. 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 
  • PMID: 34624224
  •     242 References
  •     18 citations


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
Highly Cited. Review.
Subgroup-specific immune and stromal microenvironment in medulloblastoma.
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.
Noa Stanietsky, Hrvoje Simic, +11 authors, Ofer Mandelboim.
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.
Highly Cited.
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.
Highly Cited. Review.
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.
Jianjun Gao, John F Ward, +16 authors, Padmanee Sharma.
Nat Med, 2017 Mar 28; 23(5). PMID: 28346412    Free PMC article.
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Association of Checkpoint Inhibitor-Induced Toxic Effects With Shared Cancer and Tissue Antigens in Non-Small Cell Lung Cancer.
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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Manuel Rojas, Paula Restrepo-Jiménez, +7 authors, Juan-Manuel Anaya.
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.
Highly Cited.
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.
Amita Patnaik, S Peter Kang, +19 authors, Anthony W Tolcher.
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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The expression profiles and regulation of PD-L1 in tumor-induced myeloid-derived suppressor cells.
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.
M H Pollack, A Betof, +9 authors, A N Shoushtari.
Ann Oncol, 2017 Oct 19; 29(1). PMID: 29045547    Free PMC article.
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Treg-mediated acquired resistance to immune checkpoint inhibitors.
Reem Saleh, Eyad Elkord.
Cancer Lett, 2019 May 13; 457. PMID: 31078738
Transcriptome-based network analysis reveals a spectrum model of human macrophage activation.
Jia Xue, Susanne V Schmidt, +18 authors, Joachim L Schultze.
Immunity, 2014 Feb 18; 40(2). PMID: 24530056    Free PMC article.
Highly Cited.
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Merav E Shaul, Zvi G Fridlender.
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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Microbiome analyses of blood and tissues suggest cancer diagnostic approach.
Gregory D Poore, Evguenia Kopylova, +14 authors, Rob Knight.
Nature, 2020 Mar 28; 579(7800). PMID: 32214244    Free PMC article.
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Mark Yarchoan, Alexander Hopkins, Elizabeth M Jaffee.
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
Highly Cited. Review.
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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J Folkman.
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Highly Cited. Review.
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Michael A Postow, Robert Sidlow, Matthew D Hellmann.
N Engl J Med, 2018 Jan 11; 378(2). PMID: 29320654
Highly Cited. Review.
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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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Shom Goel, Molly J DeCristo, +17 authors, Jean J Zhao.
Nature, 2017 Aug 17; 548(7668). PMID: 28813415    Free PMC article.
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Maturation and activation of dendritic cells induced by lymphocyte activation gene-3 (CD223).
Susanne Andreae, Fabienne Piras, Nicolas Burdin, Frédéric Triebel.
J Immunol, 2002 Apr 09; 168(8). PMID: 11937541
Glutamine blockade induces divergent metabolic programs to overcome tumor immune evasion.
Robert D Leone, Liang Zhao, +14 authors, Jonathan D Powell.
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.
Immune checkpoint blockade in infectious diseases.
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.
Highly Cited.
Pituitary expression of CTLA-4 mediates hypophysitis secondary to administration of CTLA-4 blocking antibody.
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.
Highly Cited.
Neoantigens in cancer immunotherapy.
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.
NPJ Genom Med, 2017 Aug 19; 2. PMID: 28819565    Free PMC article.
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.
Phase II trial of tremelimumab (CP-675,206) in patients with advanced refractory or relapsed melanoma.
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.
Marie Vétizou, Jonathan M Pitt, +35 authors, Laurence Zitvogel.
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.
Metabolic stress in cancer cells induces immune escape through a PI3K-dependent blockade of IFNγ receptor signaling.
Koen A Marijt, Marjolein Sluijter, +4 authors, Thorbald van Hall.
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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J Clin Invest, 2018 Jan 09; 128(2). PMID: 29309048    Free PMC article.
Highly Cited.
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.
Cross-talk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response.
Pratima Sinha, Virginia K Clements, +2 authors, Suzanne Ostrand-Rosenberg.
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.
Susceptible loci associated with autoimmune disease as potential biomarkers for checkpoint inhibitor-induced immune-related adverse events.
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.
