Differential usage of cellular niches by cytomegalovirus versus EBV- and influenza virus-specific CD8+ T cells
Open accessAbstract
Immunological memory provides long-term protection against reinfection or reactivation of pathogens. Murine memory T cell populations may be compressed following infections with new pathogens. Humans have to retain memory T cells directed against a variety of microbes for many decades. Under these circumstances, the effect of pathogens that mount robust T cell reactivity on the pre-existing memory directed against unrelated microbes is unknown. In this study, we studied peripheral blood memory CD8+ T cells directed against different viruses following primary CMV infection in renal transplant recipients. The entrance of CMV-specific CD8+ T cells expanded the Ag-primed CD8+ T cell compartment rather than competing for space with pre-existing memory T cells specific for persistent or cleared viruses. Neither numbers nor phenotype of EBV- or influenza-specific CD8+ T cells was altered by primary CMV infection. CMV-specific CD8+ T cells accumulated over time, resulting in increased total CD8+ T cell numbers. Additionally, they acquired a highly differentiated cytolytic phenotype that was clearly distinct from EBV- or influenza-reactive T cells. Thus, the human immune system appears to be flexible and is able to expand when encountering CMV. In view of the phenotypic differences between virus-specific T cells, this expansion may take place in cellular niches different from those occupied by EBV- or influenza-specific T cells, thereby preserving immunity to these pathogens.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The text we found for this paper looks like another document, so the self-check wasn’t run.
Cites
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 · cited 1× · see citing works
“In contrast, it has been described that, after clearance of a virus, 90–95% of the effector cells die and only a very small population survives to become memory T cells (20).”
BackgroundInterleukin-7 mediates the homeostasis of naïve and memory CD8 T cells in vivo
Schluns, K. S., Kieper, W. C., Jameson, S. C., & Lefrançois, L. (2000) · Nature Immunology · doi:10.1038/80868 · Cited by 1,619 · see citing works
Memory CD8+ T cells vary in differentiation phenotype in different persistent virus infections
Appay, V., Dunbar, P. R., Callan, M. F. C., Klenerman, P., Gillespie, G. M. A., Papagno, L., Ogg, G. S., King, A., Lechner, F., Spina, C. A., et al. (2002) · Nature Medicine · doi:10.1038/nm0402-379 · Cited by 1,556 · see citing works
Sylwester, A. W., Mitchell, B. L., Edgar, J. B., Taormina, C., Pelte, C., Ruchti, F., Sleath, P. R., Grabstein, K. H., Hosken, N. A., Kern, F., et al. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20050882 · Cited by 1,339 · cited 1× · see citing works
“This implies that the total response to CMV is much larger, also considering the broad immune response to CMV that has recently been described (27).”
BackgroundPotent and Selective Stimulation of Memory-Phenotype CD8+ T Cells In Vivo by IL-15
Zhang, X. M., Sun, S., Hwang, I., Tough, D. F., & Sprent, J. (1998) · Immunity · doi:10.1016/s1074-7613(00)80564-6 · Cited by 1,248 · see citing works
Tan, J. T., Ernst, B., Kieper, W. C., LeRoy, E., Sprent, J., & Surh, C. D. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20020066 · Cited by 790 · see citing works
Persistence of Memory CD8 T Cells in MHC Class I-Deficient Mice
Murali‐Krishna, K., Lau, L. L., Sambhara, S. R., Lemonnier, F. A., Altman, J. D., & Ahmed, R. (1999) · Science · doi:10.1126/science.286.5443.1377 · Cited by 718 · see citing works
Interleukin 15 Is Required for Proliferative Renewal of Virus-specific Memory CD8 T Cells
Becker, T. C., Wherry, E. J., Boone, D. L., Murali‐Krishna, K., Antia, R., Ma, A. I., & Ahmed, R. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20020369 · Cited by 685 · see citing works
Cytotoxic T-cell memory without antigen
Lau, L. L., Jamieson, B. D., Somasundaram, T., & Ahmed, R. (1994) · Nature · doi:10.1038/369648a0 · Cited by 657 · see citing works
Virus-specific CD8+ T-cell memory determined by clonal burst size
Hou, S., Hyland, L., Ryan, K., Portner, A., & Doherty, P. C. (1994) · Nature · doi:10.1038/369652a0 · Cited by 514 · see citing works
Antigen-independent memory CD8 T cells do not develop during chronic viral infection
Wherry, E. J., Barber, D. L., Kaech, S. M., Blattman, J. N., & Ahmed, R. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407192101 · Cited by 495 · see citing works
Gamadia, L. E., Remmerswaal, E. B. M., Weel, J. F. L., Bemelman, F. J., van Lier, R. A. W., & ten Berge, I. J. M. (2003) · Blood · doi:10.1182/blood-2002-08-2502 · Cited by 423 · see citing works
Self-citationKhan, N., Hislop, A. D., Gudgeon, N. H., Cobbold, M., Khanna, R., Nayak, L., Rickinson, A. B., & Moss, P. A. H. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.12.7481 · Cited by 351 · see citing works
Human CD8+ T-cell differentiation in response to viruses
van Lier, R. A. W., ten Berge, I. J. M., & Gamadia, L. E. (2003) · Nature Reviews Immunology · doi:10.1038/nri1254 · Cited by 297 · see citing works
Self-citationAntigens and immunoevasins: opponents in cytomegalovirus immune surveillance
Reddehase, M. J. (2002) · Nature reviews. Immunology · doi:10.1038/nri932 · Cited by 291 · see citing works
