Tissue-resident memory features are linked to the magnitude of cytotoxic T cell responses in human lung cancer
Open accessAbstract
Therapies that boost the anti-tumor responses of cytotoxic T lymphocytes (CTLs) have shown promise; however, clinical responses to the immunotherapeutic agents currently available vary considerably, and the molecular basis of this is unclear. We performed transcriptomic profiling of tumor-infiltrating CTLs from treatment-naive patients with lung cancer to define the molecular features associated with the robustness of anti-tumor immune responses. We observed considerable heterogeneity in the expression of molecules associated with activation of the T cell antigen receptor (TCR) and of immunological-checkpoint molecules such as 4-1BB, PD-1 and TIM-3. Tumors with a high density of CTLs showed enrichment for transcripts linked to tissue-resident memory cells (T RM cells), such as CD103, and CTLs from CD103 hi tumors displayed features of enhanced cytotoxicity. A greater density of T RM cells in tumors was predictive of a better survival outcome in lung cancer, and this effect was independent of that conferred by CTL density. Here we define the 'molecular fingerprint' of tumor-infiltrating CTLs and identify potentially new targets for immunotherapy.
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The presence of CD103+CD8+ TILs is a positive prognostic marker in several cancers.
“Further research revealed that the presence of CD103+CD8+ TILs is a positive prognostic marker in several cancers [269-272].”
From Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition) (2021) · cites this paper as [272]
The Results section, “CD103 density is predictive of survival in lung cancer” (page not available), reports better survival and lower mortality in patients with CD103-high lung tumors, including among patients with high CD8+ TIL density. This supports lung cancer as one example, but the paper does not establish the prognostic claim across several cancers; its survival analysis also uses CD103 density rather than directly counting CD103+CD8+ TILs. (LLM, conf=0.84)
Experimental — accuracy not yet measuredA subset of TILs in tumors of NSCLC shares the phenotype of Trm in adjacent lung tissue (expression of CD103, CD69, CXCR6, CD49a).
“A subset of TILs in tumors of NSCLC shares the phenotype of Trm in adjacent lung tissue (expression of CD103, CD69, CXCR6, CD49a) [272, 273].”
From Guidelines for the use of flow cytometry and cell sorting in immunological studies (third edition) (2021) · cites this paper as [272]
The Results section, “TILhi tumors show enrichment for CD8+ TRM cells” (page unavailable), reports CD103+CD8+ TILs co-expressing CD69 and CD49a, and higher CXCR6 transcript expression in TIL-high tumors. These findings support a subset of lung-cancer TILs having tissue-resident-memory features, but the cited passages do not establish that this subset shares its phenotype specifically with TRM cells in adjacent lung tissue. (LLM, conf=0.85)
Experimental — accuracy not yet measured
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Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
Love, M. I., Huber, W., & Anders, S. (2014) · Genome Biology · doi:10.1186/s13059-014-0550-8 · Cited by 95,106 · see citing works
Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506580102 · Cited by 53,625 · see citing works
PD-1 and PD-L1 Immune Checkpoint Blockade to Treat Breast Cancer
Hartkopf, A. D., Taran, F., Wallwiener, M., Walter, C. B., Krämer, B., Grischke, E., & Brucker, S. Y. (2016) · Breast Care · doi:10.1159/000453569 · Cited by 30,989 · see citing works
