☆ 4.6 Review

Axes of heterogeneity in human tissue-resident memory T cells

IMMUNOLOGICAL REVIEWS (2023)

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Article Immunology

Small intestine and colon tissue-resident memory CD8+T cells exhibit molecular heterogeneity and differential dependence on Eomes

Yun Hsuan Lin et al.

Summary: Tissue-resident memory CD8+ T (TRM) cells are a subset of memory T cells that are important for controlling infection. TRM cells in the small intestine and colon exhibit heterogeneity in terms of cytokine and granzyme expression, transcriptional and epigenetic regulation, and functional characteristics. The transcription factor Eomes plays a context-specific role in supporting the maintenance of established TRM cells in the small intestine but not in the colon.

IMMUNITY (2023)

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Article Immunology

Tissue adaptation and clonal segregation of human memory T cells in barrier sites

Maya M. L. Poon et al.

Summary: This study examines the differences in phenotypic, transcriptomic, clonal, and functional characteristics between tissue-resident T cells and circulating T cells in various barrier tissue sites in humans. The findings suggest that circulating T cells are more disseminated and differentiated, while tissue-resident T cells exhibit tissue-specific adaptation and clonal segregation, highlighting the importance of tissue targeting strategies for promoting barrier immunity.

NATURE IMMUNOLOGY (2023)

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Article Cell Biology

The aryl hydrocarbon receptor cell intrinsically promotes resident memory CD8+T cell differentiation and function

Joseph W. Dean et al.

Summary: Ahr acts as a promoter for the differentiation and function of resident memory CD8+ T cells. Ahr deletion diminishes a tumor resident polyfunctional CD8+ T cell population and compromises anti-tumor immunity. AHR in human intestinal intraepithelial CD8+ T cells regulates TRM differentiation and granzyme B production in vitro.

CELL REPORTS (2023)

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Review Immunology

Cellular interactions in resident memory T cell establishment and function

Mohammad H. Hasan et al.

Summary: This article highlights recent studies on cellular interactions that regulate the establishment and function of tissue resident memory T cells (T-RM). A deeper understanding of these processes is instrumental in designing new means to target T-RM for desirable outcomes in infectious diseases, cancers, and autoimmunity.

CURRENT OPINION IN IMMUNOLOGY (2022)

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Article Immunology

Engagement of the costimulatory molecule ICOS in tissues promotes establishment of CD8+tissue-resident T cells

Changwei Peng et al.

Summary: ICOS signaling pathway plays a critical role in the generation of CD8+ tissue-resident memory (Trm) T cells, promoting their production but not affecting their maintenance. This study reveals the importance of costimulatory signals in the generation of tissue-resident populations.

IMMUNITY (2022)

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Review Immunology

Regulation of tissue-resident memory T cells by the Microbiota

Abigail E. Overacre-Delgoffe et al.

Summary: Resident memory T cells (Trms) play a crucial role in rapidly protecting tissues against invasive pathogens and are influenced by the microbiota residing within tissues. The microbiota's influence on Trms is mediated by microbial metabolites and activation of the immune response, but the actual memory potential of these cells remains unclear.

MUCOSAL IMMUNOLOGY (2022)

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Article Gastroenterology & Hepatology

The human liver microenvironment shapes the homing and function of CD4+ T-cell populations

Benjamin G. Wiggins et al.

Summary: This study found that high and intermediate CD69 expressions marked human hepatic CD4(+) T-RM and a novel functionally distinct recirculating population, both shaped by the liver microenvironment to achieve diverse immunosurveillance.

GUT (2022)

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Review Immunology

Liver-resident memory T cells: life in lockdown

Laura J. Pallett et al.

Summary: This article reviews the characteristics and functions of liver-specific memory T cells, including their residency and adaptation to the hepatic microenvironment, as well as their interactions with other cell types. Additionally, the importance of liver sampling for disease monitoring and targeted immunotherapy is discussed.

SEMINARS IN IMMUNOPATHOLOGY (2022)

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Review Immunology

Two sides of the same coin: Protective versus pathogenic CD4+ resident memory T cells

Anna E. Oja et al.

Summary: The ability of the adaptive immune system to form memory is crucial for protection against secondary infections. CD4(+) TRM play important roles in health and disease, including protection against SARS-CoV-2 and potential contributions to immunopathology associated with COVID-19.

SCIENCE IMMUNOLOGY (2022)

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Article Immunology

Tissue-resident memory CD8(+) T cells possess unique transcriptional, epigenetic and functional adaptations to different tissue environments

John T. Crowl et al.

