Buildup from birth onward of short telomeres in human hematopoietic cells
Telomere length (TL) limits somatic cell replication. However, the shortest among the telomeres in each nucleus, not mean TL, is thought to induce replicative senescence. Researchers have relied on Southern blotting (SB), and techniques calibrated by SB, for precise measurements of TL in epidemiolog...
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| Published in | Aging cell Vol. 22; no. 6; pp. e13844 - n/a |
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| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
John Wiley & Sons, Inc
01.06.2023
Wiley Open Access John Wiley and Sons Inc |
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| Online Access | Get full text |
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| Abstract | Telomere length (TL) limits somatic cell replication. However, the shortest among the telomeres in each nucleus, not mean TL, is thought to induce replicative senescence. Researchers have relied on Southern blotting (SB), and techniques calibrated by SB, for precise measurements of TL in epidemiological studies. However, SB provides little information on the shortest telomeres among the 92 telomeres in the nucleus of human somatic cells. Therefore, little is known about the accumulation of short telomeres with age, or whether it limits the human lifespan. To fill this knowledge void, we used the Telomere‐Shortest‐Length‐Assay (TeSLA), a method that tallies and measures single telomeres of all chromosomes. We charted the age‐dependent buildup of short telomeres (<3 kb) in human hematopoietic cells from 334 individuals (birth‐89 years) from the general population, and 18 patients with dyskeratosis congenita‐telomere biology disorders (DC/TBDs), whose hematopoietic cells have presumably reached or are close to their replicative limit. For comparison, we also measured TL with SB. We found that in hematopoietic cells, the buildup of short telomeres occurs in parallel with the shortening with age of mean TL. However, the proportion of short telomeres was lower in octogenarians from the general population than in patients with DC/TBDs. At any age, mean TL was longer and the proportion of short telomeres lower in females than in males. We conclude that though converging to the TL‐mediated replicative limit, hematopoietic cell telomeres are unlikely to reach this limit during the lifespan of most contemporary humans.
Population studies have principally focused on the role of mean telomere length in human health and longevity. The availability of new telomere length measurement techniques enables examining the relations between the shortest telomeres and human diseases. |
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| AbstractList | Telomere length (TL) limits somatic cell replication. However, the shortest among the telomeres in each nucleus, not mean TL, is thought to induce replicative senescence. Researchers have relied on Southern blotting (SB), and techniques calibrated by SB, for precise measurements of TL in epidemiological studies. However, SB provides little information on the shortest telomeres among the 92 telomeres in the nucleus of human somatic cells. Therefore, little is known about the accumulation of short telomeres with age, or whether it limits the human lifespan. To fill this knowledge void, we used the Telomere‐Shortest‐Length‐Assay (TeSLA), a method that tallies and measures single telomeres of all chromosomes. We charted the age‐dependent buildup of short telomeres (<3 kb) in human hematopoietic cells from 334 individuals (birth‐89 years) from the general population, and 18 patients with dyskeratosis congenita‐telomere biology disorders (DC/TBDs), whose hematopoietic cells have presumably reached or are close to their replicative limit. For comparison, we also measured TL with SB. We found that in hematopoietic cells, the buildup of short telomeres occurs in parallel with the shortening with age of mean TL. However, the proportion of short telomeres was lower in octogenarians from the general population than in patients with DC/TBDs. At any age, mean TL was longer and the proportion of short telomeres lower in females than in males. We conclude that though converging to the TL‐mediated replicative limit, hematopoietic cell telomeres are unlikely to reach this limit during the lifespan of most contemporary humans. Telomere length (TL) limits somatic cell replication. However, the shortest among the telomeres in each nucleus, not mean TL, is thought to induce replicative senescence. Researchers have relied on Southern blotting (SB), and techniques calibrated by SB, for precise measurements of TL in epidemiological studies. However, SB provides little information on the shortest telomeres among the 92 telomeres in the nucleus of human somatic cells. Therefore, little is known about the accumulation of short telomeres with age, or whether it limits the human lifespan. To fill this knowledge void, we used the Telomere-Shortest-Length-Assay (TeSLA), a method that tallies and measures single telomeres of all chromosomes. We charted the age-dependent buildup of short telomeres (<3 kb) in human hematopoietic cells from 334 individuals (birth-89 years) from the general population, and 18 patients with dyskeratosis congenita-telomere biology disorders (DC/TBDs), whose hematopoietic cells have presumably reached or are close to their replicative limit. For