{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,22]],"date-time":"2026-06-22T11:14:16Z","timestamp":1782126856102,"version":"3.54.5"},"reference-count":62,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2022,8,18]],"date-time":"2022-08-18T00:00:00Z","timestamp":1660780800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,8,18]],"date-time":"2022-08-18T00:00:00Z","timestamp":1660780800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    Immune checkpoint blockade (ICB) leads to durable and complete tumour regression in some patients but in others gives temporary, partial or no response. Accordingly, significant efforts are underway to identify tumour-intrinsic mechanisms underlying ICB resistance. Results from a published CRISPR screen in a mouse model suggested that targeting STUB1, an E3 ligase involved in protein homeostasis, may overcome ICB resistance but the molecular basis of this effect remains unclear. Herein, we report an under-appreciated role of STUB1 to dampen the interferon gamma (IFN\u03b3) response. Genetic deletion of STUB1 increased IFNGR1 abundance on the cell surface and thus enhanced the downstream IFN\u03b3 response as showed by multiple approaches including Western blotting, flow cytometry, qPCR, phospho-STAT1 assay, immunopeptidomics, proteomics, and gene expression profiling. Human prostate and breast cancer cells with STUB1 deletion were also susceptible to cytokine-induced growth inhibition. Furthermore, blockade of STUB1 protein function recapitulated the\n                    <jats:italic>STUB1<\/jats:italic>\n                    -null phenotypes. Despite these encouraging in vitro data and positive implications from clinical datasets, we did not observe in vivo benefits of inactivating\n                    <jats:italic>Stub1<\/jats:italic>\n                    in mouse syngeneic tumour models\u2014with or without combination with anti-PD-1 therapy. However, our findings elucidate STUB1 as a barrier to IFN\u03b3 sensing, prompting further investigations to assess if broader inactivation of human STUB1 in both tumors and immune cells could overcome ICB resistance.\n                  <\/jats:p>","DOI":"10.1038\/s41598-022-18404-4","type":"journal-article","created":{"date-parts":[[2022,8,18]],"date-time":"2022-08-18T11:05:09Z","timestamp":1660820709000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":13,"title":["STUB1 is an intracellular checkpoint for interferon gamma sensing"],"prefix":"10.1038","volume":"12","author":[{"given":"Simon","family":"Ng","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuhui","family":"Lim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adrian Chong Nyi","family":"Sim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ruban","family":"Mangadu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ally","family":"Lau","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunsheng","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarah Bollinger","family":"Martinez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arun","family":"Chandramohan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"U-Ming","family":"Lim","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Samantha Shu Wen","family":"Ho","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shih Chieh","family":"Chang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pooja","family":"Gopal","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lewis Z.","family":"Hong","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adam","family":"Schwaid","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aaron Zefrin","family":"Fernandis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrey","family":"Loboda","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cai","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Uyen","family":"Phan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brian","family":"Henry","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anthony