Tissue-Resident Memory T Cells

Schenkel, Jason M.; Masopust, David

doi:10.1016/j.immuni.2014.12.007

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

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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Trm are specially programmed to persist in their host tissues.
“These Trm are specially programmed to persist in their host tissues [249, 250].”
From Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition) (2021) · cites this paper as [249]

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A local macrophage chemokine network sustains protective tissue-resident memory CD4 T cells
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“For instance, aggregates generated in the vagina of HSV-2-infected mice are composed mostly ofmacrophages andCD4+ T cells, whereas aggregates that form in the brain after local vesicular stomatitis virus infection are composed of CD8+ T cells and CD103+ DCs (Iijima and Iwasaki, 2014; Wakim et al., 2010).”
BackgroundInfluential
Activated Antigen-Specific CD8+ T Cells Persist in the Lungs Following Recovery from Respiratory Virus Infections
Hogan, R. J., Usherwood, E. J., Zhong, W., Roberts, A. D., Dutton, R. W., Harmsen, A. G., & Woodland, D. L. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.3.1813 · Cited by 409 · cited 3× · see citing works
“Indeed, CD8+ and CD4+ T cell memory in the lung and lung airways wanes within months after influenza infection, leading to the loss of protective heterosubtypic immunity (Hogan et al., 2001; Liang et al., 1994; Wu et al., 2014).”
Background
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. (2013) · Immunity · doi:10.1016/j.immuni.2013.08.019 · Cited by 403 · see citing works
Heterosubtypic immunity to influenza type A virus in mice. Effector mechanisms and their longevity.
Liang, S., Mozdzanowska, K., Palladino, G., & Gerhard, W. (1994) · The Journal of Immunology · doi:10.4049/jimmunol.152.4.1653 · Cited by 400 · cited 1× · see citing works
“Indeed, CD8+ and CD4+ T cell memory in the lung and lung airways wanes within months after influenza infection, leading to the loss of protective heterosubtypic immunity (Hogan et al., 2001; Liang et al., 1994; Wu et al., 2014).”
Background
Lung niches for the generation and maintenance of tissue-resident memory T cells
Turner, D., Bickham, K. L., Thome, J. J. C., Kim, C. Y., D’Ovidio, F., Wherry, E. J., & Färber, D. L. (2013) · Mucosal Immunology · doi:10.1038/mi.2013.67 · Cited by 399 · cited 1× · see citing works
“In human cadavers, it was recently shown that 50%–80%of CD4+ andCD8+ T cells express CD69 in spleen and LNs (Sathaliyawala et al., 2013) and CD69+ CD8+ T cells included those with defined specificity for CMV and influenza (Turner et al., 2014).”
Mucosal T Lymphocyte Numbers Are Selectively Reduced in Integrin αE (CD103)-Deficient Mice
Schön, M. P., Arya, A., Murphy, E. A., Adams, C. M., Strauch, U., Agace, W. W., Marsal, J., Donohue, J. P., Her, H., Beier, D. R., et al. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.11.6641 · Cited by 399 · see citing works
Noncytotoxic Lytic Granule–Mediated CD8 + T Cell Inhibition of HSV-1 Reactivation from Neuronal Latency
Knickelbein, J. E., Khanna, K. M., Yee, M. B., Baty, C. J., Kinchington, P. R., & Hendricks, R. L. (2008) · Science · doi:10.1126/science.1164164 · Cited by 395 · cited 1× · see citing works
“Rather than killing these infected neurons and causing immunopathology, granzyme B degrades the immediate early protein ICP4, which is important for viral replication (Knickelbein et al., 2008).”
Background
Tertiary lymphoid organs in infection and autoimmunity
Neyt, K., Perros, F., GeurtsvanKessel, C. H., Hammad, H., & Lambrecht, B. N. (2012) · Trends in Immunology · doi:10.1016/j.it.2012.04.006 · Cited by 389 · cited 1× · see citing works
“TLOs (Neyt et al., 2012) and leukocyte aggregates (TLOs have HEVs, whereas leukocyte aggregates do not) have long been noted within NLTs. Historically, they have occasionally been referred to as ectopic lymphoid structures, or abnormal sites of inflammation.”
Background
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 · see citing works
A Spatially-Organized Multicellular Innate Immune Response in Lymph Nodes Limits Systemic Pathogen Spread
Kastenmüller, W., Torabi‐Parizi, P., Subramanian, N., Lämmermann, T., & Germain, R. N. (2012) · Cell · doi:10.1016/j.cell.2012.07.021 · Cited by 372 · see citing works
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 365 · cited 6× · see citing works
“Interestingly, E-cadherin is also expressed by memory CD8 T cells isolated from the salivary gland, small intestine epithelium, lung, skin, thymus, and brain and might contribute to maintenance via homophilic E-cadherin interactions between Trm cells and epithelial cells (Hofmann and Pircher, 2011; Mackay et al., 2013…”
BackgroundInfluential
Persistence of HIV-1 receptor–positive cells after HSV-2 reactivation is a potential mechanism for increased HIV-1 acquisition
Zhu, J., Hladik, F., Davis, A. S. W., Klock, A. M., Peng, T., Johnston, C., Remington, M. L., Magaret, A., Koelle, D. M., Wald, A., et al. (2009) · Nature Medicine · doi:10.1038/nm.2006 · Cited by 357 · cited 1× · see citing works
“Although more abundant during infection (Cromwell et al., 2011; Kobayashi et al., 2002;; Zhu et al., 2009), they are present in healthy humans and to a lesser degree in SPF mice, which have comparatively little infectious history.”
Background
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 · cited 20× · see citing works
“In this regard, it will be crucial to determine whether the total number of Trm cells established within NLTs is tightly regulated, as it appears to be for Tcm cells within LNs, or whether it is flexible, as shown for Tem cells (Vezys et al., 2009).”
BackgroundInfluentialSelf-citation
Afferent lymph-derived T cells and DCs use different chemokine receptor CCR7-dependent routes for entry into the lymph node and intranodal migration
Braun, A., Worbs, T., Moschovakis, G. L., Halle, S., Hoffmann, K., Bölter, J., Münk, A., & Förster, R. (2011) · Nature Immunology · doi:10.1038/ni.2085 · Cited by 337 · cited 17× · see citing works
“Similarly, dendritic cells upregulate CCR7 after activation in tissues, which then acts in concert with S1PR1 to promote migration to downstream SLOs (Braun et al., 2011; Czeloth et al., 2005; Lamana et al., 2011; Ohl et al., 2004; Saeki et al., 1999).”
