Review
. 2020 Mar; 21(5):.
doi: 10.3390/ijms21051594.

Determinants of Resistance to Checkpoint Inhibitors

Linda Tran 1 Dan Theodorescu 1 
Affiliations
  • PMID: 32111080
  •     195 References
  •     13 citations

Abstract

The development of immune checkpoint inhibitors (ICIs) has drastically altered the landscape of cancer treatment. Since approval of the first ICI for the treatment of advanced melanoma in 2011, several therapeutic agents have been Food and Drug Administration (FDA)-approved for multiple cancers, and hundreds of clinical trials are currently ongoing. These antibodies disrupt T-cell inhibitory pathways established by tumor cells and thus re-activate the host's antitumor immune response. While successful in many cancers, several types remain relatively refractory to treatment or patients develop early recurrence. Hence, there is a great need to further elucidate mechanisms of resistant disease and determine novel, effective, and tolerable combination therapies to enhance efficacy of ICIs.

Keywords: cancer; combination therapy; functional genomics; immune checkpoint inhibitors; immune checkpoints; immunotherapy; next generation sequencing; predictive markers; prognostic markers.

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Ann Surg Oncol, 2003 May 08; 10(4). PMID: 12734098
Human CAR T cells with cell-intrinsic PD-1 checkpoint blockade resist tumor-mediated inhibition.
Leonid Cherkassky, Aurore Morello, +5 authors, Prasad S Adusumilli.
J Clin Invest, 2016 Jul 28; 126(8). PMID: 27454297    Free PMC article.
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Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/regulatory T cell ratio are associated with favorable prognosis in ovarian cancer.
Eiichi Sato, Sara H Olson, +15 authors, Kunle Odunsi.
Proc Natl Acad Sci U S A, 2005 Dec 14; 102(51). PMID: 16344461    Free PMC article.
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Costimulation through the CD137/4-1BB pathway protects human melanoma tumor-infiltrating lymphocytes from activation-induced cell death and enhances antitumor effector function.
Jessica Ann Hernandez-Chacon, Yufeng Li, +5 authors, Laszlo G Radvanyi.
J Immunother, 2011 Mar 11; 34(3). PMID: 21389874    Free PMC article.
Immunological correlates of treatment and response in stage IV malignant melanoma patients treated with Ipilimumab.
Jon Bjoern, Nikolaj Juul Nitschke, +3 authors, Inge Marie Svane.
Oncoimmunology, 2016 May 04; 5(4). PMID: 27141381    Free PMC article.
Fractionated but not single-dose radiotherapy induces an immune-mediated abscopal effect when combined with anti-CTLA-4 antibody.
M Zahidunnabi Dewan, Ashley E Galloway, +4 authors, Sandra Demaria.
Clin Cancer Res, 2009 Aug 27; 15(17). PMID: 19706802    Free PMC article.
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MHC class I antigens and immune surveillance in transformed cells.
Natalia Aptsiauri, Teresa Cabrera, +3 authors, Federico Garrido.
Int Rev Cytol, 2007 Jan 24; 256. PMID: 17241907
Review.
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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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Robert H Vonderheide.
Clin Cancer Res, 2007 Feb 24; 13(4). PMID: 17317815
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A Hutloff, A M Dittrich, +4 authors, R A Kroczek.
Nature, 1999 Feb 04; 397(6716). PMID: 9930702
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CD27 promotes survival of activated T cells and complements CD28 in generation and establishment of the effector T cell pool.
Jenny Hendriks, Yanling Xiao, Jannie Borst.
J Exp Med, 2003 Oct 29; 198(9). PMID: 14581610    Free PMC article.
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Major abdominal surgery increases plasma levels of vascular endothelial growth factor: open more so than minimally invasive methods.
Avraham Belizon, Emre Balik, +8 authors, Richard L Whelan.
Ann Surg, 2006 Oct 25; 244(5). PMID: 17060773    Free PMC article.
Effector memory T cells, early metastasis, and survival in colorectal cancer.
Franck Pagès, Anne Berger, +13 authors, Jérôme Galon.
N Engl J Med, 2005 Dec 24; 353(25). PMID: 16371631
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Anti-PD-1 antibody therapy potently enhances the eradication of established tumors by gene-modified T cells.
Liza B John, Christel Devaud, +7 authors, Phillip K Darcy.
Clin Cancer Res, 2013 Jul 23; 19(20). PMID: 23873688
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Helper T Cells and Cancer-Associated Inflammation: A New Direction for Immunotherapy?
