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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Background
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Background
The TNF Superfamily Molecule LIGHT Promotes the Generation of Circulating and Lung-Resident Memory CD8 T Cells following an Acute Respiratory Virus Infection
Desai, P., Tahiliani, V., Hutchinson, T. E., Dastmalchi, F., Stanfield, J., Abboud, G., Thomas, P. G., Ware, C. F., Song, J. J., Croft, M., et al. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1701499 · Cited by 27
“Adding to this growing complexity, resident memory T cells (TRM) can become committed to permanent retention within the tissue to which they localize (11), and they have been suggested to enhance the recruitment of circulating”
Background
Diminished CD103 (aEb7) Expression on Resident T cells from the Female Genital Tract of HIV-positive women
Moylan, D. C., Goepfert, P., Kempf, M.-C., Saag, M. S., Richter, H. E., Mestecky, J. F., & Sabbaj, S. (2017) · Pathogens and Immunity · doi:10.20411/pai.v1i2.166 · Cited by 29
“The expression of αEβ7 (mucosal retention receptor, CD103), and the downregulation of CCR7 and CD62L (lymph node homing receptors) are known mechanisms leading to the maintenance of cells in mucosal tissue such as the lung, gut, and genital tract [1-5].”
Background
Visualizing T Cell Migration in situ
Benechet, A. P., Menon, M., & Khanna, K. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00363 · Cited by 26
Memory T Cells in Transplantation
Su, C. A., & Fairchild, R. L. (2014) · Current Transplantation Reports · doi:10.1007/s40472-014-0018-5 · Cited by 24
Epithelial HVEM maintains intraepithelial T cell survival and contributes to host protection
Seo, G., Takahashi, D., Wang, Q., Mikulski, Z., Chen, A., Chou, T.-F., Marcovecchio, P., McArdle, S., Sethi, A., Shui, J., et al. (2022) · Science Immunology · doi:10.1126/sciimmunol.abm6931 · Cited by 31
TLR4 signaling improves PD-1 blockade therapy during chronic viral infection
Wang, Y., Chung, Y. R., Eitzinger, S., Palacio, N. M., Gregory, S., Bhattacharyya, M., & Penaloza‐MacMaster, P. (2019) · PLoS Pathogens · doi:10.1371/journal.ppat.1007583 · Cited by 24
An animated landscape representation of CD4+ T‐cell differentiation, variability, and plasticity: Insights into the behavior of populations versus cells
Rebhahn, J. A., Deng, N., Gaurav Sharma, A., Livingstone, A. M., Huang, S., & Mosmann, T. R. (2014) · European Journal of Immunology · doi:10.1002/eji.201444645 · Cited by 26
Heterogeneous Memory T Cells in Antiviral Immunity and Immunopathology
Verhoeven, D. E., Teijaro, J. R., & Färber, D. L. (2008) · Viral Immunology · doi:10.1089/vim.2007.0002 · Cited by 29
“Lung memory CD4 and CD8 T cells produce higher levels of IFN-(cid:2) compared to counterparts in peripheral blood or secondary lymphoid organs (16,86), and may be particularly adapted to mediate effective protective responses in situ .”
Differential Microenvironment Localization of Effector and Memory CD8 T Cells
Dauner, J. G., Williams, I. R., & Jacob, J. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.1.291 · Cited by 21
“The trafficking of CD8 T cell populations between various tissues during Ag-induced differentiation is well understood (11).”
Background
A Universal Strategy of Anti‐Tumor mRNA Vaccine by Harnessing “Off‐the‐Shelf” Immunity
Fu, J., Wu, S., Bao, N., Wu, L. J., Qu, H., Wang, Z., Dong, H., Wu, J. F., & Jin, Y. (2025) · Advanced Science · doi:10.1002/advs.202401287 · Cited by 20
From PsO to PsA: the role of TRM and Tregs in psoriatic disease, a systematic review of the literature
Lobão, B., Lourenço, D., Giga, A., & Mendes‐Bastos, P. (2024) · Frontiers in Medicine · doi:10.3389/fmed.2024.1346757 · Cited by 30
A Correlation Between Differentiation Phenotypes of Infused T Cells and Anti-Cancer Immunotherapy
Ren, H., Cao, K., & Wang, M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.745109 · Cited by 30
“Tscm and Tcm, which lack immediate effector function but rapidly proliferate in secondary responses, express CD62L and are found in lymph nodes, whereas effector memory T cells with immediate effector function, lack CD62L and are found in blood, peripheral tissues and spleen but not in lymph nodes (36, 37).”