BackgroundInfluential
Oral infection drives a distinct population of intestinal resident memory CD8+ T cells with enhanced protective function
Sheridan, B., Pham, Q.-M., Lee, Y.-T., Cauley, L., Puddington, L., & Lefrançois, L. (2014) · Immunity · doi:10.1016/j.immuni.2014.03.007 · Cited by 332 · cited 5× · see citing works
“After oral infection with Listeria monocytogenes, aeb7 is important for the accumulation of CD8+ T cells in the small intestine epithelium but is dispensable for long-term maintenance (Sheridan et al., 2014).”
BackgroundInfluential
Cutting Edge: Control of Mycobacterium tuberculosis Infection by a Subset of Lung Parenchyma–Homing CD4 T Cells
Sakai, S., Kauffman, K. D., Schenkel, J. M., McBerry, C., Mayer-Barber, K. D., Masopust, D., & Barber, D. L. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1400019 · Cited by 320 · cited 2× · see citing works
“In fact, within lung, intravascular NKT cells precipitate allergies (Scanlon et al., 2011) and intravascular CD4 T cells produce IFN-g in vivo in response to mTB (Sakai et al., 2014).”
BackgroundSelf-citation
Cyclical modulation of sphingosine-1-phosphate receptor 1 surface expression during lymphocyte recirculation and relationship to lymphoid organ transit
Lo, C. G., Xu, Y., Proia, R. L., & Cyster, J. G. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20041509 · Cited by 319 · cited 1× · see citing works
“Exiting SLOs is an active process and depends on gradual T cell sensitization to sphingosine-1 phosphate receptor 1 (S1PR1)-dependent chemotactic gradients (Arnon et al., 2011; Lo et al., 2005; Shannon et al., 2012).”
Background
The Collagen Binding α1β1 Integrin VLA-1 Regulates CD8 T Cell-Mediated Immune Protection against Heterologous Influenza Infection
Ray, S. J., Franki, S. N., Pierce, R. H., Dimitrova, S., Koteliansky, V., Sprague, A., Doherty, P. C., de Fougerolles, A. R., & Topham, D. J. (2004) · Immunity · doi:10.1016/s1074-7613(04)00021-4 · Cited by 317 · cited 2× · see citing works
“For instance, the integrin a1b1 binds laminins and collagens and is highly expressed on CD8+ Trm in the brain, small intestine, lung, and skin (Gebhardt et al., 2009; Mackay et al., 2013; Ray et al., 2004; Wakim et al., 2012).”
Background
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 · cited 1× · see citing works
“Following acute intraperitoneal LCMV challenge, up to 95% of memory CD8 T cells isolated from perfused lung were derived from vasculature (Anderson et al., 2012).”
BackgroundSelf-citation
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 · see citing works
Activated Primary and Memory CD8 T Cells Migrate to Nonlymphoid Tissues Regardless of Site of Activation or Tissue of Origin
Masopust, D., Vezys, V., Usherwood, E. J., Cauley, L. S., Olson, S., Marzo, A. L., Ward, R. L., Woodland, D. L., & Lefrançois, L. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.8.4875 · Cited by 281 · cited 2× · see citing works
“…and NLTs (Masopust et al., 2001b; Reinhardt et al., 2001; Woodland and Kohlmeier, 2009), and at least for CD8+ T cells, this may include NLTs that were not sites of infection (Hofmann and Pircher, 2011; Kaufman et al., 2008; Liu et al., 2006; Masopust et al., 2010; 2004; Zhu et al., 2012).”
BackgroundSelf-citation
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 · cited 2× · see citing works
“Additionally, CD8 Trm cells in the epidermis are able to adopt a ‘‘dendriticlike’’ morphology, allowing them to scan multiple host cells at once for pathogen and thus maximizing their ability to locate infected cells (Ariotti et al., 2012; Gebhardt et al., 2011).”
Background
TGF-β–dependent CD103 expression by CD8+ T cells promotes selective destruction of the host intestinal epithelium during graft-versus-host disease
El-Asady, R. S., Yuan, R., Liu, K., Wang, D., Gress, R. E., Lucas, P. J., Drachenberg, C. B., & Hadley, G. A. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20041044 · Cited by 271 · see citing works
αEβ7 integrin interaction with E-cadherin promotes antitumor CTL activity by triggering lytic granule polarization and exocytosis
Floc’h, A. L., Jalil, A., Vergnon, I., Chansac, B. L. M., Lazar, V., Bismuth, G., Chouaı̈b, S., & Mami‐Chouaib, F. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20061524 · Cited by 269 · cited 1× · see citing works
“Similarly, it has been demonstrated that T cells infiltrating the TGF-b rich microenvironment of tumors also express aeb7 (Le Floc’h et al., 2007).”
Background
Intestinal lymphocyte subpopulations in inflammatory bowel disease: an analysis by immunohistological and cell isolation techniques.
Selby, W. S., Janossy, G., Bofill, M., & Jewell, D. P. (1984) · Gut · doi:10.1136/gut.25.1.32 · Cited by 267 · cited 1× · see citing works
“However, these yieldsmight underestimate the number of lymphocytes in NLTs (Ganusov and De Boer, 2007; Selby et al., 1984).”
Background
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 · cited 2× · see citing works
“After murine lung infections associated with depots of residual antigen, there is evidence for retention of CD8 T cells within draining mediastinal LNs, and CD69 and CD103 are expressed in these contexts (Takamura et al., 2010; Zammit et al., 2006).”
Background
Capture of influenza by medullary dendritic cells via SIGN-R1 is essential for humoral immunity in draining lymph nodes
González, S., Lukacs‐Kornek, V., Kuligowski, M., Pitcher, L. A., Degn, S. E., Kim, Y., Cloninger, M. J., Martínez‐Pomares, L., Gordon, S., Turley, S. J., et al. (2010) · Nature Immunology · doi:10.1038/ni.1856 · Cited by 238 · cited 1× · see citing works
“CD8+ Trm cells exhibited biased distribution to splenic marginal zone and LN sinuses (Schenkel et al., 2014a), which often represent the initial sites of microbial entry to these organs (Aoshi et al., 2009; Gonzalez et al., 2010; Junt et al., 2007).”
