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Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells
Abstract
A major unanswered question is what distinguishes the majority of activated CD8 T cells that die after an acute viral infection from the small fraction (5-10%) that survive to become long-lived memory cells. In this study we show that increased expression of the interleukin 7 receptor alpha-chain (IL-7Ralpha) identifies the effector CD8 T cells that will differentiate into memory cells. IL-7R(hi) effector cells contained increased amounts of antiapoptotic molecules, and adoptive transfer of IL-7R(hi) and IL-7R(lo) effector cells showed that IL-7R(hi) cells preferentially gave rise to memory cells that could persist and confer protective immunity. Thus, selective expression of IL-7R identifies memory cell precursors, and this marker may be useful in predicting the number of memory T cells generated after infection or immunization.
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“Ag-specific CD8 T cells derived from the effector phase of a response can express various combinations of CD127 and KLRG1, which define either more short-lived effector cells (SLECs; CD127−KLRG1+), which are lost during the contraction phase of the immune response, or memory precursor effector cells (MPECs; CD127+KLRG1−), which are more likely to persist and contribute to memory populations [224,”
From Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition) (2021) · cites this paper as [224]
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BackgroundRoychoudhuri, R., Lefebvre, F., Honda, M., Pan, L., Ji, Y., Klebanoff, C. A., Nichols, C. N., Fourati, S., Hegazy, A. N., Goulet, J.-P., et al. (2014) · Vaccine · doi:10.1016/j.vaccine.2014.10.007 · Cited by 33
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BackgroundResultInfluentialIL‐7 is superior to IL‐2 for ex vivo expansion of tumour‐specific CD4+ T cells
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Khanna, K. M., Blair, D. A., Vella, A. T., McSorley, S. J., Datta, S. K., & Lefrançois, L. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0901047 · Cited by 32
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“While we did not observe an increase in Ag-specific CD62L cells in T cell populations stimulated under conditions of reduced Ag exposure in our model, we did observe an increase in CD127 and decrease in KLRG-1 expression at day 9 postinfection, both markers that have been shown to be expressed by long-lived memory pre…”
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Mitochondria as Playmakers of CAR T-cell Fate and Longevity
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“Costaining with CD62L and CD127 revealed that the frequencies of p60217–225-specific effector and effector memory CD8 T cells in blood and in fibrosarcoma tissue were related to the kinetics of tumor regression.”
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BackgroundResultA novel memory-like Tfh cell subset is precursor to effector Tfh cells in recall immune responses
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“cytokine receptor chain (11), indicating that the essential role for”
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BackgroundInfluentialSeo, Y., Jothikumar, P., Suthar, M. S., Zhu, C., & Grakoui, A. (2016) · Immunity · doi:10.1016/j.immuni.2016.10.024 · Cited by 31
“Short-lived effector cells are KLRG1highCD127low while memory precursor cells are KLRG1lowCD127high (Joshi et al., 2007; Kaech et al., 2003).”
InfluentialZuo, J., Stohlman, S. A., Hoskin, J. B., Hinton, D. R., Atkinson, R., & Bergmann, C. C. (2006) · Virology · doi:10.1016/j.virol.2006.01.027 · Cited by 31
“JHMV-specific CD8+ T cell responses in the CNS CNS infiltrating CD8+ T cells in both IL-15−/− and wt mice were CD44hi, CD62Llo/−, expressed similar levels of CD43, and were CD127− (data not shown), a pattern associated with effector function (Kaech et al., 2003; Onami et al., 2002).”
BackgroundRapid Memory CD8+T-Lymphocyte Induction through Priming with RecombinantMycobacterium smegmatis
Hovav, A., Cayabyab, M. J., Panas, M. W., Santra, S., Greenland, J. R., Geiben-Lynn, R., Haynes, B. F., Jacobs, W. R., & Letvin, N. L. (2006) · Journal of Virology · doi:10.1128/jvi.01269-06 · Cited by 31
“74 Biosciences), anti-CD127–PE–Cy7 (A7R34; eBioscience), anti-CD27–APC (LG.7F9; eBioscience), and anti-CD4–APC–Cy7 (GK1.”
BackgroundInfluentialPatke, D. S., & Färber, D. L. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.9.5433 · Cited by 31
“As an alternate approach to assess in vivo memory CD4 T cell activation and potential for survival, we measured expression of the IL-7R that has been correlated with memory T cell survival (7).”
