Distribution and compartmentalization of human circulating and tissue-resident memory T cell subsets
Open accessAbstract
Knowledge of human T cells derives chiefly from studies of peripheral blood, whereas their distribution and function in tissues remains largely unknown. Here, we present a unique analysis of human T cells in lymphoid and mucosal tissues obtained from individual organ donors, revealing tissue-intrinsic compartmentalization of naive, effector, and memory subsets conserved between diverse individuals. Effector memory CD4(+) T cells producing IL-2 predominated in mucosal tissues and accumulated as central memory subsets in lymphoid tissue, whereas CD8(+) T cells were maintained as naive subsets in lymphoid tissues and IFN-γ-producing effector memory CD8(+) T cells in mucosal sites. The T cell activation marker CD69 was constitutively expressed by memory T cells in all tissues, distinguishing them from circulating subsets, with mucosal memory T cells exhibiting additional distinct phenotypic and functional properties. Our results provide an assessment of human T cell compartmentalization as a new baseline for understanding human adaptive immunity.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The preferred collagenase used by multiple research groups is collagenase IV.
“The preferred collagenase used by multiple research groups is collagenase IV [253, 256, 257, 267].”
From Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition) (2021) · cites this paper as [253]
The Experimental Procedures section (Lymphocyte isolation from human lymphoid and non-lymphoid tissues; page unavailable) specifies collagenase D, not collagenase IV, in this group's digestion solution. The paper therefore contradicts the sentence insofar as it cites this group as an example of collagenase IV use; it does not establish what other groups prefer. (LLM, conf=0.89)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredTrm do not express other putative activation markers, such as CD25, CD137, CD38, or HLA-DR.
“Trm do not express other putative activation markers, such as CD25, CD137, CD38, or HLA-DR [244, 253, 258, 264].”
From Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition) (2021) · cites this paper as [253]
The Discussion (page not available in our copy) says tissue-resident CD69+ human memory T cells were CD25-negative, supporting that part of the claim. The paper does not report whether those cells express CD137, CD38, or HLA-DR; its Flow Cytometry Analysis lists CD25 among the antibodies used but not those three markers. (LLM, conf=0.88)
Experimental — accuracy not yet measuredBoth CD8+ and CD4+ Trm have been identified in human skin, lung, intestines, salivary glands, bone marrow, brain, spleen, tonsils, and lymph nodes.
“Both CD8+ and CD4+ Trm have been identified in the human skin, lung, intestines, salivary glands, bone marrow, brain, spleen, tonsils, and lymph nodes [241, 244, 246, 253-259].”
From Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition) (2021) · cites this paper as [253]
The Results section on CD69 expression identifies resident CD4+ and CD8+ memory T-cell subsets in human lung, intestines, spleen, and lymph nodes (page not available in our copy). The paper discusses skin memory T cells but does not establish the claim for salivary glands, bone marrow, brain, or tonsils; its tissue-sampling list does not include those sites. (LLM, conf=0.88)
Experimental — accuracy not yet measuredResident memory T cells seed tissues in childhood and persist throughout adulthood.
“Seeding into tissues occurs in childhood, and the resident population persists throughout adulthood”
From Successful and Maladaptive T Cell Aging (2017) · cites this paper as Sathaliyawala et al., 2013
Resident memory T cells in lungs, skin, and submucosal sites account for a large fraction of memory cells, numbering more than 5×10^10 cells per person.
“Resident memory T cells in lungs, skin, and submucosal sites account for a large fraction of memory cells numbering more than 5 × 1010 cells in an individual.”
From Successful and Maladaptive T Cell Aging (2017) · cites this paper as Sathaliyawala et al., 2013
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Two subsets of memory T lymphocytes with distinct homing potentials and effector functions
Sallusto, F., Lenig, D., Förster, R., Lipp, M., & Lanzavecchia, A. (1999) · Nature · doi:10.1038/44385 · Cited by 5,846 · see citing works
Korn, T., Bettelli, E., Oukka, M., & Kuchroo, V. K. (2009) · Annual Review of Immunology · doi:10.1146/annurev.immunol.021908.132710 · Cited by 4,873 · see citing works
Induction of Intestinal Th17 Cells by Segmented Filamentous Bacteria
Ivanov, I. I., Atarashi, K., Manel, N., Brodie, E. L., Shima, T., Karaoz, U., Wei, D., Goldfarb, K. C., Santee, C. A., Lynch, S. V., et al. (2009) · Cell · doi:10.1016/j.cell.2009.09.033 · Cited by 4,554 · see citing works
Central Memory and Effector Memory T Cell Subsets: Function, Generation, and Maintenance
Sallusto, F., Geginat, J., & Lanzavecchia, A. (2004) · Annual Review of Immunology · doi:10.1146/annurev.immunol.22.012703.104702 · Cited by 3,067 · see citing works
A human memory T cell subset with stem cell–like properties
Gattinoni, L., Lugli, E., Ji, Y., Pos, Z., Paulos, C. M., Quigley, M. F., Almeida, J. R., Gostick, E., Yu, Z., Carpenito, C., et al. (2011) · Nature Medicine · doi:10.1038/nm.2446 · Cited by 1,974 · see citing works
Preferential Localization of Effector Memory Cells in Nonlymphoid Tissue
Masopust, D., Vezys, V., Marzo, A. L., & Lefrançois, L. (2001) · Science · doi:10.1126/science.1058867 · Cited by 1,952 · cited 1× · see citing works
“CD45RO memory T cells are subdivided into two subsets: CCR7 ‘‘central memory’’ (Tcm) cells, which migrate to lymphoid tissue, and CCR7 ‘‘effector memory’’ (Tem) cells, which circulate to nonlymphoid sites (Masopust et al., 2001; Sallusto et al., 1999, 2004).”
