Cited by 1,830T-cell and B-cell ImmunologyImmunotherapy and Immune ResponsesImmune responses and vaccinations

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Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells

Kaech, Susan M, Tan, Joyce T, Wherry, E John, Konieczny, Bogumila T, Surh, Charles D, Ahmed, Rafi·2003·Nature Immunology

DOI 10.1038/ni1009

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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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BackgroundInfluential
An alternative NFAT-activation pathway mediated by IL-7 is critical for early thymocyte development
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“maintained in the antigen-naı̈ve host, whereas the IL-7Ra cells continuously declined in numbers after transfer (8, 34, 124).”
Background
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Background
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Background
The transcriptional control of the perforin locus
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“The relation appears to be (mpDHS; hpDHS): (2; 3), (3; 6,12), (4–7; 13), (9; 14), (10; 16), (11; 17) (12; 18), because conserved sequences located near the human DHS align in proximity to the DHS mapped in the mouse loci.”
Background
IL-7 Receptor Expression Provides the Potential for Long-Term Survival of Both CD62Lhigh Central Memory T Cells and Th1 Effector Cells during Leishmania major Infection
Colpitts, S. L., Dalton, N. M., & Scott, P. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0803450 · Cited by 76
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“Because Bcl-2 has a direct connection to memory cell survival, in part downstream of CD127 (Kaech et al., 2003), we further tested Bcl-2 protein expression using the miR-150 overexpression RV system as described above. miR-150 overexpression resulted in decreased Bcl-2 expression (Figure 6C).”
BackgroundMethodInfluentialSelf-citation
An early precursor CD8+ T cell that adapts to acute or chronic viral infection
McManus, D. T., Valanparambil, R. M., Medina, C. B., Scharer, C. D., McGuire, D. J., Sobierajska, E., Hu, Y., Chang, D. Y., Wieland, A., Lee, J., et al. (2025) · Nature · doi:10.1038/s41586-024-08562-y · Cited by 76
“Co-staining of the canonical memory T cells markers (CD127, KLRG1, CD62L) showed that the donor stem-like cells from clone-13-infected mice were acquiring markers associated with central memory T cells in the absence of antigen 25,26 (Fig.”
Self-citation
Generation, persistence and plasticity of CD4 T‐cell memories
Lees, J. R., & Färber, D. L. (2010) · Immunology · doi:10.1111/j.1365-2567.2010.03288.x · Cited by 75
Role of Direct Effects of IFN-γ on T Cells in the Regulation of CD8 T Cell Homeostasis
Tewari, K., Nakayama, Y., & Suresh, M. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.4.2115 · Cited by 75
“Previous studies have suggested that effector CD8 T cells that express higher levels of inhibitory killer cell lectin-like receptor G-1 (KLRG-1) and low levels of IL-7R represent apoptosis-prone terminally differentiated or senescent effector cells (18).”
BackgroundMethod
Signal transducer and activator of transcription 3 (STAT3) mutations underlying autosomal dominant hyper-IgE syndrome impair human CD8+ T-cell memory formation and function
Ives, M. L., Ma, C. S., Palendira, U., Chan, A., Bustamante, J. C., Boisson‐Dupuis, S., Arkwright, P. D., Engelhard, D., Averbuch, D., Magdorf, K., et al. (2013) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2013.05.029 · Cited by 75
Single-cell transcriptomics reveals a low CD8 + T cell infiltrating state mediated by fibroblasts in recurrent renal cell carcinoma
Peng, Y., Xiong, L., Zhou, Z., Kang, N., Li, Z., Wu, Z., Deng, M.-H., Wei, W.-S., Wang, N., Zou, X.-P., et al. (2022) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2021-004206 · Cited by 75
IL-2-driven CD8+ T cell phenotypes: implications for immunotherapy
Niederlová, V., Tsyklauri, O., Kovář, M., & Štěpánek, O. (2023) · Trends in Immunology · doi:10.1016/j.it.2023.09.003 · Cited by 78
“This is paradoxical since: (i) IL-2 treatment ex vivo [30] or without antigenic activation in vivo [3] decreases the expression of IL-7R α ; and (ii) the expression of IL-7R α is typical for memory, but not for effector T cells [31].”
Background
IFN-γ Receptor Signaling Regulates Memory CD8+ T Cell Differentiation
Sercan-Alp, Ö., Stoycheva, D., Hämmerling, G. J., Arnold, B., & Schüler, T. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0902708 · Cited by 73
Control of CD4+ T‐cell memory by cytokines and costimulators
Dooms, H., & Abbas, A. K. (2006) · Immunological Reviews · doi:10.1111/j.0105-2896.2006.00387.x · Cited by 74
“The potential significance of IL-7 in CD8 memory cell survival is further supported by the observation that a population of CD8 cells re-expressing the IL-7Ra after viral infection preferentially develops into memory cells (48, 49).”