BackgroundFormation of Tissue-Resident CD8+ T-Cell MemoryPreprint
Dijkgraaf, F. E., Kok, L., & Schumacher, T. N. (2021) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a038117 · Cited by 33
“Conversely, MPs express very low levels of KLRG1 but do express IL-7Rα and preferentially give rise to long-lived memory T cells (i.e., Tem and Tcm cells) (Kaech et al. 2003).”
BackgroundChen, Z., Zhu, Z., Hu, T., Yao, C., & Wu, T. (2025) · Cellular and Molecular Immunology · doi:10.1038/s41423-025-01378-4 · Cited by 37
The rationale for the IL‐2‐independent generation of the self‐renewing central memory CD8+ T cells
Fearon, D. T., Carr, J. M., Telaranta, A. I., Carrasco, M. J., & Thaventhiran, J. E. D. (2006) · Immunological Reviews · doi:10.1111/j.0105-2896.2006.00390.x · Cited by 30
“Even more signaling leads to acquisition of effector functions, but not loss of essential long-term survival characteristics, such as expression of CD127 [interleukin-7 receptor-a (IL-7Ra)].”
BackgroundInfluentialIFNγ in combination with IL-7 enhances immunotherapy in two rat glioma models
Fritzell, S., Eberstål, S., Sandén, E., Visse, E., Darabi, A., & Siesjö, P. (2013) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2013.02.017 · Cited by 30
“Although most activated effector T cells down-regulate IL-7Rα, CD8 effector cells that maintain IL-7Rα preferentially becomememory cells (Kaech et al., 2003).”
BackgroundDifferential Survival of Cytotoxic T Cells and Memory Cell Precursors
Zhang, M., Byrne, S., Liu, N., Wang, Y., Oxenius, A., & Ashton‐Rickardt, P. G. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.6.3483 · Cited by 30
“The expression of IL-7R (CD127) identifies a small percentage of CTLs, which have an increased likelihood of differentiating into memory CD8 T cells (22, 23).”
BackgroundHomeostasis of the Memory T Cell Pool
Marsden, V. S., Kappler, J. W., & Marrack, P. (2005) · International Archives of Allergy and Immunology · doi:10.1159/000090000 · Cited by 30
“How are these effector cells selected to survive the contraction phase and differentiate to memory cells? Responsiveness to IL-7 appears to have an important role in determining whether an effector cell will be deleted or go on to join the memory pool, at least for CD8 T cells. At the peak of the CD8 clonal expansion,…”
BackgroundThe CD8 memory T cell subsystem: Integration of homeostatic signaling during migration
Klonowski, K. D., & Lefrançois, L. (2005) · Seminars in Immunology · doi:10.1016/j.smim.2005.02.004 · Cited by 30
Influenza-Specific Lung-Resident Memory CD8+T CellsPreprint
van de Wall, S., Badovinac, V. P., & Harty, J. T. (2020) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a037978 · Cited by 31
Theoretical analysis of the evolution of immune memory
Graw, F., Magnus, C., & Regoes, R. R. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-380 · Cited by 28
“Many studies have investigated the molecular and mechanistic aspects of how immunological memory is generated and maintained [6-11].”
BackgroundSingle cell behavior in T cell differentiation
Rohr, J., Gerlach, C., Kok, L., & Schumacher, T. N. (2014) · Trends in Immunology · doi:10.1016/j.it.2014.02.006 · Cited by 28
Prabhu, N., Ho, A. W. S., Wong, K. H. S., Hutchinson, P. E., Chua, Y. L., Kandasamy, M., Lee, D. C. P., Sivasankar, B., & Kemeny, D. M. (2013) · Journal of Virology · doi:10.1128/jvi.01776-13 · Cited by 29
“IL-7 is a homeostatic cytokine which delivers survival signals to CD8 T cells by inhibiting apoptosis; IL-7 increases the levels of anti-apoptotic molecules such as Bcl-2 (25).”
BackgroundInfluentialWortzman, M. E., Lin, G. H. Y., & Watts, T. H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068911 · Cited by 28
“A significantly greater proportion of KLRG1lo CD127hi cells had the capacity to produce TNF, compared to KLRG1hi CD127lo cells, with KLRG1lo CD127lo cells producing intermediate levels upon restimulation (Figure 4B, C).”