Kaech, S. M., Tan, J. T., Wherry, E. J., Konieczny, B. T., Surh, C. D., & Ahmed, R. (2003) · Nature Immunology · doi:10.1038/ni1009 · Cited by 1,830 · cited 1× · see citing works
“CD69 memory T cells in lymphoid and mucosal sites were largely IL-7R (Figure 4B), indicative of a resting memory T cell phenotype, as IL-7R is downregulated on activated effector T cells (Dooms et al., 2007; Kaech et al., 2003; Paiardini et al., 2005; Seddiki et al., 2006).”
Ivanov, I. I., Frutos, R. D. L., Manel, N., Yoshinaga, K., Rifkin, D. B., Sartor, R. B., Finlay, B. B., & Littman, D. R. (2008) · Cell Host & Microbe · doi:10.1016/j.chom.2008.09.009 · Cited by 1,770 · see citing works
Seddiki, N., Santner-Nanan, B., Martinson, J., Zaunders, J., Sasson, S., Landay, A., Solomon, M., Selby, W., Alexander, S. I., Nanan, R., et al. (2006) · The Journal of Experimental Medicine · doi:10.1084/jem.20060468 · Cited by 1,512 · see citing works
Homeostasis of Naive and Memory T Cells
Surh, C. D., & Sprent, J. (2008) · Immunity · doi:10.1016/j.immuni.2008.11.002 · Cited by 1,193 · see citing works
CD69 acts downstream of interferon-α/β to inhibit S1P1 and lymphocyte egress from lymphoid organs
Shiow, L. R., Rosen, D. B., Brdičková, N., Xu, Y., An, J., Lanier, L. L., Cyster, J. G., & Matloubian, M. (2006) · Nature · doi:10.1038/nature04606 · Cited by 1,189 · see citing works
Gebhardt, T., Wakim, L. M., Eidsmo, L., Reading, P. C., Heath, W. R., & Carbone, F. R. (2009) · Nature Immunology · doi:10.1038/ni.1718 · Cited by 1,157 · see citing works
Skin infection generates non-migratory memory CD8+ TRM cells providing global skin immunity
Jiang, X., Clark, R. A., Liu, L., Wagers, A. J., Fuhlbrigge, R. C., & Kupper, T. S. (2012) · Nature · doi:10.1038/nature10851 · Cited by 883 · see citing works
Dutton, R. W., Bradley, L. M., & Swain, S. L. (1998) · Annual Review of Immunology · doi:10.1146/annurev.immunol.16.1.201 · Cited by 832 · see citing works
Tan, J. T., Ernst, B., Kieper, W. C., LeRoy, E., Sprent, J., & Surh, C. D. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20020066 · Cited by 790 · see citing works
Casey, K. A., Fraser, K. A., Schenkel, J. M., Moran, A. E., Abt, M. C., Beura, L. K., Lucas, P. J., Artis, D., Wherry, E. J., Hogquist, K. A., et al. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1200402 · Cited by 642 · see citing works
Teijaro, J. R., Turner, D., Pham, Q., Wherry, E. J., Lefrançois, L., & Farber, D. L. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1102243 · Cited by 641 · see citing works
Self-citationDynamic T cell migration program provides resident memory within intestinal epithelium
Masopust, D., Choo, D., Vezys, V., Wherry, E. J., Duraiswamy, J., Akondy, R., Wang, J., Casey, K. A., Barber, D. L., Kawamura, K. S., et al. (2010) · Journal of Experimental Medicine · doi:10.1084/jem.20090858 · Cited by 628 · see citing works
Ziegler, S. F., Ramsdell, F., & Alderson, M. R. (1994) · Stem Cells · doi:10.1002/stem.5530120502 · Cited by 535 · see citing works
Mucosal T lymphocyte numbers are selectively reduced in integrin alpha E (CD103)-deficient mice.