Immunomodulation by cytomegaloviruses: manipulative strategies beyond evasion
Mocarski, E. S. (2002) · Trends in Microbiology · doi:10.1016/s0966-842x(02)02393-4 · Cited by 291 · see citing works
Selin, L. K., Lin, M. Y., Kraemer, K. A., Pardoll, D. M., Schneck, J. P., Varga, S. M., Santolucito, P. A., Pinto, A. K., & Welsh, R. M. (1999) · Immunity · doi:10.1016/s1074-7613(00)80147-8 · Cited by 275 · see citing works
Gamadia, L. E., Rentenaar, R. J., Baars, P. A., Remmerswaal, E. B. M., Surachno, S., Weel, J. F. L., Toebes, M., Schumacher, T. N., ten Berge, I. J. M., & van Lier, R. A. W. (2001) · Blood · doi:10.1182/blood.v98.3.754 · Cited by 215 · see citing works
Self-citationSelin, L. K., Vergilis, K., Welsh, R. M., & Nahill, S. R. (1996) · The Journal of Experimental Medicine · doi:10.1084/jem.183.6.2489 · Cited by 211 · see citing works
Wills, M. R., Okecha, G., Weekes, M. P., Gandhi, M. K., Sissons, P., & Carmichael, A. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.168.11.5455 · Cited by 208 · see citing works
de Bree, G. J., van Leeuwen, E. M. M., Out, T. A., Jansen, H. M., Jonkers, R. E., & van Lier, R. A. W. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20051365 · Cited by 177 · see citing works
Frequencies of Circulating Cytolytic, CD45RA+CD27−, CD8+ T Lymphocytes Depend on Infection with CMV
Kuijpers, T. W., Vossen, M. T. M., Gent, M.-R., Davin, J. C., Roos, M. T. L., Dillen, P. M. E. W., Weel, J. F. L., Baars, P. A., & van Lier, R. A. W. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.170.8.4342 · Cited by 169 · see citing works
van Leeuwen, E. M. M., de Bree, G. J., Remmerswaal, E. B. M., Yong, S. L., Tesselaar, K., ten Berge, I. J. M., & van Lier, R. A. W. (2005) · Blood · doi:10.1182/blood-2005-02-0449 · Cited by 165 · see citing works
Self-citationPrlic, M., Lefrançois, L., & Jameson, S. C. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20020767 · Cited by 158 · see citing works
Functional Heterogeneity of Cytokines and Cytolytic Effector Molecules in Human CD8+ T Lymphocytes
Sandberg, J. K., Fast, N. M., & Nixon, D. F. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.1.181 · Cited by 155 · see citing works
Gamadia, L. E., van Leeuwen, E. M. M., Remmerswaal, E. B. M., Yong, S.-L., Surachno, S., Wertheim-van Dillen, P. M. E., ten Berge, I. J. M., & van Lier, R. A. W. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.10.6107 · Cited by 122 · see citing works
Self-citationKim, S.-K., & Welsh, R. M. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.5.3139 · Cited by 63 · see citing works
Liu, H., Andreansky, S. S., Diaz, G. M., et al. (2003) · Journal of Virology · doi:10.1128/jvi.77.14.7756-7763.2003 · Cited by 29 · see citing works
Apoptosis and loss of virus-specific CD8+ T-cell memory
Welsh, R. M., Bahl, K., & Wang, X. Z. (2004) · Current Opinion in Immunology · doi:10.1016/j.coi.2004.03.020 · Cited by 27 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Successful and Maladaptive T Cell Aging
Goronzy, J. J., & Weyand, C. M. (2017) · Immunity · doi:10.1016/j.immuni.2017.03.010 · Cited by 362 · see citing works
Cytomegalovirus Infection Reduces Telomere Length of the Circulating T Cell Pool
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. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0903442 · Cited by 157 · see citing works
Is immunosenescence influenced by our lifetime “dose” of exercise?
Turner, J. E. (2016) · Biogerontology · doi:10.1007/s10522-016-9642-z · Cited by 112 · see citing works
- Authors
- van Leeuwen, E. M. M., Koning, J. J., Remmerswaal, E. B. M., van Baarle, D., van Lier, R. A. W., & ten Berge, I. J. M.
- Affiliations
- Department of Experimental Immunology, Sanquin Research and Landsteiner Laboratory, Academic Medical Center , Amsterdam ,
- Amsterdam UMC Location University of Amsterdam (NL)
- Department of Viro-Immunology, Sanquin Research and Landsteiner Laboratory, Academic Medical Center , Amsterdam ,
- Department of Internal Medicine, Division of Nephrology, Sanquin Research and Landsteiner Laboratory, Academic Medical Center , Amsterdam ,
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2006-10
- Volume
- 177
- Issue
- 8
- Pages
- 4998-5005
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- OpenAlex
- W2141693247
- Cited by
- 50
- References
- 29
- Citations by year
- 2024: 1 · 2021: 1 · 2020: 1 · 2019: 3 · 2018: 3 · 2017: 4 · 2016: 3 · 2015: 3 · 2014: 4 · 2013: 4 · 2012: 5
- FWCI
- 1.77
- Type
- journal article
- Language
- en
- Open access
- green
- pure.amsterdamumc.nl
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Health Sciences › Medicine › Epidemiology › Cytomegalovirus and herpesvirus research
- Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
- Keywords
- cytomegalovirus, CD8+ T cells, memory T cells, cellular niches, T cell competition, EBV-specific T cells, influenza-specific T cells, T cell differentiation, kidney transplant recipients, immunological memory, T cell expansion
- MeSH terms
- Adolescent, Adult, Aged, Cytomegalovirus Infections, Cytomegalovirus, Herpesvirus 4, Human, Humans, Immune System, Immunologic Memory, Middle Aged, Orthomyxoviridae, Viruses, Kidney Transplantation, CD8-Positive T-Lymphocytes, Lymphocyte Count
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
