Cited by 1,952T-cell and B-cell ImmunologyImmunotherapy and Immune ResponsesImmune responses and vaccinations

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Preferential Localization of Effector Memory Cells in Nonlymphoid Tissue

Masopust, David, Vezys, Vaiva, Marzo, Amanda L., Lefrançois, Leo·2001·Science

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Abstract

Many intracellular pathogens infect a broad range of host tissues, but the importance of T cells for immunity in these sites is unclear because most of our understanding of antimicrobial T cell responses comes from analyses of lymphoid tissue. Here, we show that in response to viral or bacterial infection, antigen-specific CD8 T cells migrated to nonlymphoid tissues and were present as long-lived memory cells. Strikingly, CD8 memory T cells isolated from nonlymphoid tissues exhibited effector levels of lytic activity directly ex vivo, in contrast to their splenic counterparts. These results point to the existence of a population of extralymphoid effector memory T cells poised for immediate response to infection.

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Background
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“…the study of these subsets has brought a wealth of knowledge on the responsiveness (Bouneaud et al., 2005; Wherry et al., 2007; Hikono et al., 2007; Sallusto et al., 1999), homing (Masopust et al., 2001), and self-renewal capacities (Graef et al., 2014; Gattinoni et al., 2012) of memory cells.”
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Oral immunization induces a novel CXCR6+β7+ intraepithelial lymphocyte subset predominating in the small intestine
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Core Concept: Tissue resident memory cells emerging as key player in health and disease
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Requirement of immune system heterogeneity for protective immunity.
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Apoptosis of antigen-specific CTLs contributes to low immune response in gut-associated lymphoid tissue post vaccination
Shimada, M., Yoshizaki, S., Ichino, M., Klinman, D. M., & Okuda, K. (2014) · Vaccine · doi:10.1016/j.vaccine.2014.07.046 · Cited by 2
“Similar anatomical localization of primary and secondary responses have been observed following site-specific vaccination [43–47], although more global/systemic responses (including CD8 T cell responses) can be elicited by various pathogens and vaccination strategies [30,48,49].”
Background
Gastrointestinal Immunoregulation and the Challenges of Nanotechnology in Foods
Principato, M. (2013) · doi:10.5772/53287 · Cited by 3
“These cells primarily exhibit a cyto‐ lytic function and are recognized residents of the lamina propria, yet retain the ability to dessiminate to various anatomical sites including the gut epithelium following an antigen priming [53].”
Characteristics of CD8+ T cell subsets in Chinese patients with chronic HIV infection during initial ART
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“Here, in our study, we investigated the characteristics of naive (CD45RA +CCR7+), central memory (CM) (CD45RA - CCR7+), effector memory (EM) (CD45RACCR7-), and terminally differentiated effector (EMRA) (CD45RA+ CCR7-) cell subsets [7,8], as well as activation and proliferation levels of each subset, during initial ART…”
Background
Approaches and challenges in targeting memory T cells in transplant tolerance
Chen, M., & Li, X. C. (2007) · Archivum Immunologiae et Therapiae Experimentalis · doi:10.1007/s00005-007-0038-2 · Cited by 2
“the liver, lung, and gut) [4, 18].”
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“CD69 is transiently expressed by early activated T cells but is maintained on tissue-resident T memory effector cells in association with markers such as P2RX7 and CD103 28 – 30 .”
A viral vector prime and protein boost vaccine regimen elicits higher binding antibody titers than a homologous viral vector prime-boost regimen
