Radiation therapy and anti-tumor immunity: exposing immunogenic mutations to the immune system
Open accessAbstract
The expression of antigens that are recognized by self-reactive T cells is essential for immune-mediated tumor rejection by immune checkpoint blockade (ICB) therapy. Growing evidence suggests that mutation-associated neoantigens drive ICB responses in tumors with high mutational burden. In most patients, only a few of the mutations in the cancer exome that are predicted to be immunogenic are recognized by T cells. One factor that limits this recognition is the level of expression of the mutated gene product in cancer cells. Substantial preclinical data show that radiation can convert the irradiated tumor into a site for priming of tumor-specific T cells, that is, an in situ vaccine, and can induce responses in otherwise ICB-resistant tumors. Critical for radiation-elicited T-cell activation is the induction of viral mimicry, which is mediated by the accumulation of cytosolic DNA in the irradiated cells, with consequent activation of the cyclic GMP-AMP synthase (cGAS)/stimulator of interferon (IFN) genes (STING) pathway and downstream production of type I IFN and other pro-inflammatory cytokines. Recent data suggest that radiation can also enhance cancer cell antigenicity by upregulating the expression of a large number of genes that are involved in the response to DNA damage and cellular stress, thus potentially exposing immunogenic mutations to the immune system. Here, we discuss how the principles of antigen presentation favor the presentation of peptides that are derived from newly synthesized proteins in irradiated cells. These concepts support a model that incorporates the presence of immunogenic mutations in genes that are upregulated by radiation to predict which patients might benefit from treatment with combinations of radiotherapy and ICB.
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
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.
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?
Radiotherapy promotes the activation of T cells directed against tumor antigens.
“Radiotherapy promotes the activation of T cells directed against tumor antigens12–15.”
From Gut microbiome diversity is an independent predictor of survival in cervical cancer patients receiving chemoradiation (2021) · cites this paper as [14]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
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
Dendritic cells and the control of immunity
Banchereau, J., & Steinman, R. M. (1998) · Nature · doi:10.1038/32588 · Cited by 14,244 · see citing works
Mutational landscape determines sensitivity to PD-1 blockade in non–small cell lung cancer
Rizvi, N. A., Hellmann, M. D., Snyder, A., Kvistborg, P., Makarov, V., Havel, J. J., Lee, W., Yuan, J., Wong, P., Ho, T. S., et al. (2015) · Science · doi:10.1126/science.aaa1348 · Cited by 7,802 · see citing works
Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade
Le, D. T., Durham, J. N., Smith, K. N., Wang, H., Bartlett, B. R., Aulakh, L. K., Lu, S., Kemberling, H., Wilt, C., Luber, B. S., et al. (2017) · Science · doi:10.1126/science.aan6733 · Cited by 6,645 · 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
Genetic Basis for Clinical Response to CTLA-4 Blockade in Melanoma