W.","family":"Partridge","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2022,8,18]]},"reference":[{"key":"18404_CR1","doi-asserted-by":"publisher","first-page":"447","DOI":"10.1016\/1074-7613(94)90087-6","volume":"1","author":"AS Dighe","year":"1994","unstructured":"Dighe, A. S., Richards, E., Old, L. J. & Schreiber, R. D. Enhanced in vivo growth and resistance to rejection of tumor cells expressing dominant negative IFN\u03b3 receptors. Immunity 1, 447\u2013456 (1994).","journal-title":"Immunity"},{"key":"18404_CR2","doi-asserted-by":"publisher","first-page":"7556","DOI":"10.1073\/pnas.95.13.7556","volume":"95","author":"DH Kaplan","year":"1998","unstructured":"Kaplan, D. H. et al. Demonstration of an interferon \u03b3-dependent tumor surveillance system in immunocompetent mice. Proc. Natl. Acad. Sci. USA 95, 7556\u20137561 (1998).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"18404_CR3","doi-asserted-by":"publisher","first-page":"1107","DOI":"10.1038\/35074122","volume":"410","author":"V Shankaran","year":"2001","unstructured":"Shankaran, V. et al. IFN\u03b3 and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410, 1107\u20131111 (2001).","journal-title":"Nature"},{"key":"18404_CR4","doi-asserted-by":"publisher","first-page":"397","DOI":"10.1016\/j.cell.2016.08.069","volume":"167","author":"J Gao","year":"2016","unstructured":"Gao, J. et al. Loss of IFN-\u03b3 pathway genes in tumor cells as a mechanism of resistance to Anti-CTLA-4 therapy. Cell 167, 397-404.e399 (2016).","journal-title":"Cell"},{"key":"18404_CR5","doi-asserted-by":"publisher","first-page":"819","DOI":"10.1056\/NEJMoa1604958","volume":"375","author":"JM Zaretsky","year":"2016","unstructured":"Zaretsky, J. M. et al. Mutations associated with acquired resistance to PD-1 Blockade in melanoma. New Engl. J. Med. 375, 819\u2013829 (2016).","journal-title":"New Engl. J. Med."},{"key":"18404_CR6","doi-asserted-by":"publisher","first-page":"537","DOI":"10.1038\/nature23477","volume":"548","author":"SJ Patel","year":"2017","unstructured":"Patel, S. J. et al. Identification of essential genes for cancer immunotherapy. Nature 548, 537\u2013542 (2017).","journal-title":"Nature"},{"key":"18404_CR7","doi-asserted-by":"publisher","first-page":"2930","DOI":"10.1172\/JCI91190","volume":"127","author":"M Ayers","year":"2017","unstructured":"Ayers, M. et al. IFN-\u03b3\u2013related mRNA profile predicts clinical response to PD-1 blockade. J. Clin. Investig. 127, 2930\u20132940 (2017).","journal-title":"J. Clin. Investig."},{"key":"18404_CR8","doi-asserted-by":"publisher","first-page":"984","DOI":"10.1016\/j.cell.2018.09.006","volume":"175","author":"L Jerby-Arnon","year":"2018","unstructured":"Jerby-Arnon, L. et al. A cancer cell program promotes T cell exclusion and resistance to checkpoint blockade. Cell 175, 984-997.e924 (2018).","journal-title":"Cell"},{"key":"18404_CR9","doi-asserted-by":"publisher","first-page":"413","DOI":"10.1038\/nature23270","volume":"547","author":"RT Manguso","year":"2017","unstructured":"Manguso, R. T. et al. In vivo CRISPR screening identifies Ptpn2 as a cancer immunotherapy target. Nature 547, 413\u2013418 (2017).","journal-title":"Nature"},{"key":"18404_CR10","doi-asserted-by":"publisher","first-page":"770","DOI":"10.1126\/science.aao1710","volume":"359","author":"D Pan","year":"2018","unstructured":"Pan, D. et al. A major chromatin regulator determines resistance of tumor cells to T cell-mediated killing. Science 359, 770 (2018).","journal-title":"Science"},{"key":"18404_CR11","doi-asserted-by":"publisher","first-page":"eaar3451","DOI":"10.1126\/sciimmunol.aar3451","volume":"3","author":"CJ Kearney","year":"2018","unstructured":"Kearney, C. J. et al. Tumor immune evasion arises through loss of TNF sensitivity. Sci. Immunol. 