comparison, we also measured TL with SB. We found that in hematopoietic cells, the buildup of short telomeres occurs in parallel with the shortening with age of mean TL. However, the proportion of short telomeres was lower in octogenarians from the general population than in patients with DC/TBDs. At any age, mean TL was longer and the proportion of short telomeres lower in females than in males. We conclude that though converging to the TL-mediated replicative limit, hematopoietic cell telomeres are unlikely to reach this limit during the lifespan of most contemporary humans.Telomere length (TL) limits somatic cell replication. However, the shortest among the telomeres in each nucleus, not mean TL, is thought to induce replicative senescence. Researchers have relied on Southern blotting (SB), and techniques calibrated by SB, for precise measurements of TL in epidemiological studies. However, SB provides little information on the shortest telomeres among the 92 telomeres in the nucleus of human somatic cells. Therefore, little is known about the accumulation of short telomeres with age, or whether it limits the human lifespan. To fill this knowledge void, we used the Telomere-Shortest-Length-Assay (TeSLA), a method that tallies and measures single telomeres of all chromosomes. We charted the age-dependent buildup of short telomeres (<3 kb) in human hematopoietic cells from 334 individuals (birth-89 years) from the general population, and 18 patients with dyskeratosis congenita-telomere biology disorders (DC/TBDs), whose hematopoietic cells have presumably reached or are close to their replicative limit. For comparison, we also measured TL with SB. We found that in hematopoietic cells, the buildup of short telomeres occurs in parallel with the shortening with age of mean TL. However, the proportion of short telomeres was lower in octogenarians from the general population than in patients with DC/TBDs. At any age, mean TL was longer and the proportion of short telomeres lower in females than in males. We conclude that though converging to the TL-mediated replicative limit, hematopoietic cell telomeres are unlikely to reach this limit during the lifespan of most contemporary humans. Telomere length (TL) limits somatic cell replication. However, the shortest among the telomeres in each nucleus, not mean TL, is thought to induce replicative senescence. Researchers have relied on Southern blotting (SB), and techniques calibrated by SB, for precise measurements of TL in epidemiological studies. However, SB provides little information on the shortest telomeres among the 92 telomeres in the nucleus of human somatic cells. Therefore, little is known about the accumulation of short telomeres with age, or whether it limits the human lifespan. To fill this knowledge void, we used the Telomere‐Shortest‐Length‐Assay (TeSLA), a method that tallies and measures single telomeres of all chromosomes. We charted the age‐dependent buildup of short telomeres (<3 kb) in human hematopoietic cells from 334 individuals (birth‐89 years) from the general population, and 18 patients with dyskeratosis congenita‐telomere biology disorders (DC/TBDs), whose hematopoietic cells have presumably reached or are close to their replicative limit. For comparison, we also measured TL with SB. We found that in hematopoietic cells, the buildup of short telomeres occurs in parallel with the shortening with age of mean TL. However, the proportion of short telomeres was lower in octogenarians from the general population than in patients with DC/TBDs. At any age, mean TL was longer and the proportion of short telomeres lower in females than in males. We conclude that though converging to the TL‐mediated replicative limit, hematopoietic cell telomeres are unlikely to reach this limit during the lifespan of most contemporary humans. Population studies have principally focused on the role of mean telomere length in human health and longevity. The availability of new telomere length measurement techniques enables examining the relations between the shortest telomeres and human diseases. Telomere length (TL) limits somatic cell replication. However, the shortest among the telomeres in each nucleus, not mean TL, is thought to induce replicative senescence.Researchers have relied on Southern blotting (SB), and techniques calibrated by SB, for precise measurements of TL in epidemiological studies. However, SB provides little information on the shortest telomeres among the 92 telomeres in the nucleus of human somatic cells. Therefore, little is known about the accumulation of short telomeres with age, or whether it limits the human lifespan. To fill this knowledge void, we used the Telomere-Shortest-Length-Assay (TeSLA), a method that tallies and measures single telomeres of all chromosomes. We charted the age-dependent buildup of short telomeres (<3 kb) in human hematopoietic cells from 334 individuals (birth-89 years) from the general population, and 18 patients with dyskeratosis congenitatelomere biology disorders (DC/TBDs), whose hematopoietic cells have presumably reached or are close to their replicative limit. For comparison, we also measured TL with SB. We found that in hematopoietic cells, the buildup of short telomeres occurs in parallel with the shortening with age of mean TL. However, the proportion of short telomeres was lower in octogenarians from the general population than in |
