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Phenotype and function of human T lymphocyte subsets: Consensus and issues
Open accessAbstract
In recent years, a tremendous effort has been devoted to the detailed characterization of the phenotype and function of distinct T cell subpopulations in humans, as well as to their pathway(s) of differentiation and role in immune responses. But these studies seem to have generated more questions than definitive answers. To clarify issues related to the function and differentiation of T cell subsets, one session of the MASIR 2008 conference was dedicated to this topic. Several points of consensus and discord were highlighted in the work presented during this session. We provide here an account of these points, including the relative heterogeneity of T cell subpopulations during infections with distinct pathogens, the relationship between phenotypic and functional T cell attributes, and the pathway(s) of T cell differentiation. Finally, we discuss the problems which still limit general agreement. Published 2008 Wiley‐Liss, Inc.
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“Further, these cells re-express CD45RA in combination with markers often stated to reflect “senescence” such as CD57 and KLRG1 (Appay et al. 2008; van Lier et al. 2003).”
From Is immunosenescence influenced by our lifetime “dose” of exercise? (2016) · cites this paper as Appay et al. 2008
In the citing paper
“These CMV-specific T cells exhibit a late-stage differentiated phenotype, including loss of co-stimulatory molecules (e.g., CD27 and CD28) and cell-surface proteins associated with homing to lymphoid tissue (e.g., CD62L and CCR7) (Appay et al. 2008; van Lier et al. 2003).”
From Is immunosenescence influenced by our lifetime “dose” of exercise? (2016) · cites this paper as Appay et al. 2008
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“Lymphocytes are significant components of human cellular immunity; different lymphocyte subsets have been observed according to different phenotypes and functions [9].”
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BackgroundAntiparasitic Treatment Induces an Improved CD8+ T Cell Response in Chronic Chagasic Patients
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“The aberrant accumulation of memory CD57 T-cells, due to HIV-related impairment of the CD27 to CD27 differentiation step [18, 21], was associated with higher CD4 T-cell loss in HIV-infected individuals with viral loads higher than 10000 HIV-RNA copies/mL.”
BackgroundT-cell senescence: A crucial player in autoimmune diseases
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Clonal expansion of renal cell carcinoma-infiltrating T lymphocytes
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“However, the majority of CMV-specific 403 CD8 T cells isolated from healthy donors will express an effector-differentiated phenotype 404 (CD27/CD127/CD45RA/KLRG-1/CD57 - reviewed in (70)), and in vitro expansion of 405 CMV-specific T cells drives their differentiation towards an effector phenotype (40).”
BackgroundActive Tuberculosis Is Characterized by Highly Differentiated Effector Memory Th1 Cells
Arrigucci, R., Lakehal, K., Vir, P., Handler, D., Davidow, A. L., Herrera, R. M. B., Estrada-Guzmán, J. D., Bushkin, Y., Tyagi, S., Lardizabal, A. A., et al. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02127 · Cited by 34
Jiao, X., Rongyi, C., Xuesen, C., Jianzhou, Z., Ji, J., Ding, X., & Yu, X. (2019) · BMC Nephrology · doi:10.1186/s12882-019-1475-y · Cited by 36
“T cells, the major mediator of adaptive immunity, can be classified according to the surface markers (CD45RO and CCR7) into four subsets: naïve, central memory (CM), effector memory (EM) and effector memory RA (EMRA) T cells [5].”
