The DOI matches its Crossref record; 71 of the 73 references it cites were found in a registry or an index.
Telomerase Activity in Hematopoietic Cells Is Associated with Self-Renewal Potential
Open accessAbstract
It has been proposed that the biological clock underlying the limited division potential of eukaryotic cells is telomere length. We assayed telomerase activity in single cells of the hematopoietic and immune systems. We examined hematopoietic stem cells at four stages of differentiation, lineage-committed progenitors, and mature myeloid and lymphoid cells. The frequency of telomerase-expressing cells within each population was proportional to the frequency of cells thought to have self-renewal potential. Among bone marrow hematopoietic stem cells, 70% exhibited detectable telomerase activity. The telomerase-expressing somatic cells observed in this study are not thought to be immortal, and expression was not correlated with cell cycle distribution or differentiation state. This study demonstrates that the developmental characteristic most consistently associated with telomerase expression is self-renewal potential.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“our data suggest that Terc is specific to cells of hematopoietic origin.”
From A mouse tissue atlas of small noncoding RNA (2020) · cites this paper as [39]
In the citing paper
“In stem cell and progenitor cell compartments3–5, TERT serves an important role in keeping telomeres sufficiently long and stable to prevent the adverse consequences of dysfunctional telomeres on cell viability and chromosomal stability6–8.”
From Conditional telomerase induction causes proliferation of hair follicle stem cells (2005) · cites this paper as [3]
In the citing paper
“In normal tissues, TERT is expressed in stem cells and in progenitor cells3, but its role in these compartments is not fully understood.”
From Conditional telomerase induction causes proliferation of hair follicle stem cells (2005) · cites this paper as [3]
Citations
Cites
The serial cultivation of human diploid cell strains
Hayflick, L., & Moorhead, P. S. (1961) · Experimental Cell Research · doi:10.1016/0014-4827(61)90192-6 · Cited by 8,508
Specific Association of Human Telomerase Activity with Immortal Cells and Cancer
Kim, N. W., Piatyszek, M. A., Prowse, K. R., Harley, C. B., West, M. D., Ho, P. L. C., Coviello, G. M., Wright, W. E., Weinrich, S. L., & Shay, J. W. (1994) · Science · doi:10.1126/science.7605428 · Cited by 7,091
Self-citationThe limited in vitro lifetime of human diploid cell strains
Hayflick, L. (1965) · Experimental Cell Research · doi:10.1016/0014-4827(65)90211-9 · Cited by 5,876
Telomeres shorten during ageing of human fibroblasts
Harley, C. B., Futcher, A. B., & Greider, C. W. (1990) · Nature · doi:10.1038/345458a0 · Cited by 5,750
Identification of a specific telomere terminal transferase activity in tetrahymena extracts
Greider, C. W., & Blackburn, E. H. (1985) · Cell · doi:10.1016/0092-8674(85)90170-9 · Cited by 3,400
Purification and Characterization of Mouse Hematopoietic Stem Cells
Spangrude, G. J., Heimfeld, S., & Weissman, I. L. (1988) · Science · doi:10.1126/science.2898810 · Cited by 2,908
Self-citationMoyzis, R. K., Buckingham, J. M., Cram, L. S., Dani, M. A. C., Deaven, L. L., Jones, M. D., Meyne, J., Ratliff, R. L., & Wu, J. R. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.18.6622 · Cited by 2,326
Telomere length predicts replicative capacity of human fibroblasts.
Allsopp, R. C., Vaziri, H., Patterson, C., Goldstein, S., Younglai, E. V., Futcher, A. B., Greider, C. W., & Harley, C. B. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.21.10114 · Cited by 2,200
Counter, C. M., Avilion, A. A., LeFeuvre, C. E., Stewart, N. G., Greider, C. W., Harley, C. B., & Bacchetti, S. (1992) · The EMBO Journal · doi:10.1002/j.1460-2075.1992.tb05245.x · Cited by 2,096
Telomere reduction in human colorectal carcinoma and with ageing
Hastie, N. D., Dempster, M., Dunlop, M. G., Thompson, A. M., Green, D. K., & Allshire, R. C. (1990) · Nature · doi:10.1038/346866a0 · Cited by 1,650
WATSON, J. D. (1972) · Nature New Biology · doi:10.1038/newbio239197a0 · Cited by 1,632
Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow.
