Cancer immunoediting: from immunosurveillance to tumor escape

Dunn, Gavin P.; Bruce, Allen T.; Ikeda, Hiroaki; Old, Lloyd J.; Schreiber, Robert D.

doi:10.1038/ni1102-991

Cited by 5,393Cancer Immunotherapy and BiomarkersImmunotherapy and Immune ResponsesT-cell and B-cell Immunology

Cancer immunoediting: from immunosurveillance to tumor escape

Dunn, Gavin P., Bruce, Allen T., Ikeda, Hiroaki, Old, Lloyd J., Schreiber, Robert D.·2002·Nature Immunology

DOI 10.1038/ni1102-991

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Abstract

The concept that the immune system can recognize and destroy nascent transformed cells was originally embodied in the cancer immunosurveillance hypothesis of Burnet and Thomas. This hypothesis was abandoned shortly afterwards because of the absence of strong experimental evidence supporting the concept. New data, however, clearly show the existence of cancer immunosurveillance and also indicate that it may function as a component of a more general process of cancer immunoediting. This process is responsible for both eliminating tumors and sculpting the immunogenic phenotypes of tumors that eventually form in immunocompetent hosts. In this review, we will summarize the historical and experimental basis of cancer immunoediting and discuss its dual roles in promoting host protection against cancer and facilitating tumor escape from immune destruction.

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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
Cancer Immunoediting: Integrating Immunity’s Roles in Cancer Suppression and Promotion
Schreiber, R. D., Old, L. J., & Smyth, M. J. (2011) · Science · doi:10.1126/science.1203486 · Cited by 6,474 · see citing works
Self-citation
Primary, Adaptive, and Acquired Resistance to Cancer Immunotherapy
Sharma, P., Hu-Lieskovan, S., Wargo, J. A., & Ribas, A. (2017) · Cell · doi:10.1016/j.cell.2017.01.017 · Cited by 5,588 · see citing works
Interferon-γ: an overview of signals, mechanisms and functions
Schroder, K., Hertzog, P. J., Ravasi, T., & Hume, D. A. (2004) · Journal of Leukocyte Biology · doi:10.1189/jlb.0603252 · Cited by 4,120 · see citing works
Mutations Associated with Acquired Resistance to PD-1 Blockade in Melanoma
Zaretsky, J. M., Garcia-Diaz, A., Shin, D. S., Escuin-Ordinas, H., Hugo, W., Hu-Lieskovan, S., Torrejon, D. Y., Abril-Rodriguez, G., Sandoval, S., Barthly, L., et al. (2016) · New England Journal of Medicine · doi:10.1056/nejmoa1604958 · Cited by 3,237 · see citing works
Social support and health: a review of physiological processes potentially underlying links to disease outcomes.
Uchino, B. N. (2006) · Journal of Behavioral Medicine · doi:10.1007/s10865-006-9056-5 · Cited by 2,507 · see citing works
Ido expression by dendritic cells: tolerance and tryptophan catabolism
Mellor, A. L., & Munn, D. H. (2004) · Nature Reviews Immunology · doi:10.1038/nri1457 · Cited by 2,341 · see citing works
Effector Memory T Cells, Early Metastasis, and Survival in Colorectal Cancer
Pagès, F., Berger, A., Camus, M., Sanchez-Cabo, F., Costes, A., Molidor, R., Mlecnik, B., Kirilovsky, A., Nilsson, M., Damotte, D., et al. (2005) · New England Journal of Medicine · doi:10.1056/nejmoa051424 · Cited by 2,135 · see citing works
Immunotherapy in colorectal cancer: Rationale, challenges and potential
Ganesh, K., Stadler, Z. K., Cercek, A., Mendelsohn, R. B., Shia, J., Segal, N. H., & Diaz, L. A. (2019) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0126-x · Cited by 1,954 · see citing works
Immunosuppressive networks in the tumour environment and their therapeutic relevance
Zou, W. (2005) · Nature Reviews Cancer · doi:10.1038/nrc1586 · Cited by 2,057 · see citing works