Summary: This study investigates the diversity of gene expression and genome accessibility in mouse CD8(+) T-RM cells in different tissues, and identifies molecules critical for the generation of CD8(+) T-RM cells in response to acute viral infection. The research reveals both common and tissue-specific transcriptional and epigenetic signatures in T-RM cells from different organs. T-RM cells in the intestine and salivary glands express TGF-beta-induced genes and are maintained by ongoing TGF-beta signaling, while those in the fat, kidney, and liver do not. Furthermore, the study identifies the transcriptional repressor Hic1 as a critical regulator of T-RM cell differentiation in the small intestine, and shows that Hic1 overexpression enhances T-RM cell differentiation and protection from infection.

NATURE IMMUNOLOGY (2022)

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Article Immunology

Runx3 drives a CD8+ T cell tissue residency program that is absent in CD4+ T cells

Raissa Fonseca et al.

Summary: Distinct programming of tissue residency in CD8(+) and CD4(+) T-RM cell subsets is regulated by the activity of transcription factor Runx3.

NATURE IMMUNOLOGY (2022)

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News Item Multidisciplinary Sciences

HOW NASAL-SPRAY VACCINES COULD CHANGE THE PANDEMIC

Emily Waltz

Summary: Vaccines that are inhaled through the nose or mouth could potentially halt the spread of the coronavirus, but there is currently limited evidence from human trials.

NATURE (2022)

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Article Immunology

Tissue resident memory T cells- A new benchmark for the induction of vaccine-induced mucosal immunity

Mariah Hassert et al.

Summary: Historically, the induction of neutralizing antibodies in the blood has been the gold-standard benchmark for vaccine immunogenicity. However, there is now growing recognition of the importance of mucosal immunity and tissue resident memory T cells (T-rm) in the early detection and restriction of mucosal pathogens.

FRONTIERS IN IMMUNOLOGY (2022)

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Review Multidisciplinary Sciences

The evolving role of tissue-resident memory T cells in infections and cancer

Sasitorn Yenyuwadee et al.

Summary: Resident memory T cells (T-RM) are a distinct type of T memory cells that stably reside in tissues and have the ability to control local immune homeostasis and participate in immune responses. They have a well-established role in pathogen immunity and potential value in antitumor immune responses and immunotherapy.

SCIENCE ADVANCES (2022)

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Review Immunology

The precursors of CD8(+) tissue resident memory T cells: from lymphoid organs to infected tissues

Lianne Kok et al.

Summary: CD8(+) tissue resident memory T cells are crucial for immune defence against pathogens and malignancies. While it was previously believed that these cells formed locally within inflamed tissue, emerging evidence suggests the existence of circulating T-RM cell precursors. This review discusses the formation of T-RM cells and the signals within the lymphoid compartment that influence their lineage decisions.

NATURE REVIEWS IMMUNOLOGY (2022)

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Article Immunology

CD4+T cells persist for years in the human small intestine and display a TH1 cytokine profile

Raquel Bartolome-Casado et al.

Summary: Studies have shown that the majority of CD4(+)T cells in the transplanted duodenum remain donor-derived resident cells after one year, with a strong cytokine-producing capability mainly as polyfunctional T(H)1 cells. This finding is important for the development of oral vaccines and therapies for gut diseases.

MUCOSAL IMMUNOLOGY (2021)

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Article Biology

Dendritic cells maintain anti-tumor immunity by positioning CD8 skin-resident memory T cells

Jennifer L. Vella et al.

Summary: Dendritic cells play a crucial role in supporting T-RM responses to melanoma, with their close interaction being essential for maintaining immune protection. Chemotaxis and adhesion mediated by the CXCR6/CXCL16 axis are critical for T-RM migration and persistence in the skin, with the interaction between CXCR6-expressing T-RM cells and CXCL16-expressing APCs being pivotal for sustaining T-RM cell-mediated tumor protection.

LIFE SCIENCE ALLIANCE (2021)

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Article Critical Care Medicine

Human Lung-Resident Macrophages Colocalize with and Provide Costimulation to PD1hi Tissue-Resident Memory T Cells

Mark E. Snyder et al.

Summary: EVLP is used to study the spatial and functional relationship between human lung tissue-resident memory T cells and lung-resident macrophages. Human lung T-RM and M-LR colocalize preferentially around the airways, and CD8(+) T(RM) show two functionally distinct populations based on PD1 and ZNF683 protein expression. M-LR provide costimulation signaling to T-RM, enhancing their effector function.

AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE (2021)

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Article Immunology

Competition for Active TGFβ Cytokine Allows for Selective Retention of Antigen-Specific Tissue-Resident Memory T Cells in the Epidermal Niche

Toshiro Hirai et al.