Schön, M. P., Arya, A., Murphy, E. A., Adams, C. M., Strauch, U., Agace, W. W., Marsal, J., Donohue, J. P., Her, H., Beier, D. R., et al. (1999) · PubMed · Cited by 424 · see citing works
Mucosal T Lymphocyte Numbers Are Selectively Reduced in Integrin αE (CD103)-Deficient Mice
Schön, M. P., Arya, A., Murphy, E. A., Adams, C. M., Strauch, U., Agace, W. W., Marsal, J., Donohue, J. P., Her, H., Beier, D. R., et al. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.11.6641 · Cited by 399 · see citing works
Dynamics of Blood-Borne CD8 Memory T Cell Migration In Vivo
Klonowski, K. D., Williams, K., Marzo, A. L., Blair, D. A., Lingenheld, E. G., & Lefrançois, L. (2004) · Immunity · doi:10.1016/s1074-7613(04)00103-7 · Cited by 383 · see citing works
Clark, R. A., Watanabe, R., Teague, J. E., Schlapbach, C., Tawa, M. C., Adams, N., Dorosario, A. A., Chaney, K. S., Cutler, C. S., LeBoeuf, N. R., et al. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3003008 · Cited by 367 · see citing works
Type I Interferon-mediated Stimulation of T Cells by CpG DNA
Sun, S., Zhang, X. M., Tough, D. F., & Sprent, J. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.188.12.2335 · Cited by 360 · see citing works
Cutting Edge: Gut Microenvironment Promotes Differentiation of a Unique Memory CD8 T Cell Population
Masopust, D., Vezys, V., Wherry, E. J., Barber, D. L., & Ahmed, R. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.4.2079 · Cited by 357 · see citing works
Hovhannisyan, Z., Treatman, J. D., Littman, D. R., & Mayer, L. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.12.002 · Cited by 339 · see citing works
Purwar, R., Campbell, J. J., Murphy, G. F., Richards, W. G., Clark, R. A., & Kupper, T. S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016245 · Cited by 286 · see citing works
Regional and mucosal memory T cells
Sheridan, B., & Lefrançois, L. (2011) · Nature Immunology · doi:10.1038/ni.2029 · Cited by 281 · see citing works
Th17 cytokines and mucosal immunity
Dubin, P. J., & Kolls, J. K. (2008) · Immunological Reviews · doi:10.1111/j.1600-065x.2008.00703.x · Cited by 262 · see citing works
Liu, L., Zhong, Q., Tian, T., Dubin, K. A., Athale, S., & Kupper, T. S. (2010) · Nature Medicine · doi:10.1038/nm.2078 · Cited by 252 · see citing works
Antiviral CD4+ memory T cells are IL-15 dependent
Purton, J. F., Tan, J. T., Rubinstein, M. P., Kim, D. M., Sprent, J., & Surh, C. D. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20061805 · Cited by 235 · see citing works
Loss of CD127 Expression Defines an Expansion of Effector CD8+ T Cells in HIV-Infected Individuals
Paiardini, M., Cervasi, B., Albrecht, H., Muthukumar, A., Dunham, R. M., Gordon, S. N., Radziewicz, H., Piedimonte, G., Magnani, M., Montroni, M., et al. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.5.2900 · Cited by 233 · see citing works
Interleukin-2 enhances CD4+ T cell memory by promoting the generation of IL-7Rα–expressing cells
Dooms, H., Wolslegel, K., Lin, P. W., & Abbas, A. K. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20062381 · Cited by 170 · see citing works
Hidden memories: Front line memory T cells and early pathogen interception
Masopust, D., & Picker, L. (2012) · Journal of Immunology · doi:10.4049/jimmunol.1102695 · Cited by 163 · see citing works
Bentebibel, S.-E., Schmitt, N., Banchereau, J., & Ueno, H. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100898108 · Cited by 144 · see citing works
Merkenschlager, M., & Beverley, P. C. L. (1989) · International Immunology · doi:10.1093/intimm/1.4.450 · Cited by 139 · see citing works
Targeting T cell responses by selective chemokine receptor expression
Campbell, D., Debes, G. F., Johnston, B., Wilson, E., & Butcher, E. C. (2003) · Seminars in Immunology · doi:10.1016/j.smim.2003.08.005 · Cited by 76 · see citing works
Memory T cells as an occupying force
Bevan, M. (2011) · European Journal of Immunology · doi:10.1002/eji.201041377 · Cited by 73 · see citing works
Krishnan, S. K., Warke, V. G., Nambiar, M. P., Wong, H. K., Tsokos, G. C., & Färber, D. L. (2001) · Blood · doi:10.1182/blood.v97.12.3851 · Cited by 61 · see citing works
Onoe, T., Kalscheuer, H., Chittenden, M., Zhao, G., Yang, Y., & Sykes, M. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0901711 · Cited by 54 · see citing works
Self-citationMarks, B. R., & Craft, J. E. (2009) · Seminars in Immunology · doi:10.1016/j.smim.2009.03.001 · Cited by 33 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Intestinal epithelial cells: regulators of barrier function and immune homeostasis
Peterson, L. W., & Artis, D. (2014) · Nature reviews. Immunology · doi:10.1038/nri3608 · Cited by 3,191 · see citing works
Regional specialization within the intestinal immune system
Mowat, A. M., & Agace, W. W. (2014) · Nature reviews. Immunology · doi:10.1038/nri3738 · Cited by 1,769 · see citing works
Human T cell development, localization, and function throughout life
Kumar, B. V., Connors, T. J., & Farber, D. L. (2018) · Immunity · doi:10.1016/j.immuni.2018.01.007 · Cited by 1,257 · see citing works
Kumar, B. V., Ma, W., Miron, M., Granot, T., Guyer, R. S., Carpenter, D. J., Senda, T., Sun, X., Ho, S.-H., Lerner, H., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.08.078 · Cited by 1,068 · see citing works
Self-citationTissue-Resident Memory T Cells
Schenkel, J. M., & Masopust, D. (2014) · Immunity · doi:10.1016/j.immuni.2014.12.007 · Cited by 1,059 · see citing works
“In this regard, it will be crucial to determine whether the total number of Trm cells established within NLTs is tightly regulated, as it appears to be for Tcm cells within LNs, or whether it is flexible, as shown for Tem cells (Vezys et al., 2009).”
