Polygenic risk score for ulcerative colitis predicts immune checkpoint inhibitor-mediated colitis.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
26 Mar 2024
26 Mar 2024
Historique:
received:
22
05
2023
accepted:
15
12
2023
medline:
27
3
2024
pubmed:
27
3
2024
entrez:
27
3
2024
Statut:
epublish
Résumé
Immune checkpoint inhibitor-mediated colitis (IMC) is a common adverse event of treatment with immune checkpoint inhibitors (ICI). We hypothesize that genetic susceptibility to Crohn's disease (CD) and ulcerative colitis (UC) predisposes to IMC. In this study, we first develop a polygenic risk scores for CD (PRS
Identifiants
pubmed: 38531883
doi: 10.1038/s41467-023-44512-4
pii: 10.1038/s41467-023-44512-4
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2568Investigateurs
Natasha B Leighl
(NB)
Penelope A Bradbury
(PA)
Frances A Shepherd
(FA)
Adrian G Sacher
(AG)
Lawson Eng
(L)
Informations de copyright
© 2024. The Author(s).
Références
Bai, R. L., Chen, N. F., Li, L. Y. & Cui, J. W. A brand new era of cancer immunotherapy: breakthroughs and challenges. Chin. Med. J. (Engl.). 134, 1267–1275 (2021).
pubmed: 34039862
pmcid: 8183825
doi: 10.1097/CM9.0000000000001490
Wei, S. C., Duffy, C. R. & Allison, J. P. Fundamental mechanisms of immune checkpoint blockade therapy. Cancer Discov. 8, 1069–1086 (2018).
pubmed: 30115704
doi: 10.1158/2159-8290.CD-18-0367
Twomey, J. D. & Zhang, B. Cancer immunotherapy update: FDA-approved checkpoint inhibitors and companion diagnostics. AAPS J. 23, 39 (2021).
pubmed: 33677681
doi: 10.1208/s12248-021-00574-0
Topalian, S. L., Drake, C. G. & Pardoll, D. M. Immune checkpoint blockade: a common denominator approach to cancer therapy. Cancer Cell. 27, 450–461 (2015).
pubmed: 25858804
pmcid: 4400238
doi: 10.1016/j.ccell.2015.03.001
Sharpe, A. H. Introduction to checkpoint inhibitors and cancer immunotherapy. Immunol. Rev. 276, 5–8 (2017).
pubmed: 28258698
pmcid: 5362112
doi: 10.1111/imr.12531
Robert, C. A decade of immune-checkpoint inhibitors in cancer therapy. Nat. Commun. 11, 3801 (2020).
pubmed: 32732879
pmcid: 7393098
doi: 10.1038/s41467-020-17670-y
Darvin, P., Toor, S. M., Sasidharan Nair, V. & Elkord, E. Immune checkpoint inhibitors: recent progress and potential biomarkers. Exp. Mol. Med. 50, 1–11 (2018).
pubmed: 30546008
doi: 10.1038/s12276-018-0191-1
Buchbinder, E. I. & Desai, A. CTLA-4 and PD-1 pathways: similarities, differences, and implications of their inhibition. Am. J. Clin. Oncol. 39, 98–106 (2016).
pubmed: 26558876
pmcid: 4892769
doi: 10.1097/COC.0000000000000239
Waldman, A. D., Fritz, J. M. & Lenardo, M. J. A guide to cancer immunotherapy: from T cell basic science to clinical practice. Nat. Rev. Immunol. 20, 651–668 (2020).
pubmed: 32433532
pmcid: 7238960
doi: 10.1038/s41577-020-0306-5
Liu, X., Hogg, G. D. & DeNardo, D. G. Rethinking immune checkpoint blockade: ‘Beyond the T cell. J. Immunother. Cancer 9, e001460 (2021).
pubmed: 33468555
pmcid: 7817791
doi: 10.1136/jitc-2020-001460
Ribas, A. Tumor immunotherapy directed at PD-1. N. Engl. J. Med. 366, 2517–2519 (2012).
pubmed: 22658126
doi: 10.1056/NEJMe1205943
Byun, D. J., Wolchok, J. D., Rosenberg, L. M. & Girotra, M. Cancer immunotherapy—immune checkpoint blockade and associated endocrinopathies. Nat. Rev. Endocrinol. 13, 195–207 (2017).