3, eaar3451 (2018).","journal-title":"Sci. Immunol."},{"key":"18404_CR12","doi-asserted-by":"publisher","first-page":"a028480","DOI":"10.1101\/cshperspect.a028480","volume":"11","author":"E Alspach","year":"2019","unstructured":"Alspach, E., Lussier, D. M. & Schreiber, R. D. Interferon \u03b3 and its important roles in promoting and inhibiting spontaneous and therapeutic cancer immunity. Cold Spring Harb. Perspect. Biol. 11, a028480 (2019).","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"18404_CR13","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1038\/s41577-019-0218-4","volume":"20","author":"A Kalbasi","year":"2020","unstructured":"Kalbasi, A. & Ribas, A. Tumour-intrinsic resistance to immune checkpoint blockade. Nat. Rev. Immunol. 20, 25\u201339 (2020).","journal-title":"Nat. Rev. Immunol."},{"key":"18404_CR14","doi-asserted-by":"publisher","first-page":"500","DOI":"10.1016\/j.ccell.2020.08.005","volume":"38","author":"CS Grasso","year":"2020","unstructured":"Grasso, C. S. et al. Conserved interferon-\u03b3 signaling drives clinical response to immune checkpoint blockade therapy in melanoma. Cancer Cell 38, 500-515.e3 (2020).","journal-title":"Cancer Cell"},{"key":"18404_CR15","doi-asserted-by":"publisher","first-page":"1189","DOI":"10.1016\/j.celrep.2017.04.031","volume":"19","author":"A Garcia-Diaz","year":"2017","unstructured":"Garcia-Diaz, A. et al. Interferon receptor signaling pathways regulating PD-L1 and PD-L2 expression. Cell Rep. 19, 1189\u20131201 (2017).","journal-title":"Cell Rep."},{"key":"18404_CR16","doi-asserted-by":"publisher","first-page":"347","DOI":"10.1038\/nature25187","volume":"553","author":"Z Eroglu","year":"2018","unstructured":"Eroglu, Z. et al. High response rate to PD-1 blockade in desmoplastic melanomas. Nature 553, 347\u2013350 (2018).","journal-title":"Nature"},{"key":"18404_CR17","doi-asserted-by":"publisher","first-page":"568","DOI":"10.1038\/nature13954","volume":"515","author":"PC Tumeh","year":"2014","unstructured":"Tumeh, P. C. et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 515, 568\u2013571 (2014).","journal-title":"Nature"},{"key":"18404_CR18","doi-asserted-by":"publisher","first-page":"eaar3593","DOI":"10.1126\/science.aar3593","volume":"362","author":"R Cristescu","year":"2018","unstructured":"Cristescu, R. et al. Pan-tumor genomic biomarkers for PD-1 checkpoint blockade\u2013based immunotherapy. Science 362, eaar3593 (2018).","journal-title":"Science"},{"key":"18404_CR19","doi-asserted-by":"publisher","first-page":"563","DOI":"10.1038\/nature14011","volume":"515","author":"RS Herbst","year":"2014","unstructured":"Herbst, R. S. et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 515, 563\u2013567 (2014).","journal-title":"Nature"},{"key":"18404_CR20","doi-asserted-by":"publisher","first-page":"827","DOI":"10.1158\/2159-8290.CD-15-1545","volume":"6","author":"P-L Chen","year":"2016","unstructured":"Chen, P.-L. et al. Analysis of immune signatures in longitudinal tumor samples yields insight into biomarkers of response and mechanisms of resistance to immune checkpoint blockade. Cancer Discov. 6, 827 (2016).","journal-title":"Cancer Discov."},{"key":"18404_CR21","doi-asserted-by":"publisher","first-page":"eaar3342","DOI":"10.1126\/scitranslmed.aar3342","volume":"10","author":"SJ Rodig","year":"2018","unstructured":"Rodig, S. J. et al. MHC proteins confer differential sensitivity to CTLA-4 and PD-1 blockade in untreated metastatic melanoma. Sci. Transl. Med. 10, eaar3342 (2018).","journal-title":"Sci. Transl. Med."},{"key":"18404_CR22","doi-asserted-by":"publisher","first-page":"15440","DOI":"10.1038\/ncomms15440","volume":"8","author":"A Sucker","year":"2017","unstructured":"Sucker, A. et al. Acquired IFN\u03b3 resistance impairs anti-tumor immunity and gives rise to T-cell-resistant melanoma lesions. Nat. Commun. 