The DOI matches its Crossref record; 9 of the 9 references it cites were found in a registry or an index.
The Three Es of Cancer Immunoediting
Abstract
After a century of controversy, the notion that the immune system regulates cancer development is experiencing a new resurgence. An overwhelming amount of data from animal models—together with compelling data from human patients—indicate that a functional cancer immunosurveillance process indeed exists that acts as an extrinsic tumor suppressor. However, it has also become clear that the immune system can facilitate tumor progression, at least in part, by sculpting the immunogenic phenotype of tumors as they develop. The recognition that immunity plays a dual role in the complex interactions between tumors and the host prompted a refinement of the cancer immunosurveillance hypothesis into one termed “cancer immunoediting.” In this review, we summarize the history of the cancer immunosurveillance controversy and discuss its resolution and evolution into the three Es of cancer immunoediting—elimination, equilibrium, and escape.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Genetic instabilities in human cancers
Lengauer, C., Kinzler, K. W., & Vogelstein, B. (1998) · Nature · doi:10.1038/25292 · Cited by 4,168
How Matrix Metalloproteinases Regulate Cell Behavior
Sternlicht, M. D., & Werb, Z. (2001) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.17.1.463 · Cited by 3,959
Intratumoral T Cells, Recurrence, and Survival in Epithelial Ovarian Cancer
Zhang, L., Conejo-Garcia, J. R., Katsaros, D., Gimotty, P. A., Massobrio, M., Regnani, G., Makrigiannakis, A., Gray, H., Schlienger, K., Liebman, M. N., et al. (2003) · New England Journal of Medicine · doi:10.1056/nejmoa020177 · Cited by 3,397
Demonstration of an interferon γ-dependent tumor surveillance system in immunocompetent mice
Kaplan, D. H., Shankaran, V., Dighe, A. S., Stockert, E., Aguet, M., Old, L. J., & Schreiber, R. D. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.13.7556 · Cited by 1,465
Self-citationNatural selection of tumor variants in the generation of “tumor escape” phenotypes
Khong, H. T., & Restifo, N. P. (2002) · Nature Immunology · doi:10.1038/ni1102-999 · Cited by 1,058
Diefenbach, A., Jamieson, A. M., Liu, S. D., Shastri, N., & Raulet, D. H. (2000) · Nature Immunology · doi:10.1038/77793 · Cited by 878
Dighe, A. S., Richards, E., Old, L. J., & Schreiber, R. D. (1994) · Immunity · doi:10.1016/1074-7613(94)90087-6 · Cited by 663
Self-citationVicari, A. P., & Caux, C. (2002) · Cytokine & Growth Factor Reviews · doi:10.1016/s1359-6101(01)00033-8 · Cited by 351
Jinushi, M., Takehara, T., Tatsumi, T., Kanto, T., Groh, V., Spies, T., Kimura, R., Miyagi, T., Mochizuki, K., Sasaki, Y., et al. (2003) · International Journal of Cancer · doi:10.1002/ijc.10966 · Cited by 244
Cited by
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
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
Self-citationThe immune contexture in human tumours: impact on clinical outcome
Fridman, W. H., Pagès, F., Sautès-Fridman, C., & Galon, J. (2012) · Nature reviews. Cancer · doi:10.1038/nrc3245 · Cited by 4,981
Inflammation and cancer: triggers, mechanisms, and consequences
Greten, F. R., & Grivennikov, S. I. (2019) · Immunity · doi:10.1016/j.immuni.2019.06.025 · Cited by 3,806
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
Fundamental Mechanisms of Immune Checkpoint Blockade Therapy
Wei, S. C., Duffy, C. R., & Allison, J. P. (2018) · Cancer Discovery · doi:10.1158/2159-8290.cd-18-0367 · Cited by 3,088
PD-L1 expression as a predictive biomarker in cancer immunotherapy
Patel, S. P., & Kurzrock, R. (2015) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-14-0983 · Cited by 2,291