pubmed: 28106152
pmcid: 5629093
doi: 10.1038/nrendo.2016.205
Postow, M. A., Sidlow, R. & Hellmann, M. D. Immune-related adverse events associated with immune checkpoint blockade. N. Engl. J. Med. 378, 158–168 (2018).
pubmed: 29320654
doi: 10.1056/NEJMra1703481
Wang, Y. et al. Treatment-related adverse events of PD-1 and PD-L1 inhibitors in clinical trials. JAMA Oncol. 5, 1008–1019 (2019).
pubmed: 31021376
pmcid: 6487913
doi: 10.1001/jamaoncol.2019.0393
Okiyama, N. & Tanaka, R. Immune-related adverse events in various organs caused by immune checkpoint inhibitors. Allergol. Int. 71, 169–178 (2022).
pubmed: 35101349
doi: 10.1016/j.alit.2022.01.001
Shankar, B. et al. Multisystem immune-related adverse events associated with immune checkpoint inhibitors for treatment of non-small cell lung cancer. JAMA Oncol. 6, 1952–1956 (2020).
pubmed: 33119034
doi: 10.1001/jamaoncol.2020.5012
Conroy, M. & Naidoo, J. Immune-related adverse events and the balancing act of immunotherapy. Nat. Commun. 13, 392 (2022).
pubmed: 35046403
pmcid: 8770784
doi: 10.1038/s41467-022-27960-2
Som, A. et al. Immune checkpoint inhibitor-induced colitis: a comprehensive review. World J. Clin. Cases 7, 405–418 (2019).
pubmed: 30842952
pmcid: 6397821
doi: 10.12998/wjcc.v7.i4.405
Pocha, C., Roat, J. & Viskocil, K. Immune-mediated colitis: important to recognize and treat. J. Crohn’s Colitis 8, 181–182 (2014).
doi: 10.1016/j.crohns.2013.09.019
Pauken, K. E., Dougan, M., Rose, N. R., Lichtman, A. H. & Sharpe, A. H. Adverse events following cancer immunotherapy: obstacles and opportunities. Trends Immunol. 40, 511–523 (2019).
pubmed: 31053497
pmcid: 6527345
doi: 10.1016/j.it.2019.04.002
Kelly-Goss, M. R., Badran, Y. R. & Dougan, M. Update on immune checkpoint inhibitor Enterocolitis. Curr. Gastroenterol. Rep. 24, 171–181 (2022).
pubmed: 36264425
pmcid: 9583048
doi: 10.1007/s11894-022-00852-7
Chen, J. H., Pezhouh, M. K., Lauwers, G. Y. & Masia, R. Histopathologic features of colitis due to immunotherapy with anti-PD-1 antibodies. Am. J. Surg. Pathol. 41, 643–654 (2017).
pubmed: 28296676
doi: 10.1097/PAS.0000000000000829
Nahar, K. J. et al. Clinicopathological characteristics and management of colitis with anti-PD1 immunotherapy alone or in combination with ipilimumab. J. Immunother. Cancer 8, e001488 (2020).
pubmed: 33234603
pmcid: 7689081
doi: 10.1136/jitc-2020-001488
Roden, D. M. et al. Development of a large-scale de-identified DNA biobank to enable personalized medicine. Clin. Pharm. Ther. 84, 362–369 (2008).
doi: 10.1038/clpt.2008.89
Privé, F., Arbel, J. & Vilhjálmsson, B. J. LDpred2: better, faster, stronger. Bioinformatics 36, 5424–5431 (2020).
pmcid: 8016455
doi: 10.1093/bioinformatics/btaa1029
Ashton, J. J., Latham, K., Beattie, R. M. & Ennis, S. Review article: the genetics of the human leucocyte antigen region in inflammatory bowel disease. Aliment. Pharmacol. Ther. 50, 885–900 (2019).
pubmed: 31518029
doi: 10.1111/apt.15485
Goyette, P. et al. High density mapping of the MHC identifies a shared role for HLA-DRB1*01:03 in inflammatory bowel diseases and heterozygous advantage in ulcerative colitis. Nat. Genet. 47, 172–179 (2015).