Snyder, A., Makarov, V., Merghoub, T., Yuan, J., Zaretsky, J. M., Desrichard, A., Walsh, L. A., Postow, M. A., Wong, P., Ho, T. S., et al. (2014) · New England Journal of Medicine · doi:10.1056/nejmoa1406498 · Cited by 4,286 · see citing works
Immunogenic Cell Death in Cancer Therapy
Kroemer, G., Galluzzi, L., Kepp, O., & Zitvogel, L. (2013) · Annual Review of Immunology · doi:10.1146/annurev-immunol-032712-100008 · Cited by 3,303 · see citing works
Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade
McGranahan, N., Furness, A. J. S., Rosenthal, R., Ramskov, S., Lyngaa, R., Saini, S. K., Jamal-Hanjani, M., Wilson, G. A., Birkbak, N. J., Hiley, C. T., et al. (2016) · Science · doi:10.1126/science.aaf1490 · Cited by 3,065 · see citing works
Apetoh, L., Ghiringhelli, F., Tesniere, A., Obeid, M., Ortiz, C., Criollo, A., Mignot, G., Maiuri, M. C., Ullrich, E., Saulnier, P., et al. (2007) · Nature Medicine · doi:10.1038/nm1622 · Cited by 3,056 · see citing works
An immunogenic personal neoantigen vaccine for patients with melanoma
Ott, P. A., Hu, Z., Keskin, D. B., Shukla, S. A., Sun, J., Bozym, D. J., Zhang, W., Luoma, A., Giobbie-Hurder, A., Peter, L., et al. (2017) · Nature · doi:10.1038/nature22991 · Cited by 2,936 · see citing works
T-cell help for cytotoxic T lymphocytes is mediated by CD40–CD40L interactions
Schoenberger, S. P., Toes, R. E. M., van der Voort, E. I. H., Offringa, R., & Melief, C. J. M. (1998) · Nature · doi:10.1038/31002 · Cited by 2,615 · see citing works
Personalized RNA mutanome vaccines mobilize poly-specific therapeutic immunity against cancer
Sahin, U., Derhovanessian, E., Miller, M., Kloke, B.-P., Simon, P., Löwer, M., Bukur, V., Tadmor, A. D., Luxemburger, U., Schrörs, B., et al. (2017) · Nature · doi:10.1038/nature23003 · Cited by 2,488 · see citing works
Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer
Twyman-Saint Victor, C., Rech, A. J., Maity, A., Rengan, R., Pauken, K. E., Stelekati, E., Benci, J. L., Xu, B., Dada, H., Odorizzi, P. M., et al. (2015) · Nature · doi:10.1038/nature14292 · Cited by 2,434 · see citing works
Deng, L., Liang, H., Xu, M., Yang, X., Burnette, B., Arina, A., Li, X.-D., Mauceri, H., Beckett, M., Darga, T., et al. (2014) · Immunity · doi:10.1016/j.immuni.2014.10.019 · Cited by 2,182 · see citing works
Immunologic Correlates of the Abscopal Effect in a Patient with Melanoma
Postow, M. A., Callahan, M. K., Barker, C. A., Yamada, Y. J., Yuan, J. D., Kitano, S., Mu, Z., Rasalan, T. S., Adamow, M. J., Ritter, E., et al. (2012) · New England Journal of Medicine · doi:10.1056/nejmoa1112824 · Cited by 2,087 · 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
Towards a systems understanding of MHC class I and MHC class II antigen presentation
Neefjes, J., Jongsma, M. L. M., Paul, P., & Bakke, O. (2011) · Nature Reviews Immunology · doi:10.1038/nri3084 · Cited by 2,044 · see citing works
DNA exonuclease Trex1 regulates radiotherapy-induced tumour immunogenicity
Vanpouille-Box, C., Alard, A., Aryankalayil, M. J., Sarfraz, Y., Diamond, J. M., Schneider, R. J., Inghirami, G., Coleman, C. N., Formenti, S. C., & Demaria, S. (2017) · Nature Communications · doi:10.1038/ncomms15618 · Cited by 1,834 · see citing works
Self-citationcGAS surveillance of micronuclei links genome instability to innate immunity
Mackenzie, K. J., Carroll, P., Martin, C.-A., Murina, O., Fluteau, A., Simpson, D. J., Olova, N., Sutcliffe, H., Rainger, J. K., Leitch, A., et al. (2017) · Nature · doi:10.1038/nature23449 · Cited by 1,752 · see citing works
