Tissue-resident memory T cells: local specialists in immune defence

Two subsets of memory T lymphocytes with distinct homing potentials and effector functions

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Modulating Innate and Adaptive Immunity by (R)-Roscovitine: Potential Therapeutic Opportunity in Cystic Fibrosis

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Preferential Localization of Effector Memory Cells in Nonlymphoid Tissue

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Lineage relationship and protective immunity of memory CD8 T cell subsets

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Inflammation Directs Memory Precursor and Short-Lived Effector CD8+ T Cell Fates via the Graded Expression of T-bet Transcription Factor

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Immunological memory and protective immunity: understanding their relation

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Transcriptional control of effector and memory CD8+ T cell differentiation

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The developmental pathway for CD103+CD8+ tissue-resident memory T cells of skin

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Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin

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Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus

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Tissue-Resident Memory T Cells

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Visualizing the generation of memory CD4 T cells in the whole body

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Control of Effector CD8 + T Cell Function by the Transcription Factor Eomesodermin

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Intraepithelial Type 1 Innate Lymphoid Cells Are a Unique Subset of IL-12- and IL-15-Responsive IFN-γ-Producing Cells

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Skin infection generates non-migratory memory CD8+ TRM cells providing global skin immunity

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Distribution and compartmentalization of human circulating and tissue-resident memory T cell subsets

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Exogenous Stimuli Maintain Intraepithelial Lymphocytes via Aryl Hydrocarbon Receptor Activation

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Commensal–dendritic-cell interaction specifies a unique protective skin immune signature

Naik, S., Bouladoux, N., Linehan, J. L., Han, S.-J., Harrison, O. J., Wilhelm, C., Conlan, S., Himmelfarb, S., Byrd, A. L., Deming, C., et al. (2015) · Nature · doi:10.1038/nature14052 · Cited by 820

Transcriptional downregulation of S1pr1 is required for the establishment of resident memory CD8+ T cells

Skon, C. N., Lee, J.-Y., Anderson, K. G., Masopust, D., Hogquist, K. A., & Jameson, S. C. (2013) · Nature Immunology · doi:10.1038/ni.2745 · Cited by 817

Intravascular staining for discrimination of vascular and tissue leukocytes

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The Vast Majority of CLA+ T Cells Are Resident in Normal Skin

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Naive and memory T cells show distinct pathways of lymphocyte recirculation.

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Resident memory CD8 T cells trigger protective innate and adaptive immune responses

Schenkel, J. M., Fraser, K. A., Beura, L. K., Pauken, K. E., Vezys, V., & Masopust, D. (2014) · Science · doi:10.1126/science.1254536 · Cited by 731

Differentiation and persistence of memory CD8+ T cells depend on T cell factor 1

Zhou, X.-Y., Yu, S.-Y., Zhao, D.-M., Harty, J., Badovinac, V., & Xue, H.-H. (2010) · Immunity · doi:10.1016/j.immuni.2010.08.002 · Cited by 689

Quantifying Memory CD8 T Cells Reveals Regionalization of Immunosurveillance

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Intravascular Immune Surveillance by CXCR6+ NKT Cells Patrolling Liver Sinusoids

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Effector memory T cell responses are associated with protection of rhesus monkeys from mucosal simian immunodeficiency virus challenge

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A vaccine strategy that protects against genital herpes by establishing local memory T cells

Shin, H., & Iwasaki, A. (2012) · Nature · doi:10.1038/nature11522 · Cited by 665

The integration of T cell migration, differentiation and function

Masopust, D., & Schenkel, J. M. (2013) · Nature reviews. Immunology · doi:10.1038/nri3442 · Cited by 657

The multifaceted role of CD4+ T cells in CD8+ T cell memory

Laidlaw, B. J., Craft, J. E., & Kaech, S. M. (2016) · Nature Reviews Immunology · doi:10.1038/nri.2015.10 · Cited by 657

Sensing and alarm function of resident memory CD8+ T cells

Schenkel, J., Fraser, K. A., Vezys, V., & Masopust, D. (2013) · Nature Immunology · doi:10.1038/ni.2568 · Cited by 648

