Review
. 2021 Oct; 184(21):5309-5337.
doi: 10.1016/j.cell.2021.09.020.

Hallmarks of response, resistance, and toxicity to immune checkpoint blockade

Golnaz Morad 1 Beth A Helmink 2 Padmanee Sharma 3 Jennifer A Wargo 4 
Affiliations
  • PMID: 34624224
  •     242 References
  •     18 citations

Abstract

Unprecedented advances have been made in cancer treatment with the use of immune checkpoint blockade (ICB). However, responses are limited to a subset of patients, and immune-related adverse events (irAEs) can be problematic, requiring treatment discontinuation. Iterative insights into factors intrinsic and extrinsic to the host that impact ICB response and toxicity are critically needed. Our understanding of the impact of host-intrinsic factors (such as the host genome, epigenome, and immunity) has evolved substantially over the past decade, with greater insights on these factors and on tumor and immune co-evolution. Additionally, we are beginning to understand the impact of acute and cumulative exposures-both internal and external to the host (i.e., the exposome)-on host physiology and response to treatment. Together these represent the current day hallmarks of response, resistance, and toxicity to ICB. Opportunities built on these hallmarks are duly warranted.

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Science, 1995 Nov 10; 270(5238). PMID: 7481803
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A Genetic Mouse Model Recapitulates Immune Checkpoint Inhibitor-Associated Myocarditis and Supports a Mechanism-Based Therapeutic Intervention.
Spencer C Wei, Wouter C Meijers, +24 authors, James P Allison.
Cancer Discov, 2020 Dec 02; 11(3). PMID: 33257470    Free PMC article.
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Arlene H Sharpe, Gordon J Freeman.
Nat Rev Immunol, 2002 Mar 26; 2(2). PMID: 11910893
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Michael Bockmayr, Malte Mohme, +4 authors, Ulrich Schüller.
Oncoimmunology, 2018 Sep 20; 7(9). PMID: 30228931    Free PMC article.
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Roy S Herbst, Jean-Charles Soria, +19 authors, F Stephen Hodi.
Nature, 2014 Nov 28; 515(7528). PMID: 25428504    Free PMC article.
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Cisplatin increases PD-L1 expression and optimizes immune check-point blockade in non-small cell lung cancer.
Ludovic Fournel, Zherui Wu, +9 authors, Patricia Forgez.
Cancer Lett, 2019 Aug 14; 464. PMID: 31404614
The interaction of TIGIT with PVR and PVRL2 inhibits human NK cell cytotoxicity.
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Proc Natl Acad Sci U S A, 2009 Oct 10; 106(42). PMID: 19815499    Free PMC article.
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Radiomics to predict immunotherapy-induced pneumonitis: proof of concept.
Rivka R Colen, Takeo Fujii, +16 authors, Aung Naing.
Invest New Drugs, 2017 Oct 28; 36(4). PMID: 29075985    Free PMC article.
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Xiaohu Zheng, Yeben Qian, +8 authors, Haiming Wei.
Nat Immunol, 2019 Oct 23; 20(12). PMID: 31636463
Fatal Toxic Effects Associated With Immune Checkpoint Inhibitors: A Systematic Review and Meta-analysis.
Daniel Y Wang, Joe-Elie Salem, +24 authors, Douglas B Johnson.
JAMA Oncol, 2018 Sep 23; 4(12). PMID: 30242316    Free PMC article.
Highly Cited. Systematic Review.
Updated efficacy of avelumab in patients with previously treated metastatic Merkel cell carcinoma after ≥1 year of follow-up: JAVELIN Merkel 200, a phase 2 clinical trial.
Howard L Kaufman, Jeffery S Russell, +12 authors, Paul Nghiem.
J Immunother Cancer, 2018 Jan 20; 6(1). PMID: 29347993    Free PMC article.
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Defining Effective Combinations of Immune Checkpoint Blockade and Oncolytic Virotherapy.
Juan J Rojas, Padma Sampath, Weizhou Hou, Steve H Thorne.
Clin Cancer Res, 2015 Jul 19; 21(24). PMID: 26187615    Free PMC article.
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Beta blocker use correlates with better overall survival in metastatic melanoma patients and improves the efficacy of immunotherapies in mice.
Kathleen M Kokolus, Ying Zhang, +5 authors, Todd D Schell.
Oncoimmunology, 2018 Feb 06; 7(3). PMID: 29399407    Free PMC article.
Highly Cited.
Pembrolizumab for the treatment of non-small-cell lung cancer.
Edward B Garon, Naiyer A Rizvi, +25 authors, KEYNOTE-001 Investigators.
N Engl J Med, 2015 Apr 22; 372(21). PMID: 25891174
Highly Cited.
Intestinal microbiome analyses identify melanoma patients at risk for checkpoint-blockade-induced colitis.
Krista Dubin, Margaret K Callahan, +9 authors, Jedd D Wolchok.
