IFNγ and lymphocytes prevent primary tumour development and shape tumour immunogenicity
Abstract
Lymphocytes were originally thought to form the basis of a 'cancer immunosurveillance' process that protects immunocompetent hosts against primary tumour development, but this idea was largely abandoned when no differences in primary tumour development were found between athymic nude mice and syngeneic wild-type mice. However, subsequent observations that nude mice do not completely lack functional T cells and that two components of the immune system-IFNgamma and perforin-help to prevent tumour formation in mice have led to renewed interest in a tumour-suppressor role for the immune response. Here we show that lymphocytes and IFNgamma collaborate to protect against development of carcinogen-induced sarcomas and spontaneous epithelial carcinomas and also to select for tumour cells with reduced immunogenicity. The immune response thus functions as an effective extrinsic tumour-suppressor system. However, this process also leads to the immunoselection of tumour cells that are more capable of surviving in an immunocompetent host, which explains the apparent paradox of tumour formation in immunologically intact individuals.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The presence of tumor-infiltrating CD8+ T cells and the production of Th1 cytokines within tumors are correlated with favorable prognoses in overall survival and disease-free survival across various malignancies.
“The presence of tumor-infiltrating CD8+ T cells and the production of Th1 cytokines within tumors have been correlated with favorable prognoses in terms of overall survival and disease-free survival across various malignancies [11,12,13,14].”
From Mesenchymal Stem/Stromal Cells: Immunomodulatory and Bone Regeneration Potential after Tumor Excision in Osteosarcoma Patients (2023) · cites this paper as [14]
Cites
Dighe, A. S., Richards, E., Old, L. J., & Schreiber, R. D. (1994) · Immunity · doi:10.1016/1074-7613(94)90087-6 · Cited by 663 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Immunity, Inflammation, and Cancer
Grivennikov, S. I., Greten, F. R., & Karin, M. (2010) · Cell · doi:10.1016/j.cell.2010.01.025 · Cited by 10,755 · see citing works
Microenvironmental regulation of tumor progression and metastasis
Quail, D. F., & Joyce, J. A. (2013) · Nature Medicine · doi:10.1038/nm.3394 · Cited by 7,994 · 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
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-citationPrimary, 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
Cancer immunoediting: from immunosurveillance to tumor escape
Dunn, G. P., Bruce, A. T., Ikeda, H., Old, L. J., & Schreiber, R. D. (2002) · Nature Immunology · doi:10.1038/ni1102-991 · Cited by 5,393 · see citing works
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 · see citing works
Neoantigens in cancer immunotherapy
Schumacher, T. N., & Schreiber, R. D. (2015) · Science · doi:10.1126/science.aaa4971 · Cited by 4,783 · see citing works
Self-citationRoles of the immune system in cancer: From tumor initiation to metastatic progression
Gonzalez, H., Hagerling, C., & Werb, Z. (2018) · Genes & Development · doi:10.1101/gad.314617.118 · Cited by 2,111 · see citing works
Hildner, K., Edelson, B. T., Purtha, W. E., Diamond, M., Matsushita, H., Kohyama, M., Calderon, B., Schraml, B. U., Unanue, E. R., Diamond, M. S., et al. (2008) · Science · doi:10.1126/science.1164206 · Cited by 2,081 · 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
Self-citationImmunological aspects of cancer chemotherapy