Checkpoint blockade cancer immunotherapy targets tumour-specific mutant antigens
Gubin, M. M., Zhang, X., Schuster, H., Caron, E., Ward, J. P., Noguchi, T., Ivanova, Y., Hundal, J., Arthur, C. D., Krebber, W.-J., et al. (2014) · Nature · doi:10.1038/nature13988 · Cited by 1,974 · see citing works
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Immune evasion in cancer: mechanistic basis and therapeutic strategies
Vinay, D. S., Ryan, E. P., Pawelec, G., Talib, W. H., Stagg, J., Elkord, E., Lichtor, T., Decker, W. K., Whelan, R. L., Kumara, H. M. C. S., et al. (2015) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2015.03.004 · Cited by 1,625 · see citing works
Immune Inhibitory Molecules LAG-3 and PD-1 Synergistically Regulate T-cell Function to Promote Tumoral Immune Escape
Woo, S.-R., Turnis, M. E., Goldberg, M. V., Bankoti, J., Selby, M., Nirschl, C. J., Bettini, M. L., Gravano, D. M., Vogel, P., Liu, C. L., et al. (2012) · Cancer Research · doi:10.1158/0008-5472.can-11-1620 · Cited by 1,647 · see citing works
Interferons, immunity and cancer immunoediting
Dunn, G. P., Koebel, C. M., & Schreiber, R. D. (2006) · Nature Reviews Immunology · doi:10.1038/nri1961 · Cited by 1,617 · see citing works
Self-citation
CRISPR-engineered T cells in patients with refractory cancer
Stadtmauer, E. A., Fraietta, J. A., Davis, M. M., Cohen, A. D., Weber, K. L., Lancaster, E., Mangan, P. A., Kulikovskaya, I., Gupta, M., Chen, F., et al. (2020) · Science · doi:10.1126/science.aba7365 · Cited by 1,478 · see citing works
Primary Resistance to PD-1 Blockade Mediated by <i>JAK1/2</i> Mutations
Shin, D. S., Zaretsky, J. M., Escuin-Ordinas, H., Garcia-Diaz, A., Hu-Lieskovan, S., Kalbasi, A., Grasso, C. S., Hugo, W., Sandoval, S., Torrejon, D. Y., et al. (2017) · Cancer Discovery · doi:10.1158/2159-8290.cd-16-1223 · Cited by 1,337 · see citing works
Neutrophil: A Cell with Many Roles in Inflammation or Several Cell Types?
Rosales, C. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00113 · Cited by 1,334 · see citing works
Targeting neoantigens to augment antitumour immunity
Yarchoan, M., Johnson, B. A., Lutz, E. R., Laheru, D. A., & Jaffee, E. M. (2017) · Nature Reviews Cancer · doi:10.1038/nrc.2016.154 · Cited by 997 · see citing works
Fat, fibre and cancer risk in African Americans and rural Africans
O’Keefe, S. J. D., Li, J. V., Lahti, L., Ou, J., Carbonero, F., Mohammed, K., Posma, J. M., Kinross, J., Wahl, E., Ruder, E., et al. (2015) · Nature Communications · doi:10.1038/ncomms7342 · Cited by 982 · see citing works
β-Catenin Activation Promotes Immune Escape and Resistance to Anti–PD-1 Therapy in Hepatocellular Carcinoma
Ruiz de Galarreta, M., Bresnahan, E., Molina-Sánchez, P., Lindblad, K. E., Maier, B., Sia, D., Puigvehi, M., Miguela, V., Casanova-Acebes, M., Dhainaut, M., et al. (2019) · Cancer Discovery · doi:10.1158/2159-8290.cd-19-0074 · Cited by 912 · see citing works
NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy
Guerra, N., Tan, Y. X., Joncker, N. T., Choy, A., Gallardo, F., Xiong, N., Knoblaugh, S., Cado, D., Greenberg, N. R., & Raulet, D. H. (2008) · Immunity · doi:10.1016/j.immuni.2008.02.016 · Cited by 850 · see citing works
IFN-γ from lymphocytes induces PD-L1 expression and promotes progression of ovarian cancer
Abiko, K., Matsumura, N., Hamanishi, J., Horikawa, N., Murakami, R., Yamaguchi, K., Yoshioka, Y., Baba, T., Konishi, I., & Mandai, M. (2015) · British Journal of Cancer · doi:10.1038/bjc.2015.101 · Cited by 725 · see citing works
The circadian clock: pacemaker and tumour suppressor
Fu, L., & Lee, C. C. (2003) · Nature reviews. Cancer · doi:10.1038/nrc1072 · Cited by 678 · see citing works