Background
Cutting Edge: IL-7-Independent Regulation of IL-7 Receptor α Expression and Memory CD8 T Cell Development
Klonowski, K. D., Williams, K., Marzo, A. L., & Lefrançois, L. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.7.4247 · Cited by 74
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Early events governing memory CD8+ T-cell differentiation
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Immune responsiveness and protective immunity after transplantation
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“In addition, murine CD8 T cells expressing high levels of the IL-7Ra chain (CD127) bypass the death phase, differentiating into memory T cells [26].”
BackgroundSelf-citation
Regulated expression of the inhibitory receptor LAIR‐1 on human peripheral T cells during T cell activation and differentiation
Jansen, C. A., Cruijsen, C. W. A., Ruiter, T. E.-D., Nanlohy, N. M., Willems, N., Janssens-Korpela, P. L., & Meyaard, L. (2007) · European Journal of Immunology · doi:10.1002/eji.200636678 · Cited by 73
CD127 expression and regulation are altered in the memory CD8 T cells of HIV-infected patients − reversal by highly active anti-retroviral therapy (HAART)
Colle, J., Moreau, J. L., Fontanet, A. L., Lambotte, O., Joussemet, M., Jf, D., & Thèze, J. (2006) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.2006.03022.x · Cited by 72
PARP-1/PARP-2 double deficiency in mouse T cells results in faulty immune responses and T lymphomas
Navarro, J., Gozalbo-López, B., Méndez, A. C., Dantzer, F., Schreiber, V., Martínez, C. M., Arana, D. M., Farrés, J., Revilla‐Nuin, B., Bueno, M. F., et al. (2017) · Scientific Reports · doi:10.1038/srep41962 · Cited by 72
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Hanna, B. S., Roessner, P. M., Yazdanparast, H., Colomer, D., Campo, E., Kugler, S. J., Yosifov, D. Y., Stilgenbauer, S., Schmidt, M., Gabriel, R., et al. (2018) · Leukemia · doi:10.1038/s41375-018-0250-6 · Cited by 72
Differential expansion of T central memory precursor and effector subsets is regulated by division speed
Kretschmer, L., Floßdorf, M., Mir, J., Cho, Y.-L., Plambeck, M., Treise, I., Toska, A., Heinzel, S., Schiemann, M., Busch, D. H., et al. (2020) · Nature Communications · doi:10.1038/s41467-019-13788-w · Cited by 72
PTPN2 Deficiency Enhances Programmed T Cell Expansion and Survival Capacity of Activated T Cells
Flosbach, M., Oberle, S. G., Scherer, S., Zecha, J., von Hoesslin, M., Wiede, F., Chennupati, V., Cullen, J. G., List, M., Pauling, J. K., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107957 · Cited by 71
An Il12 mRNA-LNP adjuvant enhances mRNA vaccine–induced CD8 T cell responses
Aunins, E., Phan, A. T., Alameh, M., Dwivedi, G., Cruz-Morales, E., Christian, D. A., Tam, Y. K., Bunkofske, M. E., Zabala-Peñafiel, A., O’Dea, K. M., et al. (2025) · Science Immunology · doi:10.1126/sciimmunol.ads1328 · Cited by 75
Virus-Specific CD8+ T Cells Upregulate Programmed Death-1 Expression during Acute Friend Retrovirus Infection but Are Highly Cytotoxic and Control Virus Replication
Zelinskyy, G., Myers, L. M., Dietze, K. K., Sutter, K., Roggendorf, M., Liu, J., Lu, M., Kraft, A. R. M., Teichgräber, V., Hasenkrug, K. J., et al. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1101612 · Cited by 72
“but had phenotypic markers indicative of effector memory precursor cells, a population of long-lived effector cells that develop into central or effector memory T cells (29).”
Background
Late Priming and Variability of Epitope-Specific CD8+ T Cell Responses during a Persistent Virus Infection
Kemball, C. C., Lee, E. D. H., Vezys, V., Pearson, T. C., Larsen, C. P., & Lukacher, A. E. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.12.7950 · Cited by 72
“However, in contrast to the concordance in IFN- and TNF- production by antiviral CD8 T cells to resolved LCMV infection (28), no 50% of any of the epitope-specific CD8 T cells in persistent PyV infection were coproducers of IFN- and TNF- .”
