The who's who of T ‐cell differentiation: Human memory T ‐cell subsets
Open accessAbstract
Following antigen encounter and subsequent resolution of the immune response, a single naïve T cell is able to generate multiple subsets of memory T cells with different phenotypic and functional properties and gene expression profiles. Single‐cell technologies, first and foremost flow cytometry, have revealed the complex heterogeneity of the memory T ‐cell compartment and its organization into subsets. However, a consensus has still to be reached, both at the semantic (nomenclature) and phenotypic level, regarding the identification of these subsets. Here, we review recent developments in the characterization of the heterogeneity of the memory T ‐cell compartment, and propose a unified classification of both human and nonhuman primate T cells on the basis of phenotypic traits and in vivo properties. Given that vaccine studies and adoptive cell transfer immunotherapy protocols are influenced by these recent findings, it is important to use uniform methods for identifying and discussing functionally distinct subsets of T cells.
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Multidimensional flow cytometry with up to 40 parameters enables deeper phenotyping and characterization of the immune system, which is required as cellular subsets require more and more markers for accurate definition.
“Multidimensional flow cytometry with up to 40 parameters enables a deeper phenotyping and characterization of the immune system, which is required as cellular subsets require more and more markers for accurate definition [81].”
From Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition) (2021) · cites this paper as [81]
The Introduction says flow cytometry enables single-cell phenotyping, and “Why multiple makers are necessary” explains why more markers can improve the identification of naïve T-cell subsets. But the paper reports 18 markers for fluorescence-based flow cytometry and 34 parameters for mass cytometry, not up to 40 parameters for flow cytometry. Its discussion of marker requirements concerns T-cell subsets rather than cellular subsets across the immune system. (LLM, conf=0.88)
Experimental — accuracy not yet measuredTCMs further differentiated into transitional memory T cells (TTMs) in vitro during viral outgrowth.
“Moreover, by tSNE, we confirmed that TCMs further differentiated into transitional memory T cells (TTMs) in vitro during viral outgrowth (Figures 4C and 4D) as a logical consequence after stimulation.”
From Revealing viral and cellular dynamics of HIV-1 at the single-cell level during early treatment periods (2023) · cites this paper as [51]
The ‘Additional memory T-cell subsets’ section places transitional memory T cells at a more differentiated stage than TCM cells, and ‘Central and effector memory T cells defined by function’ describes TCM cells as progenitors of more differentiated cells. The review does not report TCM-to-TTM differentiation in vitro during viral outgrowth; that specific observation is presented as the citing authors’ own finding. (LLM, conf=0.85)
Experimental — accuracy not yet measuredThe patient showed increased number of CD8+ T cells, which showed a more activated and differentiated phenotype as indicated by an elevated proportion of HLA-DR+ or CD38+ cells.
“The patient showed increased number of CD8 + T cells, which showed a more activated and differentiated phenotype as indicated by an elevated proportion of HLA-DR + or CD38 + cells (7).”
From A Novel Homozygous RHOH Variant Associated with T Cell Dysfunction and Recurrent Opportunistic Infections (2024) · cites this paper as [7]
Table 1 (Concluding remarks; page unavailable) lists HLA-DR and CD38 under activation, supporting their use as activation markers. It does not support treating a higher proportion of cells positive for either marker as evidence of greater differentiation; the table shows CD38 expression declining across the listed differentiation stages. The paper does not report the citing authors’ patient observation. (LLM, conf=0.85)
Experimental — accuracy not yet measuredA small population of memory T cells with elevated proliferative and self-renewal capacities has been identified within the CD45RA+CCR7+ naïve T-cell gate; these are stem cell-like memory (Tscm) cells and can be distinguished from truly naïve T cells based on FAS receptor (CD95) expression.
“a small population of memory T cells endowed with elevated proliferative and self-renewal capacities has been identified within the CD45RA+CCR7+ naïve T-cell gate. These cells have been termed stem cell-like memory (Tscm) cells [140] and can be distinguished from truly naïve T cells based on the expression of the FAS receptor (CD95) (Figure 8A) [81].”
From Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition) (2021) · cites this paper as [81]
Both the CD4+ and CD8+ T-cell subsets displayed a significantly lower proportion of CD28+ cells, suggesting a decrease in naïve T cells.
“Both the CD4 + and CD8 + T-cell subsets displayed a signi cantly lower proportion of CD28 + cells, suggesting a decrease in naïve T cell which express a high level of differentiation marker CD28 (7).”
From A Novel Homozygous RHOH Variant Associated with T Cell Dysfunction and Recurrent Opportunistic Infections (2024) · cites this paper as [7]
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CD40L expression permits CD8+ T cells to execute immunologic helper functions
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Guidelines for the use of flow cytometry and cell sorting in immunological studies (second edition)
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“In agreement with the naive and/or CM state of T cells in these clusters, high expression of IL-7 receptor IL7R (CD127) was also detected (Mahnke et al., 2013).”
BackgroundWeiskopf, D., Schmitz, K. S., Raadsen, M. P., Grifoni, A., Okba, N. M. A., Endeman, H., van den Akker, J. P. C., Molenkamp, R., Koopmans, M. P. G., van Gorp, E. C. M., et al. (2020) · Science Immunology · doi:10.1126/sciimmunol.abd2071 · Cited by 907 · see citing works
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“It is known that both naïve and memory T cells express CCR7 and SELL genes, which are required for lymph node migration, whereas these genes are not expressed in effector T cells 36,37 .”
BackgroundImmune Landscape of Viral- and Carcinogen-Driven Head and Neck Cancer
Cillo, A. R., Kürten, C. H. L., Tabib, T., Qi, Z., Onkar, S., Wang, T., Liu, A., Duvvuri, U., Kim, S., Soose, R. J., et al. (2020) · Immunity · doi:10.1016/j.immuni.2019.11.014 · Cited by 654 · see citing works
“DC2 was associated with a memory phenotype (Figure S3C), governed by co-expression of CD27, CCR7, EOMES and other genes associated with memory formation (Banerjee et al., 2010; Mahnke et al., 2013).”
BackgroundGuidelines for the use of flow cytometry and cell sorting in immunological studies (third edition)
Cossarizza, A., Chang, H., Radbruch, A., Abrignani, S., Addo, R., Akdis, M., Andrä, I., Andreata, F., Annunziato, F., Arranz, E., et al. (2021) · European Journal of Immunology · doi:10.1002/eji.202170126 · Cited by 531 · see citing works
Single cell transcriptomic landscape of diabetic foot ulcers
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“CD27 which characterizes central memory T-cells that lack immediate cytotoxicity 28 , was also more in the DFU-Healers (Supplementary Fig.”
BackgroundImmune Reconstitution after Allogeneic Hematopoietic Stem Cell Transplantation
Ogonek, J., Juric, M. K., Ghimire, S., Varanasi, P. R., Holler, E., Greinix, H., & Weissinger, E. M. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00507 · Cited by 461 · see citing works
α-Synuclein-specific T cell reactivity is associated with preclinical and early Parkinson’s disease
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“3,4 Memory T cells represent cells at an intermediate state of differentiation that can be further divided into memory stem cells (TSCM), central memory cells (TCM), and effector memory cells (TEM) along a progressive developmental path.(3,4) Which T-cell subsets should be used for adoptive immunotherapy has been deba…”
BackgroundElla, R., Reddy, S., Jogdand, H., Sarangi, V., Ganneru, B., Prasad, S. D., Das, D., Raju, D., Praturi, U., Sapkal, G. N., et al. (2021) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(21)00070-0 · Cited by 374 · see citing works
The CD8 T Cell Response to Respiratory Virus Infections
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“Based on the expression of activation marker CD45RA and lymphoid homing receptor CCR7, human memory CD8 T cells have been broadly separated into four major subsets: (1) naive (CD45RA + CCR7 + ), (2) central memory (TCM; CD45RA -CCR7 + ), (3) effector memory (TEM; CD45RA − CCR7 − ), and (4) late effector memory (TEMRA;…”
BackgroundPark, L. M., Lannigan, J., & Jaimes, M. C. (2020) · Cytometry Part A · doi:10.1002/cyto.a.24213 · Cited by 350 · see citing works
“Using CD45RA and CCR7, T cells can be classified into naïve (CD45RACCR7), central memory (CD45RACCR7), effector memory (CD45RACCR7), and terminal effector memory (CD45RACCR7) subsets (40,41).”