Adverse Renal Effects of Immune Checkpoint Inhibitors: A Narrative Review
Wanchoo, R., Karam, S., Uppal, N. N., Barta, V. S., Deray, G., Devoe, C., Launay‐Vacher, V., Jhaveri, K. D., & on behalf of Cancer and Kidney International Network Workgroup on Immune Checkpoint Inhibitors (2017) · American Journal of Nephrology · doi:10.1159/000455014 · Cited by 15,314 · see citing works
The blockade of immune checkpoints in cancer immunotherapy
Pardoll, D. M. (2012) · Nature Reviews Cancer · doi:10.1038/nrc3239 · Cited by 13,838 · see citing works
TopHat: discovering splice junctions with RNA-Seq
Trapnell, C., Pachter, L. S., & Salzberg, S. L. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp120 · Cited by 11,477 · see citing works
PD-1 blockade induces responses by inhibiting adaptive immune resistance
Tumeh, P. C., Harview, C. L., Yearley, J. H., Shintaku, I. P., Taylor, E. J. M., Robert, L., Chmielowski, B., Spasic, M., Henry, G., Ciobanu, V., et al. (2014) · Nature · doi:10.1038/nature13954 · Cited by 6,609 · see citing works
Type, Density, and Location of Immune Cells Within Human Colorectal Tumors Predict Clinical Outcome
Galon, J., Costes, A., Sanchez-Cabo, F., Kirilovsky, A., Mlecnik, B., Lagorce-Pagès, C., Tosolini, M., Camus, M., Berger, A., Wind, P., et al. (2006) · Science · doi:10.1126/science.1129139 · Cited by 6,516 · see citing works
Pembrolizumab for the Treatment of Non–Small-Cell Lung Cancer
Garon, E. B., Rizvi, N. A., Hui, R., Leighl, N., Balmanoukian, A. S., Eder, J. P., Patnaik, A., Aggarwal, C., Gubens, M., Horn, L., et al. (2015) · New England Journal of Medicine · doi:10.1056/nejmoa1501824 · Cited by 6,198 · see citing works
Dissecting the multicellular ecosystem of metastatic melanoma by single-cell RNA-seq
Tirosh, I., Izar, B., Prakadan, S. M., Wadsworth, M. H., Treacy, D., Trombetta, J. J., Rotem, A., Rodman, C., Lian, C., Murphy, G., et al. (2016) · Science · doi:10.1126/science.aad0501 · Cited by 4,944 · see citing works
Spatiotemporal Dynamics of Intratumoral Immune Cells Reveal the Immune Landscape in Human Cancer
Bindea, G., Mlecnik, B., Tosolini, M., Kirilovsky, A., Waldner, M. J., Obenauf, A. C., Angell, H. K., Fredriksen, T., Lafontaine, L., Berger, A., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.10.003 · Cited by 4,390 · see citing works
Immune Checkpoint Blockade: A Common Denominator Approach to Cancer Therapy
Topalian, S. L., Drake, C. G., & Pardoll, D. M. (2015) · Cancer Cell · doi:10.1016/j.ccell.2015.03.001 · Cited by 4,229 · see citing works
Full-length RNA-seq from single cells using Smart-seq2
Picelli, S., Faridani, O. R., Björklund, Å. K., Winberg, G., Sagasser, S., & Sandberg, R. (2014) · Nature Protocols · doi:10.1038/nprot.2014.006 · Cited by 4,137 · see citing works
Immune checkpoint targeting in cancer therapy: toward combination strategies with curative potential
Sharma, P., & Allison, J. P. (2015) · Cell · doi:10.1016/j.cell.2015.03.030 · Cited by 2,345 · see citing works
Molecular Signature of CD8+ T Cell Exhaustion during Chronic Viral Infection
Wherry, E. J., Ha, S.-J., Kaech, S. M., Haining, W. N., Sarkar, S., Kalia, V., Subramaniam, S., Blattman, J. N., Barber, D. L., & Ahmed, R. (2007) · Immunity · doi:10.1016/j.immuni.2007.09.006 · Cited by 2,103 · see citing works
MiXCR: software for comprehensive adaptive immunity profiling
Bolotin, D. A., Poslavskii, S., Mitrophanov, I., Shugay, M., Mamedov, I. Z., Putintseva, E. V., & Chudakov, D. M. (2015) · Nature Methods · doi:10.1038/nmeth.3364 · Cited by 1,730 · see citing works
Cancer immunotherapy: harnessing the immune system to battle cancer
Yang, Y. (2015) · Journal of Clinical Investigation · doi:10.1172/jci83871 · Cited by 1,366 · see citing works