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
The Tumour Microenvironment after Radiotherapy: Mechanisms of Resistance and Recurrence
Barker, H. E., Paget, J. T. E., Khan, A. A., & Harrington, K. J. (2015) · Nature Reviews Cancer · doi:10.1038/nrc3958 · Cited by 2,144
Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity
Sakuishi, K., Apetoh, L., Sullivan, J. M., Blazar, B. R., Kuchroo, V. K., & Anderson, A. C. (2010) · Journal of Experimental Medicine · doi:10.1084/jem.20100643 · Cited by 2,072
Terzić, J., Grivennikov, S., Karin, E., & Karin, M. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.01.058 · Cited by 1,974
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
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
Self-citationRole of tumor microenvironment in tumorigenesis
Wang, M., Zhao, J., Zhang, L., Wei, F., Lian, Y., Wu, Y., Gong, Z., Zhang, S., Zhou, J., Cao, K., et al. (2017) · Journal of Cancer · doi:10.7150/jca.17648 · Cited by 1,404
Cancer despite immunosurveillance: immunoselection and immunosubversion
Zitvogel, L., Tesniere, A., & Kroemer, G. (2006) · Nature reviews. Immunology · doi:10.1038/nri1936 · Cited by 1,324
Type I interferons in anticancer immunity
Zitvogel, L., Galluzzi, L., Kepp, O., Smyth, M. J., & Kroemer, G. (2015) · Nature Reviews Immunology · doi:10.1038/nri3845 · Cited by 1,305
Dangerous liaisons: STAT3 and NF-κB collaboration and crosstalk in cancer
Grivennikov, S. I., & Karin, M. (2010) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2009.11.005 · Cited by 1,160
Tosolini, M., Kirilovsky, A., Mlecnik, B., Fredriksen, T., Mauger, S., Bindea, G., Berger, A., Bruneval, P., Fridman, W.-H., Pagès, F., et al. (2011) · Cancer Research · doi:10.1158/0008-5472.can-10-2907 · Cited by 1,146
Type I interferon is selectively required by dendritic cells for immune rejection of tumors
Diamond, M. S., Kinder, M., Matsushita, H., Mashayekhi, M., Dunn, G. P., Archambault, J. M., Lee, H., Arthur, C. D., White, J. M., Kalinke, U., et al. (2011) · Journal of Experimental Medicine · doi:10.1084/jem.20101158 · Cited by 1,081
Self-citationCD8+ T cell differentiation and dysfunction in cancer
Philip, M., & Schietinger, A. (2022) · Nature Reviews Immunology · doi:10.1038/s41577-021-00574-3 · Cited by 1,052
Mlecnik, B., Tosolini, M., Kirilovsky, A., Berger, A., Bindea, G., Meatchi, T., Bruneval, P., Trajanoski, Z., Fridman, W.-H., Pagès, F., et al. (2011) · Journal of Clinical Oncology · doi:10.1200/jco.2010.30.5425 · Cited by 1,009
Intratumor Heterogeneity: The Rosetta Stone of Therapy Resistance
Marusyk, A., Janiszewska, M., & Polyak, K. (2020) · Cancer Cell · doi:10.1016/j.ccell.2020.03.007 · Cited by 1,009
Dynamics of the immune reaction to pancreatic cancer from inception to invasion
Clark, C. E., Hingorani, S. R., Mick, R., Combs, C., Tuveson, D. A., & Vonderheide, R. H. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-0175 · Cited by 990
Palucka, A. K., & Coussens, L. M. (2016) · Cell · doi:10.1016/j.cell.2016.01.049 · Cited by 843
Lipid Nanoparticle Assisted mRNA Delivery for Potent Cancer Immunotherapy
Oberli, M. A., Reichmuth, A. M., Dorkin, J. R., Mitchell, M. J., Fenton, O. S., Jaklenec, A., Anderson, D. G., Langer, R., & Blankschtein, D. (2017) · Nano Letters · doi:10.1021/acs.nanolett.6b03329 · Cited by 719
NK cells and cancer immunosurveillance
Waldhauer, I., & Steinle, A. (2008) · Oncogene · doi:10.1038/onc.2008.267 · Cited by 682
Arlauckas, S. P., Garris, C. S., Kohler, R. H., Kitaoka, M., Cuccarese, M. F., Yang, K. S., Miller, M. A., Carlson, J. C., Freeman, G. J., Anthony, R. M., et al. (2017) · Science Translational Medicine · doi:10.1126/scitranslmed.aal3604 · Cited by 669