Chen Dong.
J Interferon Cytokine Res, 2017 Jul 21; 37(9). PMID: 28727936
Review.
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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A basal membrane-like structure surrounding tumour nodules may prevent intraepithelial leucocyte infiltration in colorectal cancer.
Anand G Menon, Gert Jan Fleuren, +7 authors, Peter J K Kuppen.
Cancer Immunol Immunother, 2003 Feb 21; 52(2). PMID: 12594576
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.
Highly Cited.
Ionizing radiation inhibition of distant untreated tumors (abscopal effect) is immune mediated.
Sandra Demaria, Bruce Ng, +4 authors, Silvia C Formenti.
Int J Radiat Oncol Biol Phys, 2004 Feb 18; 58(3). PMID: 14967443
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Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy.
Ayelet Sivan, Leticia Corrales, +9 authors, Thomas F Gajewski.
Science, 2015 Nov 07; 350(6264). PMID: 26541606    Free PMC article.
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Combination therapy with anti-CTLA-4 and anti-PD-1 leads to distinct immunologic changes in vivo.
Rituparna Das, Rakesh Verma, +8 authors, Kavita M Dhodapkar.
J Immunol, 2014 Dec 30; 194(3). PMID: 25539810    Free PMC article.
Highly Cited.
Immunologic correlates of the abscopal effect in a patient with melanoma.
Michael A Postow, Margaret K Callahan, +18 authors, Jedd D Wolchok.
N Engl J Med, 2012 Mar 09; 366(10). PMID: 22397654    Free PMC article.
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Ipilimumab in combination with paclitaxel and carboplatin as first-line therapy in extensive-disease-small-cell lung cancer: results from a randomized, double-blind, multicenter phase 2 trial.
M Reck, I Bondarenko, +7 authors, T J Lynch.
Ann Oncol, 2012 Aug 04; 24(1). PMID: 22858559
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Structural basis for cancer immunotherapy by the first-in-class checkpoint inhibitor ipilimumab.
Udupi A Ramagopal, Weifeng Liu, +10 authors, Steven C Almo.
Proc Natl Acad Sci U S A, 2017 May 10; 114(21). PMID: 28484017    Free PMC article.
Genomic Features of Response to Combination Immunotherapy in Patients with Advanced Non-Small-Cell Lung Cancer.
Matthew D Hellmann, Tavi Nathanson, +29 authors, Jedd D Wolchok.
Cancer Cell, 2018 Apr 17; 33(5). PMID: 29657128    Free PMC article.
Highly Cited.
Overall Survival with Combined Nivolumab and Ipilimumab in Advanced Melanoma.
Jedd D Wolchok, Vanna Chiarion-Sileni, +30 authors, James Larkin.
N Engl J Med, 2017 Sep 12; 377(14). PMID: 28889792    Free PMC article.
Highly Cited.
Immunogenic Chemotherapy Sensitizes Tumors to Checkpoint Blockade Therapy.
Christina Pfirschke, Camilla Engblom, +18 authors, Mikael J Pittet.
Immunity, 2016 Feb 14; 44(2). PMID: 26872698    Free PMC article.
Highly Cited.
Acquired IFNγ resistance impairs anti-tumor immunity and gives rise to T-cell-resistant melanoma lesions.
Antje Sucker, Fang Zhao, +20 authors, Annette Paschen.
Nat Commun, 2017 Jun 01; 8. PMID: 28561041    Free PMC article.
Highly Cited.
A biological role for the major histocompatibility antigens.
P C Doherty, R M Zinkernagel.
Lancet, 1975 Jun 28; 1(7922). PMID: 49564
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4-1BB costimulatory signals preferentially induce CD8+ T cell proliferation and lead to the amplification in vivo of cytotoxic T cell responses.
W W Shuford, K Klussman, +11 authors, R S Mittler.
J Exp Med, 1997 Jul 07; 186(1). PMID: 9206996    Free PMC article.
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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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Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy.
Steven A Rosenberg, James C Yang, +12 authors, Mark E Dudley.
Clin Cancer Res, 2011 Apr 19; 17(13). PMID: 21498393    Free PMC article.
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Immune Priming of the Tumor Microenvironment by Radiation.
Wen Jiang, Charles K Chan, +2 authors, Stephen M Hahn.
Trends Cancer, 2017 Jul 26; 2(11). PMID: 28741502
Review.
Mechanisms regulating T-cell infiltration and activity in solid tumors.