8, 15440 (2017).","journal-title":"Nat. Commun."},{"key":"18404_CR23","doi-asserted-by":"publisher","first-page":"46278","DOI":"10.1074\/jbc.M304721200","volume":"278","author":"L Klampfer","year":"2003","unstructured":"Klampfer, L. et al. Oncogenic Ki-Ras inhibits the expression of interferon-responsive genes through inhibition of STAT1 and STAT2 expression. J. Biol. Chem. 278, 46278\u201346287 (2003).","journal-title":"J. Biol. Chem."},{"key":"18404_CR24","doi-asserted-by":"publisher","first-page":"2395","DOI":"10.1158\/1541-7786.MCR-19-0545","volume":"17","author":"S Chandrasekaran","year":"2019","unstructured":"Chandrasekaran, S. et al. Phosphoinositide 3-kinase signaling can modulate MHC class I and II expression. Mol. Cancer Res. 17, 2395 (2019).","journal-title":"Mol. Cancer Res."},{"key":"18404_CR25","doi-asserted-by":"publisher","first-page":"1414","DOI":"10.3389\/fimmu.2018.01414","volume":"9","author":"S Alavi","year":"2018","unstructured":"Alavi, S. et al. Interferon signaling is frequently downregulated in melanoma. Front. Immunol. 9, 1414 (2018).","journal-title":"Front. Immunol."},{"key":"18404_CR26","doi-asserted-by":"publisher","first-page":"100","DOI":"10.1038\/s41586-020-2229-5","volume":"581","author":"K Yamamoto","year":"2020","unstructured":"Yamamoto, K. et al. Autophagy promotes immune evasion of pancreatic cancer by degrading MHC-I. Nature 581, 100\u2013105 (2020).","journal-title":"Nature"},{"key":"18404_CR27","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1016\/j.coi.2015.12.007","volume":"39","author":"F Garrido","year":"2016","unstructured":"Garrido, F., Aptsiauri, N., Doorduijn, E. M., Garcia Lora, A. M. & van Hall, T. The urgent need to recover MHC class I in cancers for effective immunotherapy. Curr. Opin. Immunol. 39, 44\u201351 (2016).","journal-title":"Curr. Opin. Immunol."},{"key":"18404_CR28","doi-asserted-by":"publisher","first-page":"888","DOI":"10.1002\/ijc.30489","volume":"140","author":"F Perea","year":"2017","unstructured":"Perea, F. et al. The absence of HLA class I expression in non-small cell lung cancer correlates with the tumor tissue structure and the pattern of T cell infiltration. Int. J. Cancer 140, 888\u2013899 (2017).","journal-title":"Int. J. Cancer"},{"key":"18404_CR29","doi-asserted-by":"publisher","first-page":"1420","DOI":"10.1158\/2159-8290.CD-17-0593","volume":"7","author":"S Gettinger","year":"2017","unstructured":"Gettinger, S. et al. Impaired HLA class I antigen processing and presentation as a mechanism of acquired resistance to immune checkpoint inhibitors in lung cancer. Cancer Discov. 7, 1420 (2017).","journal-title":"Cancer Discov."},{"key":"18404_CR30","doi-asserted-by":"publisher","first-page":"1897","DOI":"10.1038\/s41467-020-15726-7","volume":"11","author":"JH Lee","year":"2020","unstructured":"Lee, J. H. et al. Transcriptional downregulation of MHC class I and melanoma de- differentiation in resistance to PD-1 inhibition. Nat. Commun. 11, 1897 (2020).","journal-title":"Nat. Commun."},{"key":"18404_CR31","doi-asserted-by":"publisher","first-page":"D529","DOI":"10.1093\/nar\/gky1079","volume":"47","author":"R Oughtred","year":"2019","unstructured":"Oughtred, R. et al. The BioGRID interaction database: 2019 update. Nucleic Acids Res. 47, D529\u2013D541 (2019).","journal-title":"Nucleic Acids Res."