Zitvogel, L., Apetoh, L., Ghiringhelli, F., & Kroemer, G. (2008) · Nature Reviews Immunology · doi:10.1038/nri2216 · Cited by 1,712 · 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-citationLlosa, N. J., Cruise, M., Tam, A., Wicks, E. C., Hechenbleikner, E. M., Taube, J. M., Blosser, R. L., Fan, H., Wang, H., Luber, B. S., et al. (2015) · Cancer Discovery · doi:10.1158/2159-8290.cd-14-0863 · Cited by 1,487 · see citing works
Mittal, D., Gubin, M. M., Schreiber, R. D., & Smyth, M. J. (2014) · Current Opinion in Immunology · doi:10.1016/j.coi.2014.01.004 · Cited by 1,471 · see citing works
Self-citationTGF-β directly targets cytotoxic T cell functions during tumor evasion of immune surveillance
Thomas, D. A., & Massagué, J. (2005) · Cancer Cell · doi:10.1016/j.ccr.2005.10.012 · Cited by 1,355 · see citing works
Interferon-Gamma at the Crossroads of Tumor Immune Surveillance or Evasion
Castro, F., Cardoso, A. P., Gonçalves, R. M., Serre, K., & Oliveira, M. J. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00847 · Cited by 1,224 · see citing works
Cancer Immune Evasion Through Loss of MHC Class I Antigen Presentation
Dhatchinamoorthy, K., Colbert, J. D., & Rock, K. L. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.636568 · Cited by 1,077 · 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
Natural 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 · see citing works
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 · 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
Chen, M.-L., Pittet, M. J., Gorelik, L., Flavell, R. A., Weissleder, R., von Boehmer, H., & Khazaie, K. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0408197102 · Cited by 806 · see citing works
Hezaveh, K., Shinde, R. S., Klötgen, A., Halaby, M. J., Lamorte, S., Ciudad, M. T., Quevedo, R., Neufeld, L., Liu, Z. Q., Jin, R., et al. (2022) · Immunity · doi:10.1016/j.immuni.2022.01.006 · Cited by 746 · see citing works
NK cells and cancer immunosurveillance
Waldhauer, I., & Steinle, A. (2008) · Oncogene · doi:10.1038/onc.2008.267 · Cited by 682 · see citing works
TREM2 Modulation Remodels the Tumor Myeloid Landscape Enhancing Anti-PD-1 Immunotherapy
Molgora, M., Esaulova, E., Vermi, W., Hou, J., Chen, Y., Luo, J., Brioschi, S., Bugatti, M., Omodei, A. S., Ricci, B., et al. (2020) · Cell · doi:10.1016/j.cell.2020.07.013 · Cited by 656 · see citing works
“Since these tumors were developed in immunocompetent WT mice, their immunogenic profiles were edited by the immune system, and hence, they grow unopposed when transplanted into naive syngeneic WT hosts (Alspach et al., 2019; Schreiber et al., 2011; Shankaran et al., 2001).”
Self-citationDoedens, A. L., Stockmann, C., Rubinstein, M. P., Liao, D., Zhang, N., DeNardo, D. G., Coussens, L. M., Karin, M., Goldrath, A. W., & Johnson, R. S. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-1439 · Cited by 652 · see citing works
Inflammation as a Tumor Promoter in Cancer Induction
Philip, M., Rowley, D. A., & Schreiber, H. (2004) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2004.06.006 · Cited by 640 · see citing works
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
An HIF-1α/VEGF-A Axis in Cytotoxic T Cells Regulates Tumor Progression
Palazon, A., Tyrakis, P. A., Macias, D., Veliça, P., Rundqvist, H., Fitzpatrick, S., Vojnovic, N., Phan, A. T., Loman, N., Hedenfalk, I., et al. (2017) · Cancer Cell · doi:10.1016/j.ccell.2017.10.003 · Cited by 521 · see citing works
“These immunologic molecules are key in immunosurveillance (Kaplan et al., 1998; Shankaran et al., 2001).”