BackgroundInfluential
The JAK3 inhibitor CP-690550 selectively reduces NK and CD8+ cell numbers in cynomolgus monkey blood following chronic oral dosing
Conklyn, M. J., Andresen, C. J., Changelian, P. S., & Kudlacz, E. M. (2004) · Journal of Leukocyte Biology · doi:10.1189/jlb.0504282 · Cited by 72
“In fact, increased expression of the IL-7R chain identifies CD8 T cells, which will differentiate into memory cells [32].”
Background
Dendritic Cells and CD28 Costimulation Are Required To Sustain Virus-Specific CD8+ T Cell Responses during the Effector Phase In Vivo
Dolfi, D. V., Duttagupta, P. A., Boesteanu, A. C., Mueller, Y. M., Oliai, C. H., Borowski, A. B., & Katsikis, P. D. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1001972 · Cited by 71
IL2Rβ-dependent signals drive terminal exhaustion and suppress memory development during chronic viral infection
Beltra, J., Bourbonnais, S., Bédard, N., Charpentier, T., Boulangé, M., Michaud, E., Boufaied, I., Bruneau, J., Shoukry, N. H., Lamarre, A., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1604256113 · Cited by 72
“Sustaining an IL-7–Stat5–Bcl2 survival axis would provide considerable survival advantage to antiviral T cells following treatment-induced viral decline and would provide an interesting complementary approach to anti-PDL1 therapies, because a limitation of such treatment is its ineffectiveness in rescuing terminally d…”
BackgroundInfluential
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Patel, M. A., Kim, J., Ruzevick, J., Li, G., & Lim, M. K. (2014) · Cancers · doi:10.3390/cancers6041953 · Cited by 73
“Cytokine IL-7 is involved in T-cell development and is expressed by stromal and parenchymal cells [69,70].”
Background
Recalling the Future: Immunological Memory Toward Unpredictable Influenza Viruses
Auladell, M. A., Jia, X., Hensen, L., Chua, B. Y. L., Fox, A., Nguyen, T. H. O., Doherty, P. C., & Kedzierska, K. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01400 · Cited by 78
“Compared to the IL7RloKLGR1hi set, CD8 T cells expressing high levels of IL7R and low levels of KLGR1 are 10-fold more likely to survive (147) in mice infected with lymphocytic choriomeningitis virus (LCMV).”
Background
Metabolic plasticity and regulation of T cell exhaustion
Li, F., Liu, H., Zhang, D., Ma, Y., & Zhu, B. (2022) · Immunology · doi:10.1111/imm.13575 · Cited by 73
“6–8 Traditionally, it is believed that following antigen stimulation, the majority of T cells differentiate into short-lived effector cells, which would die by apoptosis following antigen clearance.(9) Only a small fraction of T cells (about 5%–10%) survive, known as memory precursor T cells, which further differentia…”
BackgroundInfluential
Novel Exosome-Targeted CD4+ T Cell Vaccine Counteracting CD4+25+ Regulatory T Cell-Mediated Immune Suppression and Stimulating Efficient Central Memory CD8+ CTL Responses
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“Taken together, our results indicate that DCOVAprimed CD44 CD62LIL-7R and aTEXO-primed CD44 CD62LIL-7R CTL, which have high and low cytotoxicity to tumor cells, are consistent with typical effector and central memory CTL (emCTL and cmCTL), respectively (12, 25).”
Result
Cell-Intrinsic Defects in the Proliferative Response of Antiviral Memory CD8 T Cells in Aged Mice upon Secondary Infection
Decman, V., Laidlaw, B. J., DiMenna, L. J., Abdulla, S., Mozdzanowska, K., Erikson, J., Ertl, H. C. J., & Wherry, E. J. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0902063 · Cited by 71
Self-citation
Chemotherapy rescues tumor-driven aberrant CD4+ T-cell differentiation and restores an activated polyfunctional helper phenotype
Ding, Z., Blazar, B. R., Mellor, A. L., Munn, D. H., & Zhou, G. (2010) · Blood · doi:10.1182/blood-2009-11-253336 · Cited by 71
Role of Bim in Regulating CD8+T-Cell Responses during Chronic Viral Infection
Grayson, J. M., Weant, A. E., Holbrook, B. C., & Hildeman, D. A. (2006) · Journal of Virology · doi:10.1128/jvi.00855-06 · Cited by 72
“become Bcl-2 (15) and IL-7 receptor (21) low and are susFIG.”