BackgroundResultKalina, T., Bakardjieva, M., Blom, M., Pérez‐Andrés, M., Barendregt, B. H., Kanderová, V., Bonroy, C., Philippé, J., Blanco, E., Pico‐Knijnenburg, I., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00371 · Cited by 37
Analysis of stem-cell-like properties of human CD161++IL-18Rα+ memory CD8+ T cells
Havenith, S. H. C., Yong, S. L., Henson, S. M., Piet, B., Idu, M. M., Koch, X. S. D., Jonkers, R. E., Kragten, N. A. M., Akbar, A. N., van Lier, R. A. W., et al. (2012) · International Immunology · doi:10.1093/intimm/dxs069 · Cited by 35
Nose, Y., Saito, T., Yamamoto, K., Yamashita, K., Tanaka, K., Yamamoto, K., Makino, T., Takahashi, T., Kawashima, A., Haruna, M., et al. (2022) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-022-03240-2 · Cited by 36
Meijers, R. W. J., Litjens, N. H. R., de Wit, E. A., Langerak, A. W., van der Spek, A., Baan, C. C., Weimar, W., & Betjes, M. G. H. (2013) · Clinical & Experimental Immunology · doi:10.1111/cei.12188 · Cited by 36
Menstrual Blood as a Potential Source of Endometrial Derived CD3+ T Cells
Sabbaj, S., Hel, Z., Richter, H. E., Mestecky, J. F., & Goepfert, P. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028894 · Cited by 37
“) suggest that menstrual blood CD4+ T cells are predominantly CCR7+CD45RA+ (naive cells) consistent with cells emerging from a lymphoid organ. The endometrium is not a lymphoid organ and thus should not be capable of signaling T cells to differentiate. As such, finding a predominance of CD4+ naive T cells in this comp…”
CD8+ T Lymphocyte Expansion, Proliferation and Activation in Dengue Fever
de Matos, A. M., Carvalho, K. I., Rosa, D. S., Villas-Boas, L. S., da Silva, W. C., Rodrigues, C. L. D. L., Oliveira, O. M. N. P. F., Levi, J. E., de Araújo, E. S. A., Pannuti, C. S., et al. (2015) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0003520 · Cited by 34
Lorentzen, C. L., & Straten, P. T. (2015) · Scandinavian Journal of Immunology · doi:10.1111/sji.12331 · Cited by 35
Jensen, J. M. B., Holm, M., & Christiansen, M. (2015) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2015.07.047 · Cited by 34
Unusual CD4+CD28−T Cells and Their Pathogenic Role in Chronic Inflammatory Disorders
Lee, G. H., & Lee, W. (2016) · Immune Network · doi:10.4110/in.2016.16.6.322 · Cited by 35
“However, in humans there is a marked loss of CD28 expression on terminally-differentiated effector memory T cells (5).”
BackgroundInfluence of age, sex and HCMV-serostatus on blood lymphocyte subpopulations in healthy adults
Apoil, P. A., Puissant‐Lubrano, B., Congy‐Jolivet, N., Pérès, M., Tkaczuk, J., Roubinet, F., & Blancher, A. (2017) · Cellular Immunology · doi:10.1016/j.cellimm.2017.02.001 · Cited by 34
Time-resolved assessment of single-cell protein secretion by sequencing
Wu, T., Womersley, H. J., Wang, J. R., Scolnick, J. A., & Cheow, L. F. (2023) · Nature Methods · doi:10.1038/s41592-023-01841-y · Cited by 33
Colleton, B. A., Huang, X., Melhem, N. M., Fan, Z., Borowski, L., Rappocciolo, G., & Rinaldo, C. R. (2009) · Journal of Virology · doi:10.1128/jvi.02611-08 · Cited by 34
Developmental Immunology and Role of Host Defenses in Fetal and Neonatal Susceptibility to Infection
Lewis, D. B., & Wilson, C. B. (2010) · Elsevier eBooks · doi:10.1016/b978-1-4160-6400-8.00004-3 · Cited by 35
Acute aerobic exercise in humans increases cytokine expression in CD27− but not CD27+ CD8+ T-cells
LaVoy, E. C., Bosch, J. A., Lowder, T. W., & Simpson, R. J. (2013) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.09.006 · Cited by 33
Immune-surveillance through exhausted effector T-cells
Zehn, D., Utzschneider, D. T., & Thimme, R. (2016) · Current Opinion in Virology · doi:10.1016/j.coviro.2016.01.002 · Cited by 33
Teniente‐Serra, A., Hervás, J. V., Quirant‐Sánchez, B., Mansilla, M. J., Grau‐López, L., Ramo-Tello, C. M., & Martínez-Cáceres, E. M. (2016) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.12548 · Cited by 32
Almanzar, G., Kienle, F., Schmalzing, M., Maas, A., Tony, H., & Prelog, M. (2019) · Lara D. Veeken · doi:10.1093/rheumatology/kez175 · Cited by 33
Application of specialized pro‐resolving mediators in periodontitis and peri‐implantitis: a review
Ali, M., Yang, F., Plachokova, A. S., Jansen, J. A., & Walboomers, X. F. (2021) · European Journal Of Oral Sciences · doi:10.1111/eos.12759 · Cited by 35
“Th1 type responses are promoted by the production of inflammatory mediators (mainly IL- 12 and IFN- γ) by antigen- presenting cells (such as dendritic cells), leading to osteoclastogenesis and bone loss in vivo [71, 72].”