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Ann Oncol, 2017 Oct 19; 28(suppl_12). PMID: 29045511
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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.
Differential Expression of Immune-Regulatory Genes Associated with PD-L1 Display in Melanoma: Implications for PD-1 Pathway Blockade.
Janis M Taube, Geoffrey D Young, +10 authors, Suzanne L Topalian.
Clin Cancer Res, 2015 May 07; 21(17). PMID: 25944800    Free PMC article.
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Escape of human solid tumors from T-cell recognition: molecular mechanisms and functional significance.
F M Marincola, E M Jaffee, D J Hicklin, S Ferrone.
Adv Immunol, 1999 Dec 22; 74. PMID: 10605607
Highly Cited. Review.
Molecular mechanism and function of CD40/CD40L engagement in the immune system.
Raul Elgueta, Micah J Benson, +3 authors, Randolph J Noelle.
Immunol Rev, 2009 May 12; 229(1). PMID: 19426221    Free PMC article.
Highly Cited. Review.
Previous radiotherapy and the clinical activity and toxicity of pembrolizumab in the treatment of non-small-cell lung cancer: a secondary analysis of the KEYNOTE-001 phase 1 trial.
Narek Shaverdian, Aaron E Lisberg, +5 authors, Percy Lee.
Lancet Oncol, 2017 May 30; 18(7). PMID: 28551359    Free PMC article.
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Sean P Arlauckas, Christopher S Garris, +9 authors, Mikael J Pittet.
Sci Transl Med, 2017 May 12; 9(389). PMID: 28490665    Free PMC article.
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W Joost Lesterhuis, Joanne Salmons, +6 authors, Richard A Lake.
PLoS One, 2013 Apr 30; 8(4). PMID: 23626745    Free PMC article.
Radiation improves antitumor effect of immune checkpoint inhibitor in murine hepatocellular carcinoma model.
Kyoung-Jin Kim, Ji-Hye Kim, +3 authors, Jinsil Seong.
Oncotarget, 2017 May 04; 8(25). PMID: 28465485    Free PMC article.
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.
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Impact of oncogenic pathways on evasion of antitumour immune responses.
Stefani Spranger, Thomas F Gajewski.
Nat Rev Cancer, 2018 Jan 13; 18(3). PMID: 29326431    Free PMC article.
Highly Cited. Review.
Lymphocyte activation gene-3 (CD223) regulates the size of the expanding T cell population following antigen activation in vivo.
Creg J Workman, Linda S Cauley, +3 authors, Dario A A Vignali.
J Immunol, 2004 Apr 22; 172(9). PMID: 15100286
Chimeric antigen receptor T-cell therapy for ALL.
Shannon L Maude, Elizabeth J Shpall, Stephan A Grupp.
Hematology Am Soc Hematol Educ Program, 2015 Feb 20; 2014(1). PMID: 25696911
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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
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K Yamaguchi, Y Takagi, +2 authors, S Saji.
Ann Surg, 2000 Jun 22; 232(1). PMID: 10862196    Free PMC article.
The dual-function CD150 receptor subfamily: the viral attraction.
Svetlana P Sidorenko, Edward A Clark.
Nat Immunol, 2002 Dec 24; 4(1). PMID: 12496974
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New Hope for Therapeutic Cancer Vaccines in the Era of Immune Checkpoint Modulation.
Michael A Curran, Bonnie S Glisson.
Annu Rev Med, 2018 Nov 01; 70. PMID: 30379596
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.
Acquired resistance to fractionated radiotherapy can be overcome by concurrent PD-L1 blockade.
Simon J Dovedi, Amy L Adlard, +11 authors, Tim M Illidge.
Cancer Res, 2014 Oct 03; 74(19). PMID: 25274032
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.
Prospects for gene-engineered T cell immunotherapy for solid cancers.
Christopher A Klebanoff, Steven A Rosenberg, Nicholas P Restifo.
Nat Med, 2016 Jan 07; 22(1). PMID: 26735408    Free PMC article.
Highly Cited.
Sipuleucel-T (provenge) injection: the first immunotherapy agent (vaccine) for hormone-refractory prostate cancer.
Enock Anassi, Uche Anadu Ndefo.
P T, 2011 May 17; 36(4). PMID: 21572775    Free PMC article.
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.
Hira Rizvi, Francisco Sanchez-Vega, +29 authors, Matthew D Hellmann.
J Clin Oncol, 2018 Jan 18; 36(7). PMID: 29337640    Free PMC article.