},{"key":"18404_CR32","doi-asserted-by":"publisher","first-page":"120","DOI":"10.1038\/s41586-020-2746-2","volume":"586","author":"KA Lawson","year":"2020","unstructured":"Lawson, K. A. et al. Functional genomic landscape of cancer-intrinsic evasion of killing by T cells. Nature 586, 120\u2013126 (2020).","journal-title":"Nature"},{"key":"18404_CR33","doi-asserted-by":"publisher","first-page":"106","DOI":"10.1038\/nature23669","volume":"549","author":"R Mezzadra","year":"2017","unstructured":"Mezzadra, R. et al. Identification of CMTM6 and CMTM4 as PD-L1 protein regulators. Nature 549, 106\u2013110 (2017).","journal-title":"Nature"},{"key":"18404_CR34","doi-asserted-by":"publisher","first-page":"42938","DOI":"10.1074\/jbc.M101968200","volume":"276","author":"J Jiang","year":"2001","unstructured":"Jiang, J. et al. CHIP Is a U-box-dependent E3 Ubiquitin Ligase. J. Biol. Chem. 276, 42938\u201342944 (2001).","journal-title":"J. Biol. Chem."},{"key":"18404_CR35","doi-asserted-by":"publisher","first-page":"1133","DOI":"10.1093\/embo-reports\/kve246","volume":"2","author":"S Murata","year":"2001","unstructured":"Murata, S., Minami, Y., Minami, M., Chiba, T. & Tanaka, K. CHIP is a chaperone-dependent E3 ligase that ubiquitylates unfolded protein. EMBO Rep. 2, 1133\u20131138 (2001).","journal-title":"EMBO Rep."},{"key":"18404_CR36","doi-asserted-by":"publisher","first-page":"551","DOI":"10.1038\/nature04600","volume":"440","author":"S-B Qian","year":"2006","unstructured":"Qian, S.-B., McDonough, H., Boellmann, F., Cyr, D. M. & Patterson, C. CHIP-mediated stress recovery by sequential ubiquitination of substrates and Hsp70. Nature 440, 551\u2013555 (2006).","journal-title":"Nature"},{"key":"18404_CR37","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1158\/2326-6066.CIR-16-0114","volume":"5","author":"SIS Mosely","year":"2017","unstructured":"Mosely, S. I. S. et al. Rational selection of syngeneic preclinical tumor models for immunotherapeutic drug discovery. Cancer Immunol. Res. 5, 29 (2017).","journal-title":"Cancer Immunol. Res."},{"key":"18404_CR38","doi-asserted-by":"publisher","first-page":"868","DOI":"10.1038\/nmeth.3993","volume":"13","author":"WL Chew","year":"2016","unstructured":"Chew, W. L. et al. A multifunctional AAV\u2013CRISPR\u2013Cas9 and its host response. Nat. Methods 13, 868\u2013874 (2016).","journal-title":"Nat. Methods"},{"key":"18404_CR39","doi-asserted-by":"publisher","first-page":"571","DOI":"10.1016\/j.immuni.2021.01.001","volume":"54","author":"J Dubrot","year":"2021","unstructured":"Dubrot, J. et al. In vivo screens using a selective CRISPR antigen removal lentiviral vector system reveal immune dependencies in renal cell carcinoma. Immunity 54, 571-585.e576 (2021).","journal-title":"Immunity"},{"key":"18404_CR40","doi-asserted-by":"publisher","first-page":"1136","DOI":"10.1038\/s41467-017-01062-w","volume":"8","author":"M Sade-Feldman","year":"2017","unstructured":"Sade-Feldman, M. et al. Resistance to checkpoint blockade therapy through inactivation of antigen presentation. Nat. Commun. 8, 1136 (2017).","journal-title":"Nat. Commun."},{"key":"18404_CR41","doi-asserted-by":"publisher","first-page":"896","DOI":"10.1038\/s41467-020-14639-9","volume":"11","author":"S Kalaora","year":"2020","unstructured":"Kalaora, S. et al. Immunoproteasome expression is associated with better prognosis and response to checkpoint therapies in melanoma. Nat. Commun. 11, 896 (2020).","journal-title":"Nat. Commun."},{"key":"18404_CR42","doi-asserted-by":"publisher","first-page":"19626","DOI":"10.1016\/S0021-9258(18)55039-0","volume":"266","author":"MA Farrar","year":"1991","unstructured":"Farrar, M. A., Fernandez-Luna, J. & Schreiber, R. D. Identification of two regions within the cytoplasmic domain of the human interferon-gamma receptor required for function. J. Biol. Chem. 266, 19626\u201319635 (1991).","journal-title":"J. Biol. Chem."},{"key":"18404_CR43","doi-asserted-by":"publisher","first-page":"786","DOI":"10.1038\/s41589-019-0322-6","volume":"15","author":"M Ravalin","year":"2019","unstructured":"Ravalin, M. et al. Specificity for latent C termini links the E3 ubiquitin ligase CHIP to caspases. Nat. Chem. Biol. 15, 786\u2013794 (2019).","journal-title":"Nat. Chem. Biol."