Background
Type I Interferons Regulate Cytolytic Activity of Memory CD8+ T Cells in the Lung Airways during Respiratory Virus Challenge
Kohlmeier, J. E., Cookenham, T. S., Roberts, A. D., Miller, S. C., & Woodland, D. L. (2010) · Immunity · doi:10.1016/j.immuni.2010.06.016 · Cited by 237 · cited 1× · see citing works
“For example, type I interferon (IFN), interleukin-33 (IL-33), and tumor necrosis factor-a (TNFa) and other cytokines all induce CD69 upregulation on T cells (Casey et al., 2012; Kohlmeier et al., 2010; López-Cabrera et al., 1995; Skon et al., 2013).”
Background
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 · see citing works
Chemokine Guidance of Central Memory T Cells Is Critical for Antiviral Recall Responses in Lymph Nodes
Sung, J. H., Zhang, H., Moseman, E. A., Álvarez, D., Iannacone, M., Henrickson, S. E., de la Torre, J. C., Groom, J. R., Luster, A. D., & von Andrian, U. H. (2012) · Cell · doi:10.1016/j.cell.2012.08.015 · Cited by 228 · cited 1× · see citing works
“T cell reactivation within these LN barrier sites precipitates rapid detection, innate immune activation, and recruitment of CXCR3+ memory T cells, all of which likely contribute to accelerating pathogen control (Kastenmüller et al., 2013; Sung et al., 2012).”
Background
Peripheral Prepositioning and Local CXCL9 Chemokine-Mediated Guidance Orchestrate Rapid Memory CD8+ T Cell Responses in the Lymph Node
Kastenmüller, W., Brandes, M., Wang, Z., Herz, J., Egen, J. G., & Germain, R. N. (2013) · Immunity · doi:10.1016/j.immuni.2012.11.012 · Cited by 225 · see citing works
Differential expression of transforming growth factors alpha and beta in rat intestinal epithelial cells.
Koyama, S., & Podolsky, D. K. (1989) · Journal of Clinical Investigation · doi:10.1172/jci114080 · Cited by 221 · cited 1× · see citing works
“Active TGF-b is constitutively available at many epithelial surfaces, including skin epidermis and small intestine epithelium (Koyama and Podolsky, 1989; Yang et al., 1999).”
Background
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 218 · cited 2× · see citing works
“In this regard, it will be crucial to determine whether the total number of Trm cells established within NLTs is tightly regulated, as it appears to be for Tcm cells within LNs, or whether it is flexible, as shown for Tem cells (Vezys et al., 2009).”
BackgroundSelf-citation
Intrahepatic myeloid-cell aggregates enable local proliferation of CD8+ T cells and successful immunotherapy against chronic viral liver infection
Huang, L.-R., Wohlleber, D., Reisinger, F., Jenne, C. N., Cheng, R.-L., Abdullah, Z., Schildberg, F. A., Odenthal, M., Dienes, H.-P., van Rooijen, N., et al. (2013) · Nature Immunology · doi:10.1038/ni.2573 · Cited by 216 · cited 3× · see citing works
“Leukocyte aggregates have been characterized in the brain, salivary gland, lung, female reproductive tract, skin, and liver under a variety of infectious or inflammatory conditions (Anderson et al., 2014; Huang et al., 2013; Iijima and Iwasaki, 2014; Natsuaki et al., 2014; Stahl et al., 2013; Wakim et al., 2010; Walto…”
Background
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 · cited 24× · see citing works
“Parabiosis experiments demonstrated that 1%–5% of memory CD8+ T cells within spleen and LNs are Trm cells after acute LCMV infection (Schenkel et al., 2014a).”
BackgroundInfluentialSelf-citation
γδ T Cells Exhibit Multifunctional and Protective Memory in Intestinal Tissues
Sheridan, B. S., Romagnoli, P. A., Pham, Q.-M., Fu, H.-H., Alonzo, F., Schubert, W., Freitag, N. E., & Lefrançois, L. (2013) · Immunity · doi:10.1016/j.immuni.2013.06.015 · Cited by 209 · cited 1× · see citing works
“A network of natural killer (NK) cells, gd T cells, and innate-like CD8+ T cells are also prepositioned near lymph node sinuses, and when activated, prevent systemic pathogen dissemination (Kastenmüller et al., 2012; Sheridan et al., 2013).”
Background
GRK2-Dependent S1PR1 Desensitization Is Required for Lymphocytes to Overcome Their Attraction to Blood
Arnon, T. I., Xu, Y., Lo, C. G., Pham, T. H. M., An, J., Coughlin, S. R., Dorn, G. W., & Cyster, J. G. (2011) · Science · doi:10.1126/science.1208248 · Cited by 202 · see citing works
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 · see citing works
Intestinal macrophages: well educated exceptions from the rule
Zigmond, E., & Jung, S. (2013) · Trends in Immunology · doi:10.1016/j.it.2013.02.001 · Cited by 198 · cited 1× · see citing works
“Taken together, it appears that localization to certain NLTs is sufficient to drive adoption of specific phenotypes, much like inductive cues that drivemonocyte differentiation in the small intestine (Zigmond and Jung, 2013).”
Background
Sphingosine-1-Phosphate Mediates Migration of Mature Dendritic Cells
Czeloth, N., Bernhardt, G., Hofmann, F., Genth, H., & Förster, R. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.175.5.2960 · Cited by 195 · cited 18× · see citing works
“Similarly, dendritic cells upregulate CCR7 after activation in tissues, which then acts in concert with S1PR1 to promote migration to downstream SLOs (Braun et al., 2011; Czeloth et al., 2005; Lamana et al., 2011; Ohl et al., 2004; Saeki et al., 1999).”
BackgroundInfluential
Opposing Effects of TGF-β and IL-15 Cytokines Control the Number of Short-Lived Effector CD8+ T Cells
Sanjabi, S., Mosaheb, M. M., & Flavell, R. A. (2009) · Immunity · doi:10.1016/j.immuni.2009.04.020 · Cited by 193 · cited 1× · see citing works
“KLRG1+ effectors are also particularly vulnerable to apoptosis when treated with TGF-b in vitro (Sanjabi et al., 2009).”
Background
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 187 · cited 1× · see citing works
“It was not demonstrated in these studies whether recirculating memory T cells migrate to tissues to replenish Trm cells, which has been proposed for lung airways (Ely et al., 2006), or whether Trm cells were self-sustaining.”
