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Molecular Biomarkers of Response to Cancer Immunotherapy

Published:August 22, 2022DOI:https://doi.org/10.1016/j.cll.2022.05.004

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      References

        • Ishida Y.
        • Agata Y.
        • Shibahara K.
        • et al.
        Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death.
        EMBO J. 1992; 11: 3887-3895
        • Krummel M.F.
        • Allison J.P.
        CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation.
        J Exp Med. 1995; 182: 459-465
        • Sharma P.
        • Allison J.P.
        The future of immune checkpoint therapy.
        Science. 2015; 348: 56-61
        • Leach D.R.
        • Krummel M.F.
        • Allison J.P.
        Enhancement of antitumor immunity by CTLA-4 blockade.
        Science. 1996; 271: 1734-1736
        • Cameron F.
        • Whiteside G.
        • Perry C.
        Ipilimumab: first global approval.
        Drugs. 2011; 71: 1093-1104
        • Davis A.A.
        • Patel V.G.
        The role of PD-L1 expression as a predictive biomarker: an analysis of all US Food and Drug Administration (FDA) approvals of immune checkpoint inhibitors.
        J Immunother Cancer. 2019; 7: 278
        • Postow M.A.
        • Chesney J.
        • Pavlick A.C.
        • et al.
        Nivolumab and ipilimumab versus ipilimumab in untreated melanoma.
        N Engl J Med. 2015; 372: 2006-2017
        • Vaddepally R.K.
        • Kharel P.
        • Pandey R.
        • et al.
        Review of indications of FDA-approved immune checkpoint inhibitors per NCCN guidelines with the level of evidence.
        Cancers. 2020; 12: 738
        • Ribas A.
        • Wolchok J.D.
        Cancer immunotherapy using checkpoint blockade.
        Science. 2018; 359: 1350-1355
        • Woo S.-R.
        • Turnis M.E.
        • Goldberg M.V.
        • et al.
        Immune inhibitory molecules LAG-3 and PD-1 synergistically regulate T-cell function to promote tumoral immune escape.
        Cancer Res. 2012; 72: 917-927
        • Xu F.
        • Liu J.
        • Liu Di
        • et al.
        LSECtin expressed on melanoma cells promotes tumor progression by inhibiting antitumor T-cell responses.
        Cancer Res. 2014; 74: 3418-3428
        • Ascierto P.A.
        • Bono P.
        • Bhatia S.
        • et al.
        LBA18 - efficacy of BMS-986016, a monoclonal antibody that targets lymphocyte activation gene-3 (LAG-3), in combination with nivolumab in pts with melanoma who progressed during prior anti–PD-1/PD-L1 therapy (mel prior IO) in all-comer and biomarker-enriched populations.
        Ann Oncol. 2017; 28: v611-v612
        • Long L.
        • Zhang X.
        • Chen F.
        • et al.
        The promising immune checkpoint LAG-3: from tumor microenvironment to cancer immunotherapy.
        Genes Cancer. 2018; 9: 176-189
        • Acharya N.
        • Sabatos-Peyton C.
        • Anderson A.C.
        Tim-3 finds its place in the cancer immunotherapy landscape.
        J Immunother Cancer. 2020; 8: e000911
        • Fourcade J.
        • Sun Z.
        • Benallaoua M.
        • et al.
        Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen-specific CD8+ T cell dysfunction in melanoma patients.
        J Exp Med. 2010; 207: 2175-2186
        • Rezaei M.
        • Tan J.
        • Zeng C.
        • et al.
        TIM-3 in leukemia; immune response and beyond.
        Front Oncol. 2021; 11: 753677
        • Gao X.
        • Zhu Y.
        • Li G.
        • et al.
        TIM-3 expression characterizes regulatory T cells in tumor tissues and is associated with lung cancer progression.
        PLoS One. 2012; 7: e30676
        • Ngiow S.F.
        • Scheidt, von B.
        • Akiba H.
        • et al.
        Anti-TIM3 antibody promotes T cell IFN-γ-mediated antitumor immunity and suppresses established tumors.
        Cancer Res. 2011; 71: 3540-3551
        • Sakuishi K.
        • Apetoh L.
        • Sullivan J.M.
        • et al.
        Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity.
        J Exp Med. 2010; 207: 2187-2194
        • Zhou Q.
        • Munger M.E.
        • Veenstra R.G.
        • et al.