Reits, E. A., Hodge, J. W., Herberts, C. A., Groothuis, T. A., Chakraborty, M., K.Wansley, E., Camphausen, K., Luiten, R. M., de Ru, A. H., Neijssen, J., et al. (2006) · The Journal of Experimental Medicine · doi:10.1084/jem.20052494 · Cited by 1,737 · see citing works
Wood, R., Mitchell, M., Sgouros, J., & Lindahl, T. (2001) · Science · doi:10.1126/science.1056154 · Cited by 1,719 · see citing works
Cancer Immunotherapy Based on Mutation-Specific CD4+ T Cells in a Patient with Epithelial Cancer
Tran, E., Turcotte, S., Gros, A., Robbins, P. F., Lu, Y., Dudley, M. E., Wunderlich, J. R., Somerville, R. P. T., Hogan, K., Hinrichs, C. S., et al. (2014) · Science · doi:10.1126/science.1251102 · Cited by 1,710 · see citing works
Dewan, M. Z., Galloway, A. E., Kawashima, N., Dewyngaert, J. K., Babb, J. S., Formenti, S. C., & Demaria, S. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-0265 · Cited by 1,678 · see citing works
Self-citationMitotic progression following DNA damage enables pattern recognition within micronuclei
Harding, S. M., Benci, J. L., Irianto, J., Discher, D. E., Minn, A. J., & Greenberg, R. A. (2017) · Nature · doi:10.1038/nature23470 · Cited by 1,508 · see citing works
Neoantigen vaccine generates intratumoral T cell responses in phase Ib glioblastoma trial
Keskin, D. B., Anandappa, A. J., Sun, J., Tirosh, I., Mathewson, N. D., Li, S., Oliveira, G., Giobbie-Hurder, A., Felt, K., Gjini, E., et al. (2019) · Nature · doi:10.1038/s41586-018-0792-9 · Cited by 1,432 · see citing works
Lee, Y., Auh, S. L., Wang, Y., Burnette, B., Wang, Y., Meng, Y., Beckett, M., Sharma, R., Chin, R., Tu, T., et al. (2009) · Blood · doi:10.1182/blood-2009-02-206870 · Cited by 1,324 · see citing works
Mutant MHC class II epitopes drive therapeutic immune responses to cancer
Kreiter, S., Vormehr, M., van de Roemer, N., Diken, M., Löwer, M., Diekmann, J., Boegel, S., Schrörs, B., Vascotto, F., Castle, J. C., et al. (2015) · Nature · doi:10.1038/nature14426 · Cited by 1,243 · see citing works
The ins and outs of MHC class II-mediated antigen processing and presentation
Roche, P. A., & Furuta, K. (2015) · Nature reviews. Immunology · doi:10.1038/nri3818 · Cited by 1,207 · see citing works
Identification of unique neoantigen qualities in long-term survivors of pancreatic cancer
Initiative, A. P. C. G., Balachandran, V. P., Łuksza, M., Zhao, J. N., Makarov, V., Moral, J. A., Remark, R., Herbst, B., Askan, G., Bhanot, U., et al. (2017) · Nature · doi:10.1038/nature24462 · Cited by 1,191 · see citing works
Melief, C. J. M., van Hall, T., Arens, R., OSSENDORP, F. A., & van der Burg, S. H. (2015) · Journal of Clinical Investigation · doi:10.1172/jci80009 · Cited by 1,182 · see citing works
Systemic effects of local radiotherapy
Formenti, S. C., & Demaria, S. (2009) · The Lancet Oncology · doi:10.1016/s1470-2045(09)70082-8 · Cited by 1,021 · see citing works
Self-citationDemaria, S., Kawashima, N., Yang, A. M., Devitt, M. L., Babb, J. S., Allison, J. P., & Formenti, S. C. (2005) · Clinical Cancer Research · doi:10.1158/1078-0432.728.11.2 · Cited by 1,016 · see citing works
Self-citationResistance to checkpoint blockade therapy through inactivation of antigen presentation
