Cited by 859Telomeres, Telomerase, and SenescenceGenetics, Aging, and Longevity in Model OrganismsNuclear Structure and Function

The DOI matches its Crossref record.

Activation of telomerase in human lymphocytes and hematopoietic progenitor cells

Hiyama, K, Hirai, Y, Kyoizumi, S, Akiyama, M, Hiyama, E, Piatyszek, M A, Shay, J W, Ishioka, S, Yamakido, M·1995·The Journal of Immunology

DOI 10.4049/jimmunol.155.8.3711

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Abstract

This is the first report describing up-regulation of telomerase activity in human normal cells. Telomerase, a ribonucleoprotein enzyme, has been thought to be involved in maintaining telomere length stability in germline and most cancer cells, but not in normal cells. However, in the present study, we demonstrate that telomerase activity is detectable at low levels in normal human T and B cells, increases by in vitro mitogenic stimulation, increases in hematopoietic progenitor cells upon their proliferation and differentiation, and decreases with aging. Understanding the regulation of telomerase activity in normal cells may provide important insights not only into the mechanisms of normal cellular senescence but also into the mechanisms of telomerase activity deregulation as part of cancer development.

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BackgroundInfluential
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T cells and aging (update February 1999)
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“(294) have shown that telomerase activity is detectable at very low levels in normal human T and B cells and that it increases greatly after mitogenic stimulation.”
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Self-citation
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BackgroundMethodInfluentialSelf-citation
Getting to the end: telomerase access in yeast and humans
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“Following immune stimulation, T lymphocytes show increased telomerase activity that is independent of TERT transcriptio”
Background
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“In contrast, telomerase activity is very low or absent in somatic cells, although telomerase activity has been found in normal human blood cells, proliferative basal skin layer, endometrial tissue, intestinal crypt proliferative zone, and hair follicles (40-44).”
Background
Telomeres 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
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“Telomerase activity in PBMC cells Telomerase, the enzyme that counteracts telomere shortening, has been shown to be present in most normal haemopoietic cells (Hiyama et al, 1995).”
Background
Telomeres and immunological diseases of aging.
Andrews, N. P., Fujii, H., Goronzy, J. J., & Weyand, C. M. (2010) · Gerontology · doi:10.1159/000268620 · Cited by 108
“Lymphocytes have a unique requirement for clonal expansion that necessitates robust proliferative capacity. To circumvent growth arrest due to replication-associated telomere loss, immune cells maintain their chromosome ends via telomerase induction during entry into the cell cycle. Early studies described very low to…”
Background
Inherited bone marrow failure associated with germline mutation of ACD, the gene encoding telomere protein TPP1
Guo, Y., Kartawinata, M., Li, J., Pickett, H. A., Teo, J., Kilo, T., Barbaro, P., Keating, B. J., Chen, Y., Tian, L., et al. (2014) · Blood · doi:10.1182/blood-2014-08-596445 · Cited by 123
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“In contrast, telomerase is restricted to a few normal cell types in humans, including germ cells, stem cells, activated lymphocytes and epithelial cells with high reproductive demand.(10-14) Additionally, during the germinal center (GC) reaction in lymph nodes high levels of telomerase activity is expressed in the GC…”
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Corneal endothelial regeneration and tissue engineering
Mimura, T., Yamagami, S., & Amano, S. (2013) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2013.01.003 · Cited by 119
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“In humans, telomerase is active in the germline, early in embryogenesis, in stem cells, and following stimulation of an immune response (8,9).”
BackgroundInfluential
Variation at theTERTlocus and predisposition for cancer
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Age-related telomere uncapping is associated with cellular senescence and inflammation independent of telomere shortening in human arteries
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“Telomere length homeostasis is maintained by hTERT activity (39), primarily in germ cells, white blood cells (WBCs), and adult stem cell compartments (25, 27, 34).”
Background
Derivation and large-scale expansion of multipotent astroglial neural progenitors from adult human brain