BackgroundHo, W. J., Zhu, Q., Durham, J., Popovic, A., Xavier, S., Leatherman, J., Mohan, A., Mo, G., Zhang, S., Gross, N., et al. (2021) · Nature Cancer · doi:10.1038/s43018-021-00234-4 · Cited by 360 · see citing works
Single-cell transcriptomics reveals expansion of cytotoxic CD4 T cells in supercentenarians
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“Importantly, the tumor lacked multiple subsets of CD45RA+/− CCR7– terminal effector cells (clusters 18, 23, 4, and 8), characterized by variable levels of CD57 and T-bet expression, that are known to be highly cytolytic, but replicative senescent (Takata and Takiguchi, 2006; Chattopadhyay et al., 2009; Mahnke et al.,…”
BackgroundSelf-citationTwo subsets of stem-like CD8+ memory T cell progenitors with distinct fate commitments in humans
Galletti, G., De Simone, G., Mazza, E. M. C., Puccio, S., Mezzanotte, C., Bi, T. M., Davydov, A. N., Metsger, M., Scamardella, E., Alvisi, G., et al. (2020) · Nature Immunology · doi:10.1038/s41590-020-0791-5 · Cited by 299 · see citing works
Self-citationImmunology of Mycobacterium tuberculosis Infections
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Acquired cancer resistance to combination immunotherapy from transcriptional loss of class I HLA
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Markers of T Cell Senescence in Humans
Xu, W., & Larbi, A. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18081742 · Cited by 261 · see citing works
“Lastly, terminal effector (TE) T cells (CD45RA+, CD45RO−, CD27−, CD28− and CCR7−) have limited proliferative capacity but tend to secrete a wider range of cytokines following activation [34].”
BackgroundGideon, H. P., Hughes, T. K., Tzouanas, C. N., Wadsworth, M. H., Tu, A. A., Gierahn, T. M., Peters, J. M., Hopkins, F. F., Wei, J.-R., Kummerlowe, C., et al. (2022) · Immunity · doi:10.1016/j.immuni.2022.04.004 · Cited by 278 · see citing works
“Multiple prior studies have reported a CXCR3+CCR6+ Th1/Th17 subset that contributes to Mtb-specific T cell responses (Becattini et al., 2015; Nikitina et al., 2018) and is capable of producing IFNg, IL-17, and IL-22 after stimulation, but not Th2-biased IL-4, IL-5, or IL-13 (Acosta-Rodriguez et al., 2007; Becattini et…”
BackgroundInfluentialThe immunobiology of CD27 and OX40 and their potential as targets for cancer immunotherapy
Buchan, S. L., Rogel, A., & Al‐Shamkhani, A. (2017) · Blood · doi:10.1182/blood-2017-07-741025 · Cited by 276 · see citing works
Functional Signatures of Human CD4 and CD8 T Cell Responses to Mycobacterium tuberculosis
Prezzemolo, T., Guggino, G., Manna, M. P. L., Liberto, D. D., Dieli, F., & Caccamo, N. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00180 · Cited by 268 · see citing works
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Unmodified mRNA in LNPs constitutes a competitive technology for prophylactic vaccines
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SARS-CoV-2–specific CD8+ T cell responses in convalescent COVID-19 individuals
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“The classification into functionally different T cell subsets following antigen encounter is based on the expression of different marker combinations, which describe a progressive T cell differentiation and allow to delineate a dynamic transition between memory and effector cell function (Figure 4C and Supplemental Fi…”
BackgroundMultifaceted Role of Neuropilins in the Immune System: Potential Targets for Immunotherapy
Roy, S., Bag, A. K., Singh, R. K., Talmadge, J. E., Batra, S. K., & Datta, K. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01228 · Cited by 237 · see citing works
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“For CD4þ and CD8þ T cells, antibodies to CD3, CD4, and CD8 were used as well as CD28 and CD95 for staining of memory subsets (46).”