Nat Commun, 2016 Feb 03; 7. PMID: 26837003    Free PMC article.
Highly Cited.
The human tumor microbiome is composed of tumor type-specific intracellular bacteria.
Deborah Nejman, Ilana Livyatan, +58 authors, Ravid Straussman.
Science, 2020 May 30; 368(6494). PMID: 32467386    Free PMC article.
Fecal microbiota transplantation for refractory immune checkpoint inhibitor-associated colitis.
Yinghong Wang, Diana H Wiesnoski, +22 authors, Robert R Jenq.
Nat Med, 2018 Nov 14; 24(12). PMID: 30420754    Free PMC article.
Highly Cited.
CTLA-4: a moving target in immunotherapy.
Behzad Rowshanravan, Neil Halliday, David M Sansom.
Blood, 2017 Nov 10; 131(1). PMID: 29118008    Free PMC article.
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PI(3) kinase is associated with a mechanism of immunoresistance in breast and prostate cancer.
C A Crane, A Panner, +7 authors, A T Parsa.
Oncogene, 2008 Oct 14; 28(2). PMID: 18850006    Free PMC article.
VISTA is an inhibitory immune checkpoint that is increased after ipilimumab therapy in patients with prostate cancer.
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Nat Med, 2017 Mar 28; 23(5). PMID: 28346412    Free PMC article.
Highly Cited.
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Fiamma Berner, David Bomze, +27 authors, Lukas Flatz.
JAMA Oncol, 2019 Apr 26; 5(7). PMID: 31021392    Free PMC article.
Highly Cited.
Autoantibody Development under Treatment with Immune-Checkpoint Inhibitors.
Emma C de Moel, Elisa A Rozeman, +7 authors, Diane van der Woude.
Cancer Immunol Res, 2018 Nov 15; 7(1). PMID: 30425107
Combining microenvironment normalization strategies to improve cancer immunotherapy.
Fotios Mpekris, Chrysovalantis Voutouri, +4 authors, Rakesh K Jain.
Proc Natl Acad Sci U S A, 2020 Feb 06; 117(7). PMID: 32015113    Free PMC article.
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J Autoimmun, 2018 Dec 05; 95. PMID: 30509385
Highly Cited. Review.
PD-L2 Expression in Human Tumors: Relevance to Anti-PD-1 Therapy in Cancer.
Jennifer H Yearley, Christopher Gibson, +10 authors, Terrill McClanahan.
Clin Cancer Res, 2017 Jun 18; 23(12). PMID: 28619999
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WNT signaling modulates PD-L1 expression in the stem cell compartment of triple-negative breast cancer.
Lorenzo Castagnoli, Valeria Cancila, +13 authors, Serenella M Pupa.
Oncogene, 2019 Feb 02; 38(21). PMID: 30705400    Free PMC article.
Highly Cited.
Phase I Clinical Trial of Combination Propranolol and Pembrolizumab in Locally Advanced and Metastatic Melanoma: Safety, Tolerability, and Preliminary Evidence of Antitumor Activity.
Shipra Gandhi, Manu R Pandey, +16 authors, Marc S Ernstoff.
Clin Cancer Res, 2020 Nov 01; 27(1). PMID: 33127652    Free PMC article.
Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade.
Nicholas McGranahan, Andrew J S Furness, +33 authors, Charles Swanton.
Science, 2016 Mar 05; 351(6280). PMID: 26940869    Free PMC article.
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A neoantigen fitness model predicts tumour response to checkpoint blockade immunotherapy.
Marta Łuksza, Nadeem Riaz, +9 authors, Benjamin D Greenbaum.
Nature, 2017 Nov 14; 551(7681). PMID: 29132144    Free PMC article.
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Atezolizumab plus Bevacizumab in Unresectable Hepatocellular Carcinoma.
Richard S Finn, Shukui Qin, +19 authors, IMbrave150 Investigators.
N Engl J Med, 2020 May 14; 382(20). PMID: 32402160
Phase I Study of Pembrolizumab (MK-3475; Anti-PD-1 Monoclonal Antibody) in Patients with Advanced Solid Tumors.
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Clin Cancer Res, 2015 May 16; 21(19). PMID: 25977344
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The immune system and cancer evasion strategies: therapeutic concepts.
S Muenst, H Läubli, +3 authors, S Hoeller.
J Intern Med, 2016 Jan 11; 279(6). PMID: 26748421
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Nature, 1999 Feb 04; 397(6716). PMID: 9930702
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Combining Immune Checkpoint Blockade and Tumor-Specific Vaccine for Patients With Incurable Human Papillomavirus 16-Related Cancer: A Phase 2 Clinical Trial.
Erminia Massarelli, William William, +18 authors, Bonnie Glisson.
JAMA Oncol, 2018 Sep 30; 5(1). PMID: 30267032    Free PMC article.
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Chunwan Lu, Priscilla S Redd, +2 authors, Kebin Liu.