Sade-Feldman, M., Jiao, Y. J., Chen, J. H., Rooney, M. S., Barzily-Rokni, M., Eliane, J.-P., Bjorgaard, S. L., Hammond, M. R., Vitzthum, H., Blackmon, S. M., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-01062-w · Cited by 1,005 · see citing works
The cGAS-cGAMP-STING Pathway of Cytosolic DNA Sensing and Signaling
Cai, X., Chiu, Y., & Chen, Z. J. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.03.040 · Cited by 995 · see citing works
Lugade, A. A., Moran, J. P., Gerber, S. A., Rose, R. C., Frelinger, J. G., & Lord, E. M. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.12.7516 · Cited by 966 · see citing works
Radiotherapy induces responses of lung cancer to CTLA-4 blockade
Formenti, S. C., Rudqvist, N.-P., Golden, E., Cooper, B., Wennerberg, E., Lhuillier, C., Vanpouille-Box, C., Friedman, K., Ferrari de Andrade, L., Wucherpfennig, K. W., et al. (2018) · Nature Medicine · doi:10.1038/s41591-018-0232-2 · Cited by 928 · see citing works
Self-citationGenomic Correlates of Immune-Cell Infiltrates in Colorectal Carcinoma
Giannakis, M., Mu, X. J., Shukla, S. A., Qian, Z. R., Cohen, O., Nishihara, R., Bahl, S., Cao, Y., Amin‐Mansour, A., Yamauchi, M., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.03.075 · Cited by 912 · see citing works
Comprehensive Analysis of Alternative Splicing Across Tumors from 8,705 Patients
Kahles, A., Lehmann, K.-V., Toussaint, N. C., Hüser, M., Stark, S. G., Sachsenberg, T. T., Stegle, O., Kohlbacher, O., Sander, C., Johnson, R., et al. (2018) · Cancer Cell · doi:10.1016/j.ccell.2018.07.001 · Cited by 891 · see citing works
Cancer/testis antigens: an expanding family of targets for cancer immunotherapy
Scanlan, M. J., Gure, A. O., Jungbluth, A. A., Old, L. J., & Chen., Y. (2002) · Immunological Reviews · doi:10.1034/j.1600-065x.2002.18803.x · Cited by 875 · see citing works
Cloned dendritic cells can present exogenous antigens on both MHC class I and class II molecules
Shen, Z. T., Reznikoff, G., Dranoff, G., & Rock, K. L. (1997) · The Journal of Immunology · doi:10.4049/jimmunol.158.6.2723 · Cited by 838 · see citing works
Present yourself! by MHC class I and MHC class II molecules
Rock, K. L., Reits, E., & Neefjes, J. (2016) · Trends in Immunology · doi:10.1016/j.it.2016.08.010 · Cited by 814 · see citing works
DNA repair, genome stability and cancer: a historical perspective
Jeggo, P. A., Pearl, L. H., & Carr, A. M. (2015) · Nature reviews. Cancer · doi:10.1038/nrc.2015.4 · Cited by 764 · see citing works
Golden, E. B., Demaria, S., Schiff, P. B., Chachoua, A., & Formenti, S. C. (2013) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-13-0115 · Cited by 686 · see citing works
Self-citationLinnemann, C., van Buuren, M. M., Bies, L., Verdegaal, E. M. E., Schotte, R., Calis, J. J. A., Behjati, S., Velds, A., Hilkmann, H., Atmioui, D. E., et al. (2014) · Nature Medicine · doi:10.1038/nm.3773 · Cited by 671 · see citing works
A neoantigen fitness model predicts tumor response to checkpoint blockade immunotherapy
Łuksza, M., Riaz, N., Makarov, V., Balachandran, V., Hellmann, M., Solovyov, A., Rizvi, N., Merghoub, T., Levine, A., Chan, T., et al. (2017) · Nature · doi:10.1038/nature24473 · Cited by 624 · see citing works
Epigenetic therapy in immune-oncology
Jones, P. A., Ohtani, H., Chakravarthy, A., & Carvalho, D. D. D. (2019) · Nature reviews. Cancer · doi:10.1038/s41568-019-0109-9 · Cited by 555 · see citing works
Systematic review of case reports on the abscopal effect
