Cytomegalovirus Infection Reduces Telomere Length of the Circulating T Cell Pool

van de Berg, Pablo J E J; Griffiths, Stephen J; Yong, Si-La; Macaulay, Richard; Bemelman, Frederike J; Jackson, Sarah; Henson, Sian M; ten Berge, Ineke J M; Akbar, Arne N; van Lier, René A W

doi:10.4049/jimmunol.0903442

Cited by 157Telomeres, Telomerase, and SenescenceCytomegalovirus and herpesvirus researchViral-associated cancers and disorders

Cytomegalovirus Infection Reduces Telomere Length of the Circulating T Cell Pool

van de Berg, Pablo J E J, Griffiths, Stephen J, Yong, Si-La, Macaulay, Richard, Bemelman, Frederike J, Jackson, Sarah, Henson, Sian M, ten Berge, Ineke J M +2 more·2010·The Journal of Immunology

DOI 10.4049/jimmunol.0903442

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Abstract

Short telomeres of circulating leukocytes are a risk factor for age-related diseases, such as atherosclerosis, but the exact mechanisms generating variations in telomere length are unknown. We hypothesized that induction of differentiated T cells during chronic CMV infection would affect T cell telomere length. To test this, we measured the amount of differentiated T cells and telomere length of lymphocytes during primary CMV infection as well as CMV-seropositive and -seronegative healthy individuals. After primary CMV infection, we observed an increase in highly differentiated cells that coincided with a steep drop in telomere length. Moreover, we found in a cohort of 159 healthy individuals that telomere shortening was more rapid in CMV-seropositive individuals and correlated with the amount of differentiated T cells in both CD4+ T cells and CD8+ T cells. Finally, we found that telomere length measured in blood leukocytes is correlated with lymphocyte telomere length. Thus, CMV infection induces a strong decrease in T cell telomere length, which can be explained by changes in the composition of the circulating lymphocyte pool.

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In chronic viral infections, repetitive stimulation leads to extensive proliferation and telomere shortening in antigen-specific T cells, ultimately causing exhaustion.
“As observed in chronic viral infections, repetitive stimulation leads to extensive proliferation and the shortening of telomeres in antigen-specific T cells, ultimately leading to exhaustion [228].”
From Current and Future Trends of Colorectal Cancer Treatment: Exploring Advances in Immunotherapy (2024) · cites this paper as [228]