Oncoimmunology, 2017 Jan 27; 5(12). PMID: 28123883    Free PMC article.
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Epidemiology. Environment and disease risks.
Stephen M Rappaport, Martyn T Smith.
Science, 2010 Oct 23; 330(6003). PMID: 20966241    Free PMC article.
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The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients.
Vyara Matson, Jessica Fessler, +5 authors, Thomas F Gajewski.
Science, 2018 Jan 06; 359(6371). PMID: 29302014    Free PMC article.
Highly Cited.
Epigenetic Therapy Ties MYC Depletion to Reversing Immune Evasion and Treating Lung Cancer.
Michael J Topper, Michelle Vaz, +15 authors, Stephen B Baylin.
Cell, 2017 Dec 02; 171(6). PMID: 29195073    Free PMC article.
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The nature of nurture: refining the definition of the exposome.
Gary W Miller, Dean P Jones.
Toxicol Sci, 2013 Nov 12; 137(1). PMID: 24213143    Free PMC article.
Highly Cited.
Is autoimmunity the Achilles' heel of cancer immunotherapy?
Carl H June, Jeremy T Warshauer, Jeffrey A Bluestone.
Nat Med, 2017 May 06; 23(5). PMID: 28475571
Highly Cited.
Gut microbiome modulates response to anti-PD-1 immunotherapy in melanoma patients.
V Gopalakrishnan, C N Spencer, +67 authors, J A Wargo.
Science, 2017 Nov 04; 359(6371). PMID: 29097493    Free PMC article.
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The ICOS/ICOSL pathway is required for optimal antitumor responses mediated by anti-CTLA-4 therapy.
Tihui Fu, Qiuming He, Padmanee Sharma.
Cancer Res, 2011 Jun 29; 71(16). PMID: 21708958
Safety of resuming anti-PD-1 in patients with immune-related adverse events (irAEs) during combined anti-CTLA-4 and anti-PD1 in metastatic melanoma.
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Reem Saleh, Eyad Elkord.
Cancer Lett, 2019 May 13; 457. PMID: 31078738
Review.
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FEBS J, 2018 Jun 01; 285(23). PMID: 29851227
Highly Cited. Review.
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Qiang Ma, Junning Liu, +4 authors, Yuantao Li.
Clin Exp Pharmacol Physiol, 2018 Jun 16; 45(10). PMID: 29905955
Differences in Tumor Microenvironment Dictate T Helper Lineage Polarization and Response to Immune Checkpoint Therapy.
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Cell, 2019 Nov 16; 179(5). PMID: 31730856
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Tertiary lymphoid structures improve immunotherapy and survival in melanoma.
Rita Cabrita, Martin Lauss, +22 authors, Göran Jönsson.
Nature, 2020 Jan 17; 577(7791). PMID: 31942071
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Gregory D Poore, Evguenia Kopylova, +14 authors, Rob Knight.
Nature, 2020 Mar 28; 579(7800). PMID: 32214244    Free PMC article.
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N Engl J Med, 2017 Dec 21; 377(25). PMID: 29262275    Free PMC article.
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C Lengauer, K W Kinzler, B Vogelstein.
Nature, 1999 Jan 01; 396(6712). PMID: 9872311
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Managing toxicities associated with immune checkpoint inhibitors: consensus recommendations from the Society for Immunotherapy of Cancer (SITC) Toxicity Management Working Group.
I Puzanov, A Diab, +19 authors, Society for Immunotherapy of Cancer Toxicity Management Working Group.
J Immunother Cancer, 2017 Nov 23; 5(1). PMID: 29162153    Free PMC article.
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N Engl J Med, 2018 Jan 11; 378(2). PMID: 29320654
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Kaustav P Shah, Haocan Song, +4 authors, Douglas B Johnson.
Cancer Immunol Res, 2020 May 01; 8(7). PMID: 32350001    Free PMC article.
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Nature, 2017 Aug 17; 548(7668). PMID: 28813415    Free PMC article.
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Susanne Andreae, Fabienne Piras, Nicolas Burdin, Frédéric Triebel.
J Immunol, 2002 Apr 09; 168(8). PMID: 11937541
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Science, 2019 Nov 09; 366(6468). PMID: 31699883    Free PMC article.
Highly Cited.
Genetic evolution of T-cell resistance in the course of melanoma progression.
Antje Sucker, Fang Zhao, +16 authors, Annette Paschen.
Clin Cancer Res, 2014 Oct 09; 20(24). PMID: 25294904    Free PMC article.
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Michelle N Wykes, Sharon R Lewin.
Nat Rev Immunol, 2017 Oct 11; 18(2). PMID: 28990586    Free PMC article.
Highly Cited. Review.
Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance.
Jun Shimizu, Sayuri Yamazaki, +2 authors, Shimon Sakaguchi.
Nat Immunol, 2002 Jan 29; 3(2). PMID: 11812990
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TIM-3 Regulates CD103+ Dendritic Cell Function and Response to Chemotherapy in Breast Cancer.
