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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BackgroundResult
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Background
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Background
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Background
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Background
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Background
Mathematical model reveals the role of memory CD8 T cell populations in recall responses to influenza
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Background
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Background
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Background
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Background
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Background
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Background
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Background
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Result
The Lipopolysaccharide Adjuvant Effect on T Cells Relies on Nonoverlapping Contributions from the MyD88 Pathway and CD11c+ Cells1
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BackgroundMethod
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“Effector memory (TEM) cells have recently been subdivided into conventional CD62LloCD127hi TEM cells, which circulate through nonlymphoid tissues and provide immediate effector response while maintaining multipotent capacity (Sallusto et al., 1999; Masopust et al., 2014), and TE memory (t-TEM) cells, characterized by…”
Background
Tissue Immunity in the Bladder
Bowyer, G., Loudon, K. W., Suchánek, O., & Clatworthy, M. R. (2022) · Annual Review of Immunology · doi:10.1146/annurev-immunol-101220-032117 · Cited by 43
Skin-Resident Memory T Cells: Pathogenesis and Implication for the Treatment of Psoriasis
Vu, T. T., Koguchi‐Yoshioka, H., & Watanabe, R. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10173822 · Cited by 52
“TEM are also dominant in peripheral non-lymphoid tissues and TCM have an affinity for secondary lymphoid organs [2,3].”
Background
A Prime-Pull-Amplify Vaccination Strategy To Maximize Induction of Circulating and Genital-Resident Intraepithelial CD8+ Memory T Cells
Çuburu, N., Kim, R., Guittard, G. C., Thompson, C. D., Day, P. M., Hamm, D. E., Pang, Y.-Y. S., Graham, B. S., Lowy, D. R., & Schiller, J. T. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1800219 · Cited by 45
“Therefore, it could explain the propensities of naive CD8 T cells to proliferate in the dLN and activated CD8 T cells to migrate and proliferate in the cervicovaginal mucosa (53, 54).”
Background
IgG transmitted from allergic mothers decreases allergic sensitization in breastfed offspring
Matson, A. P., Thrall, R. S., Rafti, E., Lingenheld, E. G., & Puddington, L. (2010) · Clinical and Molecular Allergy · doi:10.1186/1476-7961-8-9 · Cited by 37
“Leo Lefrançois (University of CT Health Center, Farmington, CT) and labeling of OVA-specific CD8+ cells was as described [32].”
Potent intestinal Th17 priming through peripheral lipopolysaccharide-based immunization
McAleer, J. P., Liu, B., Li, Z., Ngoi, S., Dai, J., Oft, M., & Vella, A. T. (2010) · Journal of Leukocyte Biology · doi:10.1189/jlb.0909631 · Cited by 36
“Liver lymphocytes were obtained as described previously [39].”
Method
Functional Effector Memory T Cells Enrich the Peritoneal Cavity of Patients Treated with Peritoneal Dialysis
Roberts, G. W., Baird, D. M., Gallagher, K., Jones, R. E., Pepper, C. J., Williams, J. D., & Topley, N. (2009) · Journal of the American Society of Nephrology · doi:10.1681/asn.2008101127 · Cited by 32
Differential CMV-Specific CD8+ Effector T Cell Responses in the Lung Allograft Predominate over the Blood during Human Primary Infection
Pipeling, M., West, E., Osborne, C. M., Whitlock, A., Dropulic, L., Willett, M. H., Forman, M., Valsamakis, A., Orens, J., Moller, D., et al. (2008) · Journal of Immunology · doi:10.4049/jimmunol.181.1.546 · Cited by 39
“Another factor for high effector recruitment into the lung airways may be the tissue site itself, as recent murine studies have demonstrated preferential localization of CD8 and CD4 effector/effector memory T cells in the lung airways and lung parenchyma (16, 38, 39).”
Background
Bystander Central Memory but Not Effector Memory CD8+ T Cells Suppress Allograft Rejection
Ni, W., Dai, H., Wang, T., Moore, Y., Zheng, X. X., & Dai, Z. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.1.113 · Cited by 36
Virtual memory cells make a major contribution to the response of aged influenza-naïve mice to influenza virus infection
Lanzer, K. G., Cookenham, T. S., Reiley, W. W., & Blackman, M. A. (2018) · Immunity & Ageing · doi:10.1186/s12979-018-0122-y · Cited by 38
CD4 T cell depletion substantially augments the rescue potential of PD-L1 blockade for deeply exhausted CD8 T cells
Penaloza-MacMaster, P., Provine, N., Blass, E., & Barouch, D. (2015) · Journal of Immunology · doi:10.4049/jimmunol.1403237 · Cited by 38
“Single-cell suspensions were obtained from blood and tissues as previously described (25).”