Background
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 187 · see citing works
Large intestine–targeted, nanoparticle-releasing oral vaccine to control genitorectal viral infection
Zhu, Q., Talton, J., Zhang, G., Cunningham, T., Wang, Z., Waters, R. C., Kirk, J., Eppler, B., Klinman, D. M., Sui, Y., et al. (2012) · Nature Medicine · doi:10.1038/nm.2866 · Cited by 184 · cited 2× · see citing works
“, 2001; Woodland and Kohlmeier, 2009), and at least for CD8 T cells, this may include NLTs that were not sites of infection (Hofmann and Pircher, 2011; Kaufman et al., 2008; Liu et al., 2006; Masopust et al., 2010; 2004; Zhu et al., 2012).”
Background
Preferential migration of effector CD8+ T cells into the interstitium of the normal lung
Galkina, E. (2005) · Journal of Clinical Investigation · doi:10.1172/jci24482 · Cited by 178 · cited 1× · see citing works
“In animal models, this issue can be simply addressed using in vivo intravascular-staining strategies (Galkina et al., 2005; Muppidi et al., 2011; Scanlon et al., 2011), which abrogate the need to perfuse.”
Background
E-cadherin promotes accumulation of a unique memory CD8 T-cell population in murine salivary glands
Hofmann, M., & Pircher, H. (2011) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1107200108 · Cited by 173 · cited 4× · see citing works
“Indeed, CD8 and CD4 T cell memory in the lung and lung airways wanes within months after influenza infection, leading to the loss of protective heterosubtypic immunity (Hogan et al., 2001; Liang et al., 1994; Wu et al., 2014).”
BackgroundInfluential
Recirculating Memory T Cells Are a Unique Subset of CD4+ T Cells with a Distinct Phenotype and Migratory Pattern
Bromley, S. K., Yan, S., Tomura, M., Kanagawa, O., & Luster, A. D. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1202805 · Cited by 168 · cited 1× · see citing works
“Moreover, NLT populations might be particularly prone to death during lengthy or harsh processing procedures, because they do not survive well in culture (Brunner et al., 2001; Wakim et al., 2012).”
Background
Inflammation-induced interstitial migration of effector CD4+ T cells is dependent on integrin αV
Overstreet, M. G., Gaylo, A. E., Angermann, B., Hughson, A. L., Hyun, Y., Lambert, K., Acharya, M., Billroth-MacLurg, A. C., Rosenberg, A. F., Topham, D. J., et al. (2013) · Nature Immunology · doi:10.1038/ni.2682 · Cited by 162 · cited 2× · see citing works
“Blocking integrin av results in increased parasite burden during local Leishmania major infection, suggesting that increased T cell motility is in important for pathogen control (Overstreet et al., 2013).”
Background
Dendritic cells and B cells maximize mucosal Th1 memory response to herpes simplex virus
Iijima, N., Linehan, M. M., Zamora, M., Butkus, D., Dunn, R., Kehry, M. R., Laufer, T. M., & Iwasaki, A. (2008) · The Journal of Experimental Medicine · doi:10.1084/jem.20082039 · Cited by 154 · cited 1× · see citing works
“For example, the antiviral cytokine IFN-g is critical for clearing L. major, HSV-2, and HBV infections (Guidotti et al., 1996; Iijima et al., 2008; Müller et al., 2012).”
Background
Development, trafficking, and function of memory T‐cell subsets
Lefrançois, L. (2006) · Immunological Reviews · doi:10.1111/j.0105-2896.2006.00393.x · Cited by 151 · cited 1× · see citing works
“…productively primed within SLOs, they give rise to effector cells that migrate throughout the host and leave behind a memory population that persists long after pathogen clearance (Dutton et al., 1998; Harty and Badovinac, 2008; Lefrançois, 2006; Sallusto et al., 2010; Williams and Bevan, 2007).”
Background
Direct Analysis of the Dynamics of the Intestinal Mucosa CD8 T Cell Response to Systemic Virus Infection
Masopust, D., Jiang, J. K., Shen, H., & Lefrançois, L. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.4.2348 · Cited by 148 · see citing works
Self-citation
Intravaginal immunization with HPV vectors induces tissue-resident CD8+ T cell responses
Çuburu, N., Graham, B. S., Buck, C. B., Kines, R. C., Pang, Y.-Y. S., Day, P. M., Lowy, D. R., & Schiller, J. T. (2012) · Journal of Clinical Investigation · doi:10.1172/jci63287 · Cited by 140 · see citing works
Expression of the Transcription Factor Lung Kruppel-Like Factor Is Regulated by Cytokines and Correlates with Survival of Memory T Cells In Vitro and In Vivo
Schober, S. L., Kuo, C. T., Schluns, K. S., Lefrançois, L., Leiden, J. M., & Jameson, S. C. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.163.7.3662 · Cited by 139 · cited 1× · see citing works
“S1PR1 downregulation is concomitantly associated with cell surface expression of the C-type lectin CD69 (Cyster and Schwab, 2012; Matloubian et al., 2004; Schober et al., 1999; Shiow et al., 2006; Skon et al., 2013).”
Background
Migration of CD4 T Cells and Dendritic Cells toward Sphingosine 1-Phosphate (S1P) Is Mediated by Different Receptor Subtypes: S1P Regulates the Functions of Murine Mature Dendritic Cells via S1P Receptor Type 3
Maeda, Y., Matsuyuki, H., Shimano, K., Kataoka, H., Sugahara, K., & Chiba, K. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.6.3437 · Cited by 138 · cited 1× · see citing works
“S1P is also produced by afferent lymphatic endothelial cells draining NLTs and is important for mature dendritic cells to migrate to tissue-draining lymph nodes (Czeloth et al., 2005; Lamana et al., 2011; Maeda et al., 2007; Pham et al., 2010).”
Background
CD4+ T Cells Rely on a Cytokine Gradient to Control Intracellular Pathogens beyond Sites of Antigen Presentation
Müller, A. J., Filipe‐Santos, O., Eberl, G., Aebischer, T., Späth, G. F., & Bousso, P. (2012) · Immunity · doi:10.1016/j.immuni.2012.05.015 · Cited by 138 · cited 2× · see citing works
“Additionally, IFN-g effects are not limited to infected host cells that T cells contact directly, but can also act on neighboring infected host cells (Müller et al., 2012).”
Background
Dynamic Programing of CD8+ T Cell Trafficking after Live Viral Immunization
Liu, L., Fuhlbrigge, R. C., Karibian, K., Tian, T., & Kupper, T. S. (2006) · Immunity · doi:10.1016/j.immuni.2006.06.019 · Cited by 132 · cited 2× · see citing works
“After acute viral infections in mice and humans, effector T cells transiently upregulate a4b7 integrin, which facilitates migration into the small intestine (Campbell and Butcher, 2002; Liu et al., 2006; Masopust et al., 2010).”