Background
An exhausted phenotype of TH2 cells is primed by allergen exposure, but not reinforced by allergen‐specific immunotherapy
Wang, S., Zissler, U. M., Büttner, M., Heine, S., Heldner, A., Kotz, S., Pechtold, L., Kau, J., Plaschke, M., Ullmann, J. T., et al. (2021) · Allergy · doi:10.1111/all.14896 · Cited by 37
Lower activation of CD4+ memory T cells in preeclampsia compared to healthy pregnancies persists postpartum
Kieffer, T. E. C., Scherjon, S. A., Faas, M. M., & Prins, J. R. (2019) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2019.102613 · Cited by 28
A fixed spatial structure of CD8+ T cells in tissue during chronic HSV-2 infection
Schiffer, J., Swan, D. A., Roychoudhury, P., Lund, J. M., Prlic, M., Zhu, J., Wald, A., & Corey, L. (2018) · Journal of Immunology · doi:10.4049/jimmunol.1800471 · Cited by 24
Phenotype and Tissue Residency of Lymphocytes in the Murine Oral Mucosa
Park, J., Chung, H., Choi, Y., & Park, J.-H. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00250 · Cited by 23
Characterization of the HCMV-Specific CD4 T Cell Responses that Are Associated with Protective Immunity
Wunsch, M., Zhang, W., Hanson, J., Caspell, R., Karulin, A. Y., Recks, M. S., Küerten, S., Sundararaman, S., & Lehmann, P. (2015) · Viruses · doi:10.3390/v7082828 · Cited by 20
“Antigen-specific T cells are typically in a resting state in the blood (in PBMC), and such cells do not secrete cytokines [32,33].”
Background
An Excess of the Proinflammatory Cytokines IFN-γ and IL-12 Impairs the Development of the Memory CD8+ T Cell Response to Chlamydia trachomatis
Zhang, X., & Starnbach, M. N. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1500457 · Cited by 22
“TEM are thought to provide immediate effector function at the portal of pathogen entry but exhibit reduced proliferative capacity (62).”
Background
Cytokine Diversity in the Th1-Dominated Human Anti-Influenza Response Caused by Variable Cytokine Expression by Th1 Cells, and a Minor Population of Uncommitted IL-2+IFNγ- Thpp Cells
Deng, N., Weaver, J. M., & Mosmann, T. R. (2014) · PLoS ONE · doi:10.1371/journal.pone.0095986 · Cited by 21
“Tcm and T effector memory cells (Tem) migrate preferentially to secondary lymphoid tissue and peripheral tissues, respectively [38,39].”
Background
Homeostatic cytokines orchestrate the segregation of CD4 and CD8 memory T-cell reservoirs in mice.
Yang, L.-L., Yu, Y., Kalwani, M., Tseng, T.-W. J., & Baltimore, D. (2011) · Blood · doi:10.1182/blood-2011-04-349746 · Cited by 24
“Based on their expression of CD62L and CCR7, both CD4 and CD8 TMs can be divided into TCMs and TEMs.(28,29) Despite the classic definition that TCMs home to LNs while TEMs home to peripheral tissues, analysis of MP CD4 and CD8 TEMs (CD62L ) and TCMs (CD62L ) in aged mice revealed the presence of both TEMs and TCMs in…”
BackgroundInfluential
Mucosal associated invariant T cells and the immune response to infection
Gold, M. C., & Lewinsohn, D. M. (2011) · Microbes and Infection · doi:10.1016/j.micinf.2011.03.007 · Cited by 23
“Conventional memory T cells, as well as iNKT cells, preferentially localize to non-lymphoid tissueswhere they display an activated effector phenotype [4,38].”
Background
From the thymus to longevity in the periphery
Wakim, L. M., & Bevan, M. J. (2010) · Current Opinion in Immunology · doi:10.1016/j.coi.2010.03.003 · Cited by 27
Consideration of strategies for hematopoietic cell transplantation.