Method
T Cell Memory in the Context of Persistent Herpes Viral Infections
Torti, N., & Oxenius, A. (2012) · Viruses · doi:10.3390/v4071116 · Cited by 38
“[8,10,11].”
Shaping Successful and Unsuccessful CD8 T Cell Responses Following Infection
Cox, M. A., & Zajac, A. J. (2010) · BioMed Research International · doi:10.1155/2010/159152 · Cited by 33
“By contrast, central-memory T cells generally express high levels of CCR7 and CD62L, have a higher proliferative capacity, and reside in secondary lymphoid organs [22–24].”
Selectively Reduced Intracellular Proliferation of Salmonella enterica Serovar Typhimurium within APCs Limits Antigen Presentation and Development of a Rapid CD8 T Cell Response1
Albaghdadi, H., Robinson, N., Finlay, B., Krishnan, L., & Sad, S. (2009) · Journal of Immunology · doi:10.4049/jimmunol.0900843 · Cited by 38
Induction of Tolerance to Cardiac Allografts Using Donor Splenocytes Engineered to Display on Their Surface an Exogenous FasL Protein
Yolcu, E., Gu, X., Lacelle, C., Zhao, H., Bandura‐Morgan, L., Askenasy, N., & Shirwan, H. (2008) · Journal of Immunology · doi:10.4049/jimmunol.181.2.931 · Cited by 38
“Also, it is well-established that memory immune cells reside within nonlymphoid target tissues, plausibly to generate a rapid and effective secondary immune response to recurrent infection (41).”
Background
Influenza Virus-Specific Immunological Memory Is Enhanced by Repeated Social Defeat
Mays, J. W., Bailey, M. T., Hunzeker, J. T., Powell, N. D., Papenfuss, T., Karlsson, E. A., Padgett, D. A., & Sheridan, J. F. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0900183 · Cited by 37
Cutting Edge: Memory CD8 T Cell Compartment Grows in Size with Immunological Experience but Nevertheless Can Lose Function
Huster, K. M., Stemberger, C., Gasteiger, G., Kastenmüller, W., Drexler, I., & Busch, D. H. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0902454 · Cited by 37
“stable for the lifetime of an individual mouse (9).”
Highly competent, non-exhausted CD8+ T cells continue to tightly control pathogen load throughout chronic Trypanosoma cruzi infection
Pack, A. D., Collins, M., Rosenberg, C. S., & Tarleton, R. (2018) · PLoS Pathogens · doi:10.1371/journal.ppat.1007410 · Cited by 37
Tissue Distribution of Memory T and B Cells in Rhesus Monkeys following Influenza A Infection
Pichyangkul, S., Yongvanitchit, K., Limsalakpetch, A., Kum-Arb, U., Im‐Erbsin, R., Boonnak, K., Arunee, T., Jongkaewwattana, A., Wiboon-ut, S., Mongkolsirichaikul, D., et al. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1501702 · Cited by 39
Phenotypic Differences in Leucocyte Populations among Healthy Preterm and Full‐Term Newborns
Quinello, C., Silveira-Lessa, A. L., Ceccon, M. E., Cianciarullo, M. A., Carneiro-Sampaio, M., & Palmeira, P. (2014) · Scandinavian Journal of Immunology · doi:10.1111/sji.12183 · Cited by 37
CD8 T Cell Memory Recall Is Enhanced by Novel Direct Interactions with CD4 T Cells Enabled by MHC Class II Transferred from APCs
Romagnoli, P. A., Premenko‐Lanier, M., Loria, G. D., & Altman, J. D. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056999 · Cited by 40
“Cell suspensions and flow cytometry Single cell suspensions as described [60].”