Background
Long-lived Memory T Lymphocyte Responses After Hantavirus Infection
Epps, H. L. V., Terajima, M., Mustonen, J. T., Arstila, T. P., Corey, E. A., Vaheri, A. I., & Ennis, F. A. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20011255 · Cited by 128 · cited 1× · see citing works
“Unfortunately, there are few long-term studies on the durability of T cell memory in humans, even in blood (Hammarlund et al., 2003; Nanan et al., 2000; Van Epps et al., 2002), and tracking T cell memory in NLTs is less tractable.”
Background
Transcriptional Regulation of the Gene Encoding the Human C-type Lectin Leukocyte Receptor AIM/CD69 and Functional Characterization of Its Tumor Necrosis Factor-α-responsive Elements
López‐Cabrera, M., Muñóz, E., Blazquez, M. V., Ursa, M. A., Santis, A. G., & Sánchez‐Madrid, F. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.37.21545 · Cited by 127 · cited 1× · see citing works
“For example, type I interferon (IFN), interleukin-33 (IL-33), and tumor necrosis factor-a (TNFa) and other cytokines all induce CD69 upregulation on T cells (Casey et al., 2012; Kohlmeier et al., 2010; López-Cabrera et al., 1995; Skon et al., 2013).”
Background
Gene Expression in Antigen-Specific CD8+ T Cells During Viral Infection
Grayson, J. M., Murali‐Krishna, K., Altman, J. D., & Ahmed, R. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.2.795 · Cited by 126 · see citing works
Generation of mucosal cytotoxic T cells against soluble protein by tissue-specific environmental and costimulatory signals
Kim, S.-K., Reed, D. S., Olson, S., Schnell, M. J., Rose, J. K., Morton, P. A., & Lefrançois, L. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.18.10814 · Cited by 124 · cited 3× · see citing works
“Memory CD8 T cells in certain NLT maintain constitutive granzyme B expression and like recently activated effectors, mediate ex vivo cytotoxicity (Kim et al., 1998; Masopust et al., 2006).”
Background
Airborne lipid antigens mobilize resident intravascular NKT cells to induce allergic airway inflammation
Scanlon, S. T., Thomas, S. Y., Ferreira, C. M., Bai, L., Krausz, T. N., Savage, P. B., & Bendelac, A. S. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20110522 · Cited by 113 · see citing works
Active Transforming Growth Factor-β in Wound Repair
Yang, L., Qiu, C. X., Ludlow, A., Ferguson, M. W. J., & Brunner, G. (1999) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65256-x · Cited by 105 · cited 1× · see citing works
“Active TGF-b is constitutively available at many epithelial surfaces, including skin epidermis and small intestine epithelium (Koyama and Podolsky, 1989; Yang et al., 1999).”
Background
Long-Term Persistence of Activated Cytotoxic T Lymphocytes after Viral Infection of the Central Nervous System
Hawke, S. H., Stevenson, P. G., Freeman, S., & Bangham, C. R. M. (1998) · The Journal of Experimental Medicine · doi:10.1084/jem.187.10.1575 · Cited by 105 · cited 2× · see citing works
“However, NLT-derived memory T cells also express many markers not shared by any circulating population of memory T cells within blood (Casey et al., 2012; Gebhardt et al., 2009; Hawke et al., 1998; Hofmann and Pircher, 2011; Jiang et al., 2012; Masopust et al., 2006; Ray et al., 2004).”
Background
Erythrocyte and polymorphonuclear cell transit time and concentration in human pulmonary capillaries
Hogg, J. C., Coxson, H. O., Brumwell, M. L., Beyers, N., Doerschuk, C. M., MacNee, W., & Wiggs, B. R. (1994) · Journal of Applied Physiology · doi:10.1152/jappl.1994.77.4.1795 · Cited by 101 · cited 1× · see citing works
“Work from James Hogg prognosticated this important technical issue when he reported that the ratio of neutrophils to RBCs was 100-fold higher in lung capillaries than in large-bore blood vessels (Hogg et al., 1994).”
Background
IL-15 regulates memory CD8+ T cell O-glycan synthesis and affects trafficking.
Nolz, J., & Harty, J. (2014) · Journal of Clinical Investigation · doi:10.1172/jci72039 · Cited by 98 · see citing works
The measurement of lymphocyte volume: importance of reference particle deformability and counting solution tonicity
Segel, G., Cokelet, G., & Lichtman, M. (1981) · Blood · doi:10.1182/blood.v57.5.894.894 · Cited by 96 · cited 1× · see citing works
“This issue extends to lymphocytes as well (which have a 3-fold greater volume than RBCs; 90 femtoliters versus 290 femtoliters (Segel et al., 1981)).”
Background
Absence of Cross-Presenting Cells in the Salivary Gland and Viral Immune Evasion Confine Cytomegalovirus Immune Control to Effector CD4 T Cells
Walton, S. M., Mandarić, S., Torti, N., Zimmermann, A., Hengel, H., & Oxenius, A. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002214 · Cited by 94 · cited 1× · see citing works
“…in the brain, salivary gland, lung, female reproductive tract, skin, and liver under a variety of infectious or inflammatory conditions (Anderson et al., 2014; Huang et al., 2013; Iijima and Iwasaki, 2014; Natsuaki et al., 2014; Stahl et al., 2013; Wakim et al., 2010; Walton et al., 2011).”
Background
The route of priming influences the ability of respiratory virus–specific memory CD8+ T cells to be activated by residual antigen
Takamura, S., Roberts, A. D., Jelley‐Gibbs, D. M., Wittmer, S. T., Kohlmeier, J. E., & Woodland, D. L. (2010) · The Journal of Experimental Medicine · doi:10.1084/jem.20090283 · Cited by 91 · cited 1× · see citing works
“After murine lung infections associated with depots of residual antigen, there is evidence for retention of CD8+ T cells within draining mediastinal LNs, and CD69 and CD103 are expressed in these contexts (Takamura et al., 2010; Zammit et al., 2006).”