BackgroundDustin, M. L. (2014) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-14-0161 · Cited by 502 · 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
Primary Antitumor Immune Response Mediated by CD4+ T Cells
Corthay, A., Skovseth, D. K., Lundin, K. U., Røsjø, E., Omholt, H., Hofgaard, P. O., Haraldsen, G., & Bogen, B. (2005) · Immunity · doi:10.1016/j.immuni.2005.02.003 · Cited by 478 · see citing works
Immune resistance orchestrated by the tumor microenvironment
Gajewski, T. F., Meng, Y., Blank, C., Brown, I., Kacha, A., Kline, J., & Harlin, H. (2006) · Immunological Reviews · doi:10.1111/j.1600-065x.2006.00442.x · Cited by 437 · see citing works
Zaki, M. H., Vogel, P., Body-Malapel, M., Lamkanfi, M., & Kanneganti, T.-D. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.1002046 · Cited by 411 · see citing works
Sharma, P., Pachynski, R. K., Narayan, V., Fléchon, A., Gravis, G., Galsky, M. D., Mahammedi, H., Patnaik, A., Subudhi, S. K., Ciprotti, M., et al. (2020) · Cancer Cell · doi:10.1016/j.ccell.2020.08.007 · Cited by 406 · see citing works
Arthur, J. C., Gharaibeh, R. Z., Mühlbauer, M., Perez-Chanona, E., Uronis, J. M., McCafferty, J., Fodor, A. A., & Jobin, C. (2014) · Nature Communications · doi:10.1038/ncomms5724 · Cited by 392 · see citing works
Cancer immunoediting: antigens, mechanisms, and implications to cancer immunotherapy
Vesely, M. D., & Schreiber, R. D. (2013) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12105 · Cited by 367 · see citing works
Self-citationLakshmikanth, T., Burke, S., Ali, T. H., Kimpfler, S., Ursini, F., Ruggeri, L., Capanni, M., Umansky, V., Paschen, A., Sucker, A., et al. (2009) · Journal of Clinical Investigation · doi:10.1172/jci36022 · Cited by 347 · see citing works
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 · see citing works
Self-citationp53, cancer and the immune response
Blagih, J., Buck, M. D., & Vousden, K. H. (2020) · Journal of Cell Science · doi:10.1242/jcs.237453 · Cited by 333 · see citing works
Roles of unphosphorylated STATs in signaling
Yang, J., & Stark, G. R. (2008) · Cell Research · doi:10.1038/cr.2008.41 · Cited by 347 · see citing works
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
From mice to humans: developments in cancer immunoediting
Teng, M. W. L., Galon, J., Fridman, W.-H., & Smyth, M. J. (2015) · Journal of Clinical Investigation · doi:10.1172/jci80004 · Cited by 337 · see citing works
The immune system and cancer evasion strategies: therapeutic concepts
Muenst, S., Läubli, H., Soysal, S. D., Zippelius, A., Tzankov, A., & Hoeller, S. (2016) · Journal of Internal Medicine · doi:10.1111/joim.12470 · Cited by 304 · see citing works
Müller-Hermelink, N., Braumüller, H., Pichler, B., Wieder, T., Mailhammer, R., Schaak, K., Ghoreschi, K., Yazdi, A., Haubner, R., Sander, C. A., et al. (2008) · Cancer Cell · doi:10.1016/j.ccr.2008.04.001 · Cited by 302 · see citing works
Karachaliou, N., Gonzalez-Cao, M., Crespo, G., Drozdowskyj, A., Aldeguer, E., Gimenez-Capitan, A., Teixido, C., Molina-Vila, M. A., Viteri, S., De Los Llanos Gil, M., et al. (2018) · Therapeutic Advances in Medical Oncology · doi:10.1177/1758834017749748 · Cited by 285 · see citing works
Arrested differentiation, the self-renewing memory lymphocyte, and vaccination
Fearon, D. T., Manders, P., & Wagner, S. D. (2001) · Science · doi:10.1126/science.1062589 · Cited by 265 · see citing works
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 · see citing works
Increased vessel perfusion predicts the efficacy of immune checkpoint blockade