Prognostic value of indoleamine 2,3-dioxygenase expression in colorectal cancer: effect on tumor-infiltrating T cells
Brandacher, G., Perathoner, A., Ladurner, R., Schneeberger, S., Obrist, P., Winkler, C., Werner, E. R., Werner-Felmayer, G., Weiss, H. G., G√∂bel, G., et al. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-05-1966 · Cited by 614 · see citing works
Combination Immunotherapy with CAR T Cells and Checkpoint Blockade for the Treatment of Solid Tumors
Grosser, R., Cherkassky, L., Chintala, N., & Adusumilli, P. S. (2019) · Cancer Cell · doi:10.1016/j.ccell.2019.09.006 · Cited by 603 · see citing works
Antitumor Activity in Melanoma and Anti-Self Responses in a Phase I Trial With the Anti-Cytotoxic T Lymphocyte–Associated Antigen 4 Monoclonal Antibody CP-675,206
Ribas, A., Camacho, L. H., Lopez-Berestein, G., Pavlov, D., Bulanhagui, C. A., Millham, R., Comin-Anduix, B., Reuben, J. M., Seja, E., Parker, C. A., et al. (2005) · Journal of Clinical Oncology · doi:10.1200/jco.2005.01.109 · Cited by 591 · see citing works
Chemotherapy Induces Programmed Cell Death-Ligand 1 Overexpression via the Nuclear Factor-κB to Foster an Immunosuppressive Tumor Microenvironment in Ovarian Cancer
Peng, J., Hamanishi, J., Matsumura, N., Abiko, K., Murat, K., Baba, T., Yamaguchi, K., Horikawa, N., Hosoe, Y., Murphy, S. K., et al. (2015) · Cancer Research · doi:10.1158/0008-5472.can-14-3098 · Cited by 525 · see citing works
Growth/Differentiation Factor-15 (GDF-15): From Biomarker to Novel Targetable Immune Checkpoint
Wischhusen, J., Melero, I., & Fridman, W. H. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.00951 · Cited by 506 · see citing works
The tumour glyco-code as a novel immune checkpoint for immunotherapy
RodrÍguez, E., Schetters, S. T. T., & van Kooyk, Y. (2018) · Nature Reviews Immunology · doi:10.1038/nri.2018.3 · Cited by 473 · see citing works
Silencing of Irf7 pathways in breast cancer cells promotes bone metastasis through immune escape
Bidwell, B. N., Slaney, C. Y., Withana, N. P., Forster, S., Cao, Y., Loi, S., Andrews, D., Mikeska, T., Mangan, N. E., Samarajiwa, S. A., et al. (2012) · Nature Medicine · doi:10.1038/nm.2830 · Cited by 487 · see citing works
The role of tumor-associated macrophages (TAMs) in tumor progression and relevant advance in targeted therapy
Yang, Q., Guo, N., Zhou, Y., Chen, J., Wei, Q., & Han, M. (2020) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2020.04.004 · Cited by 471 · see citing works
Exploiting the critical perioperative period to improve long-term cancer outcomes
Horowitz, M., Neeman, E., Sharon, E., & Ben-Eliyahu, S. (2015) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2014.224 · Cited by 487 · see citing works
Neutrophil-to-lymphocyte ratio and mortality in the United States general population
Song, M., Graubard, B. I., Rabkin, C. S., & Engels, E. A. (2021) · Scientific Reports · doi:10.1038/s41598-020-79431-7 · Cited by 434 · see citing works
New insights into the role of <scp>EMT</scp> in tumor immune escape
Terry, S., Savagner, P., Ortiz‐Cuaran, S., Mahjoubi, L., Saintigny, P., Thiery, J., & Chouaib, S. (2017) · Molecular Oncology · doi:10.1002/1878-0261.12093 · Cited by 414 · see citing works
CD4+ T Cells Contribute to the Remodeling of the Microenvironment Required for Sustained Tumor Regression upon Oncogene Inactivation
Rakhra, K., Bachireddy, P., Zabuawala, T., Zeiser, R., Xu, L., Kopelman, A., Fan, A. C., Yang, Q., Braunstein, L., Crosby, E., et al. (2010) · Cancer Cell · doi:10.1016/j.ccr.2010.10.002 · Cited by 339 · see citing works
Acquired resistance to cancer immunotherapy: Role of tumor-mediated immunosuppression
Saleh, R., & Elkord, E. (2020) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.07.017 · Cited by 292 · see citing works