Immune escape to PD-L1/PD-1 blockade: seven steps to success (or failure)
Kim, J. M., & Chen, D. S. (2016) · Annals of Oncology · doi:10.1093/annonc/mdw217 · Cited by 648
Anticancer effects of the microbiome and its products
Zitvogel, L., Daillère, R., Roberti, M. P., Routy, B., & Kroemer, G. (2017) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2017.44 · Cited by 538
Eyles, J., Puaux, A.-L., Wang, X., Toh, B., Prakash, C., Hong, M., Tan, T. G., Zheng, L., Ong, L. C., Jin, Y., et al. (2010) · Journal of Clinical Investigation · doi:10.1172/jci42002 · Cited by 506
López-Otín, C., & Kroemer, G. (2021) · Cell · doi:10.1016/j.cell.2020.11.034 · Cited by 499
Resistance Mechanisms to Anti-PD Cancer Immunotherapy
Vesely, M. D., Zhang, T., & Chen, L. (2022) · Annual Review of Immunology · doi:10.1146/annurev-immunol-070621-030155 · Cited by 468
Epitope Landscape in Breast and Colorectal Cancer
Segal, N. H., Parsons, D. W., Peggs, K. S., Velculescu, V., Kinzler, K. W., Vogelstein, B., & Allison, J. P. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-3095 · Cited by 416
Innate immune signaling and regulation in cancer immunotherapy
Corrales, L., Matson, V., Flood, B., Spranger, S., & Gajewski, T. F. (2017) · Cell Research · doi:10.1038/cr.2016.149 · Cited by 408
Maturation of tertiary lymphoid structures and recurrence of stage II and III colorectal cancer
Posch, F., Silina, K., Leibl, S., Mündlein, A., Moch, H., Siebenhüner, A., Samaras, P., Riedl, J., Stotz, M., Szkandera, J., et al. (2018) · OncoImmunology · doi:10.1080/2162402x.2017.1378844 · Cited by 380
Nanoparticles in tumor microenvironment remodeling and cancer immunotherapy
Lu, Q., Kou, D., Lou, S., Ashrafizadeh, M., Aref, A. R., Canadas, I., Tian, Y., Niu, X., Wang, Y., Torabian, P., et al. (2024) · Journal of Hematology & Oncology · doi:10.1186/s13045-024-01535-8 · Cited by 373
Cancer immunoediting by the innate immune system in the absence of adaptive immunity
O’Sullivan, T., Saddawi-Konefka, R., Vermi, W., Koebel, C. M., Arthur, C., White, J. M., Uppaluri, R., Andrews, D. M., Ngiow, S. F., Teng, M. W. L., et al. (2012) · Journal of Experimental Medicine · doi:10.1084/jem.20112738 · Cited by 348
Self-citationCommunication between EMT and PD-L1 signaling: New insights into tumor immune evasion
Jiang, Y., & Zhan, H. (2020) · Cancer Letters · doi:10.1016/j.canlet.2019.10.013 · Cited by 319
Tumor-infiltrating T lymphocytes: Friends or foes?
Yu, P., & Fu, Y.-X. (2006) · Laboratory Investigation · doi:10.1038/labinvest.3700389 · Cited by 299
Deep learning-based prediction of the T cell receptor–antigen binding specificity
Lu, T., Zhang, Z., Zhu, J., Wang, Y., Jiang, P., Xiao, X., Bernatchez, C., Heymach, J. V., Gibbons, D. L., Wang, J., et al. (2021) · Nature Machine Intelligence · doi:10.1038/s42256-021-00383-2 · Cited by 295
Freed-Pastor, W. A., Lambert, L. J., Ely, Z. A., Pattada, N. B., Bhutkar, A., Eng, G., Mercer, K. L., Garcia, A. P., Lin, L., Rideout, W. M., et al. (2021) · Cancer Cell · doi:10.1016/j.ccell.2021.07.007 · Cited by 273
The circadian clock in cancer development and therapy
Fu, L., & Kettner, N. M. (2013) · Progress in Molecular Biology and Translational Science · doi:10.1016/b978-0-12-396971-2.00009-9 · Cited by 251
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
McGilvray, R. W., Eagle, R. A., Watson, N. F. S., Al-Attar, A., Ball, G., Jafferji, I., Trowsdale, J., & Durrant, L. G. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-0991 · Cited by 196
“Cancer cells that survive must adapt to avoid the immune system, a process variously described as immunoediting, immune sculpting, or cancer immune evasion (21).”