BackgroundInfluentialIntrinsic TGF-β signaling promotes age-dependent CD8+ T cell polyfunctionality attrition
Bhadra, R., Moretto, M. M., Castillo, J. C., Petrovas, C., Ferrando‐Martínez, S., Shokal, U., Leal, M., Koup, R. A., Eleftherianos, I., & Khan, I. A. (2014) · Journal of Clinical Investigation · doi:10.1172/jci70522 · Cited by 29
“High expression of CD127 in concert with low KLRG1 expression is a hallmark of effector CD8 + T cells destined to become memory cells (16).”
The transcription factors GFI1 and GFI1B as modulators of the innate and acquired immune response
Fraszczak, J., & Möröy, T. (2021) · Advances in immunology · doi:10.1016/bs.ai.2021.03.003 · Cited by 28
Beider, K., Itzhaki, O., Schachter, J., Grushchenko-Polaq, A. H., Voevoda-Dimenshtein, V., Rosenberg, E., Ostrovsky, O., Devillers, O., Frommer, R. S., Zeltzer, L., et al. (2022) · Cells · doi:10.3390/cells11071140 · Cited by 30
Vidal, L. P., Taggenbrock, R. L. R. E., Beumer‐Chuwonpad, A., Aglmous, H., Kragten, N. A. M., Behr, F. M., Bovens, A. A., van Lier, R. A. W., Stark, R., & van Gisbergen, K. P. J. M. (2022) · European Journal of Immunology · doi:10.1002/eji.202149665 · Cited by 28
Imatinib Mesylate Inhibits Antigen-Specific Memory CD8 T Cell Responses In Vivo
Sinai, P., Berg, R. E., Haynie, J. M., Egorin, M. J., Ilaria, R. L., & Forman, J. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.4.2028 · Cited by 29
“More recent data indicate that IL-7R expression is required for effective memory cell generation and that effector CD8 T cells that retain high levels of this receptor give rise to long-lived memory cells (49, 50).”
BackgroundShephard, E., Burgers, W. A., Harmelen, J. H. V., Monroe, J. E., Greenhalgh, T., Williamson, C. E., & Williamson, A. (2008) · AIDS Research and Human Retroviruses · doi:10.1089/aid.2007.0206 · Cited by 29
“…The CD8 memory response that develops after immunization or infection is shaped by the level of antigen and the duration of antigen exposure, 36,50–52 and the composition of the memory subsets detected in this study are probably an outcome of the rapid clearance of the DNA and MVA vaccines after…”
Raposo, B., Rodrigues‐Santos, P., Carvalheiro, H., Agua‐Doce, A., Carvalho, L., da Silva, J. A. P., Graça, L., & Souto‐Carneiro, M. (2010) · Arthritis & Rheumatism · doi:10.1002/art.27729 · Cited by 29
Utilizing IL-12, IL-15 and IL-7 as Mucosal Vaccine Adjuvants
Stevceva, L., Moniuszko, M., & Ferrari, M. G. (2006) · Letters in Drug Design & Discovery · doi:10.2174/157018006778194655 · Cited by 29
Remmerswaal, E. B. M., Klarenbeek, P. L., Alves, N. L., Doorenspleet, M. E., van Schaik, B. D. C., Esveldt, R. E., Idu, M. M., van Leeuwen, E. M. M., van der Bom‐Baylon, N. D., van Kampen, A. H. C., et al. (2014) · Journal of Virology · doi:10.1128/jvi.02003-14 · Cited by 29
“Murine IL7R virus-specific CD8 T cells have been shown to be antigenindependent, long-lived memory cells (17).”
BackgroundWhitmire, J. K., Benning, N., Eam, B., & Whitton, J. L. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.10.6777 · Cited by 30
Ye, Z., Tang, C., Xu, S., Zhang, B., Zhang, X., Moyana, T. N., Yang, J., & Xiang, J. (2007) · PubMed · Cited by 29
The Distribution of Human Stem Cell–like Memory T Cell in Lung Cancer
Hong, H. Y., Gu, Y., Sheng, S. Y., Lu, C. G., Zou, J. Y., & Wu, C. Y. (2016) · Journal of Immunotherapy · doi:10.1097/cji.0000000000000128 · Cited by 29
Critical Requirement of GABPα for Normal T Cell Development
Yu, S., Zhao, D., Jothi, R., & Xue, H. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.088740 · Cited by 30
IL-7 in allogeneic transplant: Clinical promise and potential pitfalls
Snyder, K. M., Mackall, C. L., & Fry, T. J. (2006) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.1080/10428190600555876 · Cited by 29
“During an antigen-specific immune response such as the alloreaction, effector cells downregulate IL-7Ra, but ‘early’ antigen experienced memory T-cells re-express the receptor [41,42] and expand in response to IL-7 therapy.”