pubmed: 25559196
pmcid: 4310771
doi: 10.1038/ng.3176
Marin-Acevedo, J. A., Kimbrough, E. O. & Lou, Y. Next generation of immune checkpoint inhibitors and beyond. J. Hematol. Oncol. 14, 45 (2021).
pubmed: 33741032
pmcid: 7977302
doi: 10.1186/s13045-021-01056-8
Tang, W. F. et al. Adjuvant immunotherapy in early-stage resectable non–small cell lung cancer: a new milestone. Front. Oncol. 13, 1063183 (2023).
pubmed: 36776323
pmcid: 9909200
doi: 10.3389/fonc.2023.1063183
Mittendorf, E. A., Burgers, F., Haanen, J. & Cascone, T. Neoadjuvant immunotherapy: leveraging the immune system to treat early-stage disease. Am. Soc. Clin. Oncol. Educ. Book. 189–203 https://doi.org/10.1200/EDBK_349411 (2022)
Krishnamoorthy, M., Lenehan, J. G. & Maleki Vareki, S. Neoadjuvant immunotherapy for high-risk, resectable malignancies: scientific rationale and clinical challenges. J. Natl Cancer Inst. 113, 823–832 (2021).
pubmed: 33432320
pmcid: 8246900
doi: 10.1093/jnci/djaa216
Hu, H. G. & Li, Y. M. Emerging adjuvants for cancer immunotherapy. Front. Chem. 8, 601 (2020).
pubmed: 32850636
pmcid: 7406886
doi: 10.3389/fchem.2020.00601
Zhang, Y. et al. Biomarkers and risk factors for the early prediction of immune-related adverse events: a review. Hum. Vaccin. Immunother. 18, 2018894 (2022).
pubmed: 35108160
pmcid: 8986173
doi: 10.1080/21645515.2021.2018894
Hommes, J. W., Verheijden, R. J., Suijkerbuijk, K. P. M. & Hamann, D. Biomarkers of checkpoint inhibitor induced immune-related adverse events—a comprehensive review. Front Oncol. 10, 585311 (2021).
pubmed: 33643899
pmcid: 7905347
doi: 10.3389/fonc.2020.585311
Kennedy, L. C. & Grivas, P. Immunotherapy-related colitis: an emerging challenge and a quest for prospective data. JCO Oncol. Pract. 16, 464–465 (2020).
pubmed: 32780983
doi: 10.1200/OP.20.00620
Westdorp, H. et al. Mechanisms of immune checkpoint inhibitor-mediated colitis. Front. Immunol. 2021;12. Accessed September 23, 2022. https://www.frontiersin.org/articles/10.3389/fimmu.2021.768957 .
Luo, Y. et al. Exploring the genetic architecture of inflammatory bowel disease by whole-genome sequencing identifies association at ADCY7. Nat. Genet. 49, 186–192 (2017).
pubmed: 28067910
pmcid: 5289625
doi: 10.1038/ng.3761
Onoufriadis, A. et al. Exome sequencing and genotyping identify a rare variant in NLRP7 gene associated with ulcerative colitis. J. Crohn’s Colitis 12, 321–326 (2018).
doi: 10.1093/ecco-jcc/jjx157
Ellinghaus, D., Bethune, J., Petersen, B. S. & Franke, A. The genetics of Crohn’s disease and ulcerative colitis–status quo and beyond. Scand. J. Gastroenterol. 50, 13–23 (2015).
pubmed: 25523552
doi: 10.3109/00365521.2014.990507
Luo, J. et al. Immunotherapy-mediated thyroid dysfunction: genetic risk and impact on outcomes with PD-1 blockade in non–small cell lung cancer. Clin. Cancer Res. 27, 5131–5140 (2021).
pubmed: 34244291
pmcid: 8815444
doi: 10.1158/1078-0432.CCR-21-0921
Khan, Z. et al. Genetic variation associated with thyroid autoimmunity shapes the systemic immune response to PD-1 checkpoint blockade. Nat. Commun. 12, 3355 (2021).
pubmed: 34099659
pmcid: 8184890
doi: 10.1038/s41467-021-23661-4
Khan, Z. et al. Polygenic risk for skin autoimmunity impacts immune checkpoint blockade in bladder cancer. Proc. Natl Acad. Sci. USA 117, 12288–12294 (2020).
pubmed: 32430334
pmcid: 7275757
doi: 10.1073/pnas.1922867117
Zhou, X. et al. Are immune-related adverse events associated with the efficacy of immune checkpoint inhibitors in patients with cancer? A systematic review and meta-analysis. BMC Med. 18, 87 (2020).
pubmed: 32306958
pmcid: 7169020
doi: 10.1186/s12916-020-01549-2
Zhao, Z. et al. Immune-related adverse events associated with outcomes in patients with NSCLC treated with anti-PD-1 inhibitors: a systematic review and meta-analysis. Front. Oncol. 2021;11. Accessed June 1, 2022. https://www.frontiersin.org/article/10.3389/fonc.2021.708195 .