Summary: TGF-beta is essential for the differentiation of skin-recruited CD8(+) T cells into epidermal resident memory T cells and their persistence in the epidermis. Competition for active TGF-beta among T cells promotes the accumulation and long-term persistence of antigen-specific Trm cells in the epidermal niche.

IMMUNITY (2021)

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Article Cell Biology

Human intestinal tissue-resident memory T cells comprise transcriptionally and functionally distinct subsets

Michael E. B. FitzPatrick et al.

Summary: This study investigates the transcriptional, phenotypic, and functional heterogeneity of human intestinal CD4(+) and CD8(+) T-RM cells using donor-derived T-RM cells from intestinal transplant recipients. Single-cell transcriptional profiling identifies two transcriptional states of CD8(+) T-RM cells, delineated by ITGAE and ITGB2 expression. The results describe the differential expression of cytotoxicity- and residency-associated genes in these populations, highlighting the complexity of T-RM cell diversity in the human intestine.

CELL REPORTS (2021)

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Article Immunology

Tissue-resident CD4+ T helper cells assist the development of protective respiratory B and CD8+ T cell memory responses

Young Min Son et al.

Summary: The study reveals a population of tissue-resident helper T cells in the lung, termed as T-RH cells, which play a critical role in promoting the development of protective B cell and CD8(+) T cell responses. These T-RH cells are dependent on transcription factors BCL6 and Bhlhe40 and deliver local help to CD8(+) T cells through IL-21-dependent mechanisms.

SCIENCE IMMUNOLOGY (2021)

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Article Immunology

Influenza, but not SARS-CoV-2, infection induces a rapid interferon response that wanes with age and diminished tissue-resident memory CD8+ T cells

Thi H. O. Nguyen et al.

Summary: The study found that aging leads to a decrease in a specific subset of memory CD8(+) T cells in lung tissue, which results in a weakened antiviral immune response to influenza virus in older donors. However, exposure of human lung cells to SARS-CoV-2 did not activate local immune cells or induce an early interferon response in donors of any age.

CLINICAL & TRANSLATIONAL IMMUNOLOGY (2021)

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Article Immunology

Longitudinal profiling of respiratory and systemic immune responses reveals myeloid cell-driven lung inflammation in severe COVID-19

Peter A. Szabo et al.

Summary: This study investigated the immune responses in the respiratory tract and blood of severe COVID-19 patients, revealing that T cells in the airways showed protective profiles while myeloid cells exhibited hyperinflammatory signatures. These findings provide important insights for understanding and treating COVID-19 lung pathology.

IMMUNITY (2021)

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Article Cell Biology

Heterogeneity of human anti-viral immunity shaped by virus, tissue, age, and sex

Maya M. L. Poon et al.

Summary: The study examined the maintenance and function of virus-specific T cell immunity in the body, showing that virus specificity influences the overall magnitude, tissue distribution, differentiation, and clonal repertoire of virus-specific T cells. Age and sex impact T cell differentiation and dissemination in tissues, while T cell tissue residence and functionality are highly correlated with the site.

CELL REPORTS (2021)

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Article Immunology

Donor NK and T Cells in the Periphery of Lung Transplant Recipients Contain High Frequencies of Killer Cell Immunoglobulin-Like Receptor-Positive Subsets

Anna-Maria Hitz et al.

Summary: In the early post-transplant period after double lung transplantation, higher frequencies of donor NK and T cells expressing KIR in the recipient blood suggest a potential regulatory role in immune balance and graft survival. Higher activation levels of donor NK and T cells also indicate their pre-activation status during the transplantation process.

FRONTIERS IN IMMUNOLOGY (2021)

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Review Immunology

Tissue-resident memory T cells in tumor immunity and immunotherapy

Karolina Okla et al.

Summary: Tissue-resident memory T cells (TRM) reside in peripheral tissues, patrol their surroundings, and rapidly respond to alarming signals. These features enable them to potentially serve as critical players in antitumor surveillance and immunity.

JOURNAL OF EXPERIMENTAL MEDICINE (2021)

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Article Multidisciplinary Sciences

Expansible residence decentralizes immune homeostasis

Sathi Wijeyesinghe et al.

Summary: The immune system in adult mice is integrated within tissues, with a durable maintenance of resident memory T cells contributing to tissue immunity. Tissue pliancy facilitates the accumulation of tissue-resident memory without eroding pre-existing antiviral T cell immunity, resulting in the decentralized homeostasis of organismal immunity.