BackgroundInfluentialTissue-resident memory T cells: local specialists in immune defence
Mueller, S. N., & Mackay, L. K. (2016) · Nature Reviews Immunology · doi:10.1038/nri.2015.3 · Cited by 1,006 · see citing works
Guidelines for the use of flow cytometry and cell sorting in immunological studies (second edition)
Cossarizza, A., Chang, H., Radbruch, A., Acs, A., Adam, D., Adam‐Klages, S., Agace, W. W., Aghaeepour, N., Akdiş, M., Allez, M., et al. (2019) · European Journal of Immunology · doi:10.1002/eji.201970107 · Cited by 982 · see citing works
Fuchs, A. G., Vermi, W., Lee, J. S., Lonardi, S., Gilfillan, S., Newberry, R. D., Cella, M., & Colonna, M. (2013) · Immunity · doi:10.1016/j.immuni.2013.02.010 · Cited by 904 · see citing works
Human memory T cells: generation, compartmentalization and homeostasis
Farber, D. L., Yudanin, N. A., & Restifo, N. P. (2014) · Nature Reviews Immunology · doi:10.1038/nri3567 · Cited by 897 · see citing works
Self-citationThe who's who of <scp>T</scp> ‐cell differentiation: Human memory <scp>T</scp> ‐cell subsets
Mahnke, Y. D., Brodie, T. M., Sallusto, F., Roederer, M., & Lugli, E. (2013) · European Journal of Immunology · doi:10.1002/eji.201343751 · Cited by 817 · see citing works
Szabo, P. A., Levitin, H. M., Miron, M., Snyder, M. E., Senda, T., Yuan, J., Cheng, Y. L., Bush, E. C., Dogra, P., Thapa, P., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12464-3 · Cited by 756 · see citing works
The multifaceted role of CD4+ T cells in CD8+ T cell memory
Laidlaw, B. J., Craft, J. E., & Kaech, S. M. (2016) · Nature Reviews Immunology · doi:10.1038/nri.2015.10 · Cited by 657 · see citing works
Location, location, location: Tissue resident memory T cells in mice and humans
Szabo, P. A., Miron, M., & Farber, D. L. (2019) · Science Immunology · doi:10.1126/sciimmunol.aas9673 · Cited by 651 · see citing works
The integration of T cell migration, differentiation and function
Masopust, D., & Schenkel, J. M. (2013) · Nature reviews. Immunology · doi:10.1038/nri3442 · Cited by 629 · see citing works
Innate and Adaptive Immune Memory: an Evolutionary Continuum in the Host’s Response to Pathogens
Netea, M. G., Schlitzer, A., Placek, K., Joosten, L. A. B., & Schultze, J. L. (2019) · Cell Host & Microbe · doi:10.1016/j.chom.2018.12.006 · Cited by 602 · see citing works
Mackay, L. K., Wynne-Jones, E., Freestone, D., Pellicci, D. G., Mielke, L. A., Newman, D. M., Braun, A., Masson, F., Kallies, A., Belz, G. T., et al. (2015) · Immunity · doi:10.1016/j.immuni.2015.11.008 · Cited by 597 · see citing works
Spatial map of human T cell compartmentalization and maintenance over decades of life
Thome, J. J. C., Yudanin, N., Ohmura, Y., Kubota, M., Grinshpun, B., Sathaliyawala, T., Kato, T., Lerner, H., Shen, Y., & Farber, D. L. (2014) · Cell · doi:10.1016/j.cell.2014.10.026 · Cited by 587 · see citing works
Self-citationMolecular regulation of effector and memory T cell differentiation
Chang, J. T., Wherry, E. J., & Goldrath, A. W. (2014) · Nature Immunology · doi:10.1038/ni.3031 · Cited by 578 · see citing works
Watanabe, R., Gehad, A., Yang, C., Scott, L. L., Teague, J. E., Schlapbach, C., Elco, C. P., Huang, V., Matos, T. R., Kupper, T. S., et al. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.3010302 · Cited by 569 · see citing works
Machado-Santos, J., Saji, E., Tröscher, A. R., Paunovic, M., Liblau, R., Gabriely, G., Bien, C. G., Bauer, J., & Lassmann, H. (2018) · Brain · doi:10.1093/brain/awy151 · Cited by 548 · see citing works
Guidelines 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
Understanding subset diversity in T cell memory
Jameson, S. C., & Masopust, D. (2018) · Immunity · doi:10.1016/j.immuni.2018.02.010 · Cited by 523 · see citing works
Ganesan, A.-P., Clarke, J., Wood, O., Garrido-Martin, E. M., Chee, S. J., Mellows, T., Samaniego-Castruita, D., Singh, D., Seumois, G., Alzetani, A., et al. (2017) · Nature Immunology · doi:10.1038/ni.3775 · Cited by 528 · see citing works
The emerging role of resident memory T cells in protective immunity and inflammatory disease
Park, C. O., & Kupper, T. S. (2015) · Nature Medicine · doi:10.1038/nm.3883 · Cited by 514 · see citing works
Rapid effector function of memory CD8+ T cells requires an immediate-early glycolytic switch
Gubser, P. M., Bantug, G. R., Razik, L., Fischer, M., Dimeloe, S., Höenger, G., Müller-Durovic, B., Jauch, A., & Hess, C. (2013) · Nature Immunology · doi:10.1038/ni.2687 · Cited by 487 · see citing works
Programs for the persistence, vigilance and control of human CD8+ lung-resident memory T cells
Hombrink, P., Helbig, C., Backer, R. A., Piet, B., Oja, A. E., Stark, R., Brasser, G., Jongejan, A., Jonkers, R. E., Nota, B., et al. (2016) · Nature Immunology · doi:10.1038/ni.3589 · Cited by 455 · see citing works