Abuodeh, Y. A., Venkat, P. S., & Kim, S. (2015) · Current Problems in Cancer · doi:10.1016/j.currproblcancer.2015.10.001 · Cited by 534 · see citing works
Noncoding regions are the main source of targetable tumor-specific antigens
Laumont, C. M., Vincent, K., Hesnard, L., Audemard, E. O., Bonneil, É., Laverdure, J., Gendron, P., Courcelles, M., Hardy, M., Côté, C., et al. (2018) · Science Translational Medicine · doi:10.1126/scitranslmed.aau5516 · Cited by 520 · see citing works
Pathogenic CD4 T cells in type 1 diabetes recognize epitopes formed by peptide fusion
Delong, T., Wiles, T. A., Baker, R. L., Bradley, B., Barbour, G., Reisdorph, R. M., Armstrong, M., Powell, R. L., Reisdorph, N. A., Kumar, N., et al. (2016) · Science · doi:10.1126/science.aad2791 · Cited by 507 · see citing works
Immunological Mechanisms Responsible for Radiation-Induced Abscopal Effect
Rodriguez-Ruiz, M. E., Vanpouille‐Box, C., Melero, I., Formenti, S. C., & Demaria, S. (2018) · Trends in Immunology · doi:10.1016/j.it.2018.06.001 · Cited by 502 · see citing works
Self-citationObeid, M., Panaretakis, T., Joza, N., Tufi, R., Tesniere, A., van Endert, P., Zitvogel, L., & Kroemer, G. (2007) · Cell Death & Differentiation · doi:10.1038/sj.cdd.4402201 · Cited by 474 · see citing works
Sensing Pathogens and Tuning Immune Responses
Pulendran, B., Palucka, K., & Banchereau, J. (2001) · Science · doi:10.1126/science.1062060 · Cited by 463 · see citing works
Making sense of mass destruction: quantitating MHC class I antigen presentation
Yewdell, J. W., Reits, E. A., & Neefjes, J. (2003) · Nature reviews. Immunology · doi:10.1038/nri1250 · Cited by 447 · see citing works
Systemic clinical tumor regressions and potentiation of PD1 blockade with in situ vaccination
Hammerich, L., Marron, T. U., Upadhyay, R., Svensson‐Arvelund, J., Dhainaut, M., Hussein, S., Zhan, Y., Ostrowski, D., Yellin, M. J., Marsh, H. C., et al. (2019) · Nature Medicine · doi:10.1038/s41591-019-0410-x · Cited by 438 · see citing works
Dendritic Cell Function in Vivo during the Steady State: A Role in Peripheral Tolerance
Steinman, R. M., Hawiger, D., Liu, K., Bonifaz, L. C., Bonnyay, D., Mahnke, K., Iyoda, T., Ravetch, J. V., Dhodapkar, M. V., Inaba, K., et al. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb06029.x · Cited by 427 · see citing works
Wood, R. D., Mitchell, M., & Lindahl, T. L. (2005) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2005.03.007 · Cited by 425 · see citing works
Ferrington, D. A., & Gregerson, D. S. (2012) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-397863-9.00003-1 · Cited by 416 · see citing works
A large fraction of HLA class I ligands are proteasome-generated spliced peptides
Liepe, J., Marino, F., Sidney, J., Jekő, A., Bunting, D. E., Sette, A., Kloetzel, P. M., Stumpf, M. P. H., Heck, A. J. R., & Mishto, M. (2016) · Science · doi:10.1126/science.aaf4384 · Cited by 368 · see citing works
Exosomes Shuttle TREX1-Sensitive IFN-Stimulatory dsDNA from Irradiated Cancer Cells to DCs
Diamond, J. M., Vanpouille‐Box, C., Spada, S., Rudqvist, N.-P., Chapman, J. R., Ueberheide, B. M., Pilones, K. A., Sarfraz, Y., Formenti, S. C., & Demaria, S. (2018) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-17-0581 · Cited by 367 · see citing works
Self-citationInduced sensitization of tumor stroma leads to eradication of established cancer by T cells