Petrelli, F. et al. Immune-related adverse events and survival in solid tumors treated with immune checkpoint inhibitors: a systematic review and meta-analysis. J. Immunother. 43, 1–7 (2020).
pubmed: 31574022
doi: 10.1097/CJI.0000000000000300
Toi, Y. et al. Association of immune‐related adverse events with clinical benefit in patients with advanced non‐small‐cell lung cancer treated with nivolumab. Oncologist 23, 1358–1365 (2018).
pubmed: 29934411
pmcid: 6291330
doi: 10.1634/theoncologist.2017-0384
Morimoto, K. et al. Immune-related adverse events are associated with clinical benefit in patients with non-small-cell lung cancer treated with immunotherapy plus chemotherapy: a retrospective study. Front. Oncol. 11, 630136 (2021).
pubmed: 33833990
pmcid: 8021904
doi: 10.3389/fonc.2021.630136
Abu-Sbeih, H. et al. Immune checkpoint inhibitor-induced colitis as a predictor of survival in metastatic melanoma. Cancer Immunol. Immunother. 68, 553–561 (2019).
pubmed: 30666357
doi: 10.1007/s00262-019-02303-1
Abu-Sbeih, H. et al. Outcomes of vedolizumab therapy in patients with immune checkpoint inhibitor–induced colitis: a multi-center study. J. Immunother. Cancer 6, 142 (2018).
pubmed: 30518410
pmcid: 6280383
doi: 10.1186/s40425-018-0461-4
Bergqvist, V. et al. Vedolizumab treatment for immune checkpoint inhibitor-induced enterocolitis. Cancer Immunol. Immunother. 66, 581–592 (2017).
pubmed: 28204866
pmcid: 5406433
doi: 10.1007/s00262-017-1962-6
Park, R., Lopes, L., Cristancho, C. R., Riano, I. M. & Saeed, A. Treatment-related adverse events of combination immune checkpoint inhibitors: systematic review and meta-analysis. Front. Oncol. 2020;10. Accessed March 15, 2023. https://www.frontiersin.org/articles/10.3389/fonc.2020.00258 .
Paz-Ares, L. et al. First-line nivolumab plus ipilimumab combined with two cycles of chemotherapy in patients with non-small-cell lung cancer (CheckMate 9LA): an international, randomised, open-label, phase 3 trial. Lancet Oncol. 22, 198–211 (2021).
pubmed: 33476593
doi: 10.1016/S1470-2045(20)30641-0
Da, L. et al. Organ-specific immune-related adverse events associated with immune checkpoint inhibitor monotherapy versus combination therapy in cancer: a meta-analysis of randomized controlled trials. Front. Pharmacol. 10, 1671 (2020).
pubmed: 32082164
pmcid: 7002539
doi: 10.3389/fphar.2019.01671
Carretero-González, A. et al. Comparative safety analysis of immunotherapy combined with chemotherapy versus monotherapy in solid tumors: a meta-analysis of randomized clinical trials. Oncotarget 10, 3294–3301 (2019).
pubmed: 31143375
pmcid: 6524939
doi: 10.18632/oncotarget.26908
Zhuo, M., Chi, Y. & Wang, Z. The adverse events associated with combination immunotherapy in cancers: Challenges and chances. Asia-Pac. J. Clin. Oncol. 16, e154–e159 (2020).
pubmed: 32786161
doi: 10.1111/ajco.13365
Felip, E. et al. Adjuvant atezolizumab after adjuvant chemotherapy in resected stage IB–IIIA non-small-cell lung cancer (IMpower010): a randomised, multicentre, open-label, phase 3 trial. Lancet 398, 1344–1357 (2021).