Etrolizumab as induction therapy for ulcerative colitis: a randomised, controlled, phase 2 trial
Vermeire, S., O’Byrne, S., Keir, M. E., Williams, M. B., Lu, T. T., Mansfield, J. C., Lamb, C. A., Feagan, B. G., Panés, J., Salas, A., et al. (2014) · The Lancet · doi:10.1016/s0140-6736(14)60661-9 · Cited by 452 · see citing works
Emerging insights into natural killer cells in human peripheral tissues
Björkström, N. K., Ljunggren, H., & Michaëlsson, J. (2016) · Nature reviews. Immunology · doi:10.1038/nri.2016.34 · Cited by 451 · see citing works
Resident memory T cells in human health and disease
Clark, R. A. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.3010641 · Cited by 445 · see citing works
Martin, M. D., & Badovinac, V. P. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02692 · Cited by 432 · see citing works
Edwards, J. J., Wilmott, J. S., Madore, J., Gide, T. N., Quek, C. Y. J., Tasker, A. T., Ferguson, A. L., Chen, J., Hewavisenti, R., Hersey, P., et al. (2018) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-17-2257 · Cited by 431 · see citing works
Zens, K. D., Chen, J. K., & Färber, D. L. (2016) · JCI Insight · doi:10.1172/jci.insight.85832 · Cited by 415 · see citing works
Tissue-resident memory T cells populate the human brain
Smolders, J., Heutinck, K. M., Fransen, N. L., Remmerswaal, E. B. M., Hombrink, P., ten Berge, I. J. M., van Lier, R. A. W., Huitinga, I., & Hamann, J. (2018) · Nature Communications · doi:10.1038/s41467-018-07053-9 · Cited by 406 · see citing works
Lung niches for the generation and maintenance of tissue-resident memory T cells
Turner, D., Bickham, K. L., Thome, J. J. C., Kim, C. Y., D’Ovidio, F., Wherry, E. J., & Färber, D. L. (2013) · Mucosal Immunology · doi:10.1038/mi.2013.67 · Cited by 399 · see citing works
Self-citationDutzan, N., Kajikawa, T., Abusleme, L., Greenwell-Wild, T., Zuazo, C. E., Ikeuchi, T., Brenchley, L., Abe, T., Hurabielle, C., Martin, D., et al. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aat0797 · Cited by 382 · see citing works
β 2 -adrenergic receptor–mediated negative regulation of group 2 innate lymphoid cell responses
Moriyama, S., Brestoff, J. R., Flamar, A.-L., Moeller, J. B., Klose, C. S. N., Rankin, L. C., Yudanin, N. A., Monticelli, L. A., Putzel, G., Rodewald, H.-R., et al. (2018) · Science · doi:10.1126/science.aan4829 · Cited by 379 · see citing works
Self-citationSzabo, P. A., Dogra, P., Gray, J. I., Wells, S. B., Connors, T. J., Weisberg, S. P., Krupska, I., Matsumoto, R., Poon, M. M. L., Idzikowski, E., et al. (2021) · Immunity · doi:10.1016/j.immuni.2021.03.005 · Cited by 371 · see citing works
Laidlaw, B. J., Zhang, N., Marshall, H. D., Staron, M. M., Guan, T., Hu, Y., Cauley, L. S., Craft, J. E., & Kaech, S. M. (2014) · Immunity · doi:10.1016/j.immuni.2014.09.007 · Cited by 366 · see citing works
Successful and Maladaptive T Cell Aging
Goronzy, J. J., & Weyand, C. M. (2017) · Immunity · doi:10.1016/j.immuni.2017.03.010 · Cited by 362 · see citing works
From “truly naïve” to “exhausted senescent” T cells: When markers predict functionality
Larbi, A., & Fulop, T. (2014) · Cytometry Part A · doi:10.1002/cyto.a.22351 · Cited by 359 · see citing works
IL-2high tissue-resident T cells in the human liver: Sentinels for hepatotropic infection
Pallett, L. J., Davies, J., Colbeck, E. J., Robertson, F., Hansi, N., Easom, N. J. W., Burton, A. R., Stegmann, K. A., Schurich, A., Swadling, L., et al. (2017) · Journal of Experimental Medicine · doi:10.1084/jem.20162115 · Cited by 347 · see citing works
Künzli, M., & Masopust, D. (2023) · Nature Immunology · doi:10.1038/s41590-023-01510-4 · Cited by 338 · see citing works
Pathophysiology of Crohn’s disease inflammation and recurrence
Petagna, L., Antonelli, A., Ganini, C., Bellato, V., Campanelli, M., Divizia, A., Efrati, C., Franceschilli, M., Guida, A. M., Ingallinella, S., et al. (2020) · Biology Direct · doi:10.1186/s13062-020-00280-5 · Cited by 324 · see citing works
Park, S. L., Zaid, A., Hor, J. L., Christo, S. N., Prier, J. E., Davies, B., Alexandre, Y. O., Gregory, J. L., Russell, T., Gebhardt, T., et al. (2018) · Nature Immunology · doi:10.1038/s41590-017-0027-5 · Cited by 317 · see citing works
Integrative Physiology of Pneumonia
Quinton, L. J., Walkey, A. J., & Mizgerd, J. P. (2018) · Physiological Reviews · doi:10.1152/physrev.00032.2017 · Cited by 308 · see citing works
Thome, J. J. C., Bickham, K. L., Ohmura, Y., Kubota, M., Matsuoka, N., Gordon, C., Granot, T., Griesemer, A., Lerner, H., Kato, T., et al. (2016) · Nature Medicine · doi:10.1038/nm.4008 · Cited by 305 · see citing works
Self-citationCharacterization of the human immune cell network at the gingival barrier
Dutzan, N., Konkel, J. E., Greenwell-Wild, T., & Moutsopoulos, N. M. (2016) · Mucosal Immunology · doi:10.1038/mi.2015.136 · Cited by 305 · see citing works