| Author | Savage, Sharon A. Factor‐Litvak, Pam Lai, Tsung‐Po Benetos, Athanase Aviv, Abraham Gadalla, Shahinaz M. Verhulst, Simon Susser, Ezra Toupance, Simon |
| AuthorAffiliation | 1 Center of Human Development and Aging, New Jersey Medical School, Rutgers The State University of New Jersey Newark New Jersey USA 3 Division of Cancer Epidemiology and Genetics National Cancer Institute Bethesda Maryland USA 5 CHRU‐Nancy Pôle Maladies du vieillissement Gérontologie et Soins Palliatifs and Fédération Hospitalo‐Universitaire CARTAGE‐PROFILES Université de Lorraine Nancy France 7 Department of Psychiatry New York State Psychiatric Institute New York New York USA 2 Groningen Institute for Evolutionary Life Sciences University of Groningen Groningen The Netherlands 4 INSERM DCAC Université de Lorraine Nancy France 6 Department of Epidemiology Mailman School of Public Health New York New York USA |
| AuthorAffiliation_xml | – name: 1 Center of Human Development and Aging, New Jersey Medical School, Rutgers The State University of New Jersey Newark New Jersey USA – name: 4 INSERM DCAC Université de Lorraine Nancy France – name: 7 Department of Psychiatry New York State Psychiatric Institute New York New York USA – name: 3 Division of Cancer Epidemiology and Genetics National Cancer Institute Bethesda Maryland USA – name: 2 Groningen Institute for Evolutionary Life Sciences University of Groningen Groningen The Netherlands – name: 6 Department of Epidemiology Mailman School of Public Health New York New York USA – name: 5 CHRU‐Nancy Pôle Maladies du vieillissement Gérontologie et Soins Palliatifs and Fédération Hospitalo‐Universitaire CARTAGE‐PROFILES Université de Lorraine Nancy France |
| Author_xml | – sequence: 1 givenname: Tsung‐Po surname: Lai fullname: Lai, Tsung‐Po organization: The State University of New Jersey – sequence: 2 givenname: Simon surname: Verhulst fullname: Verhulst, Simon organization: University of Groningen – sequence: 3 givenname: Sharon A. surname: Savage fullname: Savage, Sharon A. organization: National Cancer Institute – sequence: 4 givenname: Shahinaz M. surname: Gadalla fullname: Gadalla, Shahinaz M. organization: National Cancer Institute – sequence: 5 givenname: Athanase surname: Benetos fullname: Benetos, Athanase organization: Gérontologie et Soins Palliatifs and Fédération Hospitalo‐Universitaire CARTAGE‐PROFILES Université de Lorraine – sequence: 6 givenname: Simon orcidid: 0000-0001-7441-567X surname: Toupance fullname: Toupance, Simon organization: INSERM DCAC Université de Lorraine – sequence: 7 givenname: Pam surname: Factor‐Litvak fullname: Factor‐Litvak, Pam organization: Mailman School of Public Health – sequence: 8 givenname: Ezra surname: Susser fullname: Susser, Ezra organization: New York State Psychiatric Institute – sequence: 9 givenname: Abraham orcidid: 0000-0002-7441-0227 surname: Aviv fullname: Aviv, Abraham email: avivab@njms.rutgers.edu organization: The State University of New Jersey |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/37118904$$D View this record in MEDLINE/PubMed https://hal.science/hal-05031580$$DView record in HAL |
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| Copyright | 2023 The Authors. published by Anatomical Society and John Wiley & Sons Ltd. 2023 The Authors. Aging Cell published by Anatomical Society and John Wiley & Sons Ltd. 2023. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. Attribution |
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| Keywords | terminal restriction fragments sex telomeres lifetime TeSLA subtelomeric region Southern blotting telomere biology disorders age fluorescent in situ hybridization single gene product SB telomere length TRFs LTL SBmTL measured by TeSLA TeSmTL single gene product TRFs dyskeratosis congenita-related telomere biology disorders FISH TeSmTL bp Southern blotting SBmTL SB kilobase S SNP T proportion of telomeres less than 3 kb DC/TBD kilobase LTL kb amplified telomere product mean TL using TeSLA qPCR hematopoietic cell kb single-nucleotide polymorphism telomere length single-nucleotide polymorphism T measured by TeSLA amplified telomere product TeS3kb TeS3kb mean TL using SB quantitative polymerase chain reaction S mean TL using TeSLA TL quantitative polymerase chain reaction base pairs DC/TBD mean TL using SB SNP base pairs hematopoietic cell dyskeratosis congenita-related telomere biology disorders fluorescent in situ hybridization HC leukocyte telomere length qPCR TL FISH HC leukocyte telomere length |
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| License | Attribution 2023 The Authors. Aging Cell published by Anatomical Society and John Wiley & Sons Ltd. Attribution: http://creativecommons.org/licenses/by This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
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| SubjectTerms | Age Aged, 80 and over Aging Biology Cell Division Chromosomes Dyskeratosis Enzymes Epidemiology Female Hematopoietic stem cells Humans Leukocytes Life Sciences Life span lifetime Longevity Male Males Measurement techniques Polymerase chain reaction Senescence sex Sex differences Somatic cells Southern blotting subtelomeric region Telomerase Telomere - genetics telomere biology disorders Telomere Shortening Telomeres terminal restriction fragments TeSLA Yeast |
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| Title | Buildup from birth onward of short telomeres in human hematopoietic cells |
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