Background
Cannabinoid receptor 2 positions and retains marginal zone B cells within the splenic marginal zone
Muppidi, J. R., Arnon, T. I., Bronevetsky, Y., Veerapen, N., Tanaka, M., Besra, G. S., & Cyster, J. G. (2011) · The Journal of Experimental Medicine · doi:10.1084/jem.20111083 · Cited by 73 · cited 1× · see citing works
“In animal models, this issue can be simply addressed using in vivo intravascular-staining strategies (Galkina et al., 2005; Muppidi et al., 2011; Scanlon et al., 2011), which abrogate the need to perfuse.”
Background
Trafficking of Antigen-Specific CD8+ T-Lymphocytes to Mucosal Surfaces Following Intramuscular Vaccination
Kaufman, D., Liu, J.-Y., Carville, A., Mansfield, K., Havenga, M., Goudsmit, J., & Barouch, D. (2008) · Journal of Immunology · doi:10.4049/jimmunol.181.6.4188 · Cited by 72 · see citing works
The cellular niche of Listeria monocytogenes infection changes rapidly in the spleen
Aoshi, T., Carrero, J. A., Konjufca, V. H., Koide, Y., Unanue, E. R., & Miller, M. J. (2009) · European Journal of Immunology · doi:10.1002/eji.200838718 · Cited by 70 · cited 1× · see citing works
“CD8+ Trm cells exhibited biased distribution to splenic marginal zone and LN sinuses (Schenkel et al., 2014a), which often represent the initial sites of microbial entry to these organs (Aoshi et al., 2009; Gonzalez et al., 2010; Junt et al., 2007).”
Background
Resident CD4+ T cells accumulate in lymphoid organs after prolonged antigen exposure
Ugur, M., Schulz, O., Menon, M., Krueger, A., & Pabst, O. (2014) · Nature Communications · doi:10.1038/ncomms5821 · Cited by 69 · cited 18× · see citing works
“The cytokine mechanism(s) controlling KLF2 and the S1PR1CD69 axis in NLTs is less well understood.”
BackgroundInfluential
T‐cell activation in the intestinal mucosa
Montufar‐Solis, D., Garza, T., & Klein, J. R. (2007) · Immunological Reviews · doi:10.1111/j.1600-065x.2006.00471.x · Cited by 67 · cited 1× · see citing works
“Because these signatures are also constitutively expressed by T cells within the intestinal mucosa, it was originally proposed that mucosal T cells represented activated effectors (Montufar-Solis et al., 2007).”
Background
Novel Vaccination Protocol with Two Live Mucosal Vectors Elicits Strong Cell-Mediated Immunity in the Vagina and Protects against Vaginal Virus Challenge
Li, Z., Zhang, M., Zhou, C., Zhao, X., Iijima, N., & Frankel, F. R. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.4.2504 · Cited by 65 · cited 1× · see citing works
“For instance, a larger number of Trm cells within the female reproductive tract are induced to express aeb7 after local inflammation compared to systemic infection or in the presence of local inflammation (Çuburu et al., 2012; Li et al., 2008; Mackay et al., 2012; Shin and Iwasaki, 2012).”
Background
Do most lymphocytes in humans really reside in the gut?
Ganusov, V., & de Boer, R. D. (2007) · Trends in immunology · doi:10.1016/j.it.2007.08.009 · Cited by 60 · see citing works
CD69 Modulates Sphingosine-1-Phosphate-Induced Migration of Skin Dendritic Cells
Lamana, A., Martı́n, P., de la Fuente, H., Martínez‐Muñoz, L., Cruz‐Adalia, A., Ramírez‐Huesca, M., Escribano, C., Gollmer, K., Mellado, M., Stein, J. V., et al. (2011) · Journal of Investigative Dermatology · doi:10.1038/jid.2011.54 · Cited by 57 · cited 18× · see citing works
“Similarly, dendritic cells upregulate CCR7 after activation in tissues, which then acts in concert with S1PR1 to promote migration to downstream SLOs (Braun et al., 2011; Czeloth et al., 2005; Lamana et al., 2011; Ohl et al., 2004; Saeki et al., 1999).”
BackgroundInfluential
The Pulmonary Localization of Virus-Specific T Lymphocytes Is Governed by the Tissue Tropism of Infection
Knudson, C. J., Weiss, K. A., Hartwig, S. M., & Varga, S. M. (2014) · Journal of Virology · doi:10.1128/jvi.00329-14 · Cited by 55 · cited 3× · see citing works
“Vascular contamination by CD4 T cells is less than CD8 T cells in models addressed thus far (Anderson et al., 2014; Knudson et al., 2014; Teijaro et al., 2011) but is still significant.”
Background
A novel sensitive approach for frequency analysis of measles virus-specific memory T-lymphocytes in healthy adults with a childhood history of natural measles
Nanan, R. K. H., Rauch, A., Kämpgen, E., Niewiesk, S., & Kreth, H. W. (2000) · Microbiology · doi:10.1099/0022-1317-81-5-1313 · Cited by 55 · cited 2× · see citing works
“Unfortunately, there are few long-term studies on the durability of T cell memory in humans, even in blood (Hammarlund et al., 2003; Nanan et al., 2000; Van Epps et al., 2002), and tracking T cell memory in NLTs is less tractable.”
Background
Prolonged presence of effector-memory CD8 T cells in the central nervous system after dengue virus encephalitis
der Most, R. G. V. (2002) · International Immunology · doi:10.1093/intimm/dxg009 · Cited by 52 · cited 1× · see citing works
“Additionally, CD62L cells isolated fromblood and spleen did not recapitulate the panoply of phenotypes expressed by memory T cells isolated from the small intestinal mucosa, lung, and brain (Hawke et al., 1998; Hogan et al., 2001; Kim et al., 1998; Masopust et al., 2001a; van der Most et al., 2003).”
Background
The Impact of KLF2 Modulation on the Transcriptional Program and Function of CD8 T Cells
Preston, G., Feijoo‐Carnero, C., Schurch, N., Cowling, V. H., & Cantrell, D. A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077537 · Cited by 49 · cited 2× · see citing works
“transiently reduce expression of the transcription factor kruppellike factor 2 (KLF2), a positive regulator of S1PR1 transcription (Preston et al., 2013; Skon et al., 2013; Grayson et al., 2001).”
Background
Regulation of cell death and survival in intestinal intraepithelial lymphocytes
Brunner, T., Arnold, D., Wasem, C., Herren, S., & Frutschi, C. (2001) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4400854 · Cited by 48 · cited 1× · see citing works
“Moreover, NLT populations might be particularly prone to death during lengthy or harsh processing procedures, because they do not survive well in culture (Brunner et al., 2001; Wakim et al., 2012).”