BackgroundZhong, W., & Reinherz, E. L. (2005) · European Journal of Immunology · doi:10.1002/eji.200535162 · Cited by 29
The Impact of a Boosting Immunogen on the Differentiation of Secondary Memory CD8 + T Cells
Hovav, A., Panas, M. W., Osuna, C. E., Cayabyab, M. J., Autissier, P., & Letvin, N. L. (2007) · Journal of Virology · doi:10.1128/jvi.01519-07 · Cited by 30
“Expression of the interleukin-7 (IL-7) receptor -chain molecule CD127 has also been used to identify long-lived memory cells (12).”
BackgroundCutting Edge: Memory CD8 T Cell Maturation Occurs Independently of CD8αα
Chandele, A., & Kaech, S. M. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.9.5619 · Cited by 29
“from those that will die following infection (2, 4).”
BackgroundSelf-citation(2020) · doi:10.1101/2020.06.08.138826 · Cited by 31
“To better define the features of the SARS-CoV-2-specific CD8+ Temra cells, and to compare them to their CMV-specific counterparts, we gated on these cells and assessed for expression levels of CD27 and CD28.”
BackgroundMethodInfluentialXiao, Z.-G., Curtsinger, J., Prlic, M., Jameson, S., & Mescher, M. (2007) · International Immunology · doi:10.1093/intimm/dxm039 · Cited by 24
Microbiota control immune regulation in humanized mice
Gülden, E., Vudattu, N. K., Deng, S., Preston‐Hurlburt, P., Mamula, M. J., Reed, J. C., Mohandas, S., Herold, B. C., TORRES, R. A., Vieira, S. M., et al. (2017) · JCI Insight · doi:10.1172/jci.insight.91709 · Cited by 29
“The mean fluorescence index (MFI) of CD127, which is reduced with T cell activation (21), was reduced in cells from the mesenteric lymph nodes in mice that were treated with antibiotics even without teplizumab treatment (Figure 5A, P = 0.016) and unlike control mice, did not decrease further with…”
Influential
Metadata
- Authors
- Kaech, S. M., Tan, J. T., Wherry, E. J., Konieczny, B. T., Surh, C. D., & Ahmed, R.
- Affiliations
- Emory University (US)
- Scripps Research Institute (US)
- Corresponding author
- Ahmed, Rafi
- Venue
- Nature Immunology
- Published
- 2003-11-16
- Volume
- 4
- Issue
- 12
- Pages
- 1191-1198
- ISSN
- 1529-2908 (ISSN-L)
- 1529-2916
- OpenAlex
- W1974842026
- Cited by
- 1,830
- References
- 48
- Citations by year
- 2026: 41 · 2025: 57 · 2024: 42 · 2023: 63 · 2022: 67 · 2021: 69 · 2020: 67 · 2019: 70 · 2018: 56 · 2017: 59 · 2016: 77 · 2015: 73 · 2014: 73 · 2013: 96 · 2012: 91
- FWCI
- 30.27
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Immunology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Life Sciences › Immunology and Microbiology › Immunology › Immune responses and vaccinations
- Keywords
- CD127, CD8+ T cells, effector T cells, memory T cells, apoptosis, adoptive transfer, viral infection, protective immunity, memory T cell generation
- MeSH terms
- Animals, Antigens, Surface, Cell Differentiation, Immunologic Memory, Lymphocyte Activation, Lymphocytic Choriomeningitis, Lymphocytic choriomeningitis virus, Mice, Transgenic, Signal Transduction, Gene Expression, T-Lymphocyte Subsets, CD8-Positive T-Lymphocytes, Cell Lineage, Adoptive Transfer, Receptors, Interleukin-7, Oligonucleotide Array Sequence Analysis, Mice
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