Journal