Álvaro de Mingo Pulido, Alycia Gardner, +5 authors, Brian Ruffell.
Cancer Cell, 2018 Jan 10; 33(1). PMID: 29316433    Free PMC article.
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Shintaro Iwama, Alessandra De Remigis, +3 authors, Patrizio Caturegli.
Sci Transl Med, 2014 Apr 04; 6(230). PMID: 24695685
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CTLA4 blockade and GM-CSF combination immunotherapy alters the intratumor balance of effector and regulatory T cells.
Sergio A Quezada, Karl S Peggs, Michael A Curran, James P Allison.
J Clin Invest, 2006 Jun 17; 116(7). PMID: 16778987    Free PMC article.
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Paradoxical effects of obesity on T cell function during tumor progression and PD-1 checkpoint blockade.
Ziming Wang, Ethan G Aguilar, +30 authors, Arta M Monjazeb.
Nat Med, 2018 Nov 14; 25(1). PMID: 30420753    Free PMC article.
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Ton N Schumacher, Robert D Schreiber.
Science, 2015 Apr 04; 348(6230). PMID: 25838375
Highly Cited. Review.
Atezolizumab in combination with carboplatin plus nab-paclitaxel chemotherapy compared with chemotherapy alone as first-line treatment for metastatic non-squamous non-small-cell lung cancer (IMpower130): a multicentre, randomised, open-label, phase 3 trial.
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Lancet Oncol, 2019 May 28; 20(7). PMID: 31122901
Highly Cited.
Genomic and immune heterogeneity are associated with differential responses to therapy in melanoma.
Alexandre Reuben, Christine N Spencer, +51 authors, Jennifer A Wargo.
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Highly Cited.
Multi-omics prediction of immune-related adverse events during checkpoint immunotherapy.
Ying Jing, Jin Liu, +10 authors, Leng Han.
Nat Commun, 2020 Oct 04; 11(1). PMID: 33009409    Free PMC article.
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John M Kirkwood, Paul Lorigan, +7 authors, Cecile A Bulanhagui.
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Spatially resolved analyses link genomic and immune diversity and reveal unfavorable neutrophil activation in melanoma.
Akash Mitra, Miles C Andrews, +34 authors, P Andrew Futreal.
Nat Commun, 2020 Apr 17; 11(1). PMID: 32296058    Free PMC article.
Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota.
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Science, 2015 Nov 07; 350(6264). PMID: 26541610    Free PMC article.
Highly Cited.
Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma.
Tyler R Simpson, Fubin Li, +11 authors, Sergio A Quezada.
J Exp Med, 2013 Jul 31; 210(9). PMID: 23897981    Free PMC article.
Highly Cited.
Gut microbiome influences efficacy of PD-1-based immunotherapy against epithelial tumors.
Bertrand Routy, Emmanuelle Le Chatelier, +45 authors, Laurence Zitvogel.
Science, 2017 Nov 04; 359(6371). PMID: 29097494
Highly Cited.
The exposome and health: Where chemistry meets biology.
Roel Vermeulen, Emma L Schymanski, Albert-László Barabási, Gary W Miller.
Science, 2020 Jan 25; 367(6476). PMID: 31974245    Free PMC article.
Review.
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J Immunother Cancer, 2019 Jun 15; 7(1). PMID: 31196219    Free PMC article.
Early B cell changes predict autoimmunity following combination immune checkpoint blockade.
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The blockade of immune checkpoints in cancer immunotherapy.
Drew M Pardoll.
Nat Rev Cancer, 2012 Mar 23; 12(4). PMID: 22437870    Free PMC article.
Highly Cited. Review.
Loss of PTEN Promotes Resistance to T Cell-Mediated Immunotherapy.
Weiyi Peng, Jie Qing Chen, +41 authors, Patrick Hwu.
Cancer Discov, 2015 Dec 10; 6(2). PMID: 26645196    Free PMC article.
Highly Cited.
Elements of cancer immunity and the cancer-immune set point.
Daniel S Chen, Ira Mellman.
Nature, 2017 Jan 20; 541(7637). PMID: 28102259
Highly Cited. Review.
IL17A Blockade Successfully Treated Psoriasiform Dermatologic Toxicity from Immunotherapy.
Daniel Johnson, Anisha B Patel, +7 authors, Adi Diab.
Cancer Immunol Res, 2019 Apr 19; 7(6). PMID: 30996018
From the exposome to mechanistic understanding of chemical-induced adverse effects.
Beate I Escher, Jörg Hackermüller, +33 authors, John F Wambaugh.
Environ Int, 2016 Dec 13; 99. PMID: 27939949    Free PMC article.
Review.
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J Immunol, 2007 Jul 10; 179(2). PMID: 17617589
Highly Cited.
Human leukocyte antigen variation is associated with adverse events of checkpoint inhibitors.
Omar Hasan Ali, Fiamma Berner, +8 authors, Lukas Flatz.
