Cited by 1,059T-cell and B-cell ImmunologyPsoriasis: Treatment and PathogenesisImmunotherapy and Immune Responses

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Tissue-Resident Memory T Cells

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Schenkel, Jason M., Masopust, David·2014·Immunity

DOI 10.1016/j.immuni.2014.12.007PMC PMC4276131

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Abstract

Tissue-resident memory T (Trm) cells constitute a recently identified lymphocyte lineage that occupies tissues without recirculating. They provide a first response against infections reencountered at body surfaces, where they accelerate pathogen clearance. Because Trm cells are not present within peripheral blood, they have not yet been well characterized, but are transcriptionally, phenotypically, and functionally distinct from recirculating central and effector memory T cells. In this review, we will summarize current knowledge of Trm cell ontogeny, regulation, maintenance, and function and will highlight technical considerations for studying this population.

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Background
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Background
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Background
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BackgroundResultInfluentialSelf-citation
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BackgroundInfluential
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Background
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BackgroundInfluential

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“26 27 However, several studies suggest a functional importance of CD103 expression in antitumor TRM.”
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“29 A study of the aberrant metabolic microenvironment in the context of multiple myeloma revealed that CD69 + STMN1 + CD62L–CD8 + Trm cell-related TCA cycle activity and amino acid metabolism were impaired, whereas glycolysis and FAO were enhanced, 91 corroborating the pivotal effect of FAO on…”
Background
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Background
Inherent Immune Cell Variation Within Colonic Segments Presents Challenges for Clinical Trial Design
Tyler, C. J., Guzmán, M., Lundborg, L. R., Yeasmin, S., Pérez-Jeldres, T., Yarur, A. J., Behm, B. W., Dulai, P. S., Patel, D. R., Bamias, G., et al. (2020) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjaa067 · Cited by 17
ICOS signaling promotes a secondary humoral response after re-challenge with Plasmodium chabaudi chabaudi AS
Latham, L. E., Wikenheiser, D. J., & Stumhofer, J. S. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008527 · Cited by 17
“Populations of CD4 memory T cells are distinguished from one another based on localization and phenotype and include effector (TEM; CD44 CD62LCCR7), central (TCM; CD44 CD62LCCR7IL-7Rα), and tissue-resident (TRM; CD62L IL-7RαCD69CD122) memory [7,8].”
Background
Tauroursodeoxycholic acid (TUDCA) disparate pharmacological effects to lung tissue-resident memory T cells contribute to alleviated silicosis
Li, C. R., He, Y., Zhang, Y., You, Y., Yuan, H.-Y., Wei, Y., Chen, X., & Chen, J. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.113173 · Cited by 17
A lentiviral vector encoding fusion of light invariant chain and mycobacterial antigens induces protective CD4+ T cell immunity
Lopez, J., Anna, F., Authié, P., Pawlik, A., Ku, M., Blanc, C., Souque, P., Moncoq, F., Noirat, A., Hardy, D., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111142 · Cited by 17
PD-1 and ICOS counter-regulate tissue resident regulatory T cell development and IL-10 production during flu
McGee, M. C., Zhang, T., Magazine, N., Islam, R., Carossino, M., & Huang, W. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.984476 · Cited by 17
Re-programming immunosurveillance in persistent non-infectious ocular inflammation
Epps, S. J., Boldison, J., Stimpson, M. L., Khera, T. K., Lait, P. J. P., Copland, D. A., Dick, A. D., & Nicholson, L. B. (2018) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2018.03.001 · Cited by 17
The Naming of Memory T-Cell SubsetsPreprint
Jameson, S. C. (2020) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a037788 · Cited by 17
CD49a Expression Defines Tissue-Resident CD8+ T Cells Poised for Cytotoxic Function in Human Skin