Hardy, R. R., Carmack, C. E., Shinton, S. A., Kemp, J. D., & Hayakawa, K. (1991) · The Journal of Experimental Medicine · doi:10.1084/jem.173.5.1213 · Cited by 1,604
THE ORIGIN AND KINETICS OF MONONUCLEAR PHAGOCYTES
van Furth, R., & Cohn, Z. A. (1968) · The Journal of Experimental Medicine · doi:10.1084/jem.128.3.415 · Cited by 1,564
Morin, G. B. (1989) · Cell · doi:10.1016/0092-8674(89)90035-4 · Cited by 1,495
Evidence for a mitotic clock in human hematopoietic stem cells: loss of telomeric DNA with age.
Vaziri, H., Dragowska, W., Allsopp, R. C., Thomas, T. E., Harley, C. B., & Lansdorp, P. M. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.21.9857 · Cited by 1,132
Morrison, S. J., & Weissman, I. L. (1994) · Immunity · doi:10.1016/1074-7613(94)90037-x · Cited by 1,116
Self-citationTelomere end-replication problem and cell aging
Levy, M. Z., Allsopp, R. C., Futcher, A. B., Greider, C. W., & Harley, C. B. (1992) · Journal of Molecular Biology · doi:10.1016/0022-2836(92)90096-3 · Cited by 1,069
The distribution of colony‐forming cells among spleen colonies
Siminovitch, L., McCulloch, E. A., & Till, J. E. (1963) · Journal of Cellular and Comparative Physiology · doi:10.1002/jcp.1030620313 · Cited by 915
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 · Cited by 853
Conservation of the human telomere sequence (TTAGGG)n among vertebrates.
Meyne, J., Ratliff, R. L., & Moyzis, R. K. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.18.7049 · Cited by 838
The Biology of Hematopoietic Stem Cells
Morrison, S. J., Uchida, N., & Weissman, I. L. (1995) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cb.11.110195.000343 · Cited by 794
Self-citationLoss of a yeast telomere: Arrest, recovery, and chromosome loss
Sandell, L. J. (1993) · Cell · doi:10.1016/0092-8674(93)90493-a · Cited by 792
Fluorescence Activated Cell Sorting
Bonner, W. A., Hulett, H. R., Sweet, R. G., & Herzenberg, L. A. (1972) · Review of Scientific Instruments · doi:10.1063/1.1685647 · Cited by 777
Loss of telomeric DNA during aging of normal and trisomy 21 human lymphocytes.
Vaziri, H., Schächter, F., Uchida, I. A., Wei, L., Zhu, X., Effros, R. B., Cohen, D., & Harley, C. (1993) · PubMed · Cited by 737
Developmental and tissue-specific regulation of mouse telomerase and telomere length.
Prowse, K. R., & Greider, C. W. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.11.4818 · Cited by 697
Self-citationTelomerase activity in human ovarian carcinoma.