Eur J Cancer, 2018 Dec 12; 107. PMID: 30529903
Cytocidal macrophages in symbiosis with CD4 and CD8 T cells cause acute diabetes following checkpoint blockade of PD-1 in NOD mice.
Hao Hu, Pavel N Zakharov, Orion J Peterson, Emil R Unanue.
Proc Natl Acad Sci U S A, 2020 Nov 25; 117(49). PMID: 33229539    Free PMC article.
Genetic and epigenetic analysis of the beta-2-microglobulin gene in microsatellite instable colorectal cancer.
Zuzana Snahnicanova, Ivana Kasubova, +10 authors, Zora Lasabova.
Clin Exp Med, 2019 Dec 20; 20(1). PMID: 31853669
Immune evasion mediated by PD-L1 on glioblastoma-derived extracellular vesicles.
Franz L Ricklefs, Quazim Alayo, +26 authors, E Antonio Chiocca.
Sci Adv, 2018 Mar 14; 4(3). PMID: 29532035    Free PMC article.
Highly Cited.
Chemotherapy Induces Programmed Cell Death-Ligand 1 Overexpression via the Nuclear Factor-κB to Foster an Immunosuppressive Tumor Microenvironment in Ovarian Cancer.
Jin Peng, Junzo Hamanishi, +9 authors, Masaki Mandai.
Cancer Res, 2015 Nov 18; 75(23). PMID: 26573793
Highly Cited.
Nivolumab versus Docetaxel in Advanced Squamous-Cell Non-Small-Cell Lung Cancer.
Julie Brahmer, Karen L Reckamp, +22 authors, David R Spigel.
N Engl J Med, 2015 Jun 02; 373(2). PMID: 26028407    Free PMC article.
Highly Cited.
Association of body-mass index and outcomes in patients with metastatic melanoma treated with targeted therapy, immunotherapy, or chemotherapy: a retrospective, multicohort analysis.
Jennifer L McQuade, Carrie R Daniel, +43 authors, Michael A Davies.
Lancet Oncol, 2018 Feb 17; 19(3). PMID: 29449192    Free PMC article.
Highly Cited.
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Esmée P Hoefsmit, Elisa A Rozeman, John B A G Haanen, Christian U Blank.
ESMO Open, 2019 Aug 20; 4(4). PMID: 31423333    Free PMC article.
Review.
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Proc Natl Acad Sci U S A, 2016 Oct 30; 113(42). PMID: 27698113    Free PMC article.
Highly Cited.
CANCER IMMUNOLOGY. The "cancer immunogram".
Christian U Blank, John B Haanen, Antoni Ribas, Ton N Schumacher.
Science, 2016 May 07; 352(6286). PMID: 27151852
Highly Cited.
Blockade of B7-H1 and PD-1 by monoclonal antibodies potentiates cancer therapeutic immunity.
Fumiya Hirano, Katsumi Kaneko, +9 authors, Lieping Chen.
Cancer Res, 2005 Feb 12; 65(3). PMID: 15705911
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Molecular Pathways of Colon Inflammation Induced by Cancer Immunotherapy.
Adrienne M Luoma, Shengbao Suo, +13 authors, Kai W Wucherpfennig.
Cell, 2020 Jul 01; 182(3). PMID: 32603654    Free PMC article.
TGF-β-associated extracellular matrix genes link cancer-associated fibroblasts to immune evasion and immunotherapy failure.
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Nat Commun, 2018 Nov 10; 9(1). PMID: 30410077    Free PMC article.
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An Environment-Wide Association Study (EWAS) on type 2 diabetes mellitus.
Chirag J Patel, Jayanta Bhattacharya, Atul J Butte.
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Th1-specific cell surface protein Tim-3 regulates macrophage activation and severity of an autoimmune disease.
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Nature, 2002 Feb 02; 415(6871). PMID: 11823861
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DNA methyltransferase inhibition upregulates MHC-I to potentiate cytotoxic T lymphocyte responses in breast cancer.
Na Luo, Mellissa J Nixon, +10 authors, Justin M Balko.
Nat Commun, 2018 Jan 18; 9(1). PMID: 29339738    Free PMC article.
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Circulating Cytokines Predict Immune-Related Toxicity in Melanoma Patients Receiving Anti-PD-1-Based Immunotherapy.
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Clin Cancer Res, 2018 Nov 10; 25(5). PMID: 30409824
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PD-L2 is a second ligand for PD-1 and inhibits T cell activation.
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Nat Immunol, 2001 Feb 27; 2(3). PMID: 11224527
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Clinical activity and molecular correlates of response to atezolizumab alone or in combination with bevacizumab versus sunitinib in renal cell carcinoma.
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Nat Med, 2018 Jun 06; 24(6). PMID: 29867230    Free PMC article.
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David Bomze, Omar Hasan Ali, Andrew Bate, Lukas Flatz.