        Coexpression of Tim-3 and PD-1 identifies a CD8+ T-cell exhaustion phenotype in mice with disseminated acute myelogenous leukemia.
        Blood. 2011; 117: 4501-4510
        • Pan C.
        • Liu H.
        • Robins E.
        • et al.
        Next-generation immuno-oncology agents: current momentum shifts in cancer immunotherapy.
        J Hematol Oncol. 2020;
        • Carretero-González A.
        • Lora D.
        • Ghanem I.
        • et al.
        Analysis of response rate with ANTI PD1/PD-L1 monoclonal antibodies in advanced solid tumors: a meta-analysis of randomized clinical trials.
        Oncotarget. 2018; 9: 8706-8715
        • Kourie H.R.
        • Klastersky J.
        Immune checkpoint inhibitors side effects and management.
        Immunotherapy. 2016; 8: 799-807
        • Brahmer J.R.
        • Tykodi S.S.
        • Chow L.Q.M.
        • et al.
        Safety and activity of anti-PD-L1 antibody in patients with advanced cancer.
        N Engl J Med. 2012; 366: 2455-2465
        • Khunger M.
        • Jain P.
        • Rakshit S.
        • et al.
        Safety and efficacy of PD-1/PD-L1 inhibitors in treatment-naive and chemotherapy-refractory patients with non-small-cell lung cancer: a systematic review and meta-analysis.
        Clin Lung Cancer. 2018; 19: e335-e348
        • Mahoney K.M.
        • Atkins M.B.
        Prognostic and predictive markers for the new immunotherapies.
        Oncology (Williston Park). 2014; 28: 39-48
        • Robert C.
        • Long G.V.
        • Brady B.
        • et al.
        Nivolumab in previously untreated melanoma without BRAF mutation.
        N Engl J Med. 2015; 372: 320-330
        • Weber J.S.
        • D'Angelo S.P.
        • Minor D.
        • et al.
        Nivolumab versus chemotherapy in patients with advanced melanoma who progressed after anti-CTLA-4 treatment (CheckMate 037): a randomised, controlled, open-label, phase 3 trial.
        Lancet Oncol. 2015; 16: 375-384
        • Brahmer J.
        • Reckamp K.L.
        • Baas P.
        • et al.
        Nivolumab versus docetaxel in advanced squamous-cell non-small-cell lung cancer.
        N Engl J Med. 2015; 373: 123-135
        • Garon E.B.
        • Rizvi N.A.
        • Hui R.
        • et al.
        Pembrolizumab for the treatment of non-small-cell lung cancer.
        N Engl J Med. 2015; 372: 2018-2028
        • Walk E.E.
        • Yohe S.L.
        • Beckman A.
        • et al.
        • College of American pathologists personalized health care committee
        The cancer immunotherapy biomarker testing landscape.
        Arch Pathol Lab Med. 2020; 144: 706-724
        • McLaughlin J.
        • Han G.
        • Schalper K.A.
        • et al.
        Quantitative assessment of the heterogeneity of PD-L1 expression in non-small-cell lung cancer.
        JAMA Oncol. 2016; 2: 46-54
        • Rimm D.L.
        • Han G.
        • Taube J.M.
        • et al.
        A prospective, multi-institutional, pathologist-based assessment of 4 immunohistochemistry assays for PD-L1 expression in non-small cell lung cancer.
        JAMA Oncol. 2017; 3: 1051-1058
        • Haragan A.
        • Field J.K.
        • Davies M.P.A.
        • et al.
        Heterogeneity of PD-L1 expression in non-small cell lung cancer: implications for specimen sampling in predicting treatment response.
        Lung Cancer. 2019; 134: 79-84
        • Ilie M.
        • Long-Mira E.
        • Bence C.
        • et al.
        Comparative study of the PD-L1 status between surgically resected specimens and matched biopsies of NSCLC patients reveal major discordances: a potential issue for anti-PD-L1 therapeutic strategies.
        Ann Oncol. 2016; 27: 147-153
        • Liu Y.
        • Dong Z.
        • Jiang T.
        • et al.
        Heterogeneity of PD-L1 expression among the different histological components and metastatic lymph nodes in patients with resected lung adenosquamous carcinoma.
        Clin Lung Cancer. 2018; 19: e421-e430
        • Munari E.
        • Rossi G.
        • Zamboni G.
        • et al.
        PD-L1 assays 22C3 and SP263 are not interchangeable in non-small cell lung cancer when considering clinically relevant cutoffs: an interclone evaluation by differently trained pathologists.