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Uremia-associated immunological aging is stably imprinted in the T-cell system and not reversed by kidney transplantation
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T Cell Immunosenescence after Early Life Adversity: Association with Cytomegalovirus Infection
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Senescence in the Development and Response to Cancer with Immunotherapy: A Double-Edged Sword
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Multifunctional cytomegalovirus (CMV)‐specific CD8+ T cells are not restricted by telomere‐related senescence in young or old adults
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In aged primary T cells, mitochondrial stress contributes to telomere attrition measured by a novel imaging flow cytometry assay
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New Insights into Lymphocyte Differentiation and Aging from Telomere Length and Telomerase Activity Measurements
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Chronic Kidney Disease and Premature Ageing of the Adaptive Immune Response
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Leukocyte Telomere Length in HIV-Infected and HIV-Exposed Uninfected Children: Shorter Telomeres with Uncontrolled HIV Viremia
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Telomere biology in hematopoiesis and stem cell transplantation
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Molecular characterization of HCMV‐specific immune responses: Parallels between CD8+ T cells, CD4+ T cells, and NK cells
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Persistent Herpesvirus Infections and Telomere Attrition Over 3 Years in the Whitehall II Cohort
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Cellular aging dynamics after acute malaria infection: A 12‐month longitudinal study
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Loneliness and Telomere Length: Immune and Parasympathetic Function in Associations With Accelerated Aging
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Markers of T Cell Exhaustion and Senescence and Their Relationship to Plasma TGF-β Levels in Treated HIV+ Immune Non-responders
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Tracking T-cell immune reconstitution after TCRαβ/CD19-depleted hematopoietic cells transplantation in children
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Senescence mirrors the extent of liver fibrosis in chronic hepatitis C virus infection
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Genetic, Environmental and Lifestyle Determinants of Accelerated Telomere Attrition as Contributors to Risk and Severity of Multiple Sclerosis
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A killer on the road: circulating CD4+CD28null T cells as cardiovascular risk factor in ESRD patients
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Resveratrol as an Adjunctive Therapy for Excessive Oxidative Stress in Aging COVID-19 Patients
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Senescence and Host–Pathogen Interactions
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Current and Future Trends of Colorectal Cancer Treatment: Exploring Advances in Immunotherapy
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Cytomegalovirus contributes partly to uraemia-associated premature immunological ageing of the T cell compartment
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Primary Cytomegalovirus Infection Significantly Impacts Circulating T Cells in Kidney Transplant Recipients
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Myocardial Ischemia and Reperfusion Leads to Transient CD8 Immune Deficiency and Accelerated Immunosenescence in CMV-Seropositive Patients
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Cytomegalovirus is associated with reduced telomerase activity in the Whitehall II cohort
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Use of Telomere Length as a Biomarker for Aging and Age-Related Disease
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T‐cell redeployment and intracellular cytokine expression following exercise: effects of exercise intensity and cytomegalovirus infection
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The Molecular Interplay between Human Oncoviruses and Telomerase in Cancer Development
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HIV Infection Is Associated with Shortened Telomere Length in Ugandans with Suspected Tuberculosis
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Association of Premature Immune Aging and Cytomegalovirus After Solid Organ Transplant
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Roles for Cytomegalovirus in Infection, Inflammation, and Autoimmunity
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End-Stage Renal Disease Causes Skewing in the TCR Vβ-Repertoire Primarily within CD8+ T Cell Subsets
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First autologous hematopoietic SCT for ankylosing spondylitis: a case report and clues to understanding the therapy
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Clinical Impact of Telomere Length Testing for Interstitial Lung Disease
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CXCR5+CD4+ follicular helper T cells accumulate in resting human lymph nodes and have superior B cell helper activity
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Leukocyte telomere length in paediatric critical illness: effect of early parenteral nutrition
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Telomere‐dependent replicative senescence of B and T cells from patients with type 1a common variable immunodeficiency
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Comprehensive Evaluation of the Immune Risk Phenotype in Successfully Treated HIV-Infected Individuals
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Biomarkers of Aging in HIV-Infected Children on Suppressive Antiretroviral Therapy
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Early Senescence and Leukocyte Telomere Shortening in SCHIZOPHRENIA: A Role for Cytomegalovirus Infection?
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Mean Corpuscular Volume and Mortality in Incident Hemodialysis Patients
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Viruses associated with ill health in wild chimpanzees
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Lymph node and circulating T cell characteristics are strongly correlated in end-stage renal disease patients, but highly differentiated T cells reside within the circulation
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A profile of immune response to herpesvirus is associated with radiographic joint damage in rheumatoid arthritis
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Elevated HbA1c levels and the accumulation of differentiated T cells in CMV+ individuals
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Cytomegalovirus-Induced Expression of CD244 after Liver Transplantation Is Associated with CD8+ T Cell Hyporesponsiveness to Alloantigen
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Latency for cytomegalovirus impacts T cell ageing significantly in elderly end-stage renal disease patients
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Biomarkers of cellular aging during a controlled human malaria infection
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Characteristics and mechanisms of T‐cell senescence: A potential target for cancer immunotherapy
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Effect of Cytomegalovirus Infection on Survival of Older Kidney Transplant Patients (D+/R+): Impact of Valganciclovir Prophylaxis Versus Preemptive Therapy
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Lin, Z., Gao, H., Wang, B., & Wang, Y. (2021) · Mediators of Inflammation · doi:10.1155/2021/6675353 · Cited by 8 · see citing works
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Authors: van de Berg, P. J. E. J., Griffiths, S. J., Yong, S.-L., Macaulay, R., Bemelman, F. J., Jackson, S., Henson, S. M., ten Berge, I. J. M., Akbar, A. N., & van Lier, R. A. W.
Affiliations: Department of Experimental Immunology
University College London (GB)
Renal Transplant Unit, Division of Nephrology, Department of Internal Medicine, Academic Medical Center , Amsterdam,
Division of Infection and Immunity, Department of Immunology, University College London , London,
ORCID: Griffiths, Stephen J
Macaulay, Richard
Jackson, Sarah
Akbar, Arne N
Venue: The Journal of Immunology
Publisher: Oxford University Press (OUP)
Published: 2010-04-01
Volume: 184
Issue: 7
Pages: 3417-3423
ISSN: 0022-1767 (ISSN-L)
1550-6606
DOI: 10.4049/jimmunol.0903442
OpenAlex: W1518369947
Cited by: 157
References: 50
Citations by year: 2026: 4 · 2025: 6 · 2024: 7 · 2023: 3 · 2022: 5 · 2021: 12 · 2020: 9 · 2019: 8 · 2018: 9 · 2017: 14 · 2016: 7 · 2015: 13 · 2014: 14 · 2013: 13 · 2012: 12
FWCI: 9.97
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)
Data Archiving and Networked Services (DANS) (submittedVersion)
UCL Discovery (University College London) (submittedVersion)
Pure Amsterdam UMC (submittedVersion)
Funders: Biotechnology and Biological Sciences Research Council
Topics: Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
Health Sciences › Medicine › Epidemiology › Cytomegalovirus and herpesvirus research
Health Sciences › Medicine › Oncology › Viral-associated cancers and disorders
Keywords: cytomegalovirus infection, telomere length, telomere shortening, T cell differentiation, CD4+ T cells, CD8+ T cells, circulating lymphocytes, primary CMV infection, CMV serostatus, age-related diseases, atherosclerosis
MeSH terms: Adult, Aged, Aged, 80 and over, Antiviral Agents, Cell Differentiation, Cell Separation, Cytomegalovirus Infections, DNA, Viral, Flow Cytometry, Fluorescent Antibody Technique, Humans, Middle Aged, T-Lymphocytes, Viremia, Ganciclovir, Kidney Transplantation, Polymerase Chain Reaction, T-Lymphocyte Subsets, Telomere, In Situ Hybridization, Fluorescence, Young Adult

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Cytomegalovirus Infection Reduces Telomere Length of the Circulating T Cell Pool

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