Zheng, X., Fang, Z., Liu, X., Deng, S., Zhou, P., Wang, X., Zhang, C., Yin, R., Hu, H., Chen, X., et al. (2018) · Journal of Clinical Investigation · doi:10.1172/jci96582 · Cited by 239 · see citing works
In vivo CRISPR screens reveal the landscape of immune evasion pathways across cancer
Dubrot, J., Du, P. P., Lane-Reticker, S. K., Kessler, E. A., Muscato, A. J., Mehta, A., Freeman, S. S., Allen, P. M., Olander, K. E., Ockerman, K. M., et al. (2022) · Nature Immunology · doi:10.1038/s41590-022-01315-x · Cited by 218 · see citing works
Lussier, D. M., Johnson, J. L., Hingorani, P., & Blattman, J. N. (2015) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-015-0067-z · 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
Kong, M., Tang, J., Qiao, Q., Wu, T., Qi, Y., Tan, S., Gao, X., & Zhang, Z. (2017) · Theranostics · doi:10.7150/thno.19987 · Cited by 197 · see citing works
Autophagy Regulation of Metabolism Is Required for CD8+ T Cell Anti-tumor Immunity
DeVorkin, L., Pavey, N., Carleton, G., Comber, A., Ho, C., Lim, J., McNamara, E., Huang, H., Kim, P., Zacharias, L. G., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.03.037 · Cited by 185 · see citing works
PI(3) kinase is associated with a mechanism of immunoresistance in breast and prostate cancer
Crane, C. A., Panner, A., Murray, J. C., Wilson, S. P., Xu, H., Chen, L., Simko, J. P., Waldman, F. M., Pieper, R. O., & Parsa, A. T. (2009) · Oncogene · doi:10.1038/onc.2008.384 · Cited by 181 · see citing works
Immunological Mechanisms Underneath the Efficacy of Cancer Therapy
Galluzzi, L., Zitvogel, L., & Kroemer, G. (2016) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-16-0197 · Cited by 175 · see citing works
Mondello, P., Tadros, S., Teater, M., Fontan, L., Chang, A. Y., Jain, N., Yang, H., Singh, S., Ying, H.-Y., Chu, C.-S., et al. (2020) · Cancer Discovery · doi:10.1158/2159-8290.cd-19-0116 · Cited by 167 · see citing works
Glucocorticoid modulation of cytokine signaling
Rogatsky, I., & Ivashkiv, L. B. (2006) · Tissue Antigens · doi:10.1111/j.1399-0039.2006.00599.x · Cited by 150 · see citing works
Immunoprophylactic and immunotherapeutic control of hormone receptor-positive breast cancer
Buqué, A., Bloy, N., Perez-Lanzón, M., Iribarren, K., Humeau, J., Pol, J. G., Levesque, S., Mondragon, L., Yamazaki, T., Sato, A., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-17644-0 · Cited by 138 · see citing works
Dual biological effects of the cytokines interleukin-10 and interferon-γ
Wilke, C. M., Wei, S., Wang, L., Kryczek, I., Kao, J., & Zou, W. (2011) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-011-1104-5 · Cited by 138 · see citing works
An intact immune system is required for the anticancer activities of histone deacetylase inhibitors
West, A. C., Mattarollo, S. R., Shortt, J., Cluse, L. A., Christiansen, A. J., Smyth, M. J., & Johnstone, R. W. (2013) · Cancer Research · doi:10.1158/0008-5472.can-13-0890 · Cited by 137 · 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
Intermittent hypoxia induces a metastatic phenotype in breast cancer
Chen, A., Sceneay, J., Gödde, N., Kinwel, T., Ham, S., Thompson, E. W., Humbert, P. O., & Möller, A. (2018) · Oncogene · doi:10.1038/s41388-018-0259-3 · Cited by 133 · see citing works
Nrf2 Induces IL-17D to Mediate Tumor and Virus Surveillance
Saddawi-Konefka, R., Seelige, R., Gross, E. T. E., Levy, E., Searles, S. C., Washington, A., Santosa, E. K., Liu, B., O’Sullivan, T. E., Harismendy, O., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.07.075 · Cited by 126 · 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