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Ethanol induces cell-cycle activity and reduces stem cell diversity to alter both regenerative capacity and differentiation potential of cerebral cortical neuroepithelial precursors
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“The telomerase complex, a reverse transcriptase enzyme complex, maintains telomeres during DNA replication [35-37], thereby preventing genomic instability and cellular senescence.”
Background
Telomere and adaptive immunity
Weng, N.-P. (2008) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2007.11.005 · Cited by 99
“Like T cells, telomerase is not expressed in resting B cells but is rapidly activated after mitogenic stimulation (Hiyama et al., 1995; Weng et al., 1997a).”
Mitochondria, Telomeres and Telomerase Subunits
Zheng, Q., Huang, J., & Wang, G. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00274 · Cited by 118
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BackgroundMethod
Telomeres, Telomerase and Ageing
Saretzki, G. C. (2018) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-981-13-2835-0_9 · Cited by 120
Virus-Induced CD8+ T Cell Clonal Expansion Is Associated with Telomerase Up-Regulation and Telomere Length Preservation: A Mechanism for Rescue from Replicative Senescence
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“Telomerase activity has been demonstrated at very low levels in circulating lymphocytes of healthy individuals with the highly sensitive PCR-based TRAP technique, with the amount detected being inversely related to donor age (12).”
Background
IL-2 Increases Human Telomerase Reverse Transcriptase Activity Transcriptionally and Posttranslationally through Phosphatidylinositol 3′-Kinase/Akt, Heat Shock Protein 90, and Mammalian Target of Rapamycin in Transformed NK Cells
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“Our observation of full activation of telomerase activity in NK-92 cells 24 h after stimulation with IL-2 is compatible with previous findings in PBLs stimulated with mitogen (5, 12, 13, 18).”
Result
Telomere Length, Aging, and Somatic Cell Turnover
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Function of AP-1 in Transcription of the Telomerase Reverse Transcriptase Gene (TERT) in Human and Mouse Cells
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BackgroundSelf-citation
Interplay between telomere length and telomerase in human leukocyte differentiation and aging
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“Journal of Leukocyte Biology Volume 70, December 2001 861 skin and intestine-endothelial cells) [13, 14], and lymphocytes [15, 16 ].”
Background
Telomerase activity and the expression of telomerase components in acute myelogenous leukaemia
Xu, D., Gruber, A., Peterson, C. O., & Pisa, P. (1998) · British Journal of Haematology · doi:10.1046/j.1365-2141.1998.00969.x · Cited by 107
Telomerase Activity Does Not Always Imply Telomere Maintenance
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Self-citation
Telomerase activity is repressed during differentiation of maturation-sensitive but not resistant human tumor cell lines.
Albanell, J., Han, W., Mellado, B., Gunawardane, R. N., Scher, H. I., Dmitrovsky, E., & Moore, M. A. S. (1996) · PubMed · Cited by 104
Telomere Length Dynamics in Telomerase-Positive Immortal Human Cell Populations
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Self-citation
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Self-citation
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“Occasional studies have detected extremely low levels of telomerase in neutrophils (Broccoli et al, 1995) but others have not (Hiyama et al, 1995), and differentiation studies have demonstrated inhibition of telomerase activity as the mature myeloid phenotype is reached (Sharma et al, 1995).”
Background
Cytological detection of telomerase activity using an in situ telomeric repeat amplification protocol assay.
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Self-citation
Telomeres and telomerase in normal and malignant haematopoietic cells
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“Telomerase activity is extremely low or absent in unstimulated human peripheral blood T cells, but activation in vitro induces high levels of enzymic activity but only a modest increase in hTERT expression (2, 15, 23).”
Background
Telomerase Activity Is Increased and Telomere Length Shortened in T Cells from Blood of Patients with Atopic Dermatitis and Psoriasis
Wu, K., Higashi, N., Hansen, E. R., Lund, M., Bang, K., & Thestrup‐Pedersen, K. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.165.8.4742 · Cited by 95
Hypoxia Up-Regulates Telomerase Activity via Mitogen-Activated Protein Kinase Signaling in Human Solid Tumor Cells
Seimiya, H., Tanji, M., Oh‐hara, T., Tomida, A., Naasani, I., & Tsuruo, T. (1999) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1999.0910 · Cited by 96
A Multipotent Neural Crest-Derived Progenitor Cell Population Is Resident Within the Oral Mucosa Lamina Propria