Awakoaiye, B., Dangi, T., & Penaloza‐MacMaster, P. (2025) · ImmunoHorizons · doi:10.1093/immhor/vlaf027 · Cited by 2
Heterogeneity of CD8αα intraepithelial lymphocytes is transcriptionally conserved between TCRαβ and TCRγδ cell lineages
Hioki, K. A., Liang, X., Lynch, A. C., Ranjan, R., Pobezinskaya, E. L., & Pobezinsky, L. A. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1637209 · Cited by 4
“Additionally, a unique effector-like population within the TCR gd + IELs characterized by Zeb2 , Gzmk , and Ccr5 , was labeled as “ Zeb2 + ” cells (former clusters 9 and 15).”
PI3Kγ signaling controls trafficking of CD8+ T cells between lymphoid and non-lymphoid organs and drives hypertension in a murine model
Perrotta, M., Perrotta, S., Carnevale, L., Migliaccio, A., Pallante, F., Nosalski, R., Guzik, T. J., Fardella, S., Hirsch, E., Fardella, V., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-61009-4 · Cited by 2
“Instead, the subsequent step of migration, responsible for recirculation between lymphoid and non-lymphoid peripheral tissues, is dependent on chemokines typically transduced by G protein-coupled receptors (GPCR) at the cell membrane 12 – 14 .”
Impact of irae characteristics on efficacy of consolidative immunotherapy following chemoradiotherapy in locally advanced NSCLC
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“CD4 + TEMs (CD4 + TCR-β + CD44 + CD62L − ) are a parent subset of TRMs 8,9 and were also increased significantly in immunized mice; thus, it can be stated that TEMs overall—i.e., not only the CD69-positive subset but also the CD69-negative subset —were increased in immunized mice (Fig.”
Chicken adipose tissue is differentially involved in primary and secondary regional immune response to NDV through miR-20a-5p-NR4A3 pathway
Jiang, Y., Zhang, R., Xu, X., Wang, X., Tian, Y., Zhang, W., Ma, X., & Man, C. (2025) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2025.110884 · Cited by 2
mTOR signaling promotes cytokine production in T cells through 3’UTR-mediated translation controlPreprint
Jurgens, A. P., Zwijnen, J., van Alphen, F. P. J., Bradarić, A., Rooijers, K., Hoogendijk, A. J., Popović, B., & Wolkers, M. C. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.10.01.616022 · Cited by 3
Safety and practicality of an excisional lymph node study driving HIV cure research in South Africa
Khaba, T., Papadopoulos, A. O., Nkosi, T., Nxele, S., Ngubane, T., Jajbhay, I., Pansegrouw, J., & Ndhlovu, Z. M. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1442556 · Cited by 4
Location versus ID: what matters to lung-resident memory T cells?
Macedo, B. D. G., Masuda, M. Y., & da Silva, H. B. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1355910 · Cited by 2
“Since their discovery (9, 10), several studies aimed to de ﬁ ne how T RM cells form in the lung, as well as their speci ﬁ c function.”
Background
Homeostatic cytokines reciprocally modulate the emergence of prenatal effector PLZF+CD4+ T cells in humans
Locher, V., Park, S., Bunis, D. G., Makredes, S., Mayer, M., Burt, T. D., Fragiadakis, G. K., & Halkias, J. (2023) · JCI Insight · doi:10.1172/jci.insight.164672 · Cited by 4
“The majority of T cells in mice and humans reside in lymphoid and mucosal tissues, with a heterogeneous distribution of subsets and functions across specific sites (11, 12).”
Background
Immunological characteristics of CD103+CD8+ Tc cells in the liver of C57BL/6 mouse infected with plasmodium NSM
Shi, F., Tang, S., Chen, D., Mo, F., Li, J., Fang, C., Wei, H., Xing, J., Liu, L., Gong, Y., et al. (2023) · Parasitology Research · doi:10.1007/s00436-023-07950-z · Cited by 2
Mycobacterium bovis Wild-Type BCG or Recombinant BCG Secreting Murine IL-18 (rBCG/IL-18) Strains in Driving Immune Responses in Immunocompetent or Immunosuppressed Mice
Fol, M., Włodarczyk, M., Kowalewicz‐Kulbat, M., Druszczyńska, M., Krawczyk, K. T., Wawrocki, S., Rudnicka, W., & Chmiela, M. (2022) · Vaccines · doi:10.3390/vaccines10040615 · Cited by 2