Cheuk, S., Bryceson, Y. T., & Eidsmo, Y. (2018) · immuneACCESS · doi:10.21417/b76k56 · Cited by 19
Guardians and Mediators of Metastasis: Exploring T Lymphocytes, Myeloid-Derived Suppressor Cells, and Tumor-Associated Macrophages in the Breast Cancer Microenvironment
Ruocco, M. R., Gisonna, A., Acampora, V., D'Agostino, A. G., Carrese, B., Santoro, J., Venuta, A., Nasso, R., Rocco, N., Russo, D., et al. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25116224 · Cited by 19
“A population of memory T cells, named tissue-resident memory T (TRM) cells, resides in the tissues and does not recirculate, forming the first line of defense against pathogens [35].”
Background
Liver-Resident Memory CD8+ T Cells: Possible Roles in Chronic HBV Infection
Han, J. W., & Shin, E. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms22010283 · Cited by 18
Tissue-resident immune cells in the pathogenesis of multiple sclerosis
Tian, J., Jiang, L., Chen, Z.-X., Yuan, Q., Liu, C., He, L., Jiang, F., & Rui, K. (2022) · Inflammation Research · doi:10.1007/s00011-022-01677-w · Cited by 18
“CD69 is not only a marker of T cell activation, but also suppresses the expression of S1PR1, a major factor driving T cell influx into the peripheral circulation, thus promoting its residency in tissues [19, 20].”
Background
Nasal Tumor Vaccination Protects against Lung Tumor Development by Induction of Resident Effector and Memory Anti-Tumor Immune Responses
Donkor, M., Choe, J. Y., Reid, D. M., Quinn, B., Pulse, M., Ranjan, A. P., Chaudhary, P., & Jones, H. P. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15020445 · Cited by 17
“Recent evidence supports that some effector T cells do not recirculate but maintain tissue residency and can persist lifelong in tissues after clearing antigens [26,27].”
Background
Tuberculosis Vaccines and T Cell Immune Memory
Li, F., Dang, W., Du, Y., Xu, X., He, P., Zhou, Y., & Zhu, B. (2024) · Vaccines · doi:10.3390/vaccines12050483 · Cited by 19
Islet‐Resident Memory T Cells Orchestrate the Immunopathogenesis of Type 1 Diabetes through the FABP4‐CXCL10 Axis
Wu, X., Cheong, L. Y., Yuan, L., Jin, L., Zhang, Z., Xiao, Y., Zhou, Z., Xu, A., Hoo, R. L. C., & Shu, L. (2024) · Advanced Science · doi:10.1002/advs.202308461 · Cited by 15
Autoimmune Sequelae Following Rituximab Therapy
Kersh, A. E., & Feldman, R. J. (2018) · JCR Journal of Clinical Rheumatology · doi:10.1097/rhu.0000000000000756 · Cited by 16
Recall Responses from Brain-Resident Memory CD8+ T Cells (bTRM) Induce Reactive Gliosis
Prasad, S., Hu, S., Sheng, W. S., Chauhan, P., & Lokensgard, J. R. (2019) · iScience · doi:10.1016/j.isci.2019.10.005 · Cited by 16
“This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). of clearance (Mackay et al., 2013; Masopust et al., 2010; Park and Kupper, 2015; Schenkel and Masopust, 2014).”
BackgroundInfluential
Vaccination and Infection of Swine With Salmonella Typhimurium Induces a Systemic and Local Multifunctional CD4+ T-Cell Response
Schmidt, S., Sassu, E. L., Vatzia, E., Pierron, A., Lagler, J., Mair, K. H., Stadler, M., Knecht, C., Spergser, J., Dolezal, M., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2020.603089 · Cited by 16
“Indeed, it is mainly Tem cells that reach non-lymphoid tissues like the intestine (76, 77).”
Background
Knowledge-based classification of fine-grained immune cell types in single-cell RNA-Seq data
Liu, X., Gosline, S. J. C., Pflieger, L. T., Wallet, P., Iyer, A., Guinney, J., Bild, A. H., & Chang, J. T. (2021) · Briefings in Bioinformatics · doi:10.1093/bib/bbab039 · Cited by 16
Inducing Immunity Where It Matters: Orthotopic HPV Tumor Models and Therapeutic Vaccinations
Zottnick, S., Voß, A. L., & Riemer, A. B. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01750 · Cited by 15
“Its cell composition differs from that in the peripheral blood (28), and the mucosa is typically not accessed by systemically induced T cells (29).”
Background
De novo H3.3K27M-altered diffuse midline glioma in human brainstem organoids to dissect GD2 CAR T cell function
Bessler, N., Wezenaar, A. K. L., Ariese, H. C., Honhoff, C., Dommann, N., Wehrens, E. J., Ruiz-Moreno, C., van den Broek, T. J. M., Collot, R. V. U., Kloosterman, D. J., et al. (2026) · Nature Cancer · doi:10.1038/s43018-025-01084-0 · Cited by 16
“The upregulation of features associated with tissue residency 48 , including the canonical marker CD103 ( ITGAE ) used to identify tissue-resident T cells 61,62 (Fig.”