JAMA Oncol, 2019 Aug 23; 5(11). PMID: 31436791    Free PMC article.
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Review.
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Cancer Immunol Res, 2020 Apr 11; 8(6). PMID: 32273279
TLR7/8-agonist-loaded nanoparticles promote the polarization of tumour-associated macrophages to enhance cancer immunotherapy.
Christopher B Rodell, Sean P Arlauckas, +6 authors, Ralph Weissleder.
Nat Biomed Eng, 2019 Apr 25; 2(8). PMID: 31015631    Free PMC article.
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The Tumor Microenvironment Represses T Cell Mitochondrial Biogenesis to Drive Intratumoral T Cell Metabolic Insufficiency and Dysfunction.
Nicole E Scharping, Ashley V Menk, +5 authors, Greg M Delgoffe.
Immunity, 2016 Aug 09; 45(2). PMID: 27496732    Free PMC article.
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Tumor-infiltrating NY-ESO-1-specific CD8+ T cells are negatively regulated by LAG-3 and PD-1 in human ovarian cancer.
Junko Matsuzaki, Sacha Gnjatic, +9 authors, Kunle Odunsi.
Proc Natl Acad Sci U S A, 2010 Apr 14; 107(17). PMID: 20385810    Free PMC article.
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CTLA-4 blockade increases IFNgamma-producing CD4+ICOShi cells to shift the ratio of effector to regulatory T cells in cancer patients.
Chrysoula I Liakou, Ashish Kamat, +5 authors, Padmanee Sharma.
Proc Natl Acad Sci U S A, 2008 Sep 27; 105(39). PMID: 18818309    Free PMC article.
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Induction of tumor cell apoptosis in vivo increases tumor antigen cross-presentation, cross-priming rather than cross-tolerizing host tumor-specific CD8 T cells.
Anna K Nowak, Richard A Lake, +5 authors, Bruce W S Robinson.
J Immunol, 2003 May 08; 170(10). PMID: 12734333
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Systemic Immunity Is Required for Effective Cancer Immunotherapy.
Matthew H Spitzer, Yaron Carmi, +10 authors, Edgar G Engleman.
Cell, 2017 Jan 24; 168(3). PMID: 28111070    Free PMC article.
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Identification of bacteria-derived HLA-bound peptides in melanoma.
Shelly Kalaora, Adi Nagler, +50 authors, Yardena Samuels.
Nature, 2021 Mar 19; 592(7852). PMID: 33731925
STAT3 labels a subpopulation of reactive astrocytes required for brain metastasis.
Neibla Priego, Lucía Zhu, +23 authors, Manuel Valiente.
Nat Med, 2018 Jun 13; 24(7). PMID: 29892069
Highly Cited.
Melanoma-intrinsic β-catenin signalling prevents anti-tumour immunity.
Stefani Spranger, Riyue Bao, Thomas F Gajewski.
Nature, 2015 May 15; 523(7559). PMID: 25970248
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Immunotherapy to treat malignancy in patients with pre-existing autoimmunity.
Patrick Boland, Anna C Pavlick, Jeffrey Weber, Sabina Sandigursky.
J Immunother Cancer, 2020 Apr 19; 8(1). PMID: 32303614    Free PMC article.
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Frequencies of circulating MDSC correlate with clinical outcome of melanoma patients treated with ipilimumab.
Christiane Meyer, Laurène Cagnon, +6 authors, Daniel E Speiser.
Cancer Immunol Immunother, 2013 Dec 21; 63(3). PMID: 24357148
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Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade.
Dung T Le, Jennifer N Durham, +43 authors, Luis A Diaz.
Science, 2017 Jun 10; 357(6349). PMID: 28596308    Free PMC article.
Highly Cited.
Vaccine efficacy against primary and metastatic cancer with in vitro-generated CD103+ conventional dendritic cells.
Yifan Zhou, Natalie Slone, +6 authors, Stephanie S Watowich.
J Immunother Cancer, 2020 Apr 11; 8(1). PMID: 32273347    Free PMC article.
Suppression of Exosomal PD-L1 Induces Systemic Anti-tumor Immunity and Memory.
Mauro Poggio, Tianyi Hu, +8 authors, Robert Blelloch.
Cell, 2019 Apr 06; 177(2). PMID: 30951669    Free PMC article.
Highly Cited.
Management Considerations for Immune Checkpoint Inhibitor-Induced Enterocolitis Based on Management of Inflammatory Bowel Disease.
Hamzah Abu-Sbeih, Yinghong Wang.
Inflamm Bowel Dis, 2019 Sep 29; 26(5). PMID: 31560045
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Patient HLA class I genotype influences cancer response to checkpoint blockade immunotherapy.
Diego Chowell, Luc G T Morris, +17 authors, Timothy A Chan.
Science, 2017 Dec 09; 359(6375). PMID: 29217585    Free PMC article.
Highly Cited.
Safety and Efficacy of Re-treating with Immunotherapy after Immune-Related Adverse Events in Patients with NSCLC.