Background
The early cellular signatures of protective immunity induced by live viral vaccination
Köhler, S., Bethke, N., Böthe, M., Sommerick, S., Frentsch, M., Romagnani, C., Niedrig, M., & Thiel, A. (2012) · European Journal of Immunology · doi:10.1002/eji.201142306 · Cited by 71
Cytokine-Mediated Regulation of CD8 T-Cell Responses During Acute and Chronic Viral InfectionPreprint
Hashimoto, M., Im, S. J., Araki, K., & Ahmed, R. (2017) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a028464 · Cited by 78
Self-citation
Reducing Mitochondrial ROS Improves Disease-related Pathology in a Mouse Model of Ataxia-telangiectasia
D’Souza, A. D., Parish, I. A., Krause, D. S., Kaech, S. M., & Shadel, G. S. (2012) · Molecular Therapy · doi:10.1038/mt.2012.203 · Cited by 73
Self-citation
IL-7Rα Gene Expression Is Inversely Correlated with Cell Cycle Progression in IL-7-Stimulated T Lymphocytes
Swainson, L. A., Verhoeyen, E., Cosset, F., & Taylor, N. N. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.11.6702 · Cited by 70
“Irrespective of the precise mechanisms implicated in this regulation, it appears that the reappearance of IL7R on activated T cells is associated with a survival advantage conferring protective immunity (48).”
Background
T-cell receptor signals direct the composition and function of the memory CD8+ T-cell pool
Smith‐Garvin, J. E., Burns, J. C., Gohil, M., Zou, T., Kim, J. S., Maltzman, J. S., Wherry, E. J., Koretzky, G. A., & Jordan, M. S. (2010) · Blood · doi:10.1182/blood-2010-06-292748 · Cited by 70
Self-citation
Protective Efficacy of Cross-Reactive CD8+ T Cells Recognising Mutant Viral Epitopes Depends on Peptide-MHC-I Structural Interactions and T Cell Activation Threshold
Valkenburg, S. A., Gras, S., Guillonneau, C., Gruta, N. L. L., Thomas, P. G., Purcell, A. W., Rossjohn, J., Doherty, P. C., Turner, S. J., & Kedzierska, K. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1001039 · Cited by 70
“Given that the NPN3A mutation was associated with a numerically diminished response following infection with either the wt or NPN3A influenza A viruses (Fig 2), we also asked if there was any effect on CD8 T cell function or phenotype, particularly for markers (CD62L and CD127) that discriminate between memory T cell…”
Background
Electron Transport Complex I Is Required for CD8+ T Cell Function
Yi, J. S., Holbrook, B. C., Michalek, R. D., Laniewski, N. G., & Grayson, J. M. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.2.852 · Cited by 69
“After pathogen clearance, the vast majority of effector cells undergo apoptosis by a process termed contraction, with the remaining CD127 high effector cells differentiating into memory cells (18).”
Human CD8+ T Cell Memory Generation in Puumala Hantavirus Infection Occurs after the Acute Phase and Is Associated with Boosting of EBV-Specific CD8+ Memory T Cells
Tuuminen, T., Kekäläinen, E., Mäkelä, S., Ala-Houhala, I. O., Ennis, F. A., Hedman, K., Mustonen, J. T., Vaheri, A. I., & Arstila, T. P. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.3.1988 · Cited by 70
“Consistent with this scenario, the kinetics of IL-7R expression also followed closely the appearance of PUUV-specific IFN- producing cells, suggesting that they represented the emergent memory population (23).”
Result
The Transcription Factor Hobit Identifies Human Cytotoxic CD4+ T Cells
Oja, A. E., Braga, F. A. V., Remmerswaal, E. B. M., Kragten, N. A. M., Hertoghs, K. M. L., Zuo, J., Moss, P. A. H., van Lier, R. A. W., van Gisbergen, K. P. J. M., & Hombrink, P. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00325 · Cited by 73
“KLRG1 and CD127 are frequently used to differentiate between memory (precursor) cells (KLRG1−CD127+) and effector cells (KLRG1+CD127−) (23).”
Background
Metabolic regulation by PD-1 signaling promotes long-lived quiescent CD8 T cell memory in mice
Kalia, V., Yuzefpolskiy, Y., Vegaraju, A., Xiao, H., Baumann, F. M., Jatav, S., Church, C. D., Prlic, M., Jha, A., Nghiem, P., et al. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.aba6006 · Cited by 71
“2E) of short-lived effector cells (SLECs) and memory precursor effector cell (MPEC) subsets, as distinguished by cell surface markers CD127 and killer cell lectin-like receptor G1 (KLRG-1) (34, 35, 37, 61, 62), were similar between WT and PD-1–ablated donor cells in all tissues analyzed.”