BackgroundInfluentialMHC 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
Oncolytic virotherapy as immunotherapy
Melcher, A., Harrington, K., & Vile, R. (2021) · Science · doi:10.1126/science.abk3436 · Cited by 133
The impact of NF-κB signaling on pathogenesis and current treatment strategies in multiple myeloma
Vrábel, D., Pour, L., & Ševčíková, S. (2019) · Blood Reviews · doi:10.1016/j.blre.2018.11.003 · Cited by 123
The role of biomarkers in personalized immunotherapy
Sankar, K., Ye, J. C., Li, Z., Zheng, L., Song, W., & Hu-Lieskovan, S. (2022) · Biomarker Research · doi:10.1186/s40364-022-00378-0 · Cited by 111
Habashy, K. J., Mansour, R., Moussalem, C., Sawaya, R., & Massaad, M. J. (2022) · British Journal of Cancer · doi:10.1038/s41416-022-01864-w · Cited by 95
Mota Reyes, C., Teller, S., Muckenhuber, A., Konukiewitz, B., Safak, O., Weichert, W., Friess, H., Ceyhan, G. O., & Demir, I. E. (2020) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-19-1864 · Cited by 80
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
The Host Defense Peptide Cathelicidin Is Required for NK Cell-Mediated Suppression of Tumor Growth
Büchau, A. S., Morizane, S., Trowbridge, J., Schauber, J., Kotol, P., Bui, J. D., & Gallo, R. L. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0902110 · Cited by 73
Wang, A. Z., Mashimo, B. L., Schaettler, M. O., Sherpa, N. D., Leavitt, L. A., Livingstone, A. J., Khan, S. M., Li, M., Anzaldua-Campos, M. I., Bradley, J. D., et al. (2024) · Cancer Discovery · doi:10.1158/2159-8290.cd-23-0913 · Cited by 73
Self-citationConsiderations for successful cancer immunotherapy in aged hosts
Hurez, V, Padrón, Á. S., Svatek, R. S., & Curiel, T. J. (2016) · Clinical and Experimental Immunology · doi:10.1111/cei.12875 · Cited by 65
Lee, Y.-H., Bae, H. C., Noh, K. H., Song, K.-H., Ye, S.-K., Mao, C.-P., Lee, K.-M., Wu, T.-C., & Kim, T. W. (2015) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-14-1979 · Cited by 64
Jamieson, N. B., Mohamed, M., Oien, K. A., Foulis, A. K., Dickson, E. J., Imrie, C. W., Carter, C. R., McKay, C. J., & McMillan, D. C. (2012) · Annals of Surgical Oncology · doi:10.1245/s10434-012-2370-y · Cited by 60
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
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
Wang, Y., Hu, G.-F., & Wang, Z. (2017) · OncoTargets and Therapy · doi:10.2147/ott.s136259 · Cited by 21
Dendritic cells and B cells cooperate in the generation of CD4(+)CD25(+)FOXP3(+) allogeneic T cells
Moore, C., Sauma, D., Reyes, P. A., Morales, J., Rosemblatt, M., Bono, M. R., & Fierro, J. A. (2010) · Transplantation Proceedings · doi:10.1016/j.transproceed.2009.12.044 · Cited by 11
Spatiotemporal analysis of tumour-infiltrating immune cells in biliary carcinogenesis
Charbel, A., Tavernar, L., Albrecht, T., Brinkmann, F., Verheij, J., Roos, E., Vogel, M. N., Köhler, B., Springfeld, C., Brobeil, A., et al. (2022) · British Journal of Cancer · doi:10.1038/s41416-022-01933-0 · Cited by 11
Metadata
- Authors
- Dunn, G. P., Old, L. J., & Schreiber, R. D.
- Venue
- Annual Review of Immunology
- Publisher
- Annual Reviews
- Published
- 2004-04-01
- Volume
- 22
- Issue
- 1
- Pages
- 329-360
- ISSN
- 0732-0582 (ISSN-L)
- 1545-3278
- OpenAlex
- W2121626779
- Cited by
- 3,072
- References
- 9
- FWCI
- 4.32
- Type
- journal article
- Language
- en
- Open access
- closed
About these checks
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 ›
Are you an author, or do you see a problem with this page? Request a review
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.