Molecular Signature of CD8+ T Cell Exhaustion during Chronic Viral Infection
Wherry, E. J., Ha, S., Kaech, S. M., Haining, W. N., Sarkar, S., Kalia, V., Subramaniam, S., Blattman, J. N., Barber, D. L., & Ahmed, R. (2007) · Immunity · doi:10.1016/j.immuni.2007.11.006 · Cited by 1,355 · see citing works
The developmental pathway for CD103+CD8+ tissue-resident memory T cells of skin
Mackay, L. K., Rahimpour, A., Ma, J. Z., Collins, N., Stock, A. T., Hafon, M.-L., Vega-Ramos, J., Lauzurica, P., Mueller, S. N., Stefanovic, T., et al. (2013) · Nature Immunology · doi:10.1038/ni.2744 · Cited by 1,331 · see citing works
Fourcade, J., Sun, Z., Benallaoua, M., Guillaume, P., Luescher, I. F., Sander, C., Kirkwood, J. M., Kuchroo, V., & Zarour, H. M. (2010) · Journal of Experimental Medicine · doi:10.1084/jem.20100637 · Cited by 1,307 · see citing works
The Immunoreceptor TIGIT Regulates Antitumor and Antiviral CD8 + T Cell Effector Function
Johnston, R. J., Comps‐Agrar, L., Hackney, J. A., Yu, X., Huseni, M. A., Yang, Y., Park, S., Javinal, V., Chiu, H. H., Irving, B. A., et al. (2014) · Cancer Cell · doi:10.1016/j.ccell.2014.10.018 · Cited by 1,189 · see citing works
Overcoming T cell exhaustion in infection and cancer
Pauken, K. E., & Wherry, E. J. (2015) · Trends in Immunology · doi:10.1016/j.it.2015.02.008 · Cited by 1,178 · see citing works
PD-1 identifies the patient-specific CD8+ tumor-reactive repertoire infiltrating human tumors
Gros, A., Robbins, P. F., Yao, X., Li, Y. F., Turcotte, S., Tran, E., Wunderlich, J. R., Mixon, A., Farid, S., Dudley, M. E., et al. (2014) · Journal of Clinical Investigation · doi:10.1172/jci73639 · Cited by 1,113 · see citing works
Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes
Mackay, L. K., Minnich, M., Kragten, N. A. M., Liao, Y., Nota, B., Seillet, C., Zaid, A., Man, K., Preston, S., Freestone, D., et al. (2016) · Science · doi:10.1126/science.aad2035 · Cited by 1,010 · see citing works
Distribution and compartmentalization of human circulating and tissue-resident memory T cell subsets
Sathaliyawala, T., Kubota, M., Yudanin, N., Turner, D., Camp, P., Thome, J. J. C., Bickham, K. L., Lerner, H., Goldstein, M., Sykes, M., et al. (2013) · Immunity · doi:10.1016/j.immuni.2012.09.020 · Cited by 848 · see citing works
Exhaustion of tumor-specific CD8+ T cells in metastases from melanoma patients
Baitsch, L., Baumgaertner, P., Devêvre, E., Raghav, S. K., Legat, A., Barba, L., Wieckowski, S., Bouzourene, H., Deplancke, B., Romero, P., et al. (2011) · Journal of Clinical Investigation · doi:10.1172/jci46102 · Cited by 845 · see citing works
Memory T Cell Subsets, Migration Patterns, and Tissue Residence
Mueller, S. N., Gebhardt, T., Carbone, F., & Heath, W. R. (2012) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032712-095954 · Cited by 842 · see citing works
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 · see citing works
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 · see citing works
Djenidi, F., Adam, J., Goubar, A., Durgeau, A., Meurice, G., de Montpréville, V., Validire, P., Besse, B., & Mami-Chouaib, F. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1402711 · Cited by 622 · see citing works
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 · see citing works
Wölfl, M., Kuball, J. H. E., Ho, W., Nguyen, H., Manley, T. J., Bleakley, M., & Greenberg, P. D. (2007) · Blood · doi:10.1182/blood-2006-11-056168 · Cited by 460 · see citing works
Programs for the persistence, vigilance and control of human CD8+ lung-resident memory T cells