Zhang, B., Bowerman, N. A., Salama, J. K., Schmidt, H., Spiotto, M. T., Schietinger, A., Yü, P., Fu, Y., Weichselbaum, R. R., Rowley, D. A., et al. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20062056 · Cited by 359 · see citing works
DNMT and HDAC inhibitors induce cryptic transcription start sites encoded in long terminal repeats
Brocks, D., Schmidt, C. R., Daskalakis, M., Jang, H. S., Shah, N. M., Li, D., Li, J., Zhang, B., Hou, Y., Laudato, S., et al. (2017) · Nature Genetics · doi:10.1038/ng.3889 · Cited by 339 · see citing works
An Antigenic Peptide Produced by Peptide Splicing in the Proteasome
Vigneron, N., Stroobant, V., Chapiro, J., Ooms, A., Degiovanni, G., Morel, S., van der Bruggen, P., Boon, T., & den Eynde, B. J. V. (2004) · Science · doi:10.1126/science.1095522 · Cited by 329 · see citing works
Radiation Therapy to Convert the Tumor Into an In Situ Vaccine
Formenti, S. C., & Demaria, S. (2012) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2012.06.020 · Cited by 319 · see citing works
Self-citationXu, M. M., Yang, P., Han, D., Shi, Y., Cao, X., Liang, H. L., Chen, X., Li, X.-D., Deng, L., Chen, Z. J., et al. (2017) · Immunity · doi:10.1016/j.immuni.2017.07.016 · Cited by 315 · see citing works
Time to abandon single-site irradiation for inducing abscopal effects
Brooks, E. D., & Chang, J. Y. (2018) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-018-0119-7 · Cited by 312 · see citing works
MHC antigens and tumor escape from immune surveillance
Garrido, F., & Algarra, I. (2001) · Advances in cancer research · doi:10.1016/s0065-230x(01)83005-0 · Cited by 305 · see citing works
The immunoproteasome and thymoproteasome: functions, evolution and human disease
Murata, S., Takahama, Y., Kasahara, M., & Tanaka, K. (2018) · Nature Immunology · doi:10.1038/s41590-018-0186-z · Cited by 305 · see citing works
Role of Antigen Spread and Distinctive Characteristics of Immunotherapy in Cancer Treatment
Gulley, J. L., Madan, R. A., Pachynski, R. K., Mulders, P., Sheikh, N. A., Trager, J. B., & Drake, C. G. (2016) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djw261 · Cited by 215 · see citing works
Radiotherapy and CTLA-4 Blockade Shape the TCR Repertoire of Tumor-Infiltrating T Cells
Rudqvist, N.-P., Pilones, K. A., Lhuillier, C., Wennerberg, E., Sidhom, J.-W., Emerson, R., Robins, H. S., Schneck, J. P., Formenti, S. C., & Demaria, S. (2017) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-17-0134 · Cited by 214 · see citing works
Self-citationMHC Class I–Associated Phosphopeptides Are the Targets of Memory-like Immunity in Leukemia
Cobbold, M., Peña, H. D. L., Norris, A., Polefrone, J. M., Qian, J., English, A. M., Cummings, K. L., Penny, S. A., Turner, J. E., Cottine, J. M., et al. (2013) · Science Translational Medicine · doi:10.1126/scitranslmed.3006061 · Cited by 206 · see citing works
Tsai, M., Cook, J. A., Chandramouli, G. V. R., et al. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-4250 · Cited by 200 · see citing works
Identification of class I MHC-associated phosphopeptides as targets for cancer immunotherapy
Zarling, A. L., Polefrone, J. M., Evans, A. M., Mikesh, L. M., Shabanowitz, J., Lewis, S. T., Engelhard, V. H., & Hunt, D. F. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0604045103 · Cited by 193 · see citing works