MethodImmunosenescence Study of T Cells: A Systematic Review
Rodríguez, I. J., Lalinde-Ruiz, N., León, M. L., Martínez-Enriquez, L. C., Velásquez, M. D. P. M., Aguirre, J. P. O., Bohórquez, O. M. R., Vargas, E. A. V., Hernández-Álvarez, E. D., & Parra-López, C. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.604591 · Cited by 224 · see citing works
Immune awakening revealed by peripheral T cell dynamics after one cycle of immunotherapy
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Self-citationMechanisms Underlying T Cell Immunosenescence: Aging and Cytomegalovirus Infection
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“In addition, CD45RACD8 memory T cells did not accumulate with age and showed no correlation with the CD28CD8 TEM subset (Mahnke et al., 2013).”
BackgroundKruzik, A., Fetahagic, D., Hartlieb, B., Dorn, S., Koppensteiner, H., Horling, F. M., Scheiflinger, F., Reipert, B. M., & de la Rosa, M. (2019) · Molecular Therapy - Methods & Clinical Development · doi:10.1016/j.omtm.2019.05.014 · Cited by 182 · see citing works
An atlas of cells in the human tonsil
Massoni-Badosa, R., Aguilar-Fernández, S., Nieto, J. C., Soler-Vila, P., Elosua-Bayés, M., Marchese, D., Kulis, M., Vilas‐Zornoza, A., Bühler, M. M., Rashmi, S., et al. (2024) · Immunity · doi:10.1016/j.immuni.2024.01.006 · Cited by 179 · see citing works
“An upregulation of chemokine receptors drives non-Tfh cells to exit the lymphoid tissue and to traffic to primary infection or inflammation sites (Mahnke et al., 2013).”
BackgroundCD8+ T cells and NK cells: parallel and complementary soldiers of immunotherapy
Rosenberg, J. N., & Huang, J. (2017) · Current Opinion in Chemical Engineering · doi:10.1016/j.coche.2017.11.006 · Cited by 178 · see citing works
“These subsets are further divided based on specific surface markers [57].”
BackgroundMitson‐Salazar, A., Yin, Y., Wansley, D. L., Young, M. L., Bolan, H., Arceo, S. M., Ho, N., Koh, C., Milner, J. D., Stone, K. D., et al. (2015) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2015.08.007 · Cited by 164 · see citing works
Peripheral CD4+ T cell subsets and antibody response in COVID-19 convalescent individuals
Gong, F., Dai, Y., Zheng, T., Cheng, L., Zhao, D., Wang, H., Liu, M., Pei, H., Jin, T., Yu, D., et al. (2020) · Journal of Clinical Investigation · doi:10.1172/jci141054 · Cited by 160 · see citing works
“We acknowledge the limitation that the study on memory cells should include more parameters such as Ki-67, CD127, CD62L or BCL2 (44, 45).”
BackgroundAraya, P., Waugh, K. A., Sullivan, K. D., Núñez, N. G., Roselli, E., Smith, K. P., Granrath, R. E., Rachubinski, A. L., Enriquez Estrada, B., Butcher, E. T., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1908129116 · Cited by 179 · see citing works
TCRαβ + CD3 + CD4 − CD8 − (double negative) T cells in autoimmunity
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“In healthy individuals, Ki-67 is preferentially expressed by memory-phenotype T cells.(11) Combined analysis of Ki-67 expression and naive and memory markers (supplemental Figure 1B) revealed that Ki-67 expression was confined to memory subsets while bothCD4(1)andCD8(1)TNwere almost exclusivelyKi-67 2 (Figure 1B).”
Self-citationGroß, C. C., Meyer, C., Bhatia, U., Yshii, L., Kleffner, I., Bauer, J., Tröscher, A. R., Schulte‐Mecklenbeck, A., Herich, S., Schneider‐Hohendorf, T., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-13593-5 · Cited by 149 · see citing works
Butyrate as a bioactive human milk protective component against food allergy
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NKG2D-CAR-transduced natural killer cells efficiently target multiple myeloma
Leivas, A., Valeri, A., Córdoba, L., García-Ortiz, A., Ortiz, A., Sánchez-Vega, L., Graña-Castro, O., Fernández, L., Carreño-Tarragona, G., Pérez, M., et al. (2021) · Blood Cancer Journal · doi:10.1038/s41408-021-00537-w · Cited by 139 · see citing works
“Memory T cells lack of a reactive T-cell receptor and maintain T-cell immunity producing less CRS [22, 25].”