Plasticity of Human CD4 T Cell Subsets
Geginat, J., Paroni, M., Maglie, S., Alfen, J. S., Kastirr, I., Gruarin, P., Simone, M. C. D., Pagani, M., & Abrignani, S. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00630 · Cited by 289 · see citing works
Dendritic Cells Display Subset and Tissue-Specific Maturation Dynamics over Human Life
Granot, T., Senda, T., Carpenter, D. J., Matsuoka, N., Weiner, J. I., Gordon, C. L., Miron, M., Kumar, B. V., Griesemer, A. D., Ho, S., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.02.019 · Cited by 284 · see citing works
Self-citationGeneration and persistence of human tissue-resident memory T cells in lung transplantation
Snyder, M. E., Finlayson, M. O., Connors, T. J., Dogra, P., Senda, T., Bush, E. C., Carpenter, D. J., Marboe, C. C., Benvenuto, L. J., Shah, L., et al. (2019) · Science Immunology · doi:10.1126/sciimmunol.aav5581 · Cited by 281 · see citing works
Self-citationUnique aspects of the perinatal immune system
Zhang, X., Zhivaki, D., & Lo-Man, R. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2017.54 · Cited by 276 · see citing works
Chen, Z., Wang, H., D’Souza, C., Sun, S., Kostenko, L., Eckle, S. B. G., Meehan, B. S., Jackson, D. C., Strugnell, R. A., Cao, H., et al. (2016) · Mucosal Immunology · doi:10.1038/mi.2016.39 · Cited by 272 · see citing works
T cell responses in the central nervous system
Korn, T., & Kallies, A. (2017) · Nature Reviews Immunology · doi:10.1038/nri.2016.144 · Cited by 268 · see citing works
Unique phenotypes and clonal expansions of human CD4 effector memory T cells re-expressing CD45RA
Tian, Y., Babor, M., Lane, J., Schulten, V. M. J., Patil, V. S., Seumois, G., Rosales, S. L., Fu, Z., Picarda, G. G. A., Burel, J. G., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-01728-5 · Cited by 267 · see citing works
T Cells in Nonlymphoid Tissues Give Rise to Lymph-Node-Resident Memory T Cells
Beura, L. K., Wijeyesinghe, S., Thompson, E. A., Macchietto, M. G., Rosato, P. C., Pierson, M. J., Schenkel, J. M., Mitchell, J. S., Vezys, V., Fife, B. T., et al. (2018) · Immunity · doi:10.1016/j.immuni.2018.01.015 · Cited by 262 · see citing works
Lung Homeostasis: Influence of Age, Microbes, and the Immune System
Lloyd, C. M., & Marsland, B. J. (2017) · Immunity · doi:10.1016/j.immuni.2017.04.005 · Cited by 254 · see citing works
The germinal centre B cell response to SARS-CoV-2
Laidlaw, B. J., & Ellebedy, A. H. (2021) · Nature reviews. Immunology · doi:10.1038/s41577-021-00657-1 · Cited by 250 · see citing works
Hudspeth, K., Donadon, M., Cimino, M., Pontarini, E., Tentorio, P., Preti, M., Hong, M., Bertoletti, A., Bicciato, S., Invernizzi, P., et al. (2016) · Journal of Autoimmunity · doi:10.1016/j.jaut.2015.08.011 · Cited by 246 · see citing works
Wong, M. T., Ong, D. E. H., Lim, F. S. H., Teng, K. W. W., McGovern, N. N., Narayanan, S., Ho, W. Q., Cerny, D., Tan, H. K. K., Anicete, R., et al. (2016) · Immunity · doi:10.1016/j.immuni.2016.07.007 · Cited by 244 · see citing works
T cells and the skin: from protective immunity to inflammatory skin disorders
Ho, A. W., & Kupper, T. S. (2019) · Nature Reviews Immunology · doi:10.1038/s41577-019-0162-3 · Cited by 241 · see citing works
Human CD8+ T cell cross-reactivity across influenza A, B and C viruses
Koutsakos, M., Illing, P. T., Nguyen, T. H. O., Mifsud, N. A., Crawford, J. C., Rizzetto, S., Eltahla, A. A., Clemens, E. B., Sant, S. A., Chua, B. Y. L., et al. (2019) · Nature Immunology · doi:10.1038/s41590-019-0320-6 · Cited by 239 · see citing works
Single-cell RNA sequencing reveals the heterogeneity of liver-resident immune cells in human
Zhao, J., Zhang, S., Liu, Y., He, X., Qu, M., Xu, G., Wang, H., Huang, M., Pan, J., Liu, Z., et al. (2020) · Cell Discovery · doi:10.1038/s41421-020-0157-z · Cited by 237 · see citing works
CXCR6 marks a novel subset of T-betloEomeshi natural killer cells residing in human liver
Stegmann, K. A., Robertson, F., Hansi, N., Gill, U., Pallant, C., Christophides, T., Pallett, L. J., Peppa, D., Dunn, C., Fusai, G., et al. (2016) · Scientific Reports · doi:10.1038/srep26157 · Cited by 235 · see citing works
The Influence of Lung Microbiota on Lung Carcinogenesis, Immunity, and Immunotherapy
Ramírez-Labrada, A., Isla, D., Artal, A., Arias, M. A., Rezusta, A., Pardo, J., & Gálvez, E. M. (2020) · Trends in cancer · doi:10.1016/j.trecan.2019.12.007 · Cited by 234 · see citing works
Memory CD4+ T Cells in Immunity and Autoimmune Diseases
Raphael, I., Robinson, R. R., & Forsthuber, T. G. (2020) · Cells · doi:10.3390/cells9030531 · Cited by 232 · see citing works
White, K. D., Chung, W., Chung, W., Mallal, S. A., & Phillips, E. J. (2015) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2015.05.050 · Cited by 224 · see citing works
Chimeric Antigen Receptor T Cell Therapy: Challenges to Bench-to-Bedside Efficacy