Fernando C Santini, Hira Rizvi, +11 authors, Matthew D Hellmann.
Cancer Immunol Res, 2018 Jul 12; 6(9). PMID: 29991499    Free PMC article.
Highly Cited.
Loss of IFN-γ Pathway Genes in Tumor Cells as a Mechanism of Resistance to Anti-CTLA-4 Therapy.
Jianjun Gao, Lewis Zhichang Shi, +13 authors, Padmanee Sharma.
Cell, 2016 Sep 27; 167(2). PMID: 27667683    Free PMC article.
Highly Cited.
Predicting Response to Immunotherapy by Evaluating Tumors, Lymphoid Cell-Rich Organs, and Immune-Related Adverse Events Using FDG-PET/CT.
Tomomi Nobashi, Lucia Baratto, +5 authors, Erik Mittra.
Clin Nucl Med, 2019 Jan 29; 44(4). PMID: 30688730
Neoantigen-directed immune escape in lung cancer evolution.
Rachel Rosenthal, Elizabeth Larose Cadieux, +26 authors, TRACERx consortium.
Nature, 2019 Mar 22; 567(7749). PMID: 30894752    Free PMC article.
Highly Cited.
Bevacizumab plus ipilimumab in patients with metastatic melanoma.
F Stephen Hodi, Donald Lawrence, +20 authors, David McDermott.
Cancer Immunol Res, 2014 May 20; 2(7). PMID: 24838938    Free PMC article.
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Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy.
Eric A Reits, James W Hodge, +14 authors, Jacques J Neefjes.
J Exp Med, 2006 Apr 26; 203(5). PMID: 16636135    Free PMC article.
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Assessing Immune-Related Adverse Events of Efficacious Combination Immunotherapies in Preclinical Models of Cancer.
Jing Liu, Stephen J Blake, +7 authors, Michele W L Teng.
Cancer Res, 2016 Aug 10; 76(18). PMID: 27503925
Oxidized lipids block antigen cross-presentation by dendritic cells in cancer.
Rupal Ramakrishnan, Vladimir A Tyurin, +10 authors, Dmitry I Gabrilovich.
J Immunol, 2014 Feb 21; 192(6). PMID: 24554775    Free PMC article.
Bispecific antibodies: a mechanistic review of the pipeline.
Aran F Labrijn, Maarten L Janmaat, Janice M Reichert, Paul W H I Parren.
Nat Rev Drug Discov, 2019 Jun 09; 18(8). PMID: 31175342
Highly Cited. Review.
NK Cells Stimulate Recruitment of cDC1 into the Tumor Microenvironment Promoting Cancer Immune Control.
Jan P Böttcher, Eduardo Bonavita, +7 authors, Caetano Reis e Sousa.
Cell, 2018 Feb 13; 172(5). PMID: 29429633    Free PMC article.
Highly Cited.
Immune-checkpoint proteins VISTA and PD-1 nonredundantly regulate murine T-cell responses.
Jun Liu, Ying Yuan, +8 authors, Li Wang.
Proc Natl Acad Sci U S A, 2015 May 13; 112(21). PMID: 25964334    Free PMC article.
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CD4(+)CD25(+) immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor.
Rebecca S McHugh, Matthew J Whitters, +4 authors, Michael C Byrne.
Immunity, 2002 Mar 01; 16(2). PMID: 11869690
Highly Cited.
Enhancement of antitumor immunity by CTLA-4 blockade.
D R Leach, M F Krummel, J P Allison.
Science, 1996 Mar 22; 271(5256). PMID: 8596936
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Cergutuzumab amunaleukin (CEA-IL2v), a CEA-targeted IL-2 variant-based immunocytokine for combination cancer immunotherapy: Overcoming limitations of aldesleukin and conventional IL-2-based immunocytokines.
Christian Klein, Inja Waldhauer, +27 authors, Pablo Umaña.
Oncoimmunology, 2017 Apr 14; 6(3). PMID: 28405498    Free PMC article.
Highly Cited.
Long term impact of CTLA4 blockade immunotherapy on regulatory and effector immune responses in patients with melanoma.
Janet Retseck, Alexis Nasr, +4 authors, Ahmad A Tarhini.
J Transl Med, 2018 Jul 06; 16(1). PMID: 29973204    Free PMC article.
Phase I/II trial of tremelimumab in patients with metastatic melanoma.
Luis H Camacho, Scott Antonia, +8 authors, Antoni Ribas.
J Clin Oncol, 2009 Jan 14; 27(7). PMID: 19139427
Chemokines in the Landscape of Cancer Immunotherapy: How They and Their Receptors Can Be Used to Turn Cold Tumors into Hot Ones?
Nathan Karin.
Cancers (Basel), 2021 Dec 25; 13(24). PMID: 34944943    Free PMC article.
Review.
Cancer-Homing CAR-T Cells and Endogenous Immune Population Dynamics.