Hombrink, P., Helbig, C., Backer, R. A., Piet, B., Oja, A. E., Stark, R., Brasser, G., Jongejan, A., Jonkers, R. E., Nota, B., et al. (2016) · Nature Immunology · doi:10.1038/ni.3589 · Cited by 455 · see citing works
Egr-2 and Egr-3 are negative regulators of T cell activation
Safford, M., Collins, S. L., Lutz, M. A., Allen, A. N., Huang, C.-T., Kowalski, J., Blackford, A. L., Horton, M. R., Drake, C. G., Schwartz, R. H., et al. (2005) · Nature Immunology · doi:10.1038/ni1193 · Cited by 446 · see citing works
Breathing new life into immunotherapy: review of melanoma, lung and kidney cancer
Drake, C. G., Lipson, E. J., & Brahmer, J. R. (2013) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2013.208 · Cited by 418 · see citing works
Tumour-infiltrating lymphocytes predict for outcome in HPV-positive oropharyngeal cancer
Ward, M. J., Thirdborough, S. M., Mellows, T., Riley, C. L., Harris, S., Suchak, K., Webb, A., Hampton, C., Patel, N., Randall, C. J., et al. (2013) · British Journal of Cancer · doi:10.1038/bjc.2013.639 · Cited by 391 · see citing works
Self-citationCritical pathways in cellular senescence and immortalization revealed by gene expression profiling
Fridman, A. L., & Tainsky, M. A. (2008) · Oncogene · doi:10.1038/onc.2008.213 · Cited by 385 · see citing works
A Metabolic Immune Checkpoint: Adenosine in Tumor Microenvironment
Ohta, A. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00109 · Cited by 385 · see citing works
Kurachi, M., Barnitz, R. A., Yosef, N., Odorizzi, P. M., DiIorio, M. A., Lemieux, M. E., Yates, K. B., Godec, J., Klatt, M. G., Regev, A., et al. (2014) · Nature Immunology · doi:10.1038/ni.2834 · Cited by 384 · see citing works
CD39 Expression Identifies Terminally Exhausted CD8+ T Cells
Gupta, P., Godec, J., Wolski, D., Adland, E., Yates, K. B., Pauken, K. E., Cosgrove, C., Ledderose, C., JUNGER, W. G., Robson, S. C., et al. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1005177 · Cited by 384 · see citing works
Transcriptional insights into the CD8+ T cell response to infection and memory T cell formation
Best, J., Blair, D., Knell, J., Yang, E., Mayya, V., Doedens, A. L., Dustin, M. L., & Goldrath, A. W. (2013) · Nature Immunology · doi:10.1038/ni.2536 · Cited by 334 · see citing works
Stromal features are predictive of disease mortality in oral cancer patients
Marsh, D. J., Suchak, K., Moutasim, K. A., Vallath, S., Hopper, C., Jerjes, W., Upile, T., Kalavrezos, N., Violette, S. M., Weinreb, P. H., et al. (2010) · The Journal of Pathology · doi:10.1002/path.2830 · Cited by 333 · see citing works
Self-citationInnate-like functions of natural killer T cell subsets result from highly divergent gene programs
Engel, I., Seumois, G., Chávez, L., Samaniego‐Castruita, D., White, B. M., Chawla, A., Mock, D. C., Vijayanand, P., & Kronenberg, M. (2016) · Nature Immunology · doi:10.1038/ni.3437 · Cited by 311 · see citing works
Self-citationKIR2DL4 (CD158d), an NK Cell-Activating Receptor with Inhibitory Potential
Faure, M., & Long, E. O. (2002) · The Journal of Immunology · doi:10.4049/jimmunol.168.12.6208 · Cited by 267 · see citing works
KIR2DL4 (CD158d): An activation receptor for HLA-G
Rajagopalan, S., & Long, E. O. (2012) · Frontiers in Immunology · doi:10.3389/fimmu.2012.00258 · Cited by 202 · see citing works
CD74 and intratumoral immune response in breast cancer
Wang, Z., Milne, K., Webb, J. R., & Watson, P. H. (2016) · Oncotarget · doi:10.18632/oncotarget.8610 · Cited by 202 · see citing works
Invariant Natural Killer T Cells in Asthma and Chronic Obstructive Pulmonary Disease
Vijayanand, P., Seumois, G., Pickard, C., Powell, R. M., Angco, G., Sammut, D., Gadola, S. D., Friedmann, P. S., & Djukanović, R. (2007) · New England Journal of Medicine · doi:10.1056/nejmoa064691 · Cited by 192 · see citing works