pubmed: 34555333
doi: 10.1016/S0140-6736(21)02098-5
O’Brien, M. et al. Pembrolizumab versus placebo as adjuvant therapy for completely resected stage IB–IIIA non-small-cell lung cancer (PEARLS/KEYNOTE-091): an interim analysis of a randomised, triple-blind, phase 3 trial. Lancet Oncol. 23, 1274–1286 (2022).
pubmed: 36108662
doi: 10.1016/S1470-2045(22)00518-6
Luke, J. J. et al. Pembrolizumab versus placebo as adjuvant therapy in completely resected stage IIB or IIC melanoma (KEYNOTE-716): a randomised, double-blind, phase 3 trial. Lancet 399, 1718–1729 (2022).
pubmed: 35367007
doi: 10.1016/S0140-6736(22)00562-1
Klein, R. J. & Gümüş, Z. H. Are polygenic risk scores ready for the cancer clinic?-a perspective. Transl. Lung Cancer Res. 11, 910–919 (2022).
pubmed: 35693291
pmcid: 9186162
doi: 10.21037/tlcr-21-698
Lewis, A. C. F. & Green, R. C. Polygenic risk scores in the clinic: new perspectives needed on familiar ethical issues. Genome Med. 13, 14 (2021).
pubmed: 33509269
pmcid: 7844961
doi: 10.1186/s13073-021-00829-7
Lewis, A. C. F., Green, R. C. & Vassy, J. L. Polygenic risk scores in the clinic: translating risk into action. HGG Adv. 2, 100047 (2021).
pubmed: 35047839
pmcid: 8756548
Martin, A. R. et al. Clinical use of current polygenic risk scores may exacerbate health disparities. Nat. Genet. 51, 584–591 (2019).
pubmed: 30926966
pmcid: 6563838
doi: 10.1038/s41588-019-0379-x
Lee, M. & Chang, E. B. Inflammatory bowel diseases (IBD) and the microbiome—searching the crime scene for clues. Gastroenterology 160, 524–537 (2021).
pubmed: 33253681
doi: 10.1053/j.gastro.2020.09.056
Anderson, J. R., Cain, K. C. & Gelber, R. D. Analysis of survival by tumor response. J. Clin. Oncol. 1, 710–719 (1983).
pubmed: 6668489
doi: 10.1200/JCO.1983.1.11.710
Anderson, J. R., Cain, K. C. & Gelber, R. D. Analysis of survival by tumor response and other comparisons of time-to-event by outcome variables. J. Clin. Oncol. 26, 3913–3915 (2008).
pubmed: 18711176
doi: 10.1200/JCO.2008.16.1000
Morgan, C. J. Landmark analysis: a primer. J. Nucl. Cardiol. 26, 391–393 (2019).
pubmed: 30719655
doi: 10.1007/s12350-019-01624-z
Bycroft, C. et al. The UK Biobank resource with deep phenotyping and genomic data. Nature 562, 203–209 (2018).
pubmed: 30305743
pmcid: 6786975
doi: 10.1038/s41586-018-0579-z
de Lange, K. M. et al. Genome-wide association study implicates immune activation of multiple integrin genes in inflammatory bowel disease. Nat. Genet. 49, 256–261 (2017).
pubmed: 28067908
pmcid: 5289481
doi: 10.1038/ng.3760
Cook, S. et al. Accurate imputation of human leukocyte antigens with CookHLA. Nat. Commun. 12, 1264 (2021).
pubmed: 33627654
pmcid: 7904773
doi: 10.1038/s41467-021-21541-5
Choi, W., Luo, Y., Raychaudhuri, S. & Han, B. HATK: HLA analysis toolkit. Bioinformatics 37, 416–418 (2021).
pubmed: 32735319
doi: 10.1093/bioinformatics/btaa684
Brown, W. M. et al. Overview of the MHC fine mapping data. Diabetes Obes. Metab. 11, 2–7 (2009) .
pubmed: 19143809
pmcid: 2697814
doi: 10.1111/j.1463-1326.2008.00997.x
Middha, P. PoojaMiddha/GeRI_colitis: Polygenic risk score for ulcerative colitis predicts immune checkpoint inhibitor-mediated colitis. Published online November 20, 2023. https://doi.org/10.5281/ZENODO.10162343 .