere shortening can be arrested by the reactivation of telomerase (Counter et al., 1992; Harley et al., 1994).”
BackgroundPalanca-Wessels, M. C., Klingelhutz, A. J., Reid, B. J., Norwood, T. H., Opheim, K. E., Paulson, T. G., Feng, Z., & Rabinovitch, P. S. (2003) · Carcinogenesis · doi:10.1093/carcin/bgg076 · Cited by 75
Recent Advances in Stem Cell Neurobiology
Ostenfeld, T., & Svendsen, C. N. (2003) · Advances and technical standards in neurosurgery · doi:10.1007/978-3-7091-0641-9_1 · Cited by 74
Agents that target telomerase and telomeres
Raymond, É. (1996) · Current Opinion in Biotechnology · doi:10.1016/s0958-1669(96)80068-1 · Cited by 74
Development of Retinoblastoma in the Absence of Telomerase Activity
Gupta, J., Han, L.-P., Wang, P., Gallie, B. L., & Bacchetti, S. (1996) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/88.16.1152 · Cited by 74
Self-citationThe Story of CD4+CD28−T Cells Revisited: Solved or Still Ongoing?
Maly, K., & Schirmer, M. (2015) · Journal of Immunology Research · doi:10.1155/2015/348746 · Cited by 77
Significance of Immunological Detection of Human Telomerase Reverse Transcriptase
Kyo, S., Masutomi, K., Maida, Y., Kanaya, T., Yatabe, N., Nakamura, M., Tanaka, M., Takarada, M., Sugawara, I., Murakami, S., et al. (2003) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)63446-3 · Cited by 73
“Activation of this enzyme is therefore required for cells to overcome replicative senescence and be able to divide indefinitely.(4,5) This hypothesis is supported by observations that telomerase is frequently activated in the vast majority of cancers or cancer cell lines but not in most normal tissues.”
BackgroundTherapeutic targeting of replicative immortality
Yaswen, P., MacKenzie, K. L., Keith, W. N., Hentosh, P., Rodier, F., Zhu, J., Firestone, G. L., Matheu, A., Carnero, A., Bilsland, A. E., et al. (2015) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2015.03.007 · Cited by 82
“[38] Counter CM, Avilion AA, LeFeuvre CE, Stewart NG, Greider CW, Harley CB, et al.”
BackgroundEscape from Telomere-Driven Crisis Is DNA Ligase III Dependent
Jones, R. E., Oh, S., Grimstead, J. W., Zimbric, J., Roger, L., Heppel, N. H., Ashelford, K. E., Liddiard, K., Hendrickson, E. A., & Baird, D. M. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.07.007 · Cited by 74
Telomere shortening in the colonic mucosa of patients with ulcerative colitis
Kinouchi, Y., Hiwatashi, N., Chida, M., Nagashima, F., Takagi, S., Maekawa, H., & Toyota, T. (1998) · Journal of Gastroenterology · doi:10.1007/s005350050094 · Cited by 74
Immunosenescence in HIV Pathogenesis
Pommier, J., Gauthier, L., Livartowski, J., Galanaud, P., Boué, F., Dulioust, A., Marcé, D., Ducray, C., Sabatier, L., Lebeau, J., et al. (1997) · Virology · doi:10.1006/viro.1997.8512 · Cited by 74
Masutomi, K., & Hahn, W. C. (2003) · Cancer Letters · doi:10.1016/s0304-3835(02)00703-6 · Cited by 75
“[48] C.”
BackgroundInfluentialScherthan, H., Jerratsch, M., Dhar, S., Wang, Y., Goff, S. P., & Pandita, T. K. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.20.7773-7783.2000 · Cited by 74
“Telomere associations correlate with genomic instability and carcinogenicity (21, 64, 65).”
BackgroundArchitecture of telomerase RNA.
Bhattacharyya, A., & Blackburn, E. H. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06910.x · Cited by 74
Telomerase Activity in Melanocytic Lesions
Rudolph, P., Schubert, C., Tamm, S., Heidorn, K., Hauschild, A., Michalska, I., Majewski, S., Krupp, G., Jabłońska, S., & Parwaresch, R. M. (2000) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65011-0 · Cited by 75
“Accordingly, in contrast to the majority of mammalian somatic cells, most immortal cells examined to date exhibit significant levels of telomerase activity(9) and show no net loss of telomere length during proliferation.(10,11) Telomerase activity has also been found in the majority of common human cancers(12,13) and…”
BackgroundDyskeratosis congenita, telomeres and human ageing
Marciniak, R. A., Johnson, F. B., & Guarente, L. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(00)01984-3 · Cited by 74
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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