Background
Nodular Inflammatory Foci Are Sites of T Cell Priming and Control of Murine Cytomegalovirus Infection in the Neonatal Lung
Stahl, F. R., Heller, K., Halle, S., Keyser, K. A., Busche, A., Marquardt, A., Wagner, K., Boelter, J., Bischoff, Y., Kremmer, E., et al. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003828 · Cited by 46 · cited 2× · see citing works
“…in the brain, salivary gland, lung, female reproductive tract, skin, and liver under a variety of infectious or inflammatory conditions (Anderson et al., 2014; Huang et al., 2013; Iijima and Iwasaki, 2014; Natsuaki et al., 2014; Stahl et al., 2013; Wakim et al., 2010; Walton et al., 2011).”
Background
Lymphoid Follicles Are Generated in High-Grade Cervical Dysplasia and Have Differing Characteristics Depending on HIV Status
Kobayashi, A., Darragh, T. M., HERNDIER, B. G., Anastos, K., Minkoff, H., Cohen, M. H., Young, M., Levine, A. M., Grant, L. A., Hyun, W. C., et al. (2002) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64359-3 · Cited by 46 · cited 1× · see citing works
“Although more abundant during infection (Cromwell et al., 2011; Kobayashi et al., 2002;; Zhu et al., 2009), they are present in healthy humans and to a lesser degree in SPF mice, which have comparatively little infectious history.”
Background
CCR7/CCL19 Controls Expression of EDG-1 in T Cells
Shannon, L. A., McBurney, T. M., Wells, M. A., Roth, M. E., Calloway, P. A., Bill, C. A., Islam, S., & Vines, C. M. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.310045 · Cited by 30 · cited 1× · see citing works
“Exiting SLOs is an active process and depends on gradual T cell sensitization to sphingosine-1 phosphate receptor 1 (S1PR1)-dependent chemotactic gradients (Arnon et al., 2011; Lo et al., 2005; Shannon et al., 2012).”
Background
SIV‐Specific CD8+ T Cells are Enriched in Female Genital Mucosa of Rhesus Macaques and Express Receptors for Inflammatory Chemokines
Cromwell, M. A., Carville, A., Mansfield, K. G., Klumpp, S. A., Westmoreland, S. V., Lackner, A. A., & Johnson, R. P. (2011) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.2010.00966.x · Cited by 6 · cited 1× · see citing works
“Although more abundant during infection (Cromwell et al., 2011; Kobayashi et al., 2002;; Zhu et al., 2009), they are present in healthy humans and to a lesser degree in SPF mice, which have comparatively little infectious history.”
Background

Flagged first, then by citations

Sorted by citations

Control of adaptive immunity by the innate immune system
Iwasaki, A., & Medzhitov, R. (2015) · Nature Immunology · doi:10.1038/ni.3123 · Cited by 2,160 · see citing works
Lineage tracking reveals dynamic relationships of T cells in colorectal cancer
Zhang, L., Yu, X., Zheng, L., Zhang, Y., Li, Y., Fang, Q., Gao, R., Kang, B., Zhang, Q., Huang, J. Y., et al. (2018) · Nature · doi:10.1038/s41586-018-0694-x · Cited by 1,505 · see citing works
Human T cell development, localization, and function throughout life
Kumar, B. V., Connors, T. J., & Farber, D. L. (2018) · Immunity · doi:10.1016/j.immuni.2018.01.007 · Cited by 1,257 · see citing works
Human Tissue-Resident Memory T Cells Are Defined by Core Transcriptional and Functional Signatures in Lymphoid and Mucosal Sites
Kumar, B. V., Ma, W., Miron, M., Granot, T., Guyer, R. S., Carpenter, D. J., Senda, T., Sun, X., Ho, S.-H., Lerner, H., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.08.078 · Cited by 1,068 · see citing works
Normalizing the environment recapitulates adult human immune traits in laboratory mice
Beura, L. K., Hamilton, S. E., Bi, K., Schenkel, J. M., Odumade, O. A., Casey, K. A., Thompson, E. A., Fraser, K. A., Rosato, P. C., Filali-Mouhim, A., et al. (2016) · Nature · doi:10.1038/nature17655 · Cited by 1,072 · see citing works
Self-citation
Single-cell profiling of breast cancer T cells reveals a tissue-resident memory subset associated with improved prognosis
Kathleen Cuningham Foundation Consortium for Research into Familial Breast Cancer (kConFab), Savas, P., Virassamy, B., Ye, C., Salim, A., Mintoff, C. P., Caramia, F., Salgado, R., Byrne, D. J., Teo, Z. L., et al. (2018) · Nature Medicine · doi:10.1038/s41591-018-0078-7 · Cited by 992 · see citing works
Tissue-resident memory T cells: local specialists in immune defence
Mueller, S. N., & Mackay, L. K. (2016) · Nature Reviews Immunology · doi:10.1038/nri.2015.3 · Cited by 1,006 · see citing works
Co-expression of CD39 and CD103 identifies tumor-reactive CD8 T cells in human solid tumors
Duhen, T., Duhen, R., Montler, R., Moses, J., Moudgil, T., de Miranda, N. F., Goodall, C. P., Blair, T. C., Fox, B. A., McDermott, J. E., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05072-0 · Cited by 938 · see citing works
Single-cell transcriptomics of human T cells reveals tissue and activation signatures in health and disease
Szabo, P. A., Levitin, H. M., Miron, M., Snyder, M. E., Senda, T., Yuan, J., Cheng, Y. L., Bush, E. C., Dogra, P., Thapa, P., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12464-3 · Cited by 756 · see citing works
Neuroimmunology of Traumatic Brain Injury: Time for a Paradigm Shift
Jassam, Y. N., Izzy, S., Whalen, M., McGavern, D. B., & El Khoury, J. (2017) · Neuron · doi:10.1016/j.neuron.2017.07.010 · Cited by 799 · see citing works
Peripheral T cell expansion predicts tumour infiltration and clinical response
Wu, T. D., Madireddi, S., de Almeida, P. E., Banchereau, R., Chen, Y.-J. J., Chitre, A. S., Chiang, E. Y., Iftikhar, H., O’Gorman, W. E., Au-Yeung, A., et al. (2020) · Nature · doi:10.1038/s41586-020-2056-8 · Cited by 770 · see citing works
Mucosal vaccines — fortifying the frontiers
Lavelle, E. C., & Ward, R. W. (2021) · Nature reviews. Immunology · doi:10.1038/s41577-021-00583-2 · Cited by 763 · see citing works
CD49a Expression Defines Tissue-Resident CD8 + T Cells Poised for Cytotoxic Function in Human Skin
Cheuk, S., Schlums, H., Gallais Sérézal, I., Martini, E., Chiang, S. C., Marquardt, N., Gibbs, A., Detlofsson, E., Introini, A., Forkel, M., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.01.009 · Cited by 678 · see citing works
Pathogenic Mechanisms Associated With Different Clinical Courses of Multiple Sclerosis
Lassmann, H. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2018.03116 · Cited by 678 · see citing works
“CD8 resident memory cells have originally been defined and functionally characterized in experimental models of virus induced disease (114, 115).”