Kriegsman, B. A., Vangala, P., Chen, B. J., Meraner, P., Brass, A. L., Garber, M., & Rock, K. L. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1900475 · Cited by 114 · see citing works
Shi, L. Z., Fu, T., Guan, B., Chen, J., Blando, J. M., Allison, J. P., Xiong, L., Subudhi, S. K., Gao, J., & Sharma, P. (2016) · Nature Communications · doi:10.1038/ncomms12335 · Cited by 111 · 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
Colon cancer cells produce immunoregulatory glucocorticoids
Sidler, D., Renzulli, P., Schnoz, C., Berger, B., Schneider-Jakob, S., Flück, C., Inderbitzin, D., Corazza, N., Candinas, D., & Brunner, T. (2011) · Oncogene · doi:10.1038/onc.2010.629 · Cited by 107 · see citing works
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
“…was provided by the laboratory of Robert Schreiber, who observed that tumors generated in immunodeficient mice could be cleared upon transplantation into immunocompetent animals (Shankaran et al., 2001), confirming the existence of cancer immunosurveillance and immu- noediting (Dunn et al., 2002).”
MethodTheisen, D. J., Ferris, S. T., Briseño, C. G., Kretzer, N., Iwata, A., Murphy, K. M., & Murphy, T. L. (2019) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-18-0138 · Cited by 66 · 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
Donkor, M. K., Sarkar, A., & Li, M. O. (2012) · OncoImmunology · doi:10.4161/onci.1.2.18481 · Cited by 48 · 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
Rapoport, B. L., Nayler, S., Mlecnik, B., Smit, T., Heyman, L., Bouquet, I., Martel, M., Galon, J., Benn, C.-A., & Anderson, R. (2022) · Cancers · doi:10.3390/cancers14102525 · Cited by 33 · 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
Baron, M., Drohat, P., Crawford, B., Hornicek, F. J., Best, T. M., & Kouroupis, D. (2023) · Bioengineering · doi:10.3390/bioengineering10101187 · Cited by 19 · see citing works
Research progress of T cells in cholangiocarcinoma
Wang, Z., Dai, Y., Zhou, Y., Wang, Y., Chen, P., Li, Y., Zhang, Y., Wang, X., Hu, Y., Li, H., et al. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1453344 · Cited by 2 · see citing works
- Authors
- Shankaran, V., Ikeda, H., Bruce, A. T., White, J. M., Swanson, P. E., Old, L. J., & Schreiber, R. D.
- Affiliations
- Washington University in St. Louis (US)
- Memorial Sloan Kettering Cancer Center (US)
- Corresponding author
- Schreiber, Robert D.
- Venue
- Nature
- Published
- 2001-04-26
- Volume
- 410
- Issue
- 6832
- Pages
- 1107-1111
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W1642873092
- Cited by
- 2,896
- References
- 1
- Citations by year
- 2026: 56 · 2025: 85 · 2024: 108 · 2023: 141 · 2022: 145 · 2021: 138 · 2020: 175 · 2019: 142 · 2018: 152 · 2017: 154 · 2016: 143 · 2015: 149 · 2014: 121 · 2013: 133 · 2012: 127
- FWCI
- 34.13
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- 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
- interferon-gamma, lymphocytes, tumor surveillance, tumor suppression, tumor immunogenicity, immunoselection, perforin, epithelial cancers, nude mice, T cells, tumor immunology
- MeSH terms
- ATP Binding Cassette Transporter, Subfamily B, Member 2, Animals, Carcinoma, DNA-Binding Proteins, Female, H-2 Antigens, Immunocompetence, Interferon-gamma, Lymphocytes, Methylcholanthrene, Neoplasm Transplantation, Retroviridae, Sarcoma, Experimental, Immunophenotyping, ATP-Binding Cassette Transporters, Mice
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