Method
Oral Exposure to Trypanosoma cruzi Elicits a Systemic CD8+T Cell Response and Protection against Heterotopic Challenge
Collins, M. H., Weghe, J. C. V. D., Bustamante, J. M., & Tarleton, R. L. (2011) · Infection and Immunity · doi:10.1128/iai.01080-10 · Cited by 36
“While expression of 7 integrin is key for CD8 T cell homing to the LP and IEL compartments of the gut (30, 37), expression of CD103 ( E integrin) overlaps with that of 7 on Ag-specific CD8 T cells in the gut (38) and has been implicated in the localization of T cells in the intestine (59).”
Background
Hybrid alphavirus–rhabdovirus propagating replicon particles are versatile and potent vaccine vectors
Rose, N. F., Publicover, J., Chattopadhyay, A., & Rose, J. (2008) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0800280105 · Cited by 37
“Responses to VSV N were measured in vaccinated C57BL/6 mice by using the N tetramer (MHC class I Kb) described previously and containing the N peptide N-RGYVYQGL-C (20, 21).”
Method
Listeria Monocytogenes: A Model Pathogen Continues to Refine Our Knowledge of the CD8 T Cell Response
Qiu, Z., Khairallah, C. F., & Sheridan, B. S. (2018) · Pathogens · doi:10.3390/pathogens7020055 · Cited by 53
“Recent studies using an oral infection model of Lm demonstrated the robust induction of antigen-specific CD8 T cell responses in the intestine [47,48,114].”
Background
TCR‐pMHC encounter differentially regulates transcriptomes of tissue‐resident CD8 T cells
Yoshizawa, A., Bi, K., Keskin, D. B., Zhang, G., Reinhold, B. B., & Reinherz, E. L. (2017) · European Journal of Immunology · doi:10.1002/eji.201747174 · Cited by 37
Kinetic and Phenotypic Analysis of CD8+ T Cell Responses after Priming with Alphavirus Replicons and Homologous or Heterologous Booster Immunizations
Knudsen, M., Ljungberg, K., Kakoulidou, M., Kostic, L., Hallengärd, D., García-Arriaza, J., Merits, A., Esteban, M., & Liljeström, P. (2014) · Journal of Virology · doi:10.1128/jvi.02223-14 · Cited by 36
Multifunctional Double-negative T Cells in Sooty Mangabeys Mediate T-helper Functions Irrespective of SIV Infection
Sundaravaradan, V., Saleem, R., Micci, L., Gasper, M. A., Ortiz, A., Else, J., Silvestri, G., Paiardini, M., Aitchison, J., & Sodora, D. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003441 · Cited by 36
“CD62L expression on a T cell induces lymph node homing for the central memory T cells, whereas effector memory cells lose the CD62L expression upon recognition by cognate antigen in order to travel to the site of injury [13,39,40].”
Background
Concurrent Generation of Effector and Central Memory CD8 T Cells during Vaccinia Virus Infection
Laouar, A., Manocha, M., Haridas, V., & Manjunath, N. (2008) · PLoS ONE · doi:10.1371/journal.pone.0004089 · Cited by 36
“secondary lymphoid organs but can also reside in other tissues [7,9,10].”
Background
Sepsis-induced changes in differentiation, maintenance, and function of memory CD8 T cell subsets
Heidarian, M., Griffith, T. S., & Badovinac, V. P. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1130009 · Cited by 41
“However, the expression of lymph node homing receptors CCR7 and CD62L enhance the localization of TCM cells in lymph nodes (LN) and white pulp of spleen, whereas TEM cells are more prevalent in blood, red pulp of spleen, and non-lymphoid tissues (10, 68, 69).”
Background
In Sickness and in Health: The Immunological Roles of the Lymphatic System
Johnson, L. A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094458 · Cited by 40
Expression and role of VLA-1 in resident memory CD8 T cell responses to respiratory mucosal viral-vectored immunization against tuberculosis
Haddadi, S., Thanthrige-Don, N., Afkhami, S., Khera, A., Jeyanathan, M., & Xing, Z. (2017) · Scientific Reports · doi:10.1038/s41598-017-09909-4 · Cited by 38
Heterogeneity within T Cell Memory: Implications for Transplant Tolerance
Krummey, S. M., & Ford, M. L. (2012) · Frontiers in Immunology · doi:10.3389/fimmu.2012.00036 · Cited by 36
“After the contraction phase, CD8+ central memory cells are maintained in lymph tissues due to expression of CD62L and CCR7, while effector memory cells have greater cytotoxic potential and reside in peripheral tissues (Sallusto et al., 1999; Masopust et al., 2001).”