ResultInfluential
IL-7 adjuvant treatment enhances long-term tumor antigen-specific CD8+ T-cell responses after immunization with recombinant lentivector
Colombetti, S., Lévy, F., & Chapatte, L. (2009) · Blood · doi:10.1182/blood-2008-05-155309 · Cited by 69
Early Priming Minimizes the Age-Related Immune Compromise of CD8+ T Cell Diversity and Function
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“functional quality (DbPA224 CD8; Figure 3, Figure 4) or reduced in number (DbNP366 CD8; Figure 1), the further question was whether there was any effect on cell surface activation phenotype [34,40–42].”
Background
The Enigmatic Role of Viruses in Multiple Sclerosis: Molecular Mimicry or Disturbed Immune Surveillance?
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“These cytokine receptors not only control the homeostasis of CD4[684_TD$DIFF] regulatory and Th cells, respectively [81,122], but are also essential for protective CD8 T cell responses [123,124].”
Rewriting History: Epigenetic Reprogramming of CD8+ T Cell Differentiation to Enhance Immunotherapy
Zebley, C. C., Gottschalk, S. M., & Youngblood, B. (2020) · Trends in Immunology · doi:10.1016/j.it.2020.06.008 · Cited by 71
Combined IL-21 and Low-Dose IL-2 therapy induces anti-tumor immunity and long-term curative effects in a murine melanoma tumor model
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EBV-associated mononucleosis leads to long-term global deficit in T-cell responsiveness to IL-15
Sauce, D., Larsen, M., Curnow, J., Leese, A. M., Moss, P. A. H., Hislop, A. D., Salmon, M., & Rickinson, A. B. (2006) · Blood · doi:10.1182/blood-2006-01-0144 · Cited by 69
Non‐malignant clonal expansions of CD8+ memory T cells in aged individuals
Clambey, E. T., van Dyk, L. F., Kappler, J. W., & Marrack, P. (2005) · Immunological Reviews · doi:10.1111/j.0105-2896.2005.00265.x · Cited by 68
“However, recent work has shown that 5–10% of activated CD8þ T cells express IL-7Ra during an immune response and that these IL-7Raþ cells are more effective at developing into CD8þ memory T cells (19, 20).”
Background
Acquired transcriptional programming in functional and exhausted virus-specific CD8 T cells.
Youngblood, B., Wherry, E. J., & Ahmed, R. (2012) · Current Opinion in HIV and AIDS · doi:10.1097/coh.0b013e32834ddcf2 · Cited by 68
“Unau 1746-630X 2011 Wolters Kluwer Health | Lippincott Williams & Wilki The cell-intrinsic mechanisms that dictate the functional, or lack thereof, capabilities of virusspecific CD8 T cells are initiated at the effector stage of differentiation, and are dependent upon strength and duration of TCR signaling [18,19].”
BackgroundSelf-citation
Analysis of Co-inhibitory Receptor Expression in COVID-19 Infection Compared to Acute Plasmodium falciparum Malaria: LAG-3 and TIM-3 Correlate With T Cell Activation and Course of Disease
Herrmann, M., Schulte, S., Wildner, N. H., Wittner, M., Brehm, T. T., Ramharter, M., Woost, R., Lohse, A. W., Jacobs, T., & Wiesch, J. S. Z. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01870 · Cited by 68
“CD127low T cells are considered short-lived effector cells that undergo apoptosis after antigen clearance (59).”
Background
Bcl6 controls granzyme B expression in effector CD8+ T cells
Yoshida, K., Sakamoto, A., Yamashita, K., Arguni, E., Horigome, S., Arima, M., Hatano, M., Seki, N., Ichikawa, T., & Tokuhisa, T. (2006) · European Journal of Immunology · doi:10.1002/eji.200636165 · Cited by 68
Biochemical signaling pathways for memory T cell recall
Färber, D. L. (2009) · Seminars in Immunology · doi:10.1016/j.smim.2009.02.003 · Cited by 68
Radiofrequency thermal ablation of breast tumors combined with intralesional administration of IL-7 and IL-15 augments anti-tumor immune responses and inhibits tumor development and metastasis
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Characterization of Human Antiviral Adaptive Immune Responses during Hepatotropic Virus Infection in HLA-Transgenic Human Immune System Mice
Billerbeck, E., Horwitz, J. A., Labitt, R. N., Donovan, B. M., Vega, K., Budell, W. C., Koo, G. C., Rice, C. M., & Ploß, A. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1201518 · Cited by 70
“CD127, the IL-7R a-chain, is highly expressed on naive T cells and long-lived memory T cells but downregulated on effector cells after Ag recognition (28).”