BackgroundResultConsensus nomenclature for CD8+T cell phenotypes in cancer
Apétoh, L., Smyth, M. J., Drake, C. G., Abastado, J., Apte, R. N., Ayyoub, M., Blay, J., Bonneville, M., Butterfield, L. H., Caignard, A., et al. (2015) · OncoImmunology · doi:10.1080/2162402x.2014.998538 · Cited by 138 · see citing works
Self-citationIL15 and T-cell Stemness in T-cell–Based Cancer Immunotherapy
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“These cells are thought to maintain T-cell memory in a stem cell-like fashion, that is, to self-renew while simultaneously generating more differentiated progeny (15, 18).”
BackgroundSelf-citationColamatteo, A., Carbone, F., Bruzzaniti, S., Galgani, M., Fusco, C., Maniscalco, G. T., Rella, F. D., de Candia, P., & Rosa, V. D. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2019.03136 · Cited by 139 · see citing works
Antioxidant metabolism regulates CD8+ T memory stem cell formation and antitumor immunity.
Pilipow, K., Scamardella, E., Puccio, S., Gautam, S., Paoli, F. D., Mazza, E. M. C., Simone, G. D., Polletti, S., Buccilli, M., Zanon, V., et al. (2018) · JCI Insight · doi:10.1172/jci.insight.122299 · Cited by 127 · see citing works
“In accordance with such increased relative frequency of early differentiated memory phenotypes and with human data, NAC-treated Cor93-specific CD8 + T cells produced less IFN-γ but similar amounts of TNF compared with control cells at day 35 after ACT when restimulated with the cognate peptide in vitro (Figure 5H).”
InfluentialSelf-citationWeltevrede, M., Eilers, R., de Melker, H. E., & van Baarle, D. (2016) · Experimental Gerontology · doi:10.1016/j.exger.2016.02.005 · Cited by 128 · see citing works
“Based on their functionality and the expression of different surface markers memory T cells can be found in several different stages of differentiation (8-11).”
MAL2 drives immune evasion in breast cancer by suppressing tumor antigen presentation
Fang, Y., Wang, L., Wan, C., Sun, Y., der Jeught, K. V., Zhou, Z., Dong, T., So, K. M., Yu, T., Li, Y., et al. (2020) · Journal of Clinical Investigation · doi:10.1172/jci140837 · Cited by 129 · see citing works
Highly differentiated cytotoxic T cells in inclusion body myositis
Greenberg, S. A., Pinkus, J. L., Kong, S. W., Baecher‐Allan, C., Amato, A. A., & Dorfman, D. M. (2019) · Brain · doi:10.1093/brain/awz207 · Cited by 125 · see citing works
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Poch, T., Krause, J., Casar, C., Liwinski, T., Glau, L., Kaufmann, M., Ahrenstorf, A. E., Hess, L. U., Ziegler, A. E., Martrus, G., et al. (2021) · Journal of Hepatology · doi:10.1016/j.jhep.2021.03.016 · Cited by 124 · see citing works
Xu, Y., Yang, Z., Horan, L. H., Zhang, P., Liu, L., Zimdahl, B., Green, S., Lu, J., Morales, J. F., Barrett, D. M., et al. (2018) · Cell Discovery · doi:10.1038/s41421-018-0066-6 · Cited by 122 · see citing works
TCF1 expression marks self-renewing human CD8+ T cells
Kratchmarov, R., Magun, A. M., & Reiner, S. L. (2018) · Blood Advances · doi:10.1182/bloodadvances.2018016279 · Cited by 116 · see citing works
“TCM cells retain a greater proliferative capacity than TEM cells but exhibit less function immediately after restimulation.(1) TEMRA cells are thought to be terminally differentiated.”