A new nomogram model for prognosis of hepatocellular carcinoma based on novel gene signature that regulates cross-talk between immune and tumor cells
Wang, Y., Yang, Y., Zhao, Z., Sun, H., Luo, D., Huttad, L., Zhang, B., & Han, B. (2022) · BMC Cancer · doi:10.1186/s12885-022-09465-9 · Cited by 15
“When re-infected, TEM can release IFN-γ, IL-4 and other cytokines and chemokine receptors in a short period to quickly perform immune functions.”
Background
Intestinal CD8 + tissue‐resident memory T cells: From generation to function
Cheng, L., & Becattini, S. (2022) · European Journal of Immunology · doi:10.1002/eji.202149759 · Cited by 17
Tissue-resident memory T cells break tolerance to renal autoantigens and orchestrate immune-mediated nephritis
Arnold, F., Kupferschmid, L., Weissenborn, P., Heldmann, L., Hummel, J. F., Zareba, P., Sagar, Rogg, M., Schell, C., & Tanriver, Y. (2024) · Cellular and Molecular Immunology · doi:10.1038/s41423-024-01197-z · Cited by 15
“Pseudotemporal ordering for the construction of single-cell trajectories was done with monocle3 [74 – 76].”
Method
Non-pathogenic tissue-resident CD8+ T cells uniquely accumulate in the brains of lupus-prone mice
Morawski, P. A., Qi, C., & Bolland, S. M. (2017) · Scientific Reports · doi:10.1038/srep40838 · Cited by 15
Skin immunisation activates an innate lymphoid cell-monocyte axis regulating CD8+ effector recruitment to mucosal tissues
Zaric, M., Becker, P. D., Hervouet, C., Kalcheva, P., Doszpoly, A., Blattman, N. N., Neill, L. A. O., Yus, B. I., Cocita, C., Kwon, S., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09969-2 · Cited by 15
Stability and flexibility in chromatin structure and transcription underlies memory CD8 T-cell differentiation
Diao, H., & Pipkin, M. E. (2019) · F1000Research · doi:10.12688/f1000research.18211.1 · Cited by 14
Single-cell immune profiling reveals a developmentally distinct CD4+ GM-CSF+ T-cell lineage that induces GI tract GVHD
Piper, C., Hainstock, E., Yin-Yuan, C., Chen, Y., Khatun, A., Kasmani, M. Y., Evans, J., Miller, J. A., Gorski, J., Cui, W., et al. (2022) · Blood Advances · doi:10.1182/bloodadvances.2021006084 · Cited by 14
Parabiosis in Mice to Study Tissue Residency of Immune Cells
Wang, H., Gavil, N. V., Koewler, N. J., Masopust, D., & Jameson, S. C. (2022) · Current Protocols · doi:10.1002/cpz1.446 · Cited by 17
Self-citation
Tumor infiltrating CD8/CD103/TIM-3-expressing lymphocytes in epithelial ovarian cancer co-express CXCL13 and associate with improved survival
Vlaming, M. R., Bilemjian, V., Freile, J. Á., Melo, V. A., Plat, A., Huls, G. A., Nijman, H. W., de Bruyn, M., & Bremer, E. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1031746 · Cited by 14
Tissue-resident memory T cells in gastrointestinal tumors: turning immune desert into immune oasis
Liang, M., Wang, X., Cai, D., Guan, W., & Shen, X. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1119383 · Cited by 15
The immunity modulation of transforming growth factor-β in malaria and other pathological process
Wu, S., Nie, Q. H., Tan, S., Liao, G., Lv, Y., Lv, C., Chen, G., & Liu, S. (2023) · International Immunopharmacology · doi:10.1016/j.intimp.2023.110658 · Cited by 14
Tissue-Resident Memory T Cell: Ontogenetic Cellular Mechanism and Clinical Translation
Xu, H., Zhou, R., & Chen, Z. (2023) · Clinical & Experimental Immunology · doi:10.1093/cei/uxad090 · Cited by 17
From the Skin to Distant Sites: T Cells in Psoriatic Disease
Reali, E., & Ferrari, D. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242115707 · Cited by 14
“Both helper CD4 + and cytotoxic CD8 + T RM have been found in the skin [40–45] and also act as responders in autoimmunity as well as in psoriasis and other skin diseases [46].”
Background
Activation of cross-reactive mucosal T and B cell responses in human nasopharynx-associated lymphoid tissue in vitro by Modified Vaccinia Ankara-vectored influenza vaccines
Mullin, J., Ahmed, M. S., Sharma, R. S., Upile, N. S., Beer, H., Achar, P., Puksuriwong, S., Ferrara, F., Temperton, N. J., McNamara, P. S., et al. (2016) · Vaccine · doi:10.1016/j.vaccine.2016.02.028 · Cited by 14
To Go or Stay: The Development, Benefit, and Detriment of Tissue-Resident Memory CD8 T Cells during Central Nervous System Viral Infections
Mockus, T. E., Ren, H. M., Shwetank, & Lukacher, A. E. (2019) · Viruses · doi:10.3390/v11090842 · Cited by 14