},{"key":"18404_CR44","doi-asserted-by":"publisher","first-page":"1993","DOI":"10.1021\/acsmedchemlett.0c00022","volume":"11","author":"S Ng","year":"2020","unstructured":"Ng, S. et al. De-risking drug discovery of intracellular targeting peptides: Screening strategies to eliminate false-positive hits. ACS Med. Chem. Lett. 11, 1993\u20132001 (2020).","journal-title":"ACS Med. Chem. Lett."},{"key":"18404_CR45","doi-asserted-by":"publisher","first-page":"e0171257","DOI":"10.1371\/journal.pone.0171257","volume":"12","author":"Y Shen","year":"2017","unstructured":"Shen, Y., Chen, Y., Wu, J., Shaner, N. C. & Campbell, R. E. Engineering of mCherry variants with long Stokes shift, red-shifted fluorescence, and low cytotoxicity. PLoS ONE 12, e0171257 (2017).","journal-title":"PLoS ONE"},{"key":"18404_CR46","doi-asserted-by":"publisher","first-page":"453","DOI":"10.1038\/nmeth.3337","volume":"12","author":"AM Newman","year":"2015","unstructured":"Newman, A. M. et al. Robust enumeration of cell subsets from tissue expression profiles. Nat. Methods 12, 453\u2013457 (2015).","journal-title":"Nat. Methods"},{"key":"18404_CR47","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.immuni.2013.07.012","volume":"39","author":"DS Chen","year":"2013","unstructured":"Chen, D. S. & Mellman, I. Oncology meets immunology: The cancer-immunity cycle. Immunity 39, 1\u201310 (2013).","journal-title":"Immunity"},{"key":"18404_CR48","doi-asserted-by":"publisher","first-page":"361","DOI":"10.1038\/nature11824","volume":"494","author":"H Braum\u00fcller","year":"2013","unstructured":"Braum\u00fcller, H. et al. T-helper-1-cell cytokines drive cancer into senescence. Nature 494, 361\u2013365 (2013).","journal-title":"Nature"},{"key":"18404_CR49","doi-asserted-by":"publisher","first-page":"18367","DOI":"10.1074\/jbc.270.31.18367","volume":"270","author":"D-I Jeoung","year":"1995","unstructured":"Jeoung, D.-I., Tang, B. & Sonenberg, M. Effects of tumor necrosis factor-\u03b1 on antimitogenicity and cell cycle-related proteins in MCF-7 cells. J. Biol. Chem. 270, 18367\u201318373 (1995).","journal-title":"J. Biol. Chem."},{"key":"18404_CR50","doi-asserted-by":"publisher","first-page":"1243","DOI":"10.1038\/s41467-018-03563-8","volume":"9","author":"P Zhou","year":"2018","unstructured":"Zhou, P. et al. MLL5 suppresses antiviral innate immune response by facilitating STUB1-mediated RIG-I degradation. Nat. Commun. 9, 1243 (2018).","journal-title":"Nat. Commun."},{"key":"18404_CR51","doi-asserted-by":"publisher","first-page":"4535","DOI":"10.1128\/MCB.19.6.4535","volume":"19","author":"CA Ballinger","year":"1999","unstructured":"Ballinger, C. A. et al. Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Mol. Cell. Biol. 19, 4535 (1999).","journal-title":"Mol. Cell. Biol."},{"key":"18404_CR52","doi-asserted-by":"publisher","first-page":"525","DOI":"10.1016\/j.molcel.2005.09.023","volume":"20","author":"M Zhang","year":"2005","unstructured":"Zhang, M. et al. Chaperoned ubiquitylation-crystal structures of the CHIP U Box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex. Mol. Cell 20, 525\u2013538 (2005).","journal-title":"Mol. Cell"},{"key":"18404_CR53","doi-asserted-by":"publisher","first-page":"1923","DOI":"10.1038\/s41467-022-29442-x","volume":"13","author":"G Apriamashvili","year":"2022","unstructured":"Apriamashvili, G. et al. Ubiquitin ligase STUB1 destabilizes IFN\u03b3-receptor complex to suppress tumor IFN\u03b3 signaling. Nat. Commun. 13, 1923 (2022).","journal-title":"Nat. Commun."