        Am J Surg Pathol. 2018; 42: 1384-1389
        • Munari E.
        • Zamboni G.
        • Lunardi G.
        • et al.
        PD-L1 expression comparison between primary and relapsed non-small cell lung carcinoma using whole sections and clone SP263.
        Oncotarget. 2018; 9: 30465-30471
        • Iyer R.R.
        • Pluciennik A.
        • Burdett V.
        • et al.
        DNA mismatch repair: functions and mechanisms.
        Chem Rev. 2006; 106: 302-323
        • Modrich P.
        • Lahue R.
        Mismatch repair in replication fidelity, genetic recombination, and cancer biology.
        Annu Rev Biochem. 1996; 65: 101-133
        • Buza N.
        • Ziai J.
        • Hui P.
        Mismatch repair deficiency testing in clinical practice.
        Expert Rev Mol Diagn. 2016; 16: 591-604
        • Peltomäki P.
        • Vasen H.
        Mutations associated with HNPCC predisposition — update of ICG-HNPCC/INSiGHT mutation database.
        Dis Markers. 2004; 20: 269-276
        • Lynch H.T.
        • Snyder C.L.
        • Shaw T.G.
        • et al.
        Milestones of Lynch syndrome: 1895-2015.
        Nat Rev Cancer. 2015; 15: 181-194
        • Bonneville R.
        • Krook M.A.
        • Kautto E.A.
        • et al.
        Landscape of microsatellite instability across 39 cancer types.
        JCO Precis Oncol. 2017; 2017 (PO.17.00073)
        • Cortés-Ciriano I.
        • Lee J.J.-K.
        • Xi R.
        • et al.
        Comprehensive analysis of chromothripsis in 2,658 human cancers using whole-genome sequencing.
        Nat Genet. 2020; 52: 331-341
        • Van de Water N.S.
        • Jeevaratnam P.
        • Browett P.J.
        • et al.
        Direct mutational analysis in a family with hereditary non-polyposis colorectal cancer.
        Aust N Z J Med. 1994; 24: 682-686
        • Ellegren H.
        Microsatellites: simple sequences with complex evolution.
        Nat Rev Genet. 2004; 5: 435-445
        • Imai K.
        • Yamamoto H.
        Carcinogenesis and microsatellite instability: the interrelationship between genetics and epigenetics.
        Carcinogenesis. 2008; 29: 673-680
        • Li Y.-C.
        • Korol A.B.
        • Fahima T.
        • et al.
        Microsatellites within genes: structure, function, and evolution.
        Mol Biol Evol. 2004; 21: 991-1007
        • Lynch H.T.
        • Jascur T.
        • Lanspa S.
        • et al.
        Making sense of missense in Lynch syndrome: the clinical perspective.
        Cancer Prev Res (Phila). 2010; 3: 1371-1374
        • Boland C.R.
        • Thibodeau S.N.
        • Hamilton S.R.
        • et al.
        A National Cancer Institute Workshop on Microsatellite Instability for cancer detection and familial predisposition: development of international criteria for the determination of microsatellite instability in colorectal cancer.
        Cancer Res. 1998; : 5248-5257
        • Le D.T.
        • Durham J.N.
        • Smith K.N.
        • et al.
        Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade.
        Science. 2017; 357: 409-413
        • Prasad V.
        • Kaestner V.
        • Mailankody S.
        Cancer drugs approved based on biomarkers and not tumor type-FDA approval of pembrolizumab for mismatch repair-deficient solid cancers.
        JAMA Oncol. 2018; 4: 157-158
        • André T.
        • Shiu K.-K.
        • Kim T.W.
        • et al.
        Pembrolizumab in microsatellite-instability-high advanced colorectal cancer.
        N Engl J Med. 2020; 383: 2207-2218
        • Hegde M.
        • Ferber M.
        • Mao R.
        • et al.
        • Working Group of the American College of Medical Genetics and Genomics (ACMG) Laboratory Quality Assurance Committee
        ACMG technical standards and guidelines for genetic testing for inherited colorectal cancer (Lynch syndrome, familial adenomatous polyposis, and MYH-associated polyposis).
        Genet Med. 2014; 16: 101-116
        • Funkhouser W.K.
        • Lubin I.M.
        • Monzon F.A.
        • et al.
        Relevance, pathogenesis, and testing algorithm for mismatch repair–defective colorectal carcinomas.