“CD8 TRM also adopt a Ly6Clo, CD122lo, CD127-/int, CD62Llo, and granzyme B+ expression profile, but this can also differ with the tissue and the type of virus infection [49].”
Background
Age-dependency of terminal ileum tissue resident memory T cell responsiveness profiles to S. Typhi following oral Ty21a immunization in humans
Booth, J. S., Goldberg, E., Patil, S. A., Barnes, R. S., Greenwald, B. D., & Sztein, M. B. (2021) · Immunity & Ageing · doi:10.1186/s12979-021-00227-y · Cited by 14
Cutting Edge: Skin CCR10+ CD8+ T Cells Support Resident Regulatory T Cells through the B7.2/Receptor Axis To Regulate Local Immune Homeostasis and Response
Fu, Y., Yang, J., & Xiong, N. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1502662 · Cited by 14
Influenza Vaccine–Induced CD4 Effectors Require Antigen Recognition at an Effector Checkpoint to Generate CD4 Lung Memory and Antibody Production
Xia, J., Kuang, Y., Liang, J., Jones, M., & Swain, S. L. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.2000597 · Cited by 14
Redefining Memory T Cell Subsets
Rahimi, R. A., & Luster, A. D. (2020) · Trends in Immunology · doi:10.1016/j.it.2020.06.003 · Cited by 14
“The first discrepancy was clarified by the discovery that a distinct population of memory T cells establishes long-term residence in NLT [3].”
Background
A “Prime and Deploy” Strategy for Universal Influenza Vaccine Targeting Nucleoprotein Induces Lung-Resident Memory CD8 T cells
Chung, H., Kim, E.-A., & Chang, J. (2021) · Immune Network · doi:10.4110/in.2021.21.e28 · Cited by 13
Single-cell profiling of T cells uncovers a tissue-resident memory-like T-cell subset associated with bidirectional prognosis for B-cell acute lymphoblastic leukemia
Lai, W., Wang, X., Liu, L., Xu, L., Mao, L., Tan, J., Zha, X., Zhan, H., Lei, W., Lan, Y., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.957436 · Cited by 13
Mycobacterium bovis BCG Given at Birth Followed by Inactivated Respiratory Syncytial Virus Vaccine Prevents Vaccine-Enhanced Disease by Promoting Trained Macrophages and Resident Memory T Cells
Wang, Y., Ge, F., Wang, J., Li, H., Zheng, B., Li, W., Chen, S., Zheng, X., Deng, Y., Wang, Y., et al. (2023) · Journal of Virology · doi:10.1128/jvi.01764-22 · Cited by 13
“TRM are often identified by the expression of CD69, an early activation marker, and CD103, an aE integrin (19, 20).”
Background
Helicobacter pylori infection reduces the efficacy of cancer immunotherapy: A systematic review and meta‐analysis
Gong, X., Shen, L., Xie, J., Liu, D., Xie, Y., & Liu, D. (2023) · Helicobacter · doi:10.1111/hel.13011 · Cited by 13
“32 Apart from these, Koch et al. found that TRM cells, 33-35 a CD8 + T-cell subset which dominating gastric T cell– driven immune response and providing bacterial control during the early chronic infection stages, had also been found to express PD-1.”
Background
Dynamic establishment of recipient resident memory T cell repertoire after human intestinal transplantation
Jiao, W., Martínez, M., Constanza Bay, M., Zuber, J., Parks, C. A., Obradović, A., Tian, G., Wang, Z., Long, K. D., Waffarn, E., et al. (2024) · EBioMedicine · doi:10.1016/j.ebiom.2024.105028 · Cited by 13
B cells in the pneumococcus-infected lung are heterogeneous and require CD4+ T cell help including CD40L to become resident memory B cells
Etesami, N. S., Barker, K. A., Shenoy, A. T., Ana, C. L. D., Arafa, E. I., Grifno, G. N., Matschulat, A. M., Vannini, M., Pihl, R. M. F., Breen, M. P., et al. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1382638 · Cited by 14
Single-cell analysis reveals lasting immunological consequences of influenza infection and respiratory immunization in the pig lung
Muir, A., Paudyal, B., Schmidt, S., Sedaghat-Rostami, E., Chakravarti, S., Villanueva-Hernández, S., Moffat, K., Polo, N., Angelopoulos, N., Schmidt, A. P., et al. (2024) · PLoS Pathogens · doi:10.1371/journal.ppat.1011910 · Cited by 14
The Major Role of T Regulatory Cells in the Efficiency of Vaccination in General and Immunocompromised Populations: A Review
Stepkowski, S. M., Bekbolsynov, D., Oenick, J., Brar, S., Mierzejewska, B., Rees, M. A., & Ekwenna, O. (2024) · Vaccines · doi:10.3390/vaccines12090992 · Cited by 13
“Representation While T cells express CCR7 to egress NLT, Trm cells remove CCR7 to permanently reside in tissue [18].”
BackgroundInfluential