Counter, C. M., Hirte, H. W., Bacchetti, S., & Harley, C. B. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.8.2900 · Cited by 677
Athens, J. W., Haab, O. P., RAAB, S. O., Mauer, A. M., Ashenbrucker, H., Cartwright, G. E., & Wintrobe, M. M. (1961) · Journal of Clinical Investigation · doi:10.1172/jci104338 · Cited by 639
Hypervariable ultra-long telomeres in mice
Kipling, D., & Cooke, H. J. (1990) · Nature · doi:10.1038/347400a0 · Cited by 614
The purification and characterization of fetal liver hematopoietic stem cells
Morrison, S. J., Hemmati, H. D., Wandycz, A. M., & Weissman, I. L. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.22.10302 · Cited by 611
Self-citationTelomerase activity in normal leukocytes and in hematologic malignancies
Counter, C. M., Gupta, J., Harley, C., Leber, B. F., & Bacchetti, S. (1995) · Blood · doi:10.1182/blood.v85.9.2315.bloodjournal8592315 · Cited by 604
Dancey, J. T., Deubelbeiss, K. A., Harker, L. A., & Finch, C. A. (1976) · Journal of Clinical Investigation · doi:10.1172/jci108517 · Cited by 573
The telomere hypothesis of cellular aging
Harley, C. B., Vaziri, H., Counter, C. M., & Allsopp, R. (1992) · Experimental Gerontology · doi:10.1016/0531-5565(92)90068-b · Cited by 493
Wright, W. E., Shay, J. W., & Piatyszek, M. A. (1995) · Nucleic Acids Research · doi:10.1093/nar/23.18.3794 · Cited by 474
In vivo loss of telomeric repeats with age in humans
Lindsey, J., McGill, N. I., Lindsey, L. A., Green, D. K., & Cooke, H. J. (1991) · Mutation Research/DNAging · doi:10.1016/0921-8734(91)90032-7 · Cited by 463
Regulated expression of telomerase activity in human T lymphocyte development and activation.
Weng, N., Levine, B. L., June, C. H., & Hodes, R. J. (1996) · The Journal of Experimental Medicine · doi:10.1084/jem.183.6.2471 · Cited by 401
Chiu, C., Dragowska, W., Kim, N. W., Vaziri, H., Yui, J., Thomas, T. E., Harley, C. B., & Lansdorp, P. M. (1996) · STEM CELLS · doi:10.1002/stem.140239 · Cited by 388
Clonal analysis of hematopoietic stem-cell differentiation in vivo.
Smith, L., Weissman, I., & Heimfeld, S. (1991) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.88.7.2788 · Cited by 375
Self-citationCounter, C. M., Botelho, F. M., Wang, P., Harley, C. B., & Bacchetti, S. (1994) · Journal of Virology · doi:10.1128/jvi.68.5.3410-3414.1994 · Cited by 355
van Furth, R., Dulk, M. M. C. D.-D., & Mattie, H. (1973) · The Journal of Experimental Medicine · doi:10.1084/jem.138.6.1314 · Cited by 325
Developmental potential of the earliest precursor cells from the adult mouse thymus.
Wu, L., Antica, M., Johnson, G. R., Scollay, R. G., & Shortman, K. (1991) · The Journal of Experimental Medicine · doi:10.1084/jem.174.6.1617 · Cited by 293
Siminovitch, L., Till, J. E., & McCulloch, E. A. (1964) · Journal of Cellular and Comparative Physiology · doi:10.1002/jcp.1030640104 · Cited by 275
Differentiation of immortal cells inhibits telomerase activity.
Sharma, H. W., Sokoloski, J. A., Perez, J. R., Maltèse, J.-Y., Sartorelli, A. C., Stein, C., NICHOLS, G. L., Khaled, Z., Telang, N. T., & Narayanan, R. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.26.12343 · Cited by 267
Matsuzaki, Y., Gyotoku, J.-I., Ogawa, M., Nishikawa, S., Katsura, Y., Gachelin, G., & Nakauchi, H. (1993) · The Journal of Experimental Medicine · doi:10.1084/jem.178.4.1283 · Cited by 224
Germinal centers develop oligoclonally
Kroese, F. G. M., Wubbena, A. S., Seijen, H. G., & Nieuwenhuis, P. (1987) · European Journal of Immunology · doi:10.1002/eji.1830170726 · Cited by 194
Guidos, C. J., Danska, J. S., Fathman, C. G., & Weissman, I. L. (1990) · The Journal of Experimental Medicine · doi:10.1084/jem.172.3.835 · Cited by 184
Self-citationSprent, J., Schaefer, M. L., Hurd, M., Surh, C. D., & Ron, Y. (1991) · The Journal of Experimental Medicine · doi:10.1084/jem.174.3.717 · Cited by 175
Extensive telomere repeat arrays in mouse are hypervariable
Starling, J., Maule, J., Hastie, N. D., & Allshire, R. C. (1990) · Nucleic Acids Research · doi:10.1093/nar/18.23.6881 · Cited by 172
Identification of a nonprocessive telomerase activity from mouse cells.