Self-citationSystemic 4-1BB activation induces a novel T cell phenotype driven by high expression of Eomesodermin
Curran, M. A., Geiger, T. L., Montalvo-Ortiz, W., Kim, M., Reiner, S. L., Al‐Shamkhani, A., Sun, J. C.-Y., & Allison, J. P. (2013) · The Journal of Experimental Medicine · doi:10.1084/jem.20121190 · Cited by 187 · see citing works
CD73 and CD39 ectonucleotidases in T cell differentiation: Beyond immunosuppression
Bono, M. R., Fernández, D., Flores‐Santibáñez, F., Rosemblatt, M. S., & Sauma, D. (2015) · FEBS Letters · doi:10.1016/j.febslet.2015.07.027 · Cited by 185 · see citing works
Brooke, G. P., Holbrook, J. D., Brown, M. H., & Barclay, A. N. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.173.4.2562 · Cited by 171 · see citing works
Tse, S., Radtke, A. J., Espinosa, D. A., Cockburn, I. A., & Zavala, F. P. (2014) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiu281 · Cited by 158 · see citing works
CD103 and Intratumoral Immune Response in Breast Cancer
Wang, Z., Milne, K., Derocher, H., Webb, J. R., Nelson, B. H., & Watson, P. H. (2016) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-0732 · Cited by 156 · see citing works
A Critical Role of IL-21-Induced BATF in Sustaining CD8-T-Cell-Mediated Chronic Viral Control
Xin, G., Schauder, D., Lainez, B., Weinstein, J. S., Dai, Z.-X., Chen, Y., Esplugues, E., Wen, R., Wang, D., Parish, I. A., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.09.069 · Cited by 141 · see citing works
Tumor-induced senescent T cells with suppressor function: a potential form of tumor immune evasion
Montes, C. L., Chapoval, A. I., Nelson, J., Orhue, V., Zhang, X., Schulze, D. H., Strome, S. E., & Gastman, B. R. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-2282 · Cited by 127 · see citing works
Sandoval‐Montes, C., & Santos‐Argumedo, L. (2004) · Journal of Leukocyte Biology · doi:10.1189/jlb.0404262 · Cited by 126 · see citing works
Piccio, L. M., Vermi, W., Boles, K. S., Fuchs, A. G., Strader, C., Facchetti, F., Cella, M., & Colonna, M. (2004) · Blood · doi:10.1182/blood-2004-07-2823 · Cited by 124 · see citing works
Transcriptional Profiling of Th2 Cells Identifies Pathogenic Features Associated with Asthma
Seumois, G., Zapardiel‐Gonzalo, J., White, B. M., Singh, D. K., Schulten, V. M. J., Dillon, M., Hinz, D., Broide, D. H., Sette, A., Peters, B., et al. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1600397 · Cited by 92 · see citing works
Self-citationBrown, I. E., Blank, C., Kline, J., Kacha, A. K., & Gajewski, T. F. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.177.7.4521 · Cited by 91 · see citing works
Muñoz, P., Mittelbrunn, M., de la Fuente, H., Pérez‐Martínez, M., García-Pérez, A., Ariza, A., Malavasi, F., Zubiaur, M., Sánchez‐Madrid, F., & Sancho, J. (2008) · Blood · doi:10.1182/blood-2007-07-101600 · Cited by 82 · see citing works
Lee, L. N., Ronan, E. O., de Lara, C., Franken, K. L. M. C., Ottenhoff, T. H. M., Tchilian, E. Z., & Beverley, P. C. L. (2011) · Infection and Immunity · doi:10.1128/iai.01133-10 · Cited by 60 · see citing works
Willoughby, J. E., Kerr, J. P., Rogel, A., Taraban, V. Y., Buchan, S. L., Johnson, P., & Al‐Shamkhani, A. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1301217 · Cited by 54 · see citing works
Webb, J. R., Milne, K., & Nelson, B. H. (2014) · OncoImmunology · doi:10.4161/onci.27668 · Cited by 51 · see citing works
Wiśniewski, A., Kowal, A., Wyrodek, E., Nowak, I., Majorczyk, E., Wagner, M., Pawlak, E., Jankowska, R., Slesak, B., Frydecka, I., et al. (2015) · Tissue Antigens · doi:10.1111/tan.12561 · Cited by 34 · see citing works