Authors: Schenkel, J. M., & Masopust, D.
Affiliations: University of Minnesota (US)
Corresponding author: Masopust, David
ORCID: Schenkel, Jason M.
Masopust, David
Venue: Immunity
Publisher: Elsevier BV
Published: 2014-12
Volume: 41
Issue: 6
Pages: 886-897
ISSN: 1074-7613 (ISSN-L)
DOI: 10.1016/j.immuni.2014.12.007
PMC: PMC4276131
OpenAlex: W2046700010
Cited by: 1,059
References: 135
Citations by year: 2026: 74 · 2025: 84 · 2024: 88 · 2023: 92 · 2022: 108 · 2021: 113 · 2020: 103 · 2019: 102 · 2018: 96 · 2017: 81 · 2016: 71 · 2015: 45 · 2014: 1
FWCI: 6.44
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 382 d)
Locations: Immunity (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Allergy and Infectious Diseases (R01AI084913, R01AI111671, R37AI084913, T32AI007313)
National Institute of Diabetes and Digestive and Kidney Diseases (F30DK100159)
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: tissue-resident memory T cells, mucosal immunity, memory T cell differentiation
MeSH terms: Animals, Cell Differentiation, Cell Movement, Humans, Immunity, Immunologic Memory, T-Lymphocytes, T-Lymphocyte Subsets

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Tissue-Resident Memory T Cells

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