BackgroundNanomedicine-based drug delivery towards tumor biological and immunological microenvironment
Li, J., & Burgess, D. J. (2020) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2020.05.008 · Cited by 117 · see citing works
Features of Effective T Cell-Inducing Vaccines against Chronic Viral Infections
Panagioti, E., Klenerman, P., Lee, L. N., van der Burg, S. H., & Arens, R. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00276 · Cited by 106 · see citing works
Immunological memories of the bone marrow
Chang, H., Tokoyoda, K., & Radbruch, A. (2018) · Immunological Reviews · doi:10.1111/imr.12656 · Cited by 111 · see citing works
de Weerdt, I., Hofland, T., de Boer, R., Dobber, J. A., Dubois, J., van Nieuwenhuize, D., Mobasher, M., de Boer, F., Hoogendoorn, M., Velders, G. A., et al. (2019) · Blood Advances · doi:10.1182/bloodadvances.2019000360 · Cited by 110 · see citing works
“effector memory T cells based on CD27 and CD45RA expression.(43) Although the differentiation status of CD4(1) T cells did not differ between LN and PB in CLL patients and HCs, the CD8(1) compartment in CLL patients consisted of a larger proportion of central memory T cells in the LN in comparison with the PB (37.”
ResultThe Single-Cell Phenotypic Identity of Human CD8+ and CD4+ T Cells
Brummelman, J., Pilipow, K., & Lugli, E. (2018) · International review of cytology · doi:10.1016/bs.ircmb.2018.05.007 · Cited by 110 · see citing works
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Memory T Cells Expressing an NKG2D-CAR Efficiently Target Osteosarcoma Cells
Fernández, L., Metais, J.-Y., Escudero, A., Vela, M., Valentín, J., Vallcorba, I., Leivas, A., Torres, J., Valeri, A., Patiño-García, A., et al. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-17-0075 · Cited by 108 · see citing works
“CD45RA is expressed on na€ ve T cells, whereas CD45RO is expressed on memory T cells (22).”
BackgroundStem, Effector, and Hybrid States of Memory CD8+ T Cells
Lugli, E., Galletti, G., Boi, S. K., & Youngblood, B. (2019) · Trends in Immunology · doi:10.1016/j.it.2019.11.004 · Cited by 106 · see citing works
“Specifically, in recent work, our group examined wholegenome DNA methylation from cell-sorted memory CD8+ T cell subsets isolated from the blood of healthy human donors: the analysis revealed genes that were differentially targeted for methylation programming between TEM and TSCM cells, and which were enriched in path…”
BackgroundInfluentialSelf-citationMolecular Aspects and Future Perspectives of Cytokine-Based Anti-cancer Immunotherapy
Chulpanova, D. S., Kitaeva, K. V., Green, A. R., Rizvanov, A. A., & Solovyeva, V. V. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00402 · Cited by 109 · see citing works
Immunopathology of RSV: An Updated Review
Bergeron, H. C., & Tripp, R. A. (2021) · Viruses · doi:10.3390/v13122478 · Cited by 109 · see citing works
Loschinski, R., Böttcher, M., Stoll, A., Bruns, H., Mackensen, A., & Mougiakakos, D. (2018) · Oncotarget · doi:10.18632/oncotarget.24442 · Cited by 106 · see citing works
“Overall, all tested immunometabolic parameters point towards promotion of memory T-cells by IL-21, which we confirmed by the according phenotypical analyses [48].”
ResultHuman CD8+ CD57- TEMRA cells: Too young to be called "old"
Verma, K., Ogonek, J., Varanasi, P. R., Luther, S., Bünting, I., Thomay, K., Behrens, Y. L., Weissinger, E. M., & Hambach, L. (2017) · PLoS ONE · doi:10.1371/journal.pone.0177405 · Cited by 105 · see citing works
Increased CD95 (Fas) and PD‐1 expression in peripheral blood T lymphocytes in COVID‐19 patients
Bellesi, S., Metafuni, E., Hohaus, S., Maiolo, E., Marchionni, F., D’Innocenzo, S., Sorda, M. L., Ferraironi, M., Ramundo, F., Fantoni, M., et al. (2020) · British Journal of Haematology · doi:10.1111/bjh.17034 · Cited by 102 · see citing works
“CD95 is widely expressed in Memory and Effector T cells upon contact with antigen, while Naive T cells are typically CD95 negative.(7,8) Programmed cell death 1 (PD-1, CD279), an antigen of Effector T cells, is considered an exhaustion marker, also expressed during antigen-mediated T cell activation.”