Immunity, Hypoxia, and Metabolism–the Ménage à Trois of Cancer: Implications for Immunotherapy
Riera-Domingo, C., Audigé, A., Granja, S., Cheng, W.-C., Ho, P.-C., Baltazar, F., Stockmann, C., & Mazzone, M. (2020) · Physiological Reviews · doi:10.1152/physrev.00018.2019 · Cited by 310 · see citing works
Landscape of tumor-infiltrating T cell repertoire of human cancers
Li, B., Li, T., Pignon, J.-C., Wang, B., Wang, J., Shukla, S. A., Dou, R., Chen, Q., Hodi, F. S., Choueiri, T. K., et al. (2016) · Nature Genetics · doi:10.1038/ng.3581 · Cited by 306 · see citing works
The functional crosstalk between myeloid-derived suppressor cells and regulatory T cells within the immunosuppressive tumor microenvironment
Haist, M., Stege, H., Grabbe, S., & Bros, M. (2021) · Cancers · doi:10.3390/cancers13020210 · Cited by 295 · see citing works
Cell membrane coated-nanoparticles for cancer immunotherapy
Zeng, Y., Li, S., Zhang, S., Wang, L., Yuan, H., & Hu, F. (2022) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2022.02.023 · Cited by 238 · see citing works
Cytotoxic T-cells mediate exercise-induced reductions in tumor growth
Rundqvist, H., Veliça, P., Barbieri, L., Gameiro, P. A., Bargiela, D., Gojkovic, M., Mijwel, S., Reitzner, S. M., Wulliman, D., Ahlstedt, E., et al. (2020) · eLife · doi:10.7554/elife.59996 · Cited by 216 · see citing works
Pyroptosis‐Mediated Synergistic Photodynamic and Photothermal Immunotherapy Enabled by a Tumor‐Membrane‐Targeted Photosensitive Dimer
Tang, Y., Bisoyi, H. K., Chen, X., Liu, Z., Chen, X., Zhang, S., & Li, Q. (2023) · Advanced Materials · doi:10.1002/adma.202300232 · Cited by 214 · see citing works
Granulocytic Myeloid‐Derived Suppressor Cells Promote the Stemness of Colorectal Cancer Cells through Exosomal S100A9
Wang, Y., Yin, K., Tian, J., Xia, X., Ma, J., Tang, X., Xu, H., & Wang, S. (2019) · Advanced Science · doi:10.1002/advs.201901278 · Cited by 211 · see citing works
Immune system: a double-edged sword in cancer
Lakshmi Narendra, B., Eshvendar Reddy, K., Shantikumar, S., & Ramakrishna, S. (2013) · Inflammation Research · doi:10.1007/s00011-013-0645-9 · Cited by 206 · see citing works
Elimination of oncogenic neighbors by JNK-mediated engulfment in Drosophila
Ohsawa, S., Sugimura, K., Takino, K., Xu, T., Miyawaki, A., & Igaki, T. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.02.007 · Cited by 200 · see citing works
Acquired and intrinsic resistance in cancer immunotherapy
Kelderman, S., Schumacher, T. N. M., & Haanen, J. B. A. G. (2014) · Molecular Oncology · doi:10.1016/j.molonc.2014.07.011 · Cited by 197 · see citing works
Gut microbiome modulates efficacy of immune checkpoint inhibitors
Yi, M., Yu, S., Qin, S., Liu, Q., Xu, H., Zhao, W., Chu, Q., & Wu, K. (2018) · Journal of Hematology & Oncology · doi:10.1186/s13045-018-0592-6 · Cited by 179 · see citing works
Alternating electric fields (TTFields) inhibit metastatic spread of solid tumors to the lungs
Kirson, E. D., Giladi, M., Gurvich, Z., Itzhaki, A., Mordechovich, D., Schneiderman, R. S., Wasserman, Y., Ryffel, B., Goldsher, D., & Palti, Y. (2009) · Clinical & Experimental Metastasis · doi:10.1007/s10585-009-9262-y · Cited by 171 · see citing works
Targetable mechanisms driving immunoevasion of persistent senescent cells link chemotherapy-resistant cancer to aging
Muñoz, D. P., Yannone, S. M., Daemen, A., Sun, Y., Vakar-Lopez, F., Kawahara, M., Freund, A. M., Rodier, F., Wu, J. D., Desprez, P.-Y., et al. (2019) · JCI Insight · doi:10.1172/jci.insight.124716 · Cited by 162 · see citing works
Cross talk between cancer and immune cells: exploring complex dynamics in a microfluidic environment