Emanuela Guerra, Roberta Di Pietro, +2 authors, Saverio Alberti.
Int J Mol Sci, 2022 Jan 12; 23(1). PMID: 35008832    Free PMC article.
Review.
T cell characteristics associated with toxicity to immune checkpoint blockade in patients with melanoma.
Alexander X Lozano, Aadel A Chaudhuri, +17 authors, Aaron M Newman.
Nat Med, 2022 Jan 15; 28(2). PMID: 35027754    Free PMC article.
RNA demethylase ALKBH5 in cancer: from mechanisms to therapeutic potential.
Jianwei Qu, Haimeng Yan, +5 authors, Zhen Cai.
J Hematol Oncol, 2022 Jan 23; 15(1). PMID: 35063010    Free PMC article.
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Pro-Resolving Factor Administration Limits Cancer Progression by Enhancing Immune Response Against Cancer Cells.
Audrey Wetzel, Francis Bonnefoy, +6 authors, Sylvain Perruche.
Front Immunol, 2022 Feb 05; 12. PMID: 35116038    Free PMC article.
The Role of Long Non-Coding RNAs in the Tumor Immune Microenvironment.
Yingli Guo, Yajuan Xie, Yao Luo.
Front Immunol, 2022 Mar 01; 13. PMID: 35222443    Free PMC article.
Review.
The roles of thermal and mechanical stress in focused ultrasound-mediated immunomodulation and immunotherapy for central nervous system tumors.
Chulyong Kim, Michael Lim, Graeme F Woodworth, Costas D Arvanitis.
J Neurooncol, 2022 Mar 03; 157(2). PMID: 35235137    Free PMC article.
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Improving Cancer Immunotherapy: Exploring and Targeting Metabolism in Hypoxia Microenvironment.
Jinfen Wei, Meiling Hu, Hongli Du.
Front Immunol, 2022 Mar 15; 13. PMID: 35281061    Free PMC article.
Review.
Targeting oncogene and non-oncogene addiction to inflame the tumour microenvironment.
Giulia Petroni, Aitziber Buqué, Lisa M Coussens, Lorenzo Galluzzi.
Nat Rev Drug Discov, 2022 Mar 17; 21(6). PMID: 35292771
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Immune checkpoints related-LncRNAs can identify different subtypes of lung cancer and predict immunotherapy and prognosis.
Hongpan Zhang, Meihan Liu, +6 authors, Bangxian Tan.
J Cancer Res Clin Oncol, 2022 Mar 18; 148(7). PMID: 35296921
Editorial: Cellular and Molecular Mechanisms of Immune Checkpoint Blockers in Anti-leukemia/Lymphoma Immune Therapy.
Mazdak Ganjalikhani-Hakemi, Ling Xu, Andrey A Zamyatnin, Alexandr V Bazhin.
Front Oncol, 2022 Mar 25; 12. PMID: 35321430    Free PMC article.
Combined angiogenesis and PD-1 inhibition for immunomodulatory TNBC: concept exploration and biomarker analysis in the FUTURE-C-Plus trial.
Song-Yang Wu, Ying Xu, +15 authors, Zhi-Ming Shao.
Mol Cancer, 2022 Mar 27; 21(1). PMID: 35337339    Free PMC article.
Applications of Circulating Tumor DNA in Immune Checkpoint Inhibition: Emerging Roles and Future Perspectives.
Chang Lu, Yi-Chen Zhang, +2 authors, Yi-Long Wu.
Front Oncol, 2022 Apr 02; 12. PMID: 35359372    Free PMC article.
Review.
Organ-specific metastatic landscape dissects PD-(L)1 blockade efficacy in advanced non-small cell lung cancer: applicability from clinical trials to real-world practice.
Si-Cong Ma, Xue Bai, +15 authors, Zhong-Yi Dong.
BMC Med, 2022 Apr 13; 20(1). PMID: 35410334    Free PMC article.
Biophysics involved in the process of tumor immune escape.
Maonan Wang, Hui Jiang, Xiaohui Liu, Xuemei Wang.
iScience, 2022 Apr 12; 25(4). PMID: 35402878    Free PMC article.
Review.
Targeting the gut and tumor microbiota in cancer.
Elizabeth M Park, Manoj Chelvanambi, +3 authors, Jennifer A Wargo.
Nat Med, 2022 Apr 21; 28(4). PMID: 35440726
Review.
The mutual relationship between the host immune system and radiotherapy: stimulating the action of immune cells by irradiation.
Tsubasa Watanabe, Genki Edward Sato, +2 authors, Takashi Mizowaki.
Int J Clin Oncol, 2022 May 14;. PMID: 35556190
Review.
Cancer Cell Phenotype Plasticity as a Driver of Immune Escape in Melanoma.
Valentin Benboubker, Félix Boivin, Stéphane Dalle, Julie Caramel.
Front Immunol, 2022 Apr 19; 13. PMID: 35432344    Free PMC article.
Review.