Highly Cited.
PD-1 blockade enhances the vaccination-induced immune response in glioma.
Joseph P Antonios, Horacio Soto, +9 authors, Robert M Prins.
JCI Insight, 2016 Jul 28; 1(10). PMID: 27453950    Free PMC article.
Highly Cited.
PD-1/PD-L1 blockade together with vaccine therapy facilitates effector T-cell infiltration into pancreatic tumors.
Kevin C Soares, Agnieszka A Rucki, +15 authors, Lei Zheng.
J Immunother, 2014 Nov 22; 38(1). PMID: 25415283    Free PMC article.
Highly Cited.
A novel transcription factor, T-bet, directs Th1 lineage commitment.
S J Szabo, S T Kim, +3 authors, L H Glimcher.
Cell, 2000 Apr 13; 100(6). PMID: 10761931
Highly Cited.
Cancer immune contexture and immunotherapy.
Etienne Becht, Nicolas A Giraldo, +2 authors, Wolf Herman Fridman.
Curr Opin Immunol, 2015 Dec 29; 39. PMID: 26708937
Review.
Stereotactic Radiation Therapy Augments Antigen-Specific PD-1-Mediated Antitumor Immune Responses via Cross-Presentation of Tumor Antigen.
Andrew B Sharabi, Christopher J Nirschl, +5 authors, Charles G Drake.
Cancer Immunol Res, 2014 Dec 21; 3(4). PMID: 25527358    Free PMC article.
Highly Cited.
Systematic review of case reports on the abscopal effect.
Yazan Abuodeh, Puja Venkat, Sungjune Kim.
Curr Probl Cancer, 2015 Nov 20; 40(1). PMID: 26582738
Highly Cited. Systematic Review.
PD-L2 is a second ligand for PD-1 and inhibits T cell activation.
Y Latchman, C R Wood, +18 authors, G J Freeman.
Nat Immunol, 2001 Feb 27; 2(3). PMID: 11224527
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Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells.
Susanne J Szabo, Brandon M Sullivan, +3 authors, Laurie H Glimcher.
Science, 2002 Jan 12; 295(5553). PMID: 11786644
Highly Cited.
Nuclear FAK controls chemokine transcription, Tregs, and evasion of anti-tumor immunity.
Alan Serrels, Tom Lund, +15 authors, Margaret C Frame.
Cell, 2015 Sep 26; 163(1). PMID: 26406376    Free PMC article.
Highly Cited.
Tumor Mutational Burden and Efficacy of Nivolumab Monotherapy and in Combination with Ipilimumab in Small-Cell Lung Cancer.
Matthew D Hellmann, Margaret K Callahan, +13 authors, Scott J Antonia.
Cancer Cell, 2018 May 08; 33(5). PMID: 29731394    Free PMC article.
Highly Cited.
Control of lymphocyte function through CD27-CD70 interactions.
S M Lens, K Tesselaar, M H van Oers, R A van Lier.
Semin Immunol, 1998 Nov 25; 10(6). PMID: 9826582
Review.
Zooming into the binding groove of HLA molecules: which positions and which substitutions change peptide binding most?
Hanneke W M van Deutekom, Can Keşmir.
Immunogenetics, 2015 Jun 05; 67(8). PMID: 26040913    Free PMC article.
PTPN2 regulates the generation of exhausted CD8+ T cell subpopulations and restrains tumor immunity.
Martin W LaFleur, Thao H Nguyen, +9 authors, Arlene H Sharpe.
Nat Immunol, 2019 Sep 19; 20(10). PMID: 31527834    Free PMC article.
Combination anti-CTLA-4 plus anti-PD-1 checkpoint blockade utilizes cellular mechanisms partially distinct from monotherapies.
Spencer C Wei, Nana-Ama A S Anang, +8 authors, James P Allison.
Proc Natl Acad Sci U S A, 2019 Oct 23; 116(45). PMID: 31636208    Free PMC article.
The role of focal-adhesion kinase in cancer - a new therapeutic opportunity.
Gordon W McLean, Neil O Carragher, +3 authors, Margaret C Frame.
Nat Rev Cancer, 2005 Aug 03; 5(7). PMID: 16069815
Highly Cited. Review.
Radiation enhances regulatory T cell representation.
Evelyn L Kachikwu, Keisuke S Iwamoto, +5 authors, Dörthe Schaue.
Int J Radiat Oncol Biol Phys, 2010 Nov 26; 81(4). PMID: 21093169    Free PMC article.