Prowse, K. R., Avilion, A. A., & Greider, C. W. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.4.1493 · Cited by 158
Self-citationTHE FATE OF SERIALLY TRANSPLANTED BONE MARROW CELL POPULATIONS FROM YOUNG AND OLD DONORS
Ogden, D. A., & Micklem, H. S. (1976) · Transplantation · doi:10.1097/00007890-197609000-00010 · Cited by 146
THE KINETICS OF PROMONOCYTES AND MONOCYTES IN THE BONE MARROW
van Furth, R., & Dulk, M. M. C. D.-D. (1970) · The Journal of Experimental Medicine · doi:10.1084/jem.132.4.813 · Cited by 144
B cell development in the bone marrow.
Osmond, D. G. (1990) · PubMed · Cited by 141
Dual origin of mouse spleen macrophages.
van Furth, R., & Dulk, M. M. D.-D. (1984) · The Journal of Experimental Medicine · doi:10.1084/jem.160.5.1273 · Cited by 134
Heterogeneity of hematopoietic stem cells
Uchida, N., Fleming, W., Alpern, E., & Weissman, I. L. (1993) · Current Opinion in Immunology · doi:10.1016/0952-7915(93)90002-a · Cited by 133
Self-citationMonocyte retention and migration in pulmonary inflammation. Requirement for neutrophils.
Doherty, D. E., Downey, G. P., Worthen, G. S., Haslett, C., & Henson, P. M. (1988) · PubMed · Cited by 128
Parks, D. R., & Herzenberg, L. A. (1984) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(84)08086-1 · Cited by 125
Kraft, D. L., Weissman, I. L., & Waller, E. K. (1993) · The Journal of Experimental Medicine · doi:10.1084/jem.178.1.265 · Cited by 119
Self-citationThe in vivo quantitation and kinetics of monocyte migration into acute inflammatory tissue.
Issekutz, T. B., Issekutz, A. C., & Hz, M. (1981) · PubMed · Cited by 117
Macrophage Heterogeneity in Development and Differentiation.
Naito, M. (1993) · Archivum histologicum japonicum · doi:10.1679/aohc.56.331 · Cited by 96
Thymic selection: two pathways to life and two to death
Janeway, C. A. (1994) · Immunity · doi:10.1016/1074-7613(94)90003-5 · Cited by 84
Heimfeld, S., Hudak, S. A., Weissman, I. L., & Rennick, D. M. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.21.9902 · Cited by 79
Self-citationDifferential effects of chronic monocyte depletion on macrophage populations.
Volkman, A., Chang, N. C., Strausbauch, P. H., & Morahan, P. S. (1983) · PubMed · Cited by 77
Proliferative capacity of erythropoietic stem cell lines and aging: An overview
Harrison, D. E. (1979) · Mechanisms of Ageing and Development · doi:10.1016/0047-6374(79)90082-4 · Cited by 54
Proliferative Capacity of Murine Hematopoietic Stem Cells in Vitro
Reincke, U., Hannon, E. C., Rosenblatt, M., & Hellmän, S. (1982) · Science · doi:10.1126/science.7071580 · Cited by 40
Macrophage Subpopulations in the Mouse Spleen Renewed by Local Proliferation
Wijffels, J. F. A. M., Rover, Z. D., Beelen, R. H. J., Kraal, G., & van Rooijen, N. (1994) · Immunobiology · doi:10.1016/s0171-2985(11)80267-6 · Cited by 34
Up-regulation of interleukin 4 receptor expression on immature (Lyt-2-/L3T4-) thymocytes.