Businaro, L., De Ninno, A., Schiavoni, G., Lucarini, V., Ciasca, G., Gerardino, A., Belardelli, F., Gabriele, L., & Mattei, F. (2013) · Lab Chip · doi:10.1039/c2lc40887b · Cited by 162 · see citing works
Targeting the tumor microenvironment: the protumor effects of IL-17 related to cancer type
Fabre, J., Giustiniani, J., Garbar, C., Antonicelli, F., Merrouche, Y., Bensussan, A., Bagot, M., & Al-Dacak, R. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17091433 · Cited by 159 · see citing works
Overcoming Genetically Based Resistance Mechanisms to PD-1 Blockade
Torrejon, D. Y., Abril-Rodriguez, G., Champhekar, A. S., Tsoi, J., Campbell, K. M., Kalbasi, A., Parisi, G., Zaretsky, J. M., Garcia-Diaz, A., Puig-Saus, C., et al. (2020) · Cancer Discovery · doi:10.1158/2159-8290.cd-19-1409 · Cited by 146 · see citing works
Hide or defend, the two strategies of lymphoma immune evasion: potential implications for immunotherapy
de Charette, M., & Houot, R. (2018) · Haematologica · doi:10.3324/haematol.2017.184192 · Cited by 129 · see citing works
MHC Class I Antigens and Immune Surveillance in Transformed Cells
Aptsiauri, N., Cabrera, T., Garcia‐Lora, A., Lopez‐Nevot, M. A., Ruiz‐Cabello, F., & Garrido, F. (2007) · International Review of Cytology · doi:10.1016/s0074-7696(07)56005-5 · Cited by 145 · see citing works
Clonal Deletion of Tumor-Specific T Cells by Interferon-γ Confers Therapeutic Resistance to Combination Immune Checkpoint Blockade
Pai, C.-C. S., Huang, J. T., Lu, X., Simons, D. M., Park, C., Chang, A., Tamaki, W., Liu, E., Roybal, K. T., Seagal, J., et al. (2019) · Immunity · doi:10.1016/j.immuni.2019.01.006 · Cited by 141 · see citing works
The CD4/CD8 ratio of tumor-infiltrating lymphocytes at the tumor-host interface has prognostic value in triple negative breast cancer
Wang, K., Shen, T., Siegal, G. P., & Wei, S. (2017) · Human Pathology · doi:10.1016/j.humpath.2017.09.012 · Cited by 123 · see citing works
Colorectal cancer and immunity: What we know and perspectives
Pernot, S. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i14.3738 · Cited by 131 · see citing works
Loss of chromosome Y (LOY) in blood cells is associated with increased risk for disease and mortality in aging men
Forsberg, L. A. (2017) · Human Genetics · doi:10.1007/s00439-017-1799-2 · Cited by 134 · see citing works
Co-delivery of nucleoside-modified mRNA and TLR agonists for cancer immunotherapy: restoring the immunogenicity of immunosilent mRNA
Verbeke, R., Lentacker, I., Wayteck, L., Breckpot, K., Van Bockstal, M., Descamps, B., Vanhove, C., De Smedt, S. C., & Dewitte, H. (2017) · Journal of Controlled Release · doi:10.1016/j.jconrel.2017.09.041 · Cited by 132 · see citing works
T Cell Surveillance of Oncogene-Induced Prostate Cancer Is Impeded by T Cell-Derived TGF-β1 Cytokine
Donkor, M. K., Sarkar, A., Savage, P. A., Franklin, R. A., Johnson, L. K., Jungbluth, A. A., Allison, J. P., & Li, M. O. (2011) · Immunity · doi:10.1016/j.immuni.2011.04.019 · Cited by 130 · see citing works
Cell-state dynamics and therapeutic resistance in melanoma from the perspective of MITF and IFNγ pathways
Bai, X., Fisher, D. E., & Flaherty, K. T. (2019) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-019-0204-6 · Cited by 107 · see citing works
Combination therapy based on nano codelivery for overcoming cancer drug resistance
Wang, H., & Huang, Y. (2020) · Medicine in Drug Discovery · doi:10.1016/j.medidd.2020.100024 · Cited by 115 · see citing works
Senescent Cells and Their Secretory Phenotype as Targets for Cancer Therapy
Velarde, M. C., Demaria, M., & Campisi, J. (2013) · Interdisciplinary Topics in Gerontology and Geriatrics · doi:10.1159/000343572 · Cited by 112 · see citing works
The Emerging Roles of Extracellular Vesicles As Communication Vehicles within the Tumor Microenvironment and Beyond