Role of tumor-infiltrating lymphocytes in patients with solid tumors: Can a drop dig a stone?
Giuseppe Badalamenti, Daniele Fanale, +8 authors, Antonio Russo.
Cell Immunol, 2018 Feb 06; 343. PMID: 29395859
Highly Cited. Review.
Clinical and Molecular Characteristics Associated With Survival Among Patients Treated With Checkpoint Inhibitors for Advanced Non-Small Cell Lung Carcinoma: A Systematic Review and Meta-analysis.
Chee Khoon Lee, Johnathan Man, +7 authors, James Chih-Hsin Yang.
JAMA Oncol, 2017 Dec 23; 4(2). PMID: 29270615    Free PMC article.
Highly Cited. Systematic Review.
Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA-4.
Omar S Qureshi, Yong Zheng, +12 authors, David M Sansom.
Science, 2011 Apr 09; 332(6029). PMID: 21474713    Free PMC article.
Highly Cited.
Pembrolizumab versus paclitaxel for previously treated, advanced gastric or gastro-oesophageal junction cancer (KEYNOTE-061): a randomised, open-label, controlled, phase 3 trial.
Kohei Shitara, Mustafa Özgüroğlu, +18 authors, KEYNOTE-061 investigators.
Lancet, 2018 Jun 09; 392(10142). PMID: 29880231
Highly Cited.
Activation of the PD-1 pathway contributes to immune escape in EGFR-driven lung tumors.
Esra A Akbay, Shohei Koyama, +24 authors, Kwok-Kin Wong.
Cancer Discov, 2013 Oct 01; 3(12). PMID: 24078774    Free PMC article.
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
Highly Cited.
OX40 promotes Bcl-xL and Bcl-2 expression and is essential for long-term survival of CD4 T cells.
P R Rogers, J Song, +2 authors, M Croft.
Immunity, 2001 Sep 25; 15(3). PMID: 11567634
Highly Cited.
Human Th1 dichotomy: origin, phenotype and biologic activities.
Francesco Annunziato, Lorenzo Cosmi, +2 authors, Sergio Romagnani.
Immunology, 2014 Oct 07;. PMID: 25284714    Free PMC article.
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
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.
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.
Identification of a new member of the tumor necrosis factor family and its receptor, a human ortholog of mouse GITR.
A L Gurney, S A Marsters, +13 authors, A Ashkenazi.
Curr Biol, 1999 Mar 13; 9(4). PMID: 10074428
GITR, a member of the TNF receptor superfamily, is costimulatory to mouse T lymphocyte subpopulations.
Simona Ronchetti, Ornella Zollo, +5 authors, Carlo Riccardi.
Eur J Immunol, 2004 Mar 03; 34(3). PMID: 14991590
Mutations Associated with Acquired Resistance to PD-1 Blockade in Melanoma.
Jesse M Zaretsky, Angel Garcia-Diaz, +26 authors, Antoni Ribas.
N Engl J Med, 2016 Jul 20; 375(9). PMID: 27433843    Free PMC article.
Highly Cited.
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.
Ipilimumab plus nivolumab and DNA-repair defects in AR-V7-expressing metastatic prostate cancer.
Karim Boudadi, Daniel L Suzman, +25 authors, Emmanuel S Antonarakis.
Oncotarget, 2018 Jul 10; 9(47). PMID: 29983880    Free PMC article.
Highly Cited.
PDL1 Signals through Conserved Sequence Motifs to Overcome Interferon-Mediated Cytotoxicity.
Maria Gato-Cañas, Miren Zuazo, +14 authors, David Escors.
Cell Rep, 2017 Aug 24; 20(8). PMID: 28834746
Highly Cited.
Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment.
Noriho Iida, Amiran Dzutsev, +18 authors, Romina S Goldszmid.
Science, 2013 Nov 23; 342(6161). PMID: 24264989    Free PMC article.
Highly Cited.
PD-1 inhibits T-cell receptor induced phosphorylation of the ZAP70/CD3zeta signalosome and downstream signaling to PKCtheta.
Kelly-Ann Sheppard, Lori J Fitz, +8 authors, Divya Chaudhary.
FEBS Lett, 2004 Sep 11; 574(1-3). PMID: 15358536
Highly Cited.
PD-L1 on tumor cells is sufficient for immune evasion in immunogenic tumors and inhibits CD8 T cell cytotoxicity.
Vikram R Juneja, Kathleen A McGuire, +5 authors, Arlene H Sharpe.