Antigen-Independent Differentiation and Maintenance of Effector-like Resident Memory T Cells in Tissues

Casey, K. A., Fraser, K. A., Schenkel, J. M., Moran, A. E., Abt, M. C., Beura, L. K., Lucas, P. J., Artis, D., Wherry, E. J., Hogquist, K. A., et al. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1200402 · Cited by 642

Cutting Edge: Tissue-Retentive Lung Memory CD4 T Cells Mediate Optimal Protection to Respiratory Virus Infection

Teijaro, J. R., Turner, D., Pham, Q., Wherry, E. J., Lefrançois, L., & Farber, D. L. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1102243 · Cited by 641

Long-lived epithelial immunity by tissue-resident memory T (TRM) cells in the absence of persisting local antigen presentation

Mackay, L. K., Stock, A. T., Ma, J., Jones, C. M., Kent, S., Mueller, S. N., Heath, W., Carbone, F., & Gebhardt, T. (2012) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1202288109 · Cited by 638

Dynamic T cell migration program provides resident memory within intestinal epithelium

Masopust, D., Choo, D., Vezys, V., Wherry, E. J., Duraiswamy, J., Akondy, R., Wang, J., Casey, K. A., Barber, D. L., Kawamura, K. S., et al. (2010) · Journal of Experimental Medicine · doi:10.1084/jem.20090858 · Cited by 628

Molecular regulation of effector and memory T cell differentiation

Chang, J. T., Wherry, E. J., & Goldrath, A. W. (2014) · Nature Immunology · doi:10.1038/ni.3031 · Cited by 604

Spatial map of human T cell compartmentalization and maintenance over decades of life

Thome, J. J. C., Yudanin, N., Ohmura, Y., Kubota, M., Grinshpun, B., Sathaliyawala, T., Kato, T., Lerner, H., Shen, Y., & Farber, D. L. (2014) · Cell · doi:10.1016/j.cell.2014.10.026 · Cited by 587

Memory T cells persisting within the brain after local infection show functional adaptations to their tissue of residence

Wakim, L. M., Davis, A. S. W., & Bevan, M. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1010201107 · Cited by 586

CD8+ T lymphocyte mobilization to virus-infected tissue requires CD4+ T-cell help

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Liver-resident NK cells confer adaptive immunity in skin-contact inflammation

Peng, H. C., Jiang, X., Chen, Y., Sojka, D. K., Wei, H., Gao, X., Sun, R., Yokoyama, W. M., & Tian, Z. (2013) · Journal of Clinical Investigation · doi:10.1172/jci66381 · Cited by 558

Different patterns of peripheral migration by memory CD4+ and CD8+ T cells

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Tissue-resident natural killer (NK) cells are cell lineages distinct from thymic and conventional splenic NK cells

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Lung‐resident memory CD8 T cells (TRM) are indispensable for optimal cross‐protection against pulmonary virus infection

Wu, T., Hu, Y., Lee, Y.-T., Bouchard, K. R., Benechet, A. P., Khanna, K., & Cauley, L. S. (2014) · Journal of Leukocyte Biology · doi:10.1189/jlb.0313180 · Cited by 537

Skin-resident memory CD8 + T cells trigger a state of tissue-wide pathogen alert

Ariotti, S., Hogenbirk, M. A., Dijkgraaf, F. E., Visser, L. L., Hoekstra, M. E., Song, J., Jacobs, H., Haanen, J. B. A. G., & Schumacher, T. N. (2014) · Science · doi:10.1126/science.1254803 · Cited by 534

Cutting Edge: CD69 Interference with Sphingosine-1-Phosphate Receptor Function Regulates Peripheral T Cell Retention

Mackay, L. K., Braun, A., Macleod, B. L., Collins, N., Tebartz, C., Bedoui, S., Carbone, F. R., & Gebhardt, T. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1402256 · Cited by 530

Chemokine receptor CCR7 guides T cell exit from peripheral tissues and entry into afferent lymphatics