Grosovsky, A. J., de Boer, J. G., de Jong, P. J., Drobetsky, E. A., & Glickman, B. W. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.1.185 · Cited by 189 · see citing works
Virus-induced type I IFN stimulates generation of immunoproteasomes at the site of infection
Shin, E., Seifert, U., Kato, T., Rice, C. M., Feinstone, S. M., Kloetzel, P., & Rehermann, B. (2006) · Journal of Clinical Investigation · doi:10.1172/jci29832 · Cited by 186 · see citing works
Toward Precision Radiotherapy for Use with Immune Checkpoint Blockers
Vanpouille‐Box, C., Formenti, S. C., & Demaria, S. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-0037 · Cited by 173 · see citing works
Self-citationSnapShot: CGAS-STING Signaling
Galluzzi, L., Vanpouille‐Box, C., Bakhoum, S. F. W., & Demaria, S. (2018) · Cell · doi:10.1016/j.cell.2018.03.015 · Cited by 152 · see citing works
Self-citationT-Cell Responses to Survivin in Cancer Patients Undergoing Radiation Therapy
Schaue, D., Comin-Anduix, B., Ribas, A., et al. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-4462 · Cited by 143 · see citing works
Stoilov, P., Lin, C.-H., Damoiseaux, R. D., Nikolic, J. M., & Black, D. L. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0801661105 · Cited by 141 · see citing works
Translating DRiPs: MHC class I immunosurveillance of pathogens and tumors
Antón, L. C., & Yewdell, J. W. (2014) · Journal of Leukocyte Biology · doi:10.1189/jlb.1113599 · Cited by 129 · see citing works
An antigenic peptide produced by reverse splicing and double asparagine deamidation
Dalet, A., Robbins, P. F., Stroobant, V., Vigneron, N., Li, Y. F., El‐Gamil, M., Hanada, K., Yang, J. C.-H., Rosenberg, S. A., & den Eynde, B. J. V. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1101892108 · Cited by 128 · see citing works
Andersen, M. H., Bonfill, J. E., Neisig, A., Arsequell, G., Søndergaard, I., Neefjes, J., Zeuthen, J., Elliott, T. J., & Haurum, J. S. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.163.7.3812 · Cited by 117 · see citing works
Human Tumor Antigens Yesterday, Today, and Tomorrow
Finn, O. J. (2017) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-17-0112 · Cited by 116 · see citing works
Depontieu, F., Qian, J., Zarling, A. L., McMiller, T. L., Salay, T. M., Norris, A., English, A. M., Shabanowitz, J., Engelhard, V. H., Hunt, D. F., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0903852106 · Cited by 115 · see citing works
Haurum, J. S., Høier, I. B., Arsequell, G., Neisig, A., Valencia, G., Zeuthen, J., Neefjes, J., & Elliott, T. (1999) · The Journal of Experimental Medicine · doi:10.1084/jem.190.1.145 · Cited by 106 · see citing works
In Situ Vaccination for the Treatment of Cancer
Hammerich, L., Bhardwaj, N., Kohrt, H. E. K., & Brody, J. (2016) · Immunotherapy · doi:10.2217/imt.15.120 · Cited by 105 · see citing works
Khan, S., de Giuli, R., Schmidtke, G., et al. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.9.4801 · Cited by 102 · see citing works
Functional genomics as a window on radiation stress signaling
Amundson, S. A., Bittner, M. L., & Fornace, A. J. (2003) · Oncogene · doi:10.1038/sj.onc.1206681 · Cited by 102 · see citing works
Brentville, V. A., Metheringham, R. L., Gunn, B., Symonds, P., Daniels, I., Gijon, M., Cook, K., Xue, W., & Durrant, L. G. (2016) · Cancer Research · doi:10.1158/0008-5472.can-15-1085 · Cited by 98 · see citing works
A peptide's perspective on antigen presentation to the immune system