Lowenthal, J. W., Ransom, J. T., Howard, M., & Zlotnik, A. (1988) · The Journal of Immunology · doi:10.4049/jimmunol.140.2.474 · Cited by 29
Morrison, S. J., Lagasse, E., & Weissman, I. L. (1994) · Blood · doi:10.1182/blood.v83.12.3480.3480 · Cited by 29
Self-citationBlack, S. J., Tokuhisa, T., Herzenberg, L. A., & Herzenberg, L. A. (1980) · European Journal of Immunology · doi:10.1002/eji.1830101109 · Cited by 24
Ohgami, M., Doerschuk, C. M., Gie, R. P., English, D. R., & Hogg, J. C. (1991) · Journal of Applied Physiology · doi:10.1152/jappl.1991.70.1.152 · Cited by 19
Heterogeneity of hematopoietic stem cells: implications for clinical applications.
Morrison, S. J., & Weissman, I. L. (1995) · PubMed · Cited by 17
Self-citationHilbert, D. M., Anderson, A. O., Holmes, K. L., & Rudikoff, S. (1994) · Transplantation · doi:10.1097/00007890-199408270-00013 · Cited by 13
Statistics for biologists, third edition
Duffey, E. (1990) · Biological Conservation · doi:10.1016/0006-3207(90)90101-t · Cited by 9
Research works printed but not linked: 1
- Doherty, 1988, Monocyte retention and migration in pulmonary inflammation, Lab. Invest, 59, 200
Cited by
Sorted by citations
Effector and memory T-cell differentiation: implications for vaccine development
Kaech, S. M., Wherry, E. J., & Ahmed, R. (2002) · Nature Reviews Immunology · doi:10.1038/nri778 · Cited by 1,865
Weissman, I. L. (2000) · Cell · doi:10.1016/s0092-8674(00)81692-x · Cited by 1,827
Self-citationKillela, P. J., Reitman, Z. J., Jiao, Y., Bettegowda, C., Agrawal, N., Diaz, L. A., Friedman, A. H., Friedman, H., Gallia, G. L., Giovanella, B. C., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1303607110 · Cited by 1,368
Cancer Stem Cells: Models and Concepts
Dalerba, P. D., Cho, R. W., & Clarke, M. F. (2006) · Annual Review of Medicine · doi:10.1146/annurev.med.58.062105.204854 · Cited by 1,293
Outcome of Cord-Blood Transplantation from Related and Unrelated Donors
Gluckman, É., Rocha, V., Boyer-Chammard, A., Locatelli, F., Arcese, W., Pasqüini, R., Ortega, J., Souillet, G., Ferreira, E., Laporte, J. P., et al. (1997) · New England Journal of Medicine · doi:10.1056/nejm199708073370602 · Cited by 1,247
Metadata
- Authors
- Morrison, S. J., Prowse, K. R., Ho, P., & Weissman, I. L.
- Affiliations
- Stanford Medicine (US)
- Geron (United States) (US)
- Corresponding author
- Morrison, Sean J
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 1996-09
- Volume
- 5
- Issue
- 3
- Pages
- 207-216
- ISSN
- 1074-7613 (ISSN-L)
- OpenAlex
- W1973577066
- Cited by
- 394
- References
- 73
- Citations by year
- 2026: 4 · 2025: 10 · 2024: 6 · 2023: 5 · 2022: 7 · 2021: 8 · 2020: 8 · 2019: 6 · 2018: 9 · 2017: 7 · 2016: 11 · 2015: 22 · 2014: 15 · 2013: 14 · 2012: 14
- FWCI
- 9.91
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Immunity (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r35ca042551-13)
- National Cancer Institute (CA 42551)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Telomeres, Telomerase, and Senescence
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- telomerase activity, hematopoietic stem cells, self-renewal, telomere length, hematopoietic differentiation, myeloid cells, lymphoid cells, bone marrow, somatic cells
- MeSH terms
- Animals, Cell Differentiation, Hematopoietic Stem Cells, Humans, Mice, Inbred C57BL, Telomerase, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