Bromley, S. K., Thomas, S. Y., & Luster, A. D. (2005) · Nature Immunology · doi:10.1038/ni1240 · Cited by 509

Chemokine receptor CCR7 required for T lymphocyte exit from peripheral tissues

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Dendritic Cell-Induced Memory T Cell Activation in Nonlymphoid Tissues

Wakim, L., Waithman, J., van Rooijen, N., Heath, W., & Carbone, F. (2008) · Science · doi:10.1126/science.1151869 · Cited by 473

Transforming Growth Factor-β Signaling Controls the Formation and Maintenance of Gut-Resident Memory T Cells by Regulating Migration and Retention

Zhang, N., & Bevan, M. J. (2013) · Immunity · doi:10.1016/j.immuni.2013.08.019 · Cited by 450

Migration, maintenance and recall of memory T cells in peripheral tissues

Woodland, D. L., & Kohlmeier, J. E. (2009) · Nature reviews. Immunology · doi:10.1038/nri2496 · Cited by 433

Epidermal Th22 and Tc17 Cells Form a Localized Disease Memory in Clinically Healed Psoriasis

Cheuk, S., Wikén, M., Blomqvist, L., Nylén, S., Talme, T., Ståhle, M., & Eidsmo, L. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1302313 · Cited by 421

A local macrophage chemokine network sustains protective tissue-resident memory CD4 T cells

Iijima, N., & Iwasaki, A. (2014) · Science · doi:10.1126/science.1257530 · Cited by 420

The transcriptional regulators Id2 and Id3 control the formation of distinct memory CD8+ T cell subsets

Yang, C. Y., Best, J. A., Knell, J., Yang, E., Sheridan, A. D., Jesionek, A. K., Li, H. S., Rivera, R. R., Lind, K. C., D’Cruz, L. M., et al. (2011) · Nature Immunology · doi:10.1038/ni.2158 · Cited by 411

Lung niches for the generation and maintenance of tissue-resident memory T cells

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Initial T Cell Receptor Transgenic Cell Precursor Frequency Dictates Critical Aspects of the CD8+ T Cell Response to Infection

Badovinac, V. P., Haring, J. S., & Harty, J. T. (2007) · Immunity · doi:10.1016/j.immuni.2007.04.013 · Cited by 406

CCR7 provides localized access to IL-2 and defines homeostatically distinct regulatory T cell subsets

Smigiel, K. S., Richards, E. A., Srivastava, S., Thomas, K. R., Dudda, J. C., Klonowski, K. D., & Campbell, D. (2013) · The Journal of Experimental Medicine · doi:10.1084/jem.20131142 · Cited by 405

Regulatory iNKT cells lack expression of the transcription factor PLZF and control the homeostasis of Treg cells and macrophages in adipose tissue

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Dynamics of Blood-Borne CD8 Memory T Cell Migration In Vivo

Klonowski, K. D., Williams, K., Marzo, A. L., Blair, D. A., Lingenheld, E. G., & Lefrançois, L. (2004) · Immunity · doi:10.1016/s1074-7613(04)00103-7 · Cited by 383

CD4+ T Cell Help Guides Formation of CD103+ Lung-Resident Memory CD8+ T Cells during Influenza Viral Infection

Laidlaw, B. J., Zhang, N., Marshall, H. D., Staron, M. M., Guan, T., Hu, Y., Cauley, L. S., Craft, J. E., & Kaech, S. M. (2014) · Immunity · doi:10.1016/j.immuni.2014.09.007 · Cited by 382

The Molecular Signature of Tissue Resident Memory CD8 T Cells Isolated from the Brain

Wakim, L. M., Davis, A. S. W., Liu, R., Hu, Y., Villadangos, J. A., Smyth, G. K., & Bevan, M. J. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1201305 · Cited by 381

A mucosal vaccine against Chlamydia trachomatis generates two waves of protective memory T cells

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Skin Effector Memory T Cells Do Not Recirculate and Provide Immune Protection in Alemtuzumab-Treated CTCL Patients