CD39 is a negative regulator of P2X7-mediated inflammatory cell death in mast cells
Kuhny, M., Hochdörfer, T., Ayata, C. K., Idzko, M., & Huber, M. (2014) · Cell Communication and Signaling · doi:10.1186/s12964-014-0040-3 · Cited by 33 · see citing works
Nab2 regulates secondary CD8+ T-cell responses through control of TRAIL expression
Wolkers, M. C., Gerlach, C., Arens, R., Janssen, E. M., Fitzgerald, P., Schumacher, T. N., Medema, J. P., Green, D. R., & Schoenberger, S. P. (2011) · Blood · doi:10.1182/blood-2011-08-373910 · Cited by 30 · see citing works
Transcriptional Hallmarks Of Tumor Infiltrating Lymphocyte Responses To Melanoma
Collins, N. B., Godec, J., Zou, L., et al. (2013) · Blood · doi:10.1182/blood.v122.21.3491.3491 · Cited by 2 · see citing works
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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
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Kurtulus, S., Madi, A., Escobar, G., Klapholz, M., Nyman, J., Christian, E., Pawlak, M., Dionne, D., Xia, J., Rozenblatt-Rosen, O., et al. (2019) · Immunity · doi:10.1016/j.immuni.2018.11.014 · Cited by 636 · 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
Ford, K., Hanley, C. J., Mellone, M., Szyndralewiez, C., Heitz, F., Wiesel, P., Wood, O., Machado, M., Lopez, M.-A., Ganesan, A.-P., et al. (2020) · Cancer Research · doi:10.1158/0008-5472.can-19-3158 · Cited by 411 · see citing works
Self-citationOvercoming TGFβ-mediated immune evasion in cancer
Tauriello, D. V. F., Sancho, E., & Batlle, E. (2022) · Nature Reviews Cancer · doi:10.1038/s41568-021-00413-6 · Cited by 377 · see citing works
Patil, V. S., Madrigal, A., Schmiedel, B. J., Clarke, J., O’Rourke, P., de Silva, A. D., Harris, E., Peters, B., Seumois, G., Weiskopf, D., et al. (2018) · Science Immunology · doi:10.1126/sciimmunol.aan8664 · Cited by 262 · see citing works
Self-citationT cells and the skin: from protective immunity to inflammatory skin disorders
Ho, A. W., & Kupper, T. S. (2019) · Nature Reviews Immunology · doi:10.1038/s41577-019-0162-3 · Cited by 241 · see citing works
Koda, Y., Teratani, T., Chu, P.-S., Hagihara, Y., Mikami, Y., Harada, Y., Tsujikawa, H., Miyamoto, K., Suzuki, T., Taniki, N., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-24734-0 · Cited by 219 · see citing works
Trigger-happy resident memory CD4+ T cells inhabit the human lungs
Oja, A. E., Piet, B., Helbig, C., Stark, R., van der Zwan, D., Blaauwgeers, H., Remmerswaal, E. B. M., Amsen, D., Jonkers, R. E., Moerland, P. D., et al. (2018) · Mucosal Immunology · doi:10.1038/mi.2017.94 · Cited by 160 · see citing works
Cao, Y., Trillo-Tinoco, J., Sierra, R. A., Anadon, C., Dai, W., Mohamed, E., Cen, L., Costich, T. L., Magliocco, A., Marchion, D., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09263-1 · Cited by 161 · see citing works
Oja, A. E., Piet, B., van der Zwan, D., Blaauwgeers, H., Mensink, M., de Kivit, S., Borst, J., Nolte, M. A., van Lier, R. A. W., Stark, R., et al. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02654 · Cited by 130 · see citing works
Armed and Ready: Transcriptional Regulation of Tissue-Resident Memory CD8 T Cells
Behr, F. M., Chuwonpad, A., Stark, R., & van Gisbergen, K. P. J. M. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.01770 · Cited by 124 · see citing works
Metabolic programs of T cell tissue residency empower tumour immunity
Reina-Campos, M., Heeg, M., Kennewick, K., Mathews, I. T., Galletti, G., Luna, V., Nguyen, Q., Huang, H., Milner, J. J., Hu, K. H., et al. (2023) · Nature · doi:10.1038/s41586-023-06483-w · Cited by 132 · see citing works