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Background
In vitro Homeostatic Proliferation of Human CD8 T Cells
Abdelsamed, H., Zebley, C. C., & Youngblood, B. (2017) · Bio-protocol · doi:10.21769/bioprotoc.2619 · Cited by 2
“Conversely, the low proliferative effector memory (Tem) subset of CD8 T cells lacks CCR7 expression and has limited access to lymphoid tissue (Sallusto et al., 1999; Masopust et al., 2001).”
Background
Ectromelia virus N1L is essential for virulence but not dissemination in a classical model of mousepox.
Melo-Silva, C. R., Tscharke, D., Lobigs, M., Koskinen, A. M. L., Müllbacher, A., & Regner, M. (2017) · Virus Research · doi:10.1016/j.virusres.2016.11.017 · Cited by 2
The influence of ethanol extract Dioscorea alata L. on CD4+CD62L+ and CD8+CD62L+ profile of BALB/c mice model digestive tract allergy
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Skin TRM mediates distributed border patrol
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Comparison of Human Memory CD8 T Cell Responses to Adenoviral Early and Late Proteins in Peripheral Blood and Lymphoid Tissue
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BackgroundInfluential
Bone Marrow T Cells are Superior to Splenic T Cells to Induce Chimeric Conversion After Non-Myeloablative Bone Marrow Transplantation
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Background
Killing of targets by effector CD8$^+$T cells in the mouse spleen follows the law of mass action
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“This contradicts the widely accepted view that memory CD8T cells, especially those residing in lymphoid tissues, are not very efficient killers and generally require restimulation to exhibit cytotoxicity (32).”
Background
The evolving biology of T cell memory: A dynamic continuum of function and persistence
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Living rent free in your head: resident memory T cells
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Comprehensive Immune-Phenotyping of Peripheral Lymphocytes in Coronary Artery Disease Reveals Potential Roles of Effector Memory and PD-1⁺ CD4⁺ T Cells
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Authors: Masopust, D., Vezys, V., Marzo, A. L., & Lefrançois, L.
Affiliations: UConn Health (US)
Division of Immunology, Department of Medicine, University of Connecticut Health Center, Farmington, CT 06030, USA.
ORCID: Masopust, David
Vezys, Vaiva
Marzo, Amanda L.
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 2001-03-23
Volume: 291
Issue: 5512
Pages: 2413-2417
ISSN: 0036-8075 (ISSN-L)
1095-9203
DOI: 10.1126/science.1058867
OpenAlex: W2081097093
Cited by: 1,952
References: 0
Citations by year: 2026: 23 · 2025: 42 · 2024: 39 · 2023: 36 · 2022: 52 · 2021: 55 · 2020: 67 · 2019: 71 · 2018: 76 · 2017: 65 · 2016: 52 · 2015: 53 · 2014: 69 · 2013: 80 · 2012: 60
FWCI: 42.95
Type: journal article
Language: en
Open access: closed
Locations: Science (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Allergy and Infectious Diseases (AI41576, T32 AI 07080, R01AI041576, T32AI007080)
National Institute of Diabetes and Digestive and Kidney Diseases (DK45260, R01DK045260)
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: effector memory T cells, non-lymphoid tissues, CD8+ T cells, T cell migration, intracellular pathogens, viral infection, bacterial infection, lytic activity
MeSH terms: Animals, Cell Movement, Cells, Cultured, Flow Cytometry, H-2 Antigens, Immunologic Memory, Intestine, Small, Listeriosis, Listeria monocytogenes, Liver, Lung, Lymphocyte Activation, Lymphoid Tissue, Mice, Inbred C57BL, Ovalbumin, Phenotype, Vesicular stomatitis Indiana virus, T-Lymphocyte Subsets, Rhabdoviridae Infections, CD8-Positive T-Lymphocytes, Mice

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Preferential Localization of Effector Memory Cells in Nonlymphoid Tissue

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