Srivastava, S., & Riddell, S. R. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1701155 · Cited by 219 · see citing works
Memory CD8+ T cell responses to cancer
Han, J., Khatwani, N., Searles, T. G., Turk, M. J., & Angeles, C. V. (2020) · Seminars in Immunology · doi:10.1016/j.smim.2020.101435 · Cited by 219 · see citing works
A guide to adaptive immune memory
Lam, N., Lee, Y. S., & Färber, D. L. (2024) · Nature reviews. Immunology · doi:10.1038/s41577-024-01040-6 · Cited by 217 · see citing works
Cutting Edge: Resident Memory CD8 T Cells Occupy Frontline Niches in Secondary Lymphoid Organs
Schenkel, J. M., Fraser, K. A., & Masopust, D. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1400003 · Cited by 216 · see citing works
Damouche, A., Lazure, T., Avettand-Fènoël, V., Huot, N., Dejucq‐Rainsford, N., Satié, A.-P., Mélard, A., David, L., Gommet, C., Ghosn, J., et al. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1005153 · Cited by 215 · see citing works
SARS-CoV-2 infection generates tissue-localized immunological memory in humans
Poon, M. M. L., Rybkina, K., Kato, Y., Kubota, M., Matsumoto, R., Bloom, N. I., Zhang, Z., Hastie, K. M., Grifoni, A., Weiskopf, D., et al. (2021) · Science Immunology · doi:10.1126/sciimmunol.abl9105 · Cited by 214 · see citing works
Self-citationTissue‐resident memory T cells
Shin, H., & Iwasaki, A. (2013) · Immunological Reviews · doi:10.1111/imr.12087 · Cited by 206 · see citing works
Tissue‐resident memory T cells in tissue homeostasis, persistent infection, and cancer surveillance
Gebhardt, T., Palendira, U., Tscharke, D. C., & Bedoui, S. (2018) · Immunological Reviews · doi:10.1111/imr.12650 · Cited by 199 · see citing works
Mucosal Resident Memory CD4 T Cells in Protection and Immunopathology
Turner, D., & Färber, D. L. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00331 · Cited by 198 · see citing works
Self-citationDurek, P., Nordström, K. J. V., Gasparoni, G., Salhab, A., Kressler, C., de Almeida, M., Bassler, K. E., Ulas, T., Schmidt, F., Xiong, J., et al. (2016) · Immunity · doi:10.1016/j.immuni.2016.10.022 · Cited by 197 · see citing works
Transcriptional Regulation of Tissue-Resident Lymphocytes
Mackay, L. K., & Kallies, A. (2016) · Trends in Immunology · doi:10.1016/j.it.2016.11.004 · Cited by 196 · see citing works
CD4+ resident memory T cells dominate immunosurveillance and orchestrate local recall responses
Beura, L. K., Fares-Frederickson, N. J., Steinert, E. M., Scott, M. C., Thompson, E. A., Fraser, K. A., Schenkel, J. M., Vezys, V., & Masopust, D. (2019) · Journal of Experimental Medicine · doi:10.1084/jem.20181365 · Cited by 190 · see citing works
Mechanisms Underlying T Cell Immunosenescence: Aging and Cytomegalovirus Infection
Tu, W., & Rao, S. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.02111 · Cited by 189 · see citing works
Human memory T cells from the bone marrow are resting and maintain long-lasting systemic memory
Okhrimenko, A., Grün, J. R., Westendorf, K., Fang, Z., Reinke, S., von Roth, P., Wassilew, G., Kühl, A. A., Kudernatsch, R., Demski, S., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1318731111 · Cited by 188 · see citing works
Tissue-Resident Memory CD8+ T Cells: From Phenotype to Function
Topham, D. J., & Reilly, E. C. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00515 · Cited by 188 · see citing works
Ritzel, R. M., Crapser, J. D., Patel, A. R., Verma, R., Grenier, J. M., Chauhan, A., Jellison, E. R., & McCullough, L. D. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1502021 · Cited by 182 · see citing works
The function and dysfunction of memory CD 8+ T cells in tumor immunity
Reading, J. L., Gálvez‐Cancino, F., Swanton, C., Lladser, Á., Peggs, K. S., & Quezada, S. A. (2018) · Immunological Reviews · doi:10.1111/imr.12657 · Cited by 182 · see citing works
Tissue-resident immune cells in humans
Gray, J. I., & Farber, D. L. (2022) · Annual Review of Immunology · doi:10.1146/annurev-immunol-093019-112809 · Cited by 181 · see citing works
Pizzolla, A., Nguyen, T. H. O., Sant, S. A., Jaffar, J., Loudovaris, T., Mannering, S. I., Thomas, P. G., Westall, G. P., Kedzierska, K., & Wakim, L. M. (2018) · Journal of Clinical Investigation · doi:10.1172/jci96957 · Cited by 181 · see citing works
Wu, Q., Wang, Q., Mao, G., Dowling, C. A., Lundy, S. K., & Mao‐Draayer, Y. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1601532 · Cited by 179 · see citing works
Herndler‐Brandstetter, D., Shan, L., Yao, Y., Stecher, C., Plajer, V., Lietzenmayer, M., Strowig, T., de Zoete, M. R., Palm, N. W., Chen, J., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1705301114 · Cited by 176 · see citing works
Mass Cytometry Imaging for the Study of Human Diseases—Applications and Data Analysis Strategies