Clark, R. A., Watanabe, R., Teague, J. E., Schlapbach, C., Tawa, M. C., Adams, N., Dorosario, A. A., Chaney, K. S., Cutler, C. S., LeBoeuf, N. R., et al. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3003008 · Cited by 367

Oral Infection Drives a Distinct Population of Intestinal Resident Memory CD8+ T Cells with Enhanced Protective Function

Sheridan, B. S., Pham, Q.-M., Lee, Y., Cauley, L. S., Puddington, L., & Lefrançois, L. (2014) · Immunity · doi:10.1016/j.immuni.2014.03.007 · Cited by 360

Persistence of HIV-1 receptor–positive cells after HSV-2 reactivation is a potential mechanism for increased HIV-1 acquisition

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Cutting Edge: Gut Microenvironment Promotes Differentiation of a Unique Memory CD8 T Cell Population

Masopust, D., Vezys, V., Wherry, E. J., Barber, D. L., & Ahmed, R. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.4.2079 · Cited by 357

Regulatory T cells in nonlymphoid tissues

Burzyn, D., Benoist, C. O., & Mathis, D. J. (2013) · Nature Immunology · doi:10.1038/ni.2683 · Cited by 351

Virus-specific CD8+ T cells accumulate near sensory nerve endings in genital skin during subclinical HSV-2 reactivation

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Intravascular staining redefines lung CD8 T cell responses

Anderson, K., Sung, H., Skon, C. N., Lefrançois, L., Deisinger, A., Vezys, V., & Masopust, D. (2012) · Journal of Immunology · doi:10.4049/jimmunol.1201682 · Cited by 309

Persistence of skin-resident memory T cells within an epidermal niche

Zaid, A., Mackay, L. K., Rahimpour, A., Braun, A., Veldhoen, M., Carbone, F. R., Manton, J. H., Heath, W. R., & Mueller, S. N. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1322292111 · Cited by 306

Common clonal origin of central and resident memory T cells following skin immunization

Gaide, O., Emerson, R., Jiang, X., Gulati, N., Nizza, S. T., Desmarais, C., Robins, H. S., Krueger, J. G., Clark, R. A., & Kupper, T. S. (2015) · Nature Medicine · doi:10.1038/nm.3860 · Cited by 290

Resident Memory T Cells (TRM) Are Abundant in Human Lung: Diversity, Function, and Antigen Specificity

Purwar, R., Campbell, J. J., Murphy, G. F., Richards, W. G., Clark, R. A., & Kupper, T. S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016245 · Cited by 286

Immune surveillance by CD8αα+ skin-resident T cells in human herpes virus infection

Zhu, J., Peng, T., Johnston, C., Phasouk, K., Kask, A. S., Klock, A. M., Jin, L., Diem, K., Koelle, D. M., Wald, A., et al. (2013) · Nature · doi:10.1038/nature12110 · Cited by 283

Tissue-resident memory CD8 + T cells continuously patrol skin epithelia to quickly recognize local antigen

Ariotti, S., Beltman, J. B., Chodaczek, G., Hoekstra, M. E., van Beek, A. E., Gomez, R., Ritsma, L., van Rheenen, J., Marée, A. F. M., Żal, T., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1208927109 · Cited by 274

Proinflammatory microenvironments within the intestine regulate differentiation of tissue-resident CD8 T cells responding to infection

Bergsbaken, T., & Bevan, M. (2015) · Nature Immunology · doi:10.1038/ni.3108 · Cited by 269

Residual Antigen Presentation after Influenza Virus Infection Affects CD8 T Cell Activation and Migration

Zammit, D. J., Turner, D., Klonowski, K. D., Lefrançois, L., & Cauley, L. S. (2006) · Immunity · doi:10.1016/j.immuni.2006.01.015 · Cited by 262

Tissue‐specific migration pathways by phenotypically distinct subpopulations of memory T cells