Clonal expansion of CD8 T cells in the systemic circulation precedes development of ipilimumab-induced toxicities.
Sumit K Subudhi, Ana Aparicio, +14 authors, Padmanee Sharma.
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
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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.
Ankur Chakravarthy, Lubaba Khan, +2 authors, Daniel D De Carvalho.
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.
PLoS One, 2010 May 28; 5(5). PMID: 20505766    Free PMC article.
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Th1-specific cell surface protein Tim-3 regulates macrophage activation and severity of an autoimmune disease.
Laurent Monney, Catherine A Sabatos, +9 authors, Vijay K Kuchroo.
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.
Su Y Lim, Jenny H Lee, +10 authors, Helen Rizos.
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.
David F McDermott, Mahrukh A Huseni, +29 authors, Thomas Powles.
Nat Med, 2018 Jun 06; 24(6). PMID: 29867230    Free PMC article.
Highly Cited.
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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.
Myeloid Cell-associated Resistance to PD-1/PD-L1 Blockade in Urothelial Cancer Revealed Through Bulk and Single-cell RNA Sequencing.
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Cutaneous Toxicities of Immune Checkpoint Inhibitors: The Role of the Dermatologist.
Ian William Tattersall, Jonathan Scott Leventhal.
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Pembrolizumab for Early Triple-Negative Breast Cancer.
Peter Schmid, Javier Cortes, +19 authors, KEYNOTE-522 Investigators.
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TLR7/8-agonist-loaded nanoparticles promote the polarization of tumour-associated macrophages to enhance cancer immunotherapy.
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The Tumor Microenvironment Represses T Cell Mitochondrial Biogenesis to Drive Intratumoral T Cell Metabolic Insufficiency and Dysfunction.
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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.
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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.
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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
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Nat Med, 2018 Jun 13; 24(7). PMID: 29892069
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Melanoma-intrinsic β-catenin signalling prevents anti-tumour immunity.
Stefani Spranger, Riyue Bao, Thomas F Gajewski.
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J Immunother Cancer, 2020 Apr 19; 8(1). PMID: 32303614    Free PMC article.
Frequencies of circulating MDSC correlate with clinical outcome of melanoma patients treated with ipilimumab.
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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.
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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.
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Cell, 2019 Apr 06; 177(2). PMID: 30951669    Free PMC article.
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Management Considerations for Immune Checkpoint Inhibitor-Induced Enterocolitis Based on Management of Inflammatory Bowel Disease.
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Patient HLA class I genotype influences cancer response to checkpoint blockade immunotherapy.
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Safety and Efficacy of Re-treating with Immunotherapy after Immune-Related Adverse Events in Patients with NSCLC.
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Predicting Response to Immunotherapy by Evaluating Tumors, Lymphoid Cell-Rich Organs, and Immune-Related Adverse Events Using FDG-PET/CT.
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Rachel Rosenthal, Elizabeth Larose Cadieux, +26 authors, TRACERx consortium.
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Bevacizumab plus ipilimumab in patients with metastatic melanoma.
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Assessing Immune-Related Adverse Events of Efficacious Combination Immunotherapies in Preclinical Models of Cancer.
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Oxidized lipids block antigen cross-presentation by dendritic cells in cancer.
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NK Cells Stimulate Recruitment of cDC1 into the Tumor Microenvironment Promoting Cancer Immune Control.
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Cancer-Homing CAR-T Cells and Endogenous Immune Population Dynamics.
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Pro-Resolving Factor Administration Limits Cancer Progression by Enhancing Immune Response Against Cancer Cells.
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The roles of thermal and mechanical stress in focused ultrasound-mediated immunomodulation and immunotherapy for central nervous system tumors.
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Jinfen Wei, Meiling Hu, Hongli Du.
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Immune checkpoints related-LncRNAs can identify different subtypes of lung cancer and predict immunotherapy and prognosis.
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Editorial: Cellular and Molecular Mechanisms of Immune Checkpoint Blockers in Anti-leukemia/Lymphoma Immune Therapy.
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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
The mutual relationship between the host immune system and radiotherapy: stimulating the action of immune cells by irradiation.
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Cancer Cell Phenotype Plasticity as a Driver of Immune Escape in Melanoma.
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