Baharlou, H., Canete, N. P., Cunningham, A. L., Harman, A. N., & Patrick, E. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02657 · Cited by 176 · see citing works
Phenotypic signatures of immune selection in HIV-1 reservoir cells
Sun, W., Gao, C., Hartana, C. A., Osborn, M. R., Einkauf, K. B., Lian, X., Bone, B., Bonheur, N., Chun, T., Rosenberg, E. S., et al. (2023) · Nature · doi:10.1038/s41586-022-05538-8 · Cited by 173 · see citing works
An atlas of B-cell clonal distribution in the human body
Meng, W., Zhang, B., Schwartz, G. W., Rosenfeld, A. M., Ren, D., Thome, J. J. C., Carpenter, D. J., Matsuoka, N., Lerner, H., Friedman, A. L., et al. (2017) · Nature Biotechnology · doi:10.1038/nbt.3942 · Cited by 172 · see citing works
Self-citationExit Strategies: S1P Signaling and T Cell Migration
Baeyens, A., Fang, V., Chen, C., & Schwab, S. R. (2015) · Trends in Immunology · doi:10.1016/j.it.2015.10.005 · Cited by 167 · see citing works
Wang, B., Wu, S., Zeng, H., Liu, Z., Dong, W., He, W., Chen, X., Dong, X., Zheng, L., Lin, T., et al. (2015) · The Journal of Urology · doi:10.1016/j.juro.2015.02.2941 · Cited by 166 · see citing works
Antigen Presentation by Vascular Cells
Pober, J. S., Merola, J., Liu, R., & Manes, T. D. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01907 · Cited by 165 · see citing works
Vesely, M. C. A., Pallis, P., Bielecki, P., Low, J. S., Zhao, J., Harman, C. C. D., Kroehling, L., Jackson, R. P., Bailis, W., Licona-Limón, P., et al. (2019) · Cell · doi:10.1016/j.cell.2019.07.032 · Cited by 165 · see citing works
Long-term maintenance of human naive T cells through in situ homeostasis in lymphoid tissue sites
Thome, J. J. C., Grinshpun, B., Kumar, B. V., Kubota, M., Ohmura, Y., Lerner, H., Sempowski, G. D., Shen, Y., & Farber, D. L. (2016) · Science Immunology · doi:10.1126/sciimmunol.aah6506 · Cited by 162 · see citing works
Self-citationBuggert, M., Nguyen, S., de Oca, G. S. M., Bengsch, B., Darko, S. W., Ransier, A., Roberts, E. R., Alcazar, D. D., Brody, I. B., Vella, L. A., et al. (2018) · Science Immunology · doi:10.1126/sciimmunol.aar4526 · Cited by 162 · see citing works
Trigger-happy resident memory CD4+ T cells inhabit the human lungs
Oja, A. E., Piet, B., Helbig, C., Stark, R., van der Zwan, D., Blaauwgeers, H., Remmerswaal, E. B. M., Amsen, D., Jonkers, R. E., Moerland, P. D., et al. (2018) · Mucosal Immunology · doi:10.1038/mi.2017.94 · Cited by 160 · see citing works
PET of Adoptively Transferred Chimeric Antigen Receptor T Cells with 89 Zr-Oxine
Weist, M. R., Starr, R., Aguilar, B., Chea, J., Miles, J. K., Poku, E. K., Gerdts, E. A., Yang, X., Priceman, S. J., Forman, S. J., et al. (2018) · Journal of Nuclear Medicine · doi:10.2967/jnumed.117.206714 · Cited by 159 · see citing works
IL-17 in the immunopathogenesis of spondyloarthritis
Taams, L. S., Steel, K. J. A., Srenathan, U., Burns, L. A., & Kirkham, B. W. (2018) · Nature Reviews Rheumatology · doi:10.1038/s41584-018-0044-2 · Cited by 159 · see citing works
Tissue adaptation and clonal segregation of human memory T cells in barrier sites
Poon, M. M. L., Caron, D. P., Wang, Z., Wells, S. B., Chen, D., Meng, W., Szabo, P. A., Lam, N., Kubota, M., Matsumoto, R., et al. (2023) · Nature Immunology · doi:10.1038/s41590-022-01395-9 · Cited by 157 · see citing works
Self-citation
- Authors
- Sathaliyawala, T., Kubota, M., Yudanin, N., Turner, D., Camp, P., Thome, J. J. C., Bickham, K. L., Lerner, H., Goldstein, M., Sykes, M., Kato, T., & Farber, D. L.
- Affiliations
- Columbia University Irving Medical Center (US)
- ORCID
- Venue
- Immunity
- Publisher
- Elsevier BV
- Published
- 2013-01
- Volume
- 38
- Issue
- 1
- Pages
- 187-197
- ISSN
- 1074-7613 (ISSN-L)
- PMC
- PMC3557604
- OpenAlex
- W2082595913
- Cited by
- 848
- References
- 41
- Citations by year
- 2026: 33 · 2025: 39 · 2024: 50 · 2023: 54 · 2022: 74 · 2021: 77 · 2020: 78 · 2019: 96 · 2018: 95 · 2017: 75 · 2016: 69 · 2015: 47 · 2014: 40 · 2013: 20
- FWCI
- 14.97
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Immunity (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Allergy and Infectious Diseases (RC1AI086164)
- National Center for Research Resources (S10RR027050)
- 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 compartmentalization, mucosal immunity, lymphoid tissue, effector memory T cells, central memory T cells, naive T cells, CD4+ T cells, CD8+ T cells, interleukin-2, interferon-gamma, CD69, T cell activation, tissue-resident T cells
- MeSH terms
- CD69 Antigens, Adolescent, Adult, Age Factors, Antigens, Differentiation, T-Lymphocyte, Female, Humans, Immunologic Memory, Male, Middle Aged, Mucous Membrane, Organ Specificity, Tissue Donors, CD4-Positive T-Lymphocytes, Antigens, CD, Immunophenotyping, T-Lymphocyte Subsets, CD8-Positive T-Lymphocytes, Lectins, C-Type, Integrin alpha Chains, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