Background
miR-150 Regulates Differentiation and Cytolytic Effector Function in CD8+ T cells
Smith, N. L., Wissink, E. M., Grimson, A., & Rudd, B. D. (2015) · Scientific Reports · doi:10.1038/srep16399 · Cited by 69
Intrinsic 4-1BB signals are indispensable for the establishment of an influenza-specific tissue-resident memory CD8 T-cell population in the lung
Zhou, A. C., Wagar, L. E., Wortzman, M. E., & Watts, T. H. (2017) · Mucosal Immunology · doi:10.1038/mi.2016.124 · Cited by 67
“We therefore evaluated the circulating memory T cells for CD62L as well as for CD127, the IL-7Ra chain, to distinguish memory T cells from terminally differentiated effectors.(23,24) NP366–374-specific CD8 T cells from Ad-NP-4-1BBL-boosted mice showed delayed acquisition of CD62L compared with Ad-NP or control Ad-boos…”
BackgroundResult
Interleukin‐7 Enhances the Th1 Response to Promote the Development of Sjögren's Syndrome–like Autoimmune Exocrinopathy in Mice
Jin, J., Kawai, T., Cha, S., & Yu, Q. (2013) · Arthritis & Rheumatism · doi:10.1002/art.38007 · Cited by 67
Successful Vaccination Induces Multifunctional Memory T-Cell Precursors Associated With Early Control of Hepatitis C Virus
Park, S., Shin, E., Capone, S., Caggiari, L., Re, V. D., Nicosia, A., Folgori, A., & Rehermann, B. (2012) · Gastroenterology · doi:10.1053/j.gastro.2012.06.005 · Cited by 67
Impaired apoptosis and immune senescence – cause or effect?
Hsu, H., Scott, D. K., & Mountz, J. D. (2005) · Immunological Reviews · doi:10.1111/j.0105-2896.2005.00270.x · Cited by 68
“Because the lower number of cycling cells is balanced by a decrease in apoptosis, this may also be related to the requirement for IL-7/IL-7R signaling during the phase of homeostatic memory (106).”
Background
Mucosal CD8 Memory T Cells are selected in the periphery by an MHC Class I Molecule
Huang, Y., Park, Y., Wang-Zhu, Y., Larangé, A., Arens, R., Bernardo, I., Olivares-Villagómez, D., Herndler-Brandstetter, D., Abraham, N., Grubeck-loebenstein, B., et al. (2011) · Nature Immunology · doi:10.1038/ni.2106 · Cited by 54
“Similar to activation-induced expression of CD8αα, the expression of IL-7 receptor α-chain (IL-7Rα) also has been proposed as a marker for memory precursor cell”
Common γ chain cytokines: Dissidence in the details
Alves, N. L., Arosa, F. A., & van Lier, R. A. W. (2006) · Immunology Letters · doi:10.1016/j.imlet.2006.11.006 · Cited by 69
“The situation is different during chronic viral infections, in hich a subpopulation of antigen-specific memory T cells does ot express IL-7R [61–63].”
BackgroundInfluential
The small molecule TGF-β signaling inhibitor SM16 synergizes with agonistic OX40 antibody to suppress established mammary tumors and reduce spontaneous metastasis
Garrison, K., Hahn, T., Lee, W., Ling, L. E., Weinberg, A. D., & Akporiaye, E. T. (2011) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-011-1119-y · Cited by 70
Age related changes in T cell mediated immune response and effector memory to Respiratory Syncytial Virus (RSV) in healthy subjects
Cusi, M. G., Martorelli, B., Genova, G. D., Terrosi, C., Campoccia, G., & Correale, P. (2010) · Immunity & Ageing · doi:10.1186/1742-4933-7-14 · Cited by 67
“IL7-R signalling may promote lymphocyte survival necessary for long living memory T cells, protecting these cells from multiple pro-apoptotic stimula and inhibitory feedback [22,37].”