        J Mol Diagn. 2012; 14: 91-103
        • Gan C.
        • Love C.
        • Beshay V.
        • et al.
        Applicability of next generation sequencing technology in microsatellite instability testing.
        Genes. 2015; 6: 46-59
        • Kautto E.A.
        • Bonneville R.
        • Miya J.
        • et al.
        Performance evaluation for rapid detection of pan-cancer microsatellite instability with MANTIS.
        Oncotarget. 2017; 8: 7452-7463
        • Nowak J.A.
        • Yurgelun M.B.
        • Bruce J.L.
        • et al.
        Detection of mismatch repair deficiency and microsatellite instability in colorectal adenocarcinoma by targeted next-generation sequencing.
        J Mol Diagn. 2017; 19: 84-91
        • Salipante S.J.
        • Scroggins S.M.
        • Hampel H.L.
        • et al.
        Microsatellite instability detection by next generation sequencing.
        Clin Chem. 2014; 60: 1192-1199
        • Vanderwalde A.
        • Spetzler D.
        • Xiao N.
        • et al.
        Microsatellite instability status determined by next-generation sequencing and compared with PD-L1 and tumor mutational burden in 11,348 patients.
        Cancer Med. 2018; 7: 746-756
        • Hause R.J.
        • Pritchard C.C.
        • Shendure J.
        • et al.
        Classification and characterization of microsatellite instability across 18 cancer types.
        Nat Med. 2016; 22: 1342-1350
        • Middha S.
        • Zhang L.
        • Nafa K.
        • et al.
        Reliable pan-cancer microsatellite instability assessment by using targeted next-generation sequencing data.
        JCO Precis Oncol. 2017;
        • Stadler Z.K.
        • Battaglin F.
        • Middha S.
        • et al.
        Reliable detection of mismatch repair deficiency in colorectal cancers using mutational load in next-generation sequencing panels.
        J Clin Oncol. 2016; 34: 2141-2147
        • Alexandrov L.B.
        • Nik-Zainal S.
        • Wedge D.C.
        • et al.
        Signatures of mutational processes in human cancer.
        Nature. 2013; 500: 415-421
        • Boot A.
        • Covington K.R.
        • Islam S.M.A.
        • et al.
        The repertoire of mutational signatures in human cancer.
        Nature. 2020; : 1-28
        • Snyder A.
        • Makarov V.
        • Merghoub T.
        • et al.
        Genetic basis for clinical response to CTLA-4 blockade in melanoma.
        N Engl J Med. 2014; 371: 2189-2199
        • Hellmann M.D.
        • Ciuleanu T.-E.
        • Pluzanski A.
        • et al.
        Nivolumab plus ipilimumab in lung cancer with a high tumor mutational burden.
        N Engl J Med. 2018; 378: 2093-2104
        • Hellmann M.D.
        • Nathanson T.
        • Rizvi H.
        • et al.
        Genomic features of response to combination immunotherapy in patients with advanced non- small-cell lung cancer.
        Cancer Cell. 2018; 33: 843-852.e844
        • Rizvi N.A.
        • Hellmann M.D.
        • Snyder A.
        • et al.
        Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer.
        Science. 2015; 348: 124-128
        • Goodman A.M.
        • Kato S.
        • Bazhenova L.
        • et al.
        Tumor mutational burden as an independent predictor of response to immunotherapy in diverse cancers.
        Mol Cancer Ther. 2017; 16: 2598-2608
        • Yarchoan M.
        • Hopkins A.
        • Jaffee E.M.
        Tumor mutational burden and response rate to PD-1 inhibition.
        N Engl J Med. 2017; 377: 2500-2501
        • Marabelle A.
        • Fakih M.
        • Lopez J.
        • et al.
        Association of tumour mutational burden with outcomes in patients with advanced solid tumours treated with pembrolizumab: prospective biomarker analysis of the multicohort, open-label, phase 2 KEYNOTE-158 study.
        Lancet Oncol. 2020; 21: 1353-1365
        • Rousseau B.
        • Foote M.B.
        • Maron S.B.
        • et al.
        The spectrum of benefit from checkpoint blockade in hypermutated tumors.
        N Engl J Med. 2021; 384: 1168-1170
        • Chalmers Z.R.
        • Connelly C.F.
        • Fabrizio D.
        • et al.
        Analysis of 100,000 human cancer genomes reveals the landscape of tumor mutational burden.