Mackay, C. R., Marston, W. L., Dudler, L., Spertini, O., Tedder, T. F., & Hein, W. (1992) · European Journal of Immunology · doi:10.1002/eji.1830220402 · Cited by 244

Memory CD8 T cell responses exceeding a large but definable threshold provide long-term immunity to malaria

Schmidt, N. W., Podyminogin, R. L., Butler, N. S., Badovinac, V. P., Tucker, B. J., Bahjat, K. S., Lauer, P., Reyes‐Sandoval, A., Hutchings, C. L., Moore, A., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0805452105 · Cited by 238

Perivascular leukocyte clusters are essential for efficient activation of effector T cells in the skin

Natsuaki, Y., Egawa, G., Nakamizo, S., Ono, S., Hanakawa, S., Okada, T., Kusuba, N., Otsuka, A., Kitoh, A., Honda, T., et al. (2014) · Nature Immunology · doi:10.1038/ni.2992 · Cited by 232

Lung Airway-Surveilling CXCR3hi Memory CD8+ T Cells Are Critical for Protection against Influenza A Virus

Slütter, B., Pewe, L. L., Kaech, S. M., & Harty, J. T. (2013) · Immunity · doi:10.1016/j.immuni.2013.09.013 · Cited by 228

Memory CD8 T-cell compartment grows in size with immunological experience

Vezys, V., Yates, A. J., Casey, K. A., Lanier, G., Ahmed, R., Antia, R., & Masopust, D. (2008) · Nature · doi:10.1038/nature07486 · Cited by 220

Cutting Edge: Resident Memory CD8 T Cells Occupy Frontline Niches in Secondary Lymphoid Organs

Schenkel, J. M., Fraser, K. A., & Masopust, D. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1400003 · Cited by 216

Enhanced survival of lung tissue-resident memory CD8+ T cells during infection with influenza virus due to selective expression of IFITM3

Wakim, L. M., Gupta, N., Mintern, J. D., & Villadangos, J. A. (2013) · Nature Immunology · doi:10.1038/ni.2525 · Cited by 214

Mucosal Resident Memory CD4 T Cells in Protection and Immunopathology

Turner, D., & Färber, D. L. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00331 · Cited by 204

Skin-resident memory CD4+ T cells enhance protection against Leishmania major infection

Glennie, N. D., Yeramilli, V. A., Beiting, D. P., Volk, S. W., Weaver, C. T., & Scott, P. (2015) · Journal of Experimental Medicine · doi:10.1084/jem.20142101 · Cited by 204

PLZF induces an intravascular surveillance program mediated by long-lived LFA-1–ICAM-1 interactions

Thomas, S. Y., Scanlon, S. T., Griewank, K., Constantinides, M. G., Savage, A. K., Barr, K., Meng, F., Luster, A. D., & Bendelac, A. S. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20102630 · Cited by 202

Environmental and Antigen Receptor-Derived Signals Support Sustained Surveillance of the Lungs by Pathogen-Specific Cytotoxic T Lymphocytes

Lee, Y., Suarez-Ramirez, J. E., Wu, T., Redman, J. M., Bouchard, K. R., Hadley, G. A., & Cauley, L. S. (2011) · Journal of Virology · doi:10.1128/jvi.02493-10 · Cited by 189

Memory T Cell Populations in the Lung Airways Are Maintained by Continual Recruitment

Ely, K. H., Cookenham, T. S., Roberts, A. D., & Woodland, D. L. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.1.537 · Cited by 185

E-cadherin promotes accumulation of a unique memory CD8 T-cell population in murine salivary glands

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Unaltered phenotype, tissue distribution and function of Vα14+ NKT cells in germ-free mice

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Preexisting High Frequencies of Memory CD8+ T Cells Favor Rapid Memory Differentiation and Preservation of Proliferative Potential upon Boosting

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Maintenance of T Cell Function in the Face of Chronic Antigen Stimulation and Repeated Reactivation for a Latent Virus Infection

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Cutting Edge: Generation of Effector Cells That Localize to Mucosal Tissues and Form Resident Memory CD8 T Cells Is Controlled by mTOR

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