BackgroundKratzer, B., Gattinger, P., Trapin, D., Ettel, P., Körmöczi, U., Rottal, A., Stieger, R. B., Sehgal, A. N. A., Feichter, M., Borochova, K., et al. (2024) · Allergy · doi:10.1111/all.16210 · Cited by 36
“36,37 Interestingly, the changes of T cell subsets were similar in the three Groups of patients with differential antibody decline, with regards to the significant loss of RTE (CD45RA + CD62L + CD31 + ) and the significant gain (except Group 2) of central memory T cells (CD3 + CD45RO + CCR7 + ) of…”
Wang, H., Li, Y., Li, H., Xu, Y. K., Jiang, Z., Lu, F., Hu, W., Fan, Y., Lin, S., & Li, G. (2025) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2024.12.004 · Cited by 34
“T cells can be divided into various subsets via different classification methods [104].”
Clinical consequences of circulating CD28-negative T cells for solid organ transplantation
Betjes, M. G. H. (2015) · Transplant International · doi:10.1111/tri.12658 · Cited by 33
“A substantial part of Tem and almost all Temra cells do not express CD28 [11,13].”
BackgroundVelásquez, S. Y., García, L. F., Opelz, G., Álvarez, C. M., & Süsal, C. (2013) · Transplantation · doi:10.1097/tp.0b013e318296fd69 · Cited by 32
“Effector cells elicit immediate immune responses (2), whereas other cells acquire special features and become memory T cells (3).”
BackgroundAlloreactivity Across HLA Barriers Is Mediated by Both Naïve and Antigen-Experienced T Cells
Melenhorst, J. J., Scheinberg, P., Williams, A., Ambrozak, D. R., Keyvanfar, K., Smith, M. M., McCoy, J. P., Hensel, N. F., Douek, D. C., & Barrett, A. J. (2011) · Transplantation and Cellular Therapy · doi:10.1016/j.bbmt.2010.12.711 · Cited by 32
Zhang, Z., Hara, H., Long, C. E., Iwase, H., Qi, H., Macedo, C., Mangiola, M., Zeevi, A., Ezzelarab, M. B., Ayares, D., et al. (2017) · Transplantation · doi:10.1097/tp.0000000000002060 · Cited by 32
“TEMRA cells (with the same function as TEM cells) are found mostly in peripheral inflamed tissues and can secrete effector molecules in response to antigens.(38) Our data show that, compared with the negative cPRA and healthy human groups, high cPRA patients had the highest frequency of TEMRA cells (among the total CD…”
ResultPapp, G., Szabó, K., Jámbor, I., Mile, M., Berki, A. R., Arany, A. C., Makra, G., Szodoray, P., Csiki, Z., & Balogh, L. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.639308 · Cited by 33
Area under Immunosurveillance: Dedicated Roles of Memory CD8 T-Cell SubsetsPreprint
Vidal, L. P., & van Gisbergen, K. P. J. M. (2020) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a037796 · Cited by 33
Smith‐McCune, K., Chen, J. C., Greenblatt, R. M., Shanmugasundaram, U., Shacklett, B. L., Hilton, J. F., Johnson, B., Irwin, J. C., & Giudice, L. C. (2015) · PLoS ONE · doi:10.1371/journal.pone.0129769 · Cited by 31
Matsuki, F., Saegusa, J., Miyamoto, Y., Misaki, K., Kumagai, S., & Morinobu, A. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.05.120 · Cited by 31
Role of Host Genetic Factors in the Outcome of Hepatitis C Virus Infection
Bengsch, B., Thimme, R., & Blum, H. E. (2009) · Viruses · doi:10.3390/v1020104 · Cited by 31
“The function of CD8+ T cells depends on the maturation stage, which can be assessed by the combination of several differentiation markers linked to T cell functions [94].”