NATURE (2021)

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Review Immunology

Resident Memory T Cells in Autoimmune Skin Diseases

Grace E. Ryan et al.

Summary: Tissue resident memory T cells (TRM) play a crucial role in the immune system by providing immediate and specific responses against pathogens re-infecting peripheral tissues. However, they have also been found to contribute to autoimmune diseases, where self-antigens continuously activate self-reactive TRM T cells, leading to destructive outcomes. This article focuses on how TRMs mediate disease in autoimmune skin conditions, such as vitiligo, psoriasis, cutaneous lupus erythematosus, alopecia areata, and frontal fibrosing alopecia.

FRONTIERS IN IMMUNOLOGY (2021)

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Article Biochemistry & Molecular Biology

CXCR6 positions cytotoxic T cells to receive critical survival signals in the tumor microenvironment

Mauro Di Pilato et al.

Summary: The conversion of stem-like CTLs into effector-like CTLs involves chemotactic reprogramming with upregulation of chemokine receptor CXCR6. CXCR6 expression and IL-15 trans-presentation are crucial for the survival and local expansion of effector-like CTLs in the tumor microenvironment.

CELL (2021)

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Article Immunology

Discrete tissue microenvironments instruct diversity in resident memory T cell function and plasticity

Susan N. Christo et al.

Summary: Tissue-resident memory T (T-RM) cells are non-recirculating cells distributed throughout the body, and their properties, durability, and malleability are influenced by the tissue in which they are generated. Unequal responsiveness to TGF beta plays a major role in driving diversity in T-RM cell function.

NATURE IMMUNOLOGY (2021)

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Review Immunology

Tissue-specific differentiation of CD8+ resident memory T cells

Kun Yang et al.

Summary: CD8(+) tissue-resident memory T (T-RM) cells exhibit heterogeneity across different tissues, influenced by the activity of tissue-specific molecules; transforming growth factor (TGF)-beta plays a significant role in the generation of T-RM heterogeneity.

TRENDS IN IMMUNOLOGY (2021)

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Review Immunology

LFA-1 in T cell priming, differentiation, and effector functions

Audrey Gerard et al.

Summary: The integrin LFA-1 plays a crucial role in T cell entry into lymph nodes and tissues, interactions with antigen-presenting cells, as well as additional functions such as T-T communication and support of T cell memory. Understanding the biology of LFA-1 and its mechanobiology is important for studying immunological synapses and pathologies related to LFA-1 dysregulation.

TRENDS IN IMMUNOLOGY (2021)

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Article Multidisciplinary Sciences

CD8+ tissue-resident memory T cells promote liver fibrosis resolution by inducing apoptosis of hepatic stellate cells

Yuzo Koda et al.

Summary: The study identified CD8+ tissue-resident memory T cells as key players in resolving liver fibrosis, potentially through Fas-mediated cytotoxicity to eliminate hepatic stellate cells.

NATURE COMMUNICATIONS (2021)

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Article Genetics & Heredity

Maintenance of the human memory T cell repertoire by subset and tissue site

Michelle Miron et al.

Summary: Human memory T cell repertoire exhibits both widespread clone persistence across subsets and sites, as well as clones that are more restricted. CD8(+)T cells show greater clonal expansion and distinct TRBV usage compared to CD4(+)T cell subsets, with extensive sharing of clones between different tissues observed. Tissue-specific biases in clonal similarity are also evident through edit distance analysis.

GENOME MEDICINE (2021)

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Article Immunology

Hobit identifies tissue-resident memory T cell precursors that are regulated by Eomes

Loreto Parga-Vidal et al.

Summary: Tissue-resident memory CD8(+) T cells (T-RM) are a noncirculating memory T cell subset that provides early protection against reinfection. Hobit expression is up-regulated in a subset of LCMV-specific CD8(+) T cells within peripheral tissues, identified as T-RM precursors, with a biased contribution to the T-RM lineage. Transcriptional profiling of Hobit(+) effector T cells revealed the early establishment of T-RM properties.

SCIENCE IMMUNOLOGY (2021)

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Article Medicine, Research & Experimental

Hypoxia acts as an environmental cue for the human tissue-resident memory T cell differentiation program

Farah Hasan et al.

Summary: The combination of hypoxia and TGF-beta(1) can induce the development of a T-RM phenotype in human CD8(+) T cells, leading to specific phenotypic features and enrichment of human T-RM gene signatures. This finding suggests a previously unreported cue for the T-RM differentiation program, offering potential applications in adoptive cellular therapy and basic research.