        Genome Med. 2017; 19: 94
        • Mouw K.W.
        • Goldberg M.S.
        • Konstantinopoulos P.A.
        • et al.
        DNA damage and repair biomarkers of immunotherapy response.
        Cancer Discov. 2017; 7: 675-693
        • Rizvi H.
        • Sanchez-Vega F.
        • La K.
        • et al.
        Molecular determinants of response to anti-programmed cell death (PD)-1 and anti-programmed death-ligand 1 (PD-L1) blockade in patients with non-small-cell lung cancer profiled with targeted next-generation sequencing.
        J Clin Oncol. 2018; 36: 633-641
        • Campesato L.F.
        • Barroso-Sousa R.
        • Jimenez L.
        • et al.
        Comprehensive cancer-gene panels can be used to estimate mutational load and predict clinical benefit to PD-1 blockade in clinical practice.
        Oncotarget. 2015; 6: 34221-34227
        • Singal G.
        • Miller P.G.
        • Agarwala V.
        • et al.
        Association of patient characteristics and tumor genomics with clinical outcomes among patients with non-small cell lung cancer using a clinicogenomic database.
        JAMA. 2019; 321: 1391-1399
        • Fang W.
        • Ma Y.
        • Yin J.C.
        • et al.
        Comprehensive genomic profiling identifies novel genetic predictors of response to anti-PD-(L)1 therapies in non-small cell lung cancer.
        Clin Cancer Res. 2019; 25: 5015-5026
        • Balar A.V.
        • Galsky M.D.
        • Rosenberg J.E.
        • et al.
        Atezolizumab as first-line treatment in cisplatin-ineligible patients with locally advanced and metastatic urothelial carcinoma: a single-arm, multicentre, phase 2 trial.
        Lancet. 2017; 389: 67-76
        • Gandara D.R.
        • Paul S.M.
        • Kowanetz M.
        • et al.
        Blood-based tumor mutational burden as a predictor of clinical benefit in non-small-cell lung cancer patients treated with atezolizumab.
        Nat Med. 2018; 24: 1441-1448
        • Johnson D.B.
        • Frampton G.M.
        • Rioth M.J.
        • et al.
        Targeted next generation sequencing identifies markers of response to PD-1 blockade.
        Cancer Immunol Res. 2016; 4: 959-967
        • Samstein R.M.
        • Lee C.-H.
        • Shoushtari A.N.
        • et al.
        Tumor mutational load predicts survival after immunotherapy across multiple cancer types.
        Nat Genet. 2019; 51: 202-206
        • McGranahan N.
        • Furness A.J.S.
        • Rosenthal R.
        • et al.
        Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade.
        Science. 2016; 351: 1463-1469
        • Mahmoud S.M.A.
        • Paish E.C.
        • Powe D.G.
        • et al.
        Tumor-infiltrating CD8+ lymphocytes predict clinical outcome in breast cancer.
        J Clin Oncol. 2011; 29: 1949-1955
        • Mlecnik B.
        • Tosolini M.
        • Kirilovsky A.
        • et al.
        Histopathologic-based prognostic factors of colorectal cancers are associated with the state of the local immune reaction.
        J Clin Oncol. 2011; 29: 610-618
        • Chen P.-L.
        • Roh W.
        • Reuben A.
        • 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. 2016; 6: 827-837
        • Schmid P.
        • Salgado R.
        • Park Y.H.
        • et al.
        Pembrolizumab plus chemotherapy as neoadjuvant treatment of high-risk, early-stage triple-negative breast cancer: results from the phase 1b open- label, multicohort KEYNOTE-173 study.
        Ann Oncol. 2020; 31: 569-581
        • Tumeh P.C.
        • Harview C.L.
        • Yearley J.H.
        • et al.
        PD-1 blockade induces responses by inhibiting adaptive immune resistance.
        Nature. 2014; 515: 568-571
        • Wickenhauser C.
        • Bethmann D.
        • Feng Z.
        • et al.
        Multispectral fluorescence imaging allows for distinctive topographic assessment and subclassification of tumor-infiltrating and surrounding immune cells.
        Methods Mol Biol. 2019; 1913: 13-31
        • Hofman P.
        • Badoual C.
        • Henderson F.
        • et al.
        Multiplexed immunohistochemistry for molecular and immune profiling in lung cancer-just about ready for prime-time?.
        Cancers. 2019; 12: 283
        • Parra E.R.