BackgroundInfluential
Memory formation and long-term maintenance of IL-7Rα+ ILC1s via a lymph node-liver axis
Wang, X., Peng, H. C., Cong, J., Wang, X., Lian, Z., Wei, H., Sun, R., & Tian, Z. (2018) · Nature Communications · doi:10.1038/s41467-018-07405-5 · Cited by 67
Memory T cells have gene expression patterns intermediate between naïve and effector
Holmes, S., He, M., Xu, T., & Lee, P. P. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0501437102 · Cited by 67
NKG2D signaling on CD8+ T cells represses T-bet and rescues CD4-unhelped CD8+ T cell memory recall but not effector responses
Zloza, A., Kohlhapp, F. J., Lyons, G. E., Schenkel, J. M., Moore, T. V., Lacek, A. T., O’Sullivan, J. A., Varanasi, V., Williams, J. W., Jagoda, M. C., et al. (2012) · Nature Medicine · doi:10.1038/nm.2683 · Cited by 67
Hdac3 is an epigenetic inhibitor of the cytotoxicity program in CD8 T cells
Tay, R. E., Olawoyin, O. M., Cejas, P., Xie, Y., Meyer, C. A., Ito, Y., Weng, Q. Y., Fisher, D. E., Long, H. W., Brown, M. A., et al. (2020) · The Journal of Experimental Medicine · doi:10.1084/jem.20191453 · Cited by 66
Do CD8 effector cells need IL-7R expression to become resting memory cells?
Buentke, E., Mathiot, A., Tolaini, M., Santo, J. P. D., Zamoyska, R., & Seddon, B. P. (2006) · Blood · doi:10.1182/blood-2006-04-016857 · Cited by 64
Autoreactive T effector memory differentiation mirrors β cell function in type 1 diabetes
Yeo, L., Woodwyk, A., Sood, S., Lorenc, A., Eichmann, M., Pujol‐Autonell, I., Melchiotti, R., Skowera, A., Fidanis, E., Dolton, G. M., et al. (2018) · Journal of Clinical Investigation · doi:10.1172/jci120555 · Cited by 68
Primary and secondary anti-viral response captured by the dynamics and phenotype of individual T cell clones
Minervina, A. A., Pogorelyy, M. V., Komech, E. A., Карнаухов, В. К., Bächer, P., Rosati, E., Franke, A., Chudakov, D. M., Mamedov, I. Z., Lebedev, Y. B., et al. (2020) · eLife · doi:10.7554/elife.53704 · Cited by 68
“S13B) [29–33].”
Priming with SARS CoV S DNA and boosting with SARS CoV S epitopes specific for CD4+ and CD8+ T cells promote cellular immune responses
HUANG, J., CAO, Y., Du, J., Bu, X., MA, R., & Wu, C. (2007) · Vaccine · doi:10.1016/j.vaccine.2007.06.047 · Cited by 63
The Role of Interleukin-2 in Memory CD8 Cell Differentiation
Boyman, O., Cho, J.-H., & Sprent, J. (2010) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-6451-9_3 · Cited by 66
Early Effector CD8 T Cells Display Plasticity in Populating the Short-Lived Effector and Memory-Precursor Pools Following Bacterial or Viral Infection
Plumlee, C. R., Obar, J. J., Colpitts, S. L., Jellison, E. R., Haining, W. N., Lefrançois, L., & Khanna, K. M. (2015) · Scientific Reports · doi:10.1038/srep12264 · Cited by 66
The role of CD27 in anti-viral T-cell immunity
Grant, E. J., Nüssing, S., Sant, S. A., Clemens, E. B., & Kedzierska, K. (2017) · Current Opinion in Virology · doi:10.1016/j.coviro.2016.12.001 · Cited by 68
The Selective Increase in Caspase-3 Expression in Effector but Not Memory T Cells Allows Susceptibility to Apoptosis
Sabbagh, L., Kaech, S. M., Bourbonnière, M., Woo, M., Cohen, L. Y., Haddad, E. K., Labrecque, N., Ahmed, R., & Sékaly, R. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.9.5425 · Cited by 65
“2B and 3) and the low levels of members of the Bcl-2 family in effector T cells (20–23) is likely to contribute significantly to their death by AICD.”
BackgroundInfluentialSelf-citation
CD103 fate mapping reveals that intestinal CD103−tissue-resident memory T cells are the primary responders to secondary infection
Fung, H. Y., Teryek, M., Lemenze, A. D., & Bergsbaken, T. (2022) · Science Immunology · doi:10.1126/sciimmunol.abl9925 · Cited by 65
Down-Regulation of IL-7Rα Expression in Human T Cells via DNA Methylation
Kim, H., Hwang, K., Kim, K.-C., & Kang, I. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.9.5473 · Cited by 64
“For example, in mice infected with lymphocyte choriomeningitis virus, CD8 T cells expressing IL-7R high had better survival and differentiation into memory cells compared with CD8 T cells expressing IL-7R low (3).”