Sullivan, R., Maresh, G., Zhang, X., Salomon, C., Hooper, J., Margolin, D., & Li, L. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00194 · Cited by 112 · see citing works
Tumor‐Specific Photothermal‐Therapy‐Assisted Immunomodulation via Multiresponsive Adjuvant Nanoparticles
Liu, T., Zhu, M., Chang, X., Tang, X., Yuan, P., Tian, R., Zhu, Z., Zhang, Y., & Chen, X. (2023) · Advanced Materials · doi:10.1002/adma.202300086 · Cited by 98 · see citing works
Clonality of CD4+ Blood T Cells Predicts Longer Survival With CTLA4 or PD-1 Checkpoint Inhibition in Advanced Melanoma
Arakawa, A., Vollmer, S., Tietze, J., Galinski, A., Heppt, M. V., Bürdek, M., Berking, C., & Prinz, J. C. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01336 · Cited by 74 · see citing works
Ibrutinib treatment inhibits breast cancer progression and metastasis by inducing conversion of myeloid-derived suppressor cells to dendritic cells
Varikuti, S., Singh, B., Volpedo, G., Ahirwar, D. K., Jha, B. K., Saljoughian, N., Viana, A. G., Verma, C., Hamza, O., Halsey, G., et al. (2020) · British Journal of Cancer · doi:10.1038/s41416-020-0743-8 · Cited by 76 · see citing works
Interactions between cancer stem cells, immune system and some environmental components: Friends or foes?
Vahidian, F., Duijf, P. H. G., Safarzadeh, E., Derakhshani, A., Baghbanzadeh, A., & Baradaran, B. (2019) · Immunology Letters · doi:10.1016/j.imlet.2019.03.004 · Cited by 75 · see citing works
The effects of age and systemic metabolism on anti-tumor T cell responses
Drijvers, J. M., Sharpe, A. H., & Haigis, M. C. (2020) · eLife · doi:10.7554/elife.62420 · Cited by 69 · see citing works
Distinct Role for CD8 T Cells toward Cutaneous Tumors and Visceral Metastases
Lengagne, R., Graff-Dubois, S., Garcette, M., Renia, L., Kato, M., Guillet, J.-G., Engelhard, V. H., Avril, M.-F., Abastado, J.-P., & Prévost-Blondel, A. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.1.130 · Cited by 64 · see citing works
Hypoxia-inducible factors as key regulators of tumor inflammation
Mamlouk, S., & Wielockx, B. (2013) · International Journal of Cancer · doi:10.1002/ijc.27901 · Cited by 61 · see citing works
Formate Supplementation Enhances Antitumor CD8+ T-cell Fitness and Efficacy of PD-1 Blockade
Rowe, J. H., Elia, I., Shahid, O., Gaudiano, E. F., Sifnugel, N. E., Johnson, S., Reynolds, A. G., Fung, M. E., Joshi, S., LaFleur, M. W., et al. (2023) · Cancer Discovery · doi:10.1158/2159-8290.cd-22-1301 · Cited by 59 · see citing works
An intra-patient placebo-controlled phase I trial to evaluate the safety and tolerability of intradermal IMM-101 in melanoma
Stebbing, J., Dalgleish, A., Gifford-Moore, A., Martin, A., Gleeson, C., Wilson, G., Brunet, L. R., Grange, J., & Mudan, S. (2012) · Annals of Oncology · doi:10.1093/annonc/mdr363 · Cited by 55 · see citing works
A human nk cell activation/inhibition threshold allows small changes in the target cell surface phenotype to dramatically alter susceptibility to nk cells
Holmes, T. D., El-Sherbiny, Y. M., Davison, A., Clough, S. L., Blair, G. E., & Cook, G. P. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1000951 · Cited by 52 · see citing works
High immunogenic potential of p53 mRNA-transfected dendritic cells in patients with primary breast cancer
Met, Ö., Balslev, E., Flyger, H., & Svane, I. M. (2011) · Breast Cancer Research and Treatment · doi:10.1007/s10549-010-0844-9 · Cited by 51 · see citing works
TGF-beta: a master switch in tumor immunity
Gigante, M., Gesualdo, L., & Ranieri, E. (2012) · Current Pharmaceutical Design · doi:10.2174/138161212802430378 · Cited by 45 · see citing works