J Exp Med, 2017 Mar 18; 214(4). PMID: 28302645    Free PMC article.
Highly Cited.
PD-1 Restrains Radiotherapy-Induced Abscopal Effect.
Sean S Park, Haidong Dong, +7 authors, Eugene D Kwon.
Cancer Immunol Res, 2015 Feb 24; 3(6). PMID: 25701325    Free PMC article.
Highly Cited.
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.
Cyclooxygenase-Dependent Tumor Growth through Evasion of Immunity.
Santiago Zelenay, Annemarthe G van der Veen, +9 authors, Caetano Reis e Sousa.
Cell, 2015 Sep 08; 162(6). PMID: 26343581    Free PMC article.
Highly Cited.
Serum and Glucocorticoid-Inducible Kinase 1 (SGK1) in NSCLC Therapy.
Ilaria Guerriero, Gianni Monaco, Vincenzo Coppola, Arturo Orlacchio.
Pharmaceuticals (Basel), 2020 Dec 04; 13(11). PMID: 33266470    Free PMC article.
Review.
Primary and Acquired Resistance to Immunotherapy in Lung Cancer: Unveiling the Mechanisms Underlying of Immune Checkpoint Blockade Therapy.
Laura Boyero, Amparo Sánchez-Gastaldo, +3 authors, Reyes Bernabé-Caro.
Cancers (Basel), 2020 Dec 17; 12(12). PMID: 33322522    Free PMC article.
Review.
The Sarcoma Immune Landscape: Emerging Challenges, Prognostic Significance and Prospective Impact for Immunotherapy Approaches.
Anna Koumarianou, Jose Duran-Moreno.
Cancers (Basel), 2021 Jan 28; 13(3). PMID: 33498238    Free PMC article.
Review.
Biomarkers for precision immunotherapy in the metastatic setting: hope or reality?
Elham Sajjadi, Konstantinos Venetis, Cristian Scatena, Nicola Fusco.
Ecancermedicalscience, 2021 Feb 13; 14. PMID: 33574895    Free PMC article.
Review.
Thinking Small: Small Molecules as Potential Synergistic Adjuncts to Checkpoint Inhibition in Melanoma.
Alexander C Chacon, Alexa D Melucci, Shuyang S Qin, Peter A Prieto.
Int J Mol Sci, 2021 Apr 04; 22(6). PMID: 33810078    Free PMC article.
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Immunotherapy for Hepatocellular Carcinoma: Current Limits and Prospects.
Cheng Zhong, Yirun Li, +5 authors, Hui Lin.
Front Oncol, 2021 Apr 16; 11. PMID: 33854960    Free PMC article.
Review.
Baseline Modified Glasgow Prognostic Score Associated with Survival in Metastatic Urothelial Carcinoma Treated with Immune Checkpoint Inhibitors.
Jacqueline T Brown, Yuan Liu, +14 authors, Mehmet Asim Bilen.
Oncologist, 2021 Feb 27; 26(5). PMID: 33634507    Free PMC article.
Cancer-Associated Fibroblasts and Tumor-Associated Macrophages in Cancer and Cancer Immunotherapy.
Hans Raskov, Adile Orhan, Shruti Gaggar, Ismail Gögenur.
Front Oncol, 2021 Jun 08; 11. PMID: 34094963    Free PMC article.
Review.
The Tumor Microenvironment Factors That Promote Resistance to Immune Checkpoint Blockade Therapy.
Bonnie L Russell, Selisha A Sooklal, +2 authors, Monde Ntwasa.
Front Oncol, 2021 Jul 17; 11. PMID: 34268109    Free PMC article.
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Failure of Immunotherapy-The Molecular and Immunological Origin of Immunotherapy Resistance in Lung Cancer.
Justyna Błach, Kamila Wojas-Krawczyk, Marcin Nicoś, Paweł Krawczyk.
Int J Mol Sci, 2021 Aug 28; 22(16). PMID: 34445735    Free PMC article.
Review.
Mining the Gut Microbiota for Microbial-Based Therapeutic Strategies in Cancer Immunotherapy.
Bolei Li, Tao Gong, +2 authors, Lei Cheng.
Front Oncol, 2021 Oct 01; 11. PMID: 34589427    Free PMC article.
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Acquired resistance for immune checkpoint inhibitors in cancer immunotherapy: challenges and prospects.
Xunrui Chen, Wenhui Zhang, +2 authors, Feng Liu.
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Review.
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