Background
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 · see citing works
Regulation of the Immune Response by TGF-β: From Conception to Autoimmunity and InfectionPreprint
Sanjabi, S., Oh, S. A., & Li, M. O. (2017) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a022236 · Cited by 626 · see citing works
Understanding subset diversity in T cell memory
Jameson, S. C., & Masopust, D. (2018) · Immunity · doi:10.1016/j.immuni.2018.02.010 · Cited by 523 · see citing works
Self-citation
The compartmentalized inflammatory response in the multiple sclerosis brain is composed of tissue-resident CD8+ T lymphocytes and B cells
Machado-Santos, J., Saji, E., Tröscher, A. R., Paunovic, M., Liblau, R., Gabriely, G., Bien, C. G., Bauer, J., & Lassmann, H. (2018) · Brain · doi:10.1093/brain/awy151 · Cited by 548 · see citing works
“S1P1 receptor, a key molecule of lymphocyte egress from the tissue was highly expressed on leucocytes within the vascular lumen and moderately expressed in astrocytes and endothelial cells of the brain tissue.”
BackgroundInfluential
Establishment and Maintenance of the Macrophage Niche
Guilliams, M., Thierry, G. R., Bonnardel, J., & Bajenoff, M. (2020) · Immunity · doi:10.1016/j.immuni.2020.02.015 · Cited by 512 · see citing works
Tumour-infiltrating B cells: immunological mechanisms, clinical impact and therapeutic opportunities
Laumont, C. M., Banville, A. C., Gilardi, M., Hollern, D. P., & Nelson, B. H. (2022) · Nature reviews. Cancer · doi:10.1038/s41568-022-00466-1 · Cited by 529 · see citing works
Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition)
Cossarizza, A., Chang, H., Radbruch, A., Abrignani, S., Addo, R., Akdis, M., Andrä, I., Andreata, F., Annunziato, F., Arranz, E., et al. (2021) · European Journal of Immunology · doi:10.1002/eji.202170126 · Cited by 531 · see citing works
T cell responses to cytomegalovirus
Klenerman, P., & Oxenius, A. (2016) · Nature Reviews Immunology · doi:10.1038/nri.2016.38 · Cited by 483 · see citing works
A single‐cell RNA expression atlas of normal, preneoplastic and tumorigenic states in the human breast
Pal, B., Chen, Y., Vaillant, F., Capaldo, B. D., Joyce, R., Song, X., Bryant, V. L., Penington, J. S., Stefano, L. D., Ribera, N. T., et al. (2021) · The EMBO Journal · doi:10.15252/embj.2020107333 · Cited by 476 · see citing works
“Cells resembling tissue-resident memory T (T RM ) cells (Schenkel & Masopust, 2014) were apparent in TNBC and HER2 + but not in ER + cancers (Fig EV4A).”
Non-classical Immunity Controls Microbiota Impact on Skin Immunity and Tissue Repair
Linehan, J. L., Harrison, O. J., Han, S.-J., Byrd, A. L., Vujkovic-Cvijin, I., Villarino, A. V., Sen, S. K., Shaik, J., Smelkinson, M., Tamoutounour, S., et al. (2018) · Cell · doi:10.1016/j.cell.2017.12.033 · Cited by 456 · see citing works
Progressive multiple sclerosis: from pathophysiology to therapeutic strategies
Faissner, S., Plemel, J. R., Gold, R., & Yong, V. W. (2019) · Nature Reviews Drug Discovery · doi:10.1038/s41573-019-0035-2 · Cited by 459 · see citing works
Liver-Resident Memory CD8+ T Cells Form a Front-Line Defense against Malaria Liver-Stage Infection
Fernandez-Ruiz, D., Ng, W. Y., Holz, L. E., Ma, J. Z., Zaid, A., Wong, Y. C., Lau, L. S., Mollard, V., Cozijnsen, A., Collins, N., et al. (2016) · Immunity · doi:10.1016/j.immuni.2016.08.011 · Cited by 438 · see citing works
ILC1 Confer Early Host Protection at Initial Sites of Viral Infection
Weizman, O.-E., Adams, N. M., Schuster, I. S., Krishna, C., Pritykin, Y., Lau, C. M., Degli‐Esposti, M. A., Leslie, C. S., Sun, J. C.-Y., & O’Sullivan, T. E. (2017) · Cell · doi:10.1016/j.cell.2017.09.052 · Cited by 454 · see citing works
Emerging insights into natural killer cells in human peripheral tissues
Björkström, N. K., Ljunggren, H., & Michaëlsson, J. (2016) · Nature reviews. Immunology · doi:10.1038/nri.2016.34 · Cited by 451 · see citing works
CD103+ Tumor-Resident CD8+ T Cells Are Associated with Improved Survival in Immunotherapy-Naïve Melanoma Patients and Expand Significantly During Anti–PD-1 Treatment
Edwards, J. J., Wilmott, J. S., Madore, J., Gide, T. N., Quek, C. Y. J., Tasker, A. T., Ferguson, A. L., Chen, J., Hewavisenti, R., Hersey, P., et al. (2018) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-17-2257 · Cited by 431 · see citing works
Tissue-resident memory T cells populate the human brain
Smolders, J., Heutinck, K. M., Fransen, N. L., Remmerswaal, E. B. M., Hombrink, P., ten Berge, I. J. M., van Lier, R. A. W., Huitinga, I., & Hamann, J. (2018) · Nature Communications · doi:10.1038/s41467-018-07053-9 · Cited by 406 · see citing works
The establishment of resident memory B cells in the lung requires local antigen encounter
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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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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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Tissue-Resident Memory T Cells

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

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Record

About these checks