JCI INSIGHT (2021)

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Functions of human liver CD69+CD103-CD8+ T cells depend on HIF-2α activity in healthy and pathologic livers

Jong Hoon Kim et al.

JOURNAL OF HEPATOLOGY (2020)

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Human Liver Memory CD8+ T Cells Use Autophagy for Tissue Residence

Leo Swadling et al.

CELL REPORTS (2020)

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Fatty Acid Oxidation Controls CD8+ Tissue-Resident Memory T-cell Survival in Gastric Adenocarcinoma

Run Lin et al.

CANCER IMMUNOLOGY RESEARCH (2020)

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TRM integrins CD103 and CD49a differentially support adherence and motility after resolution of influenza virus infection

Emma C. Reilly et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2020)

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CD29 identifies IFN-γ-producing human CD8+ T cells with an increased cytotoxic potential

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Type 1 Treg cells promote the generation of CD8+ tissue-resident memory T cells

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Early precursors and molecular determinants of tissue-resident memory CD8+ T lymphocytes revealed by single-cell RNA sequencing

Nadia S. Kurd et al.

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Organ-specific isoform selection of fatty acid-binding proteins in tissue-resident lymphocytes

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Transcriptional and Functional Analysis of CD1c+ Human Dendritic Cells Identifies a CD163+ Subset Priming CD8+CD103+ T Cells

Pierre Bourdely et al.

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Retrograde migration supplies resident memory T cells to lung-draining LN after influenza infection

J. Michael Stolley et al.

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A committed tissue-resident memory T cell precursor within the circulating CD8+ effector T cell pool

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Longevity and replenishment of human liver-resident memory T cells and mononuclear phagocytes

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Divergence of Tissue-Memory T Cells: Distribution and Function-Based Classification

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CD49a Regulates Cutaneous Resident Memory CD8+ T Cell Persistence and Response

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Long-term skin-resident memory T cells proliferate in situ and are involved in human graft-versus-host disease

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Peripheral and systemic antigens elicit an expandable pool of resident memory CD8+ T cells in the bone marrow

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Human CD8+ T cell cross-reactivity across influenza A, B and C viruses

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Hobit- and Blimp-1-driven CD4+ tissue-resident memory T cells control chronic intestinal inflammation

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Keratinocyte-Mediated Activation of the Cytokine TGF-β Maintains Skin Recirculating Memory CD8+ T Cells

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Tissue patrol by resident memory CD8+ T cells in human skin

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Resident memory CD8 T cells persist for years in human small intestine

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The Functional Requirement for CD69 in Establishment of Resident Memory CD8+ T Cells Varies with Tissue Location

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Characterization of donor and recipient CD8+tissue-resident memory T cells in transplant nephrectomies

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Human CD4+CD103+ cutaneous resident memory T cells are found in the circulation of healthy individuals

Maria M. Klicznik et al.

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Location, location, location: Tissue resident memory T cells in mice and humans

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The Transcription Factor Bhlhe40 Programs Mitochondria! Regulation of Resident CD8+ T Cell Fitness and Functionality

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Interstitial-resident memory CD8+ T cells sustain frontline epithelial memory in the lung

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CXCR6 regulates localization of tissue-resident memory CD8 T cells to the airways

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Tissue-Resident Memory CD8+T Cells Acting as Mediators of Salivary Gland Damage in a Murine Model of Sjogren's Syndrome

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Migratory DCs activate TGF-β to precondition naive CD8+ T cells for tissue-resident memory fate

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Microanatomical dissection of human intestinal T-cell immunity reveals site-specific changes in gut-associated lymphoid tissues over life

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Tissue-Resident Memory T Cells Mediate Immune Homeostasis in the Human Pancreas through the PD-1/PD-L1 Pathway

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Blimp-1 Rather Than Hobit Drives the Formation of Tissue-Resident Memory CD8+ T Cells in the Lungs

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Generation and persistence of human tissue-resident memory T cells in lung transplantation

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Induction of vaginal-resident HIV-specific CD8 T cells with mucosal prime-boost immunization

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Trigger-happy resident memory CD4+ T cells inhabit the human lungs

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Blimp-1 induces and Hobit maintains the cytotoxic mediator granzyme B in CD8 Tcells

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Human Lymph Nodes Maintain TCF-1hi Memory T Cells with High Functional Potential and Clonal Diversity throughout Life

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Human monocytes and macrophages regulate immune tolerance via integrin alpha v beta 8-mediated TGF beta activation

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Tissue-resident memory T cells populate the human brain

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Identification and characterization of HIV-specific resident memory CD8+ T cells in human lymphoid tissue

Marcus Buggert et al.

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