Neefjes, J., & Ovaa, H. (2013) · Nature Chemical Biology · doi:10.1038/nchembio.1391 · Cited by 91 · see citing works
The immunological consequences of radiation‐induced DNA damage
Wilkins, A. C., Patin, E. C., Harrington, K. J., & Melcher, A. A. (2019) · The Journal of Pathology · doi:10.1002/path.5232 · Cited by 60 · see citing works
Boehm, K. M., Bhinder, B., Raja, V. J., Dephoure, N., & Elemento, O. (2019) · BMC Bioinformatics · doi:10.1186/s12859-018-2561-z · Cited by 57 · see citing works
Self-citationCo‐stimulatory pathways in lymphocyte regulation: the immunoglobulin superfamily
Peggs, K. S., & Allison, J. P. (2005) · British Journal of Haematology · doi:10.1111/j.1365-2141.2005.05627.x · Cited by 49 · see citing works
The melting pot of the MHC II peptidome
Stern, L. J., & Santambrogio, L. (2016) · Current Opinion in Immunology · doi:10.1016/j.coi.2016.03.004 · Cited by 45 · see citing works
Berg, P., McConnell, E. W., Hicks, L. M., Popescu, S. C., & Popescu, G. V. (2019) · BMC Bioinformatics · doi:10.1186/s12859-019-2619-6 · Cited by 33 · see citing works
Induction of immunogenic cell death by radiation-upregulated karyopherin alpha 2 in vitro
Song, K., Jung, S.-Y., Kang, S.-M., Kim, M., Ahn, J., Hwang, S., Lee, J., Lim, D., Nam, S. Y., & Song, J. Y. (2016) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2016.04.002 · Cited by 23 · see citing works
Chemotherapy induces alternative transcription and splicing: Facts and hopes for cancer treatment
Lambert, C. A., Garbacki, N., & Colige, A. (2017) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2017.04.006 · Cited by 15 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Sims, T. T., El Alam, M. B., Karpinets, T. V., Dorta-Estremera, S., Hegde, V. L., Nookala, S., Yoshida-Court, K., Wu, X., Biegert, G. W. G., Delgado Medrano, A. Y., et al. (2021) · Communications Biology · doi:10.1038/s42003-021-01741-x · Cited by 135 · see citing works
Targeting DNA Damage Response and Immune Checkpoint for Anticancer Therapy
Huang, J.-L., Chang, Y.-T., Hong, Z.-Y., & Lin, C.-S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23063238 · Cited by 42 · see citing works
- Authors
- Lhuillier, C., Rudqvist, N.-P., Elemento, O., Formenti, S. C., & Demaria, S.
- Affiliations
- Weill Cornell Medicine (US)
- Corresponding author
- Demaria, Sandra
- Venue
- Genome Medicine
- Published
- 2019-06-20
- Volume
- 11
- Issue
- 1
- Pages
- 40-40
- ISSN
- 1756-994X (ISSN-L)
- PMC
- PMC6587285
- OpenAlex
- W2952477280
- Cited by
- 276
- References
- 96
- Citations by year
- 2026: 34 · 2025: 28 · 2024: 36 · 2023: 51 · 2022: 41 · 2021: 47 · 2020: 35 · 2019: 4
- FWCI
- 3.03
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Genome Medicine (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Cancer Institute (R01CA198533, R01CA201246)
- American Association for Cancer Research (18-40-43-LHUI)
- 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
- radiotherapy, antitumor immunity, immune checkpoint blockade, neoantigens, tumor mutational burden, viral mimicry, cytosolic DNA, cGAS-STING pathway, type I interferon, DNA damage response, antigen presentation, tumor-specific T cells, cancer immunotherapy
- MeSH terms
- Animals, Antigens, Neoplasm, Humans, Mutation, Neoplasms, Radiotherapy, Antigen Presentation
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