BackgroundPeripheral Blood-Based Biomarkers for Immune Checkpoint Inhibitors
An, H. J., Chon, H. J., & Kim, C. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179414 · Cited by 105 · see citing works
“WistubaHamprecht et al. demonstrated that high frequencies of CD8 effector-memory type 1 T cells defined as CD45 RA− CCR7− CD27+ CD28+ in the peripheral blood within 4 weeks of treatment initiation were associated with higher clinical response and longer OS [37].”
BackgroundA shift in lung macrophage composition is associated with COVID-19 severity and recovery
Chen, S. T., Park, M. D., Valle, D. M. D., Buckup, M., Tabachnikova, A., Thompson, R. C., Simons, N. W., Mouskas, K., Lee, B. H., Geanon, D., et al. (2022) · Science Translational Medicine · doi:10.1126/scitranslmed.abn5168 · Cited by 104 · see citing works
“S8, C to E) (24, 25).”
Lieber, S., Reinartz, S., Raifer, H., Finkernagel, F., Dreyer, T. F., Bronger, H., Jansen, J. M., Wagner, U. A. G., Worzfeld, T., Müller, R., et al. (2018) · OncoImmunology · doi:10.1080/2162402x.2018.1424672 · Cited by 102 · see citing works
“1D) is consistent with the known properties of CD8C TEM cells, including high cytotoxic activity and rapid effector cytokine production.(29) Therefore, we focused on the mechanisms of CD8C TEM cell migration and activation in ovarian carcinoma ascites.”
BackgroundRapidly Switchable Universal CAR-T Cells for Treatment of CD123-Positive Leukemia
Loff, S., Dietrich, J., Meyer, J.-E., Riewaldt, J., Spehr, J., Bonin, M. V., Gründer, C., Swayampakula, M., Franke, K., Feldmann, A., et al. (2020) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2020.04.009 · Cited by 102 · see citing works
Memory T-Cell Heterogeneity and TerminologyPreprint
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“Of note, identification of effector memory CD4 T cells was carried out by using the phenotypic markers CD45RO and CCR7, and therefore, this population can also contain cells with a transitional memory phenotype (53).”
MethodSouto‐Carneiro, M., Klika, K. D., Abreu, M., Meyer, A. P., Saffrich, R., Sandhoff, R., Jennemann, R., Kraus, F. V., Tykocinski, L., Eckstein, V., et al. (2020) · Arthritis & Rheumatology · doi:10.1002/art.41420 · Cited by 101 · see citing works
“Since naive RA CD8+ T cells presented metabolic and enzymatic profiles that were similar to those of antigen-experienced T cell subsets, we pondered whether the CD45RA+CCR7+ compartment of RA CD8+ T cells could also include CD95expressing stem-cell memory T cells (30), which could account for their profile resembling…”
BackgroundGeyer, M. B., Rivière, I., Sénéchal, B., Wang, X., Wang, Y., Purdon, T. J., Hsu, M., Devlin, S. M., Palomba, M. L., Halton, E. F., et al. (2019) · JCI Insight · doi:10.1172/jci.insight.122627 · Cited by 100 · see citing works
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“TRPM4 exerted this effect via membrane depolarisation, which limits the driving force for Ca2+ entry via the CRAC channel [187].”