Background
Adoptive transfer of HER2/neu-specific T cells expanded with alternating gamma chain cytokines mediate tumor regression when combined with the depletion of myeloid-derived suppressor cells
Morales, J. K., Kmieciak, M., Graham, L., Feldmesser, M., Bear, H. D., & Manjili, M. H. (2008) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-008-0609-z · Cited by 64
“IL-7 has been implicated as a pro-survival cytokine for early memory CD8+ T cell selection and maintenance, while IL-15 can protect eVector CD8 + T cells from apoptosis, as well as augment their cytotoxic eVects [21, 22, 30, 38, 40, 43].”
Background
Semaphorin 6D regulates the late phase of CD4 + T cell primary immune responses
O’Connor, B. P., Eun, S.-Y., Ye, Z., Zozulya, A. L., Lich, J. D., Moore, C. B., Iocca, H. A., Roney, K. E., Holl, E. K., Wu, Q. P., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803386105 · Cited by 64
“Inhibition of this late-phase increase in CD127 expression results in defective T cell memory (21, 24, 26).”
Background
Effector and memory CD8+ T cell differentiation: toward a molecular understanding of fate determination
Belz, G. T., & Kallies, A. (2010) · Current Opinion in Immunology · doi:10.1016/j.coi.2010.03.008 · Cited by 64
“In particular Interleukin-7 receptor a (IL-7R) [16], Killer cell lectin-like receptor G1 (KLRG1) [26], CD27 [11] and more recently Interleukin2 receptor (IL-2R) a [27 ,28 ] have been shown to be differentially expressed in subsets of CD8 T cells early after antigen stimulation.”
BackgroundResultInfluential
Homeostatic Turnover of Virus-Specific Memory CD8 T Cells Occurs Stochastically and Is Independent of CD4 T Cell Help
Choo, D. K., Murali‐Krishna, K., Anita, R., & Ahmed, R. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1001421 · Cited by 64
Self-citation
Opposing Effects of CD70 Costimulation during Acute and Chronic Lymphocytic Choriomeningitis Virus Infection of Mice
Penaloza‐MacMaster, P., Rasheed, A. U., Iyer, S. S., Yagita∥, H., Blazar, B. R., & Ahmed, R. (2011) · Journal of Virology · doi:10.1128/jvi.02205-10 · Cited by 64
“These CD127 cells are known to become long-lived cells and respond to secondary challenges (16, 21).”
BackgroundSelf-citation
Probing CD8 T Cell Responses with Listeria monocytogenes Infection
Condotta, S. A., Richer, M. J., Badovinac, V. P., & Harty, J. T. (2012) · Advances in immunology · doi:10.1016/b978-0-12-394590-7.00005-1 · Cited by 64
The PD-1: PD-L1 pathway promotes development of brain-resident memory T cells following acute viral encephalitis
Prasad, S., Hu, S., Sheng, W. S., Chauhan, P., Singh, A. R., & Lokensgard, J. R. (2017) · Journal of Neuroinflammation · doi:10.1186/s12974-017-0860-3 · Cited by 66
“Experiments using acute LCMV and Listeria infections in mice have demonstrated emergence of CD127-expressing CD8 T cells that arise during the effector phase and acquire phenotypical and functional properties of memory T cells [37, 40].”
The appropriate frequency and function of decidual Tim-3+CTLA-4+CD8+ T cells are important in maintaining normal pregnancy
Wang, S., Sun, F., Li, M., Qian, J., Chen, C., Wang, M., Zang, X., Li, D., Yu, M., & Du, M. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-1642-x · Cited by 64
Remembering to remember: T cell memory maintenance and plasticity
Omilusik, K. D., & Goldrath, A. W. (2019) · Current Opinion in Immunology · doi:10.1016/j.coi.2019.04.009 · Cited by 63
“In transfer experiments, CD8+ T cells with high expression of CD127 and low expression of KLRG1 (KLRG1loCD127hi) were found to have a significantly greater capacity to survive following infection compared to the KLRG1hiCD127lo counterparts and exhibited stem-like properties such as multipotency and the capacity for pr…”
Background

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
ORCID: Kaech, Susan M
Wherry, E John
Surh, Charles D
Ahmed, Rafi
Venue: Nature Immunology
Publisher: Springer Science and Business Media LLC
Published: 2003-11-16
Volume: 4
Issue: 12
Pages: 1191-1198
ISSN: 1529-2908 (ISSN-L)
1529-2916
DOI: 10.1038/ni1009
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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Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells

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