        • Francisco-Cruz A.
        • Wistuba I.I.
        State-of-the-Art of profiling immune contexture in the era of multiplexed staining and digital analysis to study paraffin tumor tissues.
        Cancers. 2019; 12: 247
        • Giraldo N.A.
        • Nguyen P.
        • Engle E.L.
        • et al.
        Multidimensional, quantitative assessment of PD-1/PD-L1 expression in patients with Merkel cell carcinoma and association with response to pembrolizumab.
        J Immunother Cancer. 2018; 6: 99
        • Johnson D.B.
        • Bordeaux J.
        • Kim J.Y.
        • et al.
        Quantitative spatial profiling of PD-1/PD-L1 interaction and HLA-DR/Ido-1 predicts improved outcomes of anti-PD-1 therapies in metastatic melanoma.
        Clin Cancer Res. 2018; 24: 5250-5260
        • Cristescu R.
        • Mogg R.
        • Ayers M.
        • et al.
        Pan-tumor genomic biomarkers for PD-1 checkpoint blockade-based immunotherapy.
        Science. 2018; 362: eaar3593
        • Ott P.A.
        • Bang Y.-J.
        • Piha-Paul S.A.
        • et al.
        T-Cell-Inflamed gene-expression profile, programmed death ligand 1 expression, and tumor mutational burden predict efficacy in patients treated with pembrolizumab across 20 cancers: KEYNOTE-028.
        J Clin Oncol. 2019; 37: 318-327
        • Fritsch E.F.
        • Rajasagi M.
        • Ott P.A.
        • et al.
        HLA-binding properties of tumor neoepitopes in humans.
        Cancer Immunol Res. 2014; 2: 522-529
        • Parkhurst M.R.
        • Robbins P.F.
        • Tran E.
        • et al.
        Unique neoantigens arise from somatic mutations in patients with gastrointestinal cancers.
        Cancer Discov. 2019; 9: 1022-1035
        • Schumacher T.N.
        • Schreiber R.D.
        Neoantigens in cancer immunotherapy.
        Science. 2015; 348: 69-74
        • Tran E.
        • Robbins P.F.
        • Rosenberg S.A.
        “Final common pathway” of human cancer immunotherapy: targeting random somatic mutations.
        Nat Immunol. 2017; 18: 255-262
        • Van Bergen C.A.M.
        • Rutten C.E.
        • Van Der Meijden E.D.
        • et al.
        High-throughput characterization of 10 new minor histocompatibility antigens by whole genome association scanning.
        Cancer Res. 2010; 70: 9073-9083
        • van Buuren M.M.
        • Calis J.J.
        • Schumacher T.N.
        High sensitivity of cancer exome-based CD8 T cell neo-antigen identification.
        Oncoimmunology. 2014; 3: e28836
        • Routy B.
        • Le Chatelier E.
        • Derosa L.
        • et al.
        Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors.
        Science. 2018; 359: 91-97
        • Matson V.
        • Fessler J.
        • Bao R.
        • et al.
        The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients.
        Science. 2018; 359: 104-108
        • Gopalakrishnan V.
        • Spencer C.N.
        • Nezi L.
        • et al.
        Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients.
        Science. 2018; 359: 97-103
        • Chowell D.
        • Morris L.G.T.
        • Grigg C.M.
        • et al.
        Patient HLA class I genotype influences cancer response to checkpoint blockade immunotherapy.
        Science. 2018; 359: 582-587
        • Rosenthal R.
        • Hiley C.T.
        • Rowan A.J.
        • et al.
        Allele-specific HLA loss and immune escape in lung cancer evolution.
        Cell. 2017; 171: 1259-1271.e11
        • Havel J.J.
        • Chowell D.
        • Chan T.A.
        The evolving landscape of biomarkers for checkpoint inhibitor immunotherapy.
        Nat Rev Cancer. 2019; 19: 133-150
        • Luchini C.
        • Bibeau F.
        • Ligtenberg M.J.L.
        • et al.
        ESMO recommendations on microsatellite instability testing for immunotherapy in cancer, and its relationship with PD-1/PD-L1 expression and tumour mutational burden: a systematic review-based approach.
        Ann Oncol. 2019; 30: 1232-1243
        • Chowell D.
        • Yoo S.-K.
        • Valero C.
        • et al.
        Improved prediction of immune checkpoint blockade efficacy across multiple cancer types.
        Nat Biotechnol. 2022; 40: 499-506