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Accelerated aging with HIV occurs at the time of initial HIV infection
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van der Burg, M., Kalina, T., Pérez‐Andrés, M., Vlková, M., López‐Granados, E., Blanco, E., Bonroy, C., Sousa, A. E., Kienzler, A., Wentink, M. W. J., et al. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00246 · Cited by 95 · see citing works
Systemic CD4 Immunity as a Key Contributor to PD-L1/PD-1 Blockade Immunotherapy Efficacy
Zuazo, M., Arasanz, H., Bocanegra, A., Fernández, G., Chocarro, L., Vera, R., Kochan, G. T., & Escors, D. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.586907 · Cited by 94 · see citing works
Zwijnenburg, A. J., Pokharel, J., Varnaitė, R., Zheng, W., Hoffer, E., Shryki, I., Comet, N. R., Ehrström, M., Gredmark‐Russ, S., Eidsmo, L., et al. (2023) · Immunity · doi:10.1016/j.immuni.2023.06.025 · Cited by 89 · see citing works
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Progesterone Modulation of Pregnancy-Related Immune Responses
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The secret life of ion channels: Kv1.3 potassium channels and proliferation
Pérez-García, M. T., Cidad, P., & López‐López, J. R. (2017) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00136.2017 · Cited by 90 · see citing works
“CCR7 + cells are named central memory T-cells (T CM ) because of their location in secondary lymphoid tissues, while CCR7 - cells were named effector memory (T EM ) because of their rapid effector function ex-vivo (106).”
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“In addition, Ikaros has been shown to alter the threshold for activation of T cells downstream of T cell receptor and IL2 receptor signaling as well as protein kinase C, PI3K, and calcineurin signaling (22).”
BackgroundInfluentialCirculating mucosal-associated invariant T cells identify patients responding to anti-PD-1 therapy
Biasi, S. D., Gibellini, L., Tartaro, D. L., Puccio, S., Rabacchi, C., Mazza, E. M. C., Brummelman, J., Williams, B., Kaihara, K. A., Forcato, M., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-21928-4 · Cited by 86 · see citing works
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Coordinated Regulation of NK Receptor Expression in the Maturing Human Immune System
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“maturation, many leukocytes develop into distinct subsets whose diversity correlates with vast functional heterogeneity (1).”
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T Cell–Macrophage Interactions and Granuloma Formation in Vasculitis
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Reproducibility of Flow Cytometry Through Standardization: Opportunities and Challenges
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“In the immunology field, the expansion of the number of functional subsets revealed by expanding the number of available parameters led to a need for consensus on which set of markers could be used to define and thus enumerate different cell subsets (46,47).”
BackgroundAdaptive immune responses to SARS-CoV-2 persist in the pharyngeal lymphoid tissue of children
Xu, Q., Milanez‐Almeida, P., Martins, A. J., Radtke, A. J., Hoehn, K. B., Oguz, C., Chen, J., Liu, C., Tang, J., Grubbs, G., et al. (2022) · Nature Immunology · doi:10.1038/s41590-022-01367-z · Cited by 80 · see citing works
- Authors
- Mahnke, Y. D., Brodie, T. M., Sallusto, F., Roederer, M., & Lugli, E.
- Affiliations
- University of Pennsylvania (US)
- Institute for Research in Biomedicine (CH)
- National Institutes of Health (US)
- Humanitas University (IT)
- Corresponding author
- Roederer, Mario
- Lugli, Enrico
- Venue
- European Journal of Immunology
- Publisher
- Wiley
- Published
- 2013-10-30
- Volume
- 43
- Issue
- 11
- Pages
- 2797-2809
- ISSN
- 0014-2980 (ISSN-L)
- 1521-4141
- OpenAlex
- W1572743872
- Cited by
- 817
- References
- 113
- Citations by year
- 2026: 25 · 2025: 42 · 2024: 64 · 2023: 76 · 2022: 100 · 2021: 93 · 2020: 105 · 2019: 81 · 2018: 71 · 2017: 53 · 2016: 37 · 2015: 39 · 2014: 28 · 2013: 1
- FWCI
- 3.05
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- European Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Zenodo (CERN European Organization for Nuclear Research) (submittedVersion, other-oa)
- Funders
- National Science Foundation
- European Commission (241745, 322093)
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (131092)
- Fondazione Cariplo (2012-0683)
- Associazione Italiana per la Ricerca sul Cancro
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases
- FP7 Health
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- memory T cells, T cell differentiation, T cell memory subsets, T cell heterogeneity, T cell phenotype, vaccine immunology, adoptive cell transfer, single-cell technologies
- MeSH terms
- Cell Differentiation, Humans, Immunologic Memory, Lymphocyte Activation, Gene Expression, T-Lymphocyte Subsets, Immunotherapy, Adoptive, Adoptive Transfer
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