Davies, L. C., Locke, M., Webb, R. D. J., Roberts, J. T., Langley, M. S., Thomas, D. W., Archer, C. W., & Stephens, P. (2010) · Stem Cells and Development · doi:10.1089/scd.2009.0089 · Cited by 95
“Telomerase activity is generally considered to be diminished within somatic cells with the exception of stem cells and lymphocytes [45,46].”
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Schroers, R., Huang, X. F., Hammer, J., Zhang, J., & Chen, S. (2002) · PubMed · Cited by 95
Accelerated replicative senescence of the peripheral immune system induced by HIV infection
Bestilny, L. J., Gill, M. J., Mody, C. H., & Riabowol, K. T. (2000) · AIDS · doi:10.1097/00002030-200005050-00002 · Cited by 95
Telomere maintenance in human B lymphocytes
Martens, U. M., Brass, V., Sedlacek, L., Pantić, M., Exner, C., Guo, Y., Engelhardt, M. M., Lansdorp, P. M., Waller, C. F., & Lange, W. (2002) · British Journal of Haematology · doi:10.1046/j.1365-2141.2002.03910.x · Cited by 94
“Unstimulated B cells from peripheral blood and tonsils have been reported to express low or undetectable levels of telomerase (Broccoli et al, 1995; Hiyama et al, 1995; Norrback et al, 2001).”
Background
Evidence for UV-associated activation of telomerase in human skin.
Ueda, M., Ouhtit, A., Bito, T., Nakazawa, K., Lübbe, J., Ichihashi, M., Yamasaki, H., & Nakazawa, H. (1997) · PubMed · Cited by 95
Is telomerase activity in cancer due to selection of stem cells and differentiation arrest?
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Multiple pathways for the regulation of telomerase activity
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Self-citation
Telomerase activity and in situ telomerase RNA expression in malignant and non-malignant lymph nodes.
Yashima, K., Piatyszek, M. A., Saboorian, H. M., Virmani, A. K., Brown, D. F., Shay, J. W., & Gazdar, A. F. (1997) · Journal of Clinical Pathology · doi:10.1136/jcp.50.2.110 · Cited by 90
Self-citation
Do telomeres adapt to physiological stress? Exploring the effect of exercise on telomere length and telomere-related proteins
Ludlow, A. T., Ludlow, L. W., & Roth, S. M. (2013) · BioMed Research International · doi:10.1155/2013/601368 · Cited by 93
“Mitogen stimulation of immune cells increases telomerase activity in T cells [107], suggesting that telomerase activity may be increased in long-term exercise-trained individuals in order to maintain telomere length following the repeated proliferative stress of strenuous exercise.”
Background
Telomerase in Cancer: Function, Regulation, and Clinical Translation
Robinson, N. J., & Schiemann, W. P. (2022) · Cancers · doi:10.3390/cancers14030808 · Cited by 105
“It should be noted that, while telomerase is not widely expressed throughout the body, its activity is maintained by tissue-resident stem cell populations, including hematopoietic [221], intestinal [222], and germline [223].”
Background
Normal mammalian cells negatively regulate telomere length by telomere trimming
Pickett, H. A., Henson, J. D., Au, A. Y. M., Neumann, A. A., & Reddel, R. R. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr402 · Cited by 100
“Telomerase activity is repressed or tightly controlled in most normal human somatic cells, but is readily detectable in activated lymphocytes (15).”
Telomerase Activity in Benign and Malignant Thyroid Tumors
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Authors: Hiyama, K., Hirai, Y., Kyoizumi, S., Akiyama, M., Hiyama, E., Piatyszek, M. A., Shay, J. W., Ishioka, S., & Yamakido, M.
Affiliations: Hiroshima University (JP)
ORCID: Akiyama, M
Hiyama, E
Piatyszek, M A
Shay, J W
Ishioka, S
Venue: The Journal of Immunology
Publisher: Oxford University Press (OUP)
Published: 1995-10
Volume: 155
Issue: 8
Pages: 3711-3715
ISSN: 0022-1767 (ISSN-L)
1550-6606
DOI: 10.4049/jimmunol.155.8.3711
OpenAlex: W1516272650
Cited by: 853
References: 0
Citations by year: 2026: 1 · 2025: 4 · 2024: 2 · 2023: 10 · 2022: 6 · 2021: 11 · 2020: 9 · 2019: 13 · 2018: 11 · 2017: 8 · 2016: 13 · 2015: 15 · 2014: 17 · 2013: 20 · 2012: 17
FWCI: 38.21
Type: journal article
Language: en
Open access: closed
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: The Journal of Immunology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute on Aging (AG07992, R01AG007992)
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, telomerase activity, lymphocytes, T cells, B cells, hematopoietic progenitor cells, mitogen stimulation, aging, cellular senescence, telomere length, carcinogenesis, normal cells
MeSH terms: Adolescent, Adult, Aged, Aged, 80 and over, Aging, Base Sequence, Bone Marrow Cells, Cell Separation, Child, Child, Preschool, Enzyme Activation, Hematopoietic Stem Cells, Humans, Infant, Infant, Newborn, Leukocytes, Mononuclear, Lymphocyte Activation, Lymphocytes, Male, Middle Aged, Molecular Sequence Data, Telomerase

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Activation of telomerase in human lymphocytes and hematopoietic progenitor cells

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