BackgroundDaball, P. C., Ferreira, M. S. V., Ammann, S., Klemann, C., Lorenz, M. R., Warthorst, U., Leahy, T. R., Conlon, N. P., Roche, J., Soler‐Palacín, P., et al. (2018) · Immunology and Cell Biology · doi:10.1111/imcb.12169 · Cited by 32
“However, inhibitory receptors are also highly expressed during the early/intermediate stage of effector differentiation without associated functional deficiencies.(9,27) The pattern of marker expression does not therefore allow discrimination between exhaustion and senescence without additional consideration of functi…”
BackgroundThe IL-7Rα Pathway Is Quantitatively and Functionally Altered in CD8 T Cells in Multiple Sclerosis
Kreft, K. L., Verbraak, E., Wierenga‐Wolf, A. F., van Meurs, M., Oostra, B. A., Laman, J. D., & Hintzen, R. Q. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1102559 · Cited by 30
Maternal—Fetal rejection reactions are unconstrained in preeclamptic women
Nguyen, T., Kahn, D. A., & Loewendorf, A. I. (2017) · PLoS ONE · doi:10.1371/journal.pone.0188250 · Cited by 31
T cell control of inflammaging
Shchukina, I., Boháčová, P., & Artyomov, M. N. (2023) · Seminars in Immunology · doi:10.1016/j.smim.2023.101818 · Cited by 32
Bajwa, M., Vita, S., Vescovini, R., Larsen, M., Sansoni, P., Terrazzini, N., Caserta, S., Thomas, D. W., Davies, K. A., Smith, H. E., et al. (2017) · The Journal of Infectious Diseases · doi:10.1093/infdis/jix080 · Cited by 30
Metadata
- Authors
- Appay, V., van Lier, R. A. W., Sallusto, F., & Roederer, M.
- Affiliations
- Inserm (FR)
- Institute for Research in Biomedicine (CH)
- National Institutes of Health (US)
- Corresponding author
- Appay, Victor
- Venue
- Cytometry Part A
- Publisher
- Wiley
- Published
- 2008-10-22
- Volume
- 73A
- Issue
- 11
- Pages
- 975-983
- ISSN
- 1552-4922 (ISSN-L)
- 1552-4930
- OpenAlex
- W1574493485
- Cited by
- 729
- References
- 76
- Citations by year
- 2026: 12 · 2025: 18 · 2024: 21 · 2023: 24 · 2022: 19 · 2021: 38 · 2020: 45 · 2019: 46 · 2018: 42 · 2017: 47 · 2016: 52 · 2015: 60 · 2014: 51 · 2013: 69 · 2012: 53
- FWCI
- 3.24
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- public-domain
- onlinelibrary.wiley.com/termsAndConditions#vor (vor)
- Locations
- Cytometry Part A (publishedVersion, public-domain)
- PubMed (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Pure Amsterdam UMC (submittedVersion)
- 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 › Virology › HIV Research and Treatment
- Keywords
- T cell subsets, T cell differentiation, T cell heterogeneity, T cell phenotype, T cell function, immune response, infection
- MeSH terms
- Humans, Inflammation, Lymphocyte Activation, Phenotype, T-Lymphocyte Subsets, Consensus
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