Schalck, A., Sakellariou-Thompson, D., Forget, M.-A., Sei, E., Hughes, T. G., Reuben, A., Bai, S., Hu, M., Kumar, T., Hurd, M. W., et al. (2022) · Cancer Discovery · doi:10.1158/2159-8290.cd-21-1248 · Cited by 85 · see citing works
Trial watch: immune checkpoint blockers for cancer therapy
Vanpouille-Box, C., Lhuillier, C., Bezu, L., Aranda, F., Yamazaki, T., Kepp, O., Fucikova, J., Spisek, R., Demaria, S., Formenti, S. C., et al. (2017) · OncoImmunology · doi:10.1080/2162402x.2017.1373237 · Cited by 73 · see citing works
Cancer-specific tissue-resident memory T-cells express ZNF683 in colorectal cancer
Kitakaze, M., Uemura, M., Hara, T., Chijimatsu, R., Motooka, D., Hirai, T., Konno, M., Okuzaki, D., Sekido, Y., Hata, T., et al. (2023) · British Journal of Cancer · doi:10.1038/s41416-023-02202-4 · Cited by 49 · see citing works
van Gisbergen, K. P. J. M., Zens, K. D., & Münz, C. (2021) · European Journal of Immunology · doi:10.1002/eji.202049062 · Cited by 39 · see citing works
Noble, A., Pring, E. T., Durant, L., Man, R., Dilke, S. M., Hoyles, L., James, S. A., Carding, S. R., Jenkins, J. T., & Knight, S. C. (2022) · Cancer Immunology, Immunotherapy · doi:10.1007/s00262-021-03135-8 · Cited by 34 · see citing works
Qu, Q.-X., Zhu, X.-Y., Du, W.-W., Wang, H.-B., Shen, Y., Zhu, Y.-B., & Chen, C. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00577 · Cited by 30 · see citing works
- Authors
- Ganesan, A.-P., Clarke, J., Wood, O., Garrido-Martin, E. M., Chee, S. J., Mellows, T., Samaniego-Castruita, D., Singh, D., Seumois, G., Alzetani, A., Woo, E., Friedmann, P. S., King, E. V., Thomas, G. J., Sanchez-Elsner, T., Vijayanand, P., & Ottensmeier, C. H.
- Affiliations
- La Jolla Institute for Immunology (US)
- University of Southampton (GB)
- University Hospital Southampton NHS Foundation Trust (GB)
- Corresponding author
- Vijayanand, Pandurangan
- ORCID
- Venue
- Nature Immunology
- Published
- 2017-06-19
- Volume
- 18
- Issue
- 8
- Pages
- 940-950
- ISSN
- 1529-2908 (ISSN-L)
- 1529-2916
- PMC
- PMC6036910
- OpenAlex
- W2626312449
- Cited by
- 528
- References
- 66
- Citations by year
- 2026: 28 · 2025: 45 · 2024: 51 · 2023: 60 · 2022: 68 · 2021: 85 · 2020: 64 · 2019: 65 · 2018: 52 · 2017: 10
- FWCI
- 23.03
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Nature Immunology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- ePrints Soton (University of Southampton) (submittedVersion)
- Zenodo (CERN European Organization for Nuclear Research) (submittedVersion)
- Funders
- Cancer Research UK (S_1716, 18158, 18892, 18161, 15951, 20613, 21998, 22795, 23904)
- National Institutes of Health (1s10od016262-01)
- Medical Research Council (MR/P024351/1)
- Topics
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- lung cancer, tissue-resident memory T cells, CD8+ T cells, cytotoxic T lymphocytes, tumor-infiltrating lymphocytes, CD103, T cell cytotoxicity, PD-1, TIM-3, 4-1BB, T cell receptor stimulation, immune checkpoint, tumor transcriptome, survival prediction, immunotherapy targets
- MeSH terms
- Hepatitis A Virus Cellular Receptor 2, Squamous Cell Carcinoma of Head and Neck, Adenocarcinoma, Adult, Aged, Aged, 80 and over, Carcinoma, Squamous Cell, Female, Head and Neck Neoplasms, Humans, Immunologic Memory, Immunotherapy, Lung Neoplasms, Male, Middle Aged, Prognosis, Receptors, Antigen, T-Cell, T-Lymphocytes, Cytotoxic, Antigens, CD, Survival Rate, Lymphocytes, Tumor-Infiltrating, Gene Expression Profiling, Integrin alpha Chains, Tumor Necrosis Factor Receptor Superfamily, Member 9, Programmed Cell Death 1 Receptor
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