Gastrointestinal Tract Dysbiosis Enhances Distal Tumor Progression through Suppression of Leukocyte Trafficking
Jenkins, S. V., Robeson, M. S., Griffin, R. J., Quick, C. M., Siegel, E. R., Cannon, M. J., Vang, K. B., & Dings, R. P. M. (2019) · Cancer Research · doi:10.1158/0008-5472.can-18-4108 · Cited by 41 · see citing works
Current and Future Trends of Colorectal Cancer Treatment: Exploring Advances in Immunotherapy
Nikolouzakis, T. K., Chrysos, E., Docea, A. O., Fragkiadaki, P., Souglakos, J., Tsiaoussis, J., & Tsatsakis, A. (2024) · Cancers · doi:10.3390/cancers16111995 · Cited by 37 · see citing works
Manipulating the gut and tumor microbiota for immune checkpoint inhibitor therapy: from dream to reality
Guillot, N., Roméo, B., Manesh, S. S., Milano, G., Brest, P., Zitvogel, L., Hofman, P., & Mograbi, B. (2023) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2023.08.004 · Cited by 36 · see citing works
Cancer's second genome: Microbial cancer diagnostics and redefining clonal evolution as a multispecies process: Humans and their tumors are not aseptic, and the multispecies nature of cancer modulates clinical care and clonal evolution
Sepich‐Poore, G. D., Guccione, C., Laplane, L., Pradeu, T., Curtius, K., & Knight, R. (2022) · BioEssays · doi:10.1002/bies.202100252 · Cited by 33 · see citing works
Contribution of Aging, Obesity, and Microbiota on Tumor Immunotherapy Efficacy and Toxicity
Baiden-Amissah, R. E. M., & Tuyaerts, S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20143586 · Cited by 30 · see citing works
Immunotherapy in Glioblastoma: A Clinical Perspective
Desbaillets, N., & Hottinger, A. F. (2021) · Cancers · doi:10.3390/cancers13153721 · Cited by 31 · see citing works
Psychosocial Influences in Oncology: An Expanded Model of Biobehavioral Mechanisms
LUTGENDORF, S. K., COSTANZO, E. S., & SIEGEL, S. D. (2007) · Psychoneuroimmunology · doi:10.1016/b978-012088576-3/50048-4 · Cited by 28 · see citing works
Spatiotemporal analysis of tumour-infiltrating immune cells in biliary carcinogenesis
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Authors: Dunn, G. P., Bruce, A. T., Ikeda, H., Old, L. J., & Schreiber, R. D.
Affiliations: Washington University in St. Louis (US)
Memorial Sloan Kettering Cancer Center (US)
Corresponding author: Schreiber, Robert D.
ORCID: Dunn, Gavin P.
Ikeda, Hiroaki
Old, Lloyd J.
Schreiber, Robert D.
Venue: Nature Immunology
Publisher: Springer Science and Business Media LLC
Published: 2002-11-01
Volume: 3
Issue: 11
Pages: 991-998
ISSN: 1529-2908 (ISSN-L)
1529-2916
DOI: 10.1038/ni1102-991
OpenAlex: W2046972425
Cited by: 5,393
References: 99
Citations by year: 2026: 159 · 2025: 215 · 2024: 300 · 2023: 344 · 2022: 373 · 2021: 366 · 2020: 360 · 2019: 310 · 2018: 301 · 2017: 298 · 2016: 265 · 2015: 227 · 2014: 223 · 2013: 232 · 2012: 198
FWCI: 9.64
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Immunology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (1p01ca076464-01a1)
National Cancer Institute (CA-43059, CA76464)
Topics: Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Keywords: cancer immunoediting, tumor surveillance, tumor immune evasion, tumor immunogenicity, tumor immunology
MeSH terms: Animals, Antigens, Neoplasm, Humans, Immunologic Surveillance, Immunosuppression Therapy, Mice, Inbred Strains, Mice, Nude, Neoplasms, Postoperative Complications, Selection, Genetic, Transplantation Immunology, Gene Rearrangement, Incidence, Mice, SCID, Immunocompromised Host, Mice, Knockout, Models, Immunological, Tumor Escape, Genetic Predisposition to Disease, Mice

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Cancer immunoediting: from immunosurveillance to tumor escape

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