},{"key":"18404_CR54","doi-asserted-by":"publisher","first-page":"1540","DOI":"10.1016\/j.cell.2016.11.022","volume":"167","author":"JL Benci","year":"2016","unstructured":"Benci, J. L. et al. Tumor interferon signaling regulates a multigenic resistance program to immune checkpoint blockade. Cell 167, 1540-1554.e1512 (2016).","journal-title":"Cell"},{"key":"18404_CR55","doi-asserted-by":"publisher","first-page":"933","DOI":"10.1016\/j.cell.2019.07.019","volume":"178","author":"JL Benci","year":"2019","unstructured":"Benci, J. L. et al. Opposing functions of interferon coordinate adaptive and innate immune responses to cancer immune checkpoint blockade. Cell 178, 933-948.e914 (2019).","journal-title":"Cell"},{"key":"18404_CR56","doi-asserted-by":"publisher","first-page":"158","DOI":"10.1038\/s41577-021-00566-3","volume":"22","author":"AM Gocher","year":"2022","unstructured":"Gocher, A. M., Workman, C. J. & Vignali, D. A. A. Interferon-\u03b3: teammate or opponent in the tumour microenvironment?. Nat. Rev. Immunol. 22, 158\u2013172 (2022).","journal-title":"Nat. Rev. Immunol."},{"key":"18404_CR57","doi-asserted-by":"publisher","first-page":"312","DOI":"10.1038\/ncb1839","volume":"11","author":"M Kajiro","year":"2009","unstructured":"Kajiro, M. et al. The ubiquitin ligase CHIP acts as an upstream regulator of oncogenic pathways. Nat. Cell Biol. 11, 312\u2013319 (2009).","journal-title":"Nat. Cell Biol."},{"key":"18404_CR58","doi-asserted-by":"publisher","first-page":"272","DOI":"10.1016\/j.immuni.2013.08.006","volume":"39","author":"Z Chen","year":"2013","unstructured":"Chen, Z. et al. The ubiquitin ligase Stub1 negatively modulates regulatory T cell suppressive activity by promoting degradation of the transcription factor Foxp3. Immunity 39, 272\u2013285 (2013).","journal-title":"Immunity"},{"key":"18404_CR59","doi-asserted-by":"publisher","first-page":"470","DOI":"10.1016\/j.cell.2017.04.003","volume":"169","author":"R Tawo","year":"2017","unstructured":"Tawo, R. et al. The ubiquitin ligase CHIP integrates proteostasis and aging by regulation of insulin receptor turnover. Cell 169, 470-482.e413 (2017).","journal-title":"Cell"},{"key":"18404_CR60","doi-asserted-by":"publisher","first-page":"1335","DOI":"10.1038\/s41590-019-0480-4","volume":"20","author":"MW LaFleur","year":"2019","unstructured":"LaFleur, M. W. et al. PTPN2 regulates the generation of exhausted CD8+ T cell subpopulations and restrains tumor immunity. Nat. Immunol. 20, 1335\u20131347 (2019).","journal-title":"Nat. Immunol."},{"key":"18404_CR61","doi-asserted-by":"crossref","unstructured":"Ng, S. et al. Discovery and Structure-Based Design of Macrocyclic Peptides Targeting STUB1. J. Med. Chem. (2022).","DOI":"10.26434\/chemrxiv-2021-1108b"},{"key":"18404_CR62","doi-asserted-by":"crossref","unstructured":"Panda, A. et al. Identifying a clinically applicable mutational burden threshold as a potential biomarker of response to immune checkpoint therapy in solid tumors. JCO Precis. Oncol. 1\u201313 (2017).","DOI":"10.1200\/PO.17.00146"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-022-18404-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-022-18404-4","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-022-18404-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,11,25]],"date-time":"2022-11-25T02:07:06Z","timestamp":1669342026000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-022-18404-4"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,8,18]]},"references-count":62,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["18404"],"URL":"https:\/\/doi.org\/10.1038\/s41598-022-18404-4","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2020.12.14.420539","asserted-by":"object"}]},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,8,18]]},"assertion":[{"value":"3 April 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"10 August 2022","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 August 2022","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"All authors are current or former employees of subsidiaries of Merck & Co., Inc., Kenilworth, NJ, USA.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"14087"}}