Background
CD8+ T Cells Primed in the Periphery Provide Time-Bound Immune-Surveillance to the Central Nervous System
Young, K. G., MacLean, S., Dudani, R., Krishnan, L., & Sad, S. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1100695 · Cited by 35
“whereas effector memory cells home to nonlymphoid organs (24).”
Background
IFN-γ Induces the Erosion of Preexisting CD8 T Cell Memory during Infection with a Heterologous Intracellular Bacterium1
Dudani, R., Murali-Krishna, K., Krishnan, L., & Sad, S. (2008) · Journal of Immunology · doi:10.4049/jimmunol.181.3.1700 · Cited by 35
“Cells from nonlymphoid organs were obtained after separation on Percoll gradients (26).”
Method
Collaboration between interleukin-7 and -15 enables adaptation of tissue-resident and circulating memory CD8+ T cells to cytokine deficiency
Jarjour, N. N., Dalzell, T. S., Maurice, N. J., Wanhainen, K. M., Peng, C., O’Flanagan, S. D., DePauw, T. A., Block, K. E., Valente, W. J., Ashby, K. M., et al. (2025) · Immunity · doi:10.1016/j.immuni.2025.02.009 · Cited by 41
Self-citation
Injury-induced myosin-specific tissue-resident memory T cells drive immune checkpoint inhibitor myocarditis
Kalinoski, H. M., Daoud, A. R., Rusinkevich, V., Jurčová, I., Talor, M. V., Welsh, R. A., Hughes, D., Zemanová, K., Stříž, I., Hooper, J. E., et al. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2323052121 · Cited by 40
“Tissue - resident memory T (T RM ) cells are the most recently discovered subset of memory T cells; they are noncir-culating and remain resident in the peripheral tissues ( 14 – 16 ).”
Generating long‐lived CD8+ T‐cell memory: Insights from epigenetic programs
Dogra, P., Ghoneim, H. E., Abdelsamed, H. A., & Youngblood, B. (2016) · European Journal of Immunology · doi:10.1002/eji.201545550 · Cited by 38
Current and novel approaches to vaccine development against tuberculosis
Cayabyab, M., Macovei, L., & Campos-Neto, A. (2012) · Front. Cell. Inf. Microbio. · doi:10.3389/fcimb.2012.00154 · Cited by 34
T cell vaccinology: Exploring the known unknowns
Burchill, M. A., Tamburini, B. A. J., Pennock, N. D., White, J. T., Kurche, J. S., & Kedl, R. M. (2012) · Vaccine · doi:10.1016/j.vaccine.2012.10.096 · Cited by 33
Advances in Direct T-Cell Alloreactivity: Function, Avidity, Biophysics and Structure
Smith, C., Miles, J. J., & Khanna, R. (2011) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2011.03863.x · Cited by 33
“This is particularly evident in memory T-cell populations, which respond more rapidly after activation (12,49,50), may be tissue resident (51), can be activated by a diverse range of APCs (52–54) and have a reduced antigen threshold required to induce TCR signaling (50,55,56).”
Background
Barrier immunity and IL-17
Marks, B. R., & Craft, J. E. (2009) · Seminars in Immunology · doi:10.1016/j.smim.2009.03.001 · Cited by 33
“Another important distinction between the αβ T cells that reside in the epithelial surfaces compared to the compartment within the lymph node or spleen is the reduced threshold for activation and rapid response to pathogens[8].”
Background
Are CD8+CD122+ cells regulatory T cells or memory T cells?
Suzuki, H., Shi, Z., Okuno, Y., & Isobe, K. (2008) · Human Immunology · doi:10.1016/j.humimm.2008.08.285 · Cited by 35
Sepsis leads to lasting changes in phenotype and function of memory CD8 T cells
Jensen, I. J., Li, X., McGonagill, P. W., Shan, Q., Fosdick, M. G., Tremblay, M. M., Houtman, J. C. D., Xue, H., Griffith, T. S., Peng, W., et al. (2021) · eLife · doi:10.7554/elife.70989 · Cited by 38
“Among these is the relationship to tissue resident memory CD8 T cells (TRM), which provide sensing and alarm function at sites of prior infection (Masopust et al., 2001; Schenkel et al., 2013).”
Background

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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