Yaniv, I., Ash, S., Farkas, D., Askenasy, N., & Stein, J. (2009) · Journal of Autoimmunity · doi:10.1016/j.jaut.2009.09.002 · Cited by 24
Differentiation of Central Memory CD8 T Cells Is Independent of CD62L-Mediated Trafficking to Lymph Nodes
Wirth, T. C., Badovinac, V. P., Zhao, L., Dailey, M. O., & Harty, J. T. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0803315 · Cited by 28
“Although effector memory cells retain low levels of surface CD62L and continue to travel through tertiary tissues, central memory T cells regain expression of both CD62L and CCR7 and are thus granted access to lymph nodes in addition to tertiary tissues (11, 12).”
Background
The Roles of CD8 Central and Effector Memory T-Cell Subsets in Allograft Rejection
Oberbarnscheidt, M. H., Ng, Y. ‐., & Chalasani, G. (2008) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2008.02335.x · Cited by 25
CD8+ Tissue-Resident Memory T Cells: Versatile Guardians of the Tissue
Tovar, G. M., Gallen, C., & Bergsbaken, T. (2024) · The Journal of Immunology · doi:10.4049/jimmunol.2300399 · Cited by 27
Shaping Heterogeneity of Naive CD8+ T Cell Pools
Lee, S., Lee, G.-W., Kim, H.-O., & Cho, J.-H. (2023) · Immune Network · doi:10.4110/in.2023.23.e2 · Cited by 23
Tissue-Resident Memory T Cells in Skin Diseases: A Systematic Review
Emmanuel, T., Mistegård, J., Bregnhøj, A., Johansen, C., & Iversen, L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22169004 · Cited by 30
Dietary Regulation of Memory T Cells
Collins, N. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21124363 · Cited by 25
“These highly functional cells are found throughout the body [100] but are particularly enriched within epithelial layers of barrier tissues such as the intestine, lung, reproductive tract and skin [5,46,101], sites densely populated with commensal bacteria.”
Background
The impact of oxidative stress, inflammation, and senescence on the maintenance of immunological memory in the bone marrow in old age
Naismith, E., & Pangrazzi, L. (2019) · Bioscience Reports · doi:10.1042/bsr20190371 · Cited by 24
Tissue-specific programming of memory CD8 T cell subsets impacts protection against lethal respiratory virus infection
Abboud, G., Desai, P., Dastmalchi, F., Stanfield, J., Tahiliani, V., Hutchinson, T. E., & Salek‐Ardakani, S. (2016) · The Journal of Experimental Medicine · doi:10.1084/jem.20160167 · Cited by 24
“…recirculate through the blood and secondary lymphoid organs, or effector memory cells (CCR7loCD62Llo; Tem) that transit through blood and peripheral tissues, such as the lung (Sallusto et al., 1999; Masopust et al., 2001; Jameson and Masopust, 2009; Sathaliyawala et al., 2013; Thome et al., 2014).”
Background
The smallest unit: effector and memory CD8+ T cell differentiation on the single cell level
Buchholz, V. R., Gräf, P., & Busch, D. H. (2013) · Frontiers in Immunology · doi:10.3389/fimmu.2013.00031 · Cited by 27
High-Quality CMV-Specific CD4+ Memory Is Enriched in the Lung Allograft and Is Associated With Mucosal Viral Control
Akulian, J., Pipeling, M., John, E. R., Orens, J., Lechtzin, N., & McDyer, J. (2012) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2012.04282.x · Cited by 23
“These findings differ somewhat from previous findings in the mouse showing preferential localization of CD8+ effector memory T cells at nonlymphoid sites including the lung (25).”
Result
T inflammatory memory CD8 T cells participate to antiviral response and generate secondary memory cells with an advantage in XCL1 production
Jubin, V., Ventre, E., Leverrier, Y., Djebali, S., Mayol, K., Tomkowiak, M., Mafille, J., Teixeira, M., Teoh, D., Lina, B., et al. (2012) · Immunologic research · doi:10.1007/s12026-012-8340-4 · Cited by 23
“On the other hand, effector memory T cells (TEM) express a panel of adhesion molecules and chemokine receptors that allow their recirculation to the periphery and inflamed tissues and are indeed found in non-lymphoid organs [18, 19].”
Background
Unique features of memory T cells in HIV elite controllers: a systems biology perspective
Fonseca, S. G., Procopio, F. A., Goulet, J.-P., Yassine‐Diab, B., Ancuța, P., & Sékaly, R. (2011) · Current Opinion in HIV and AIDS · doi:10.1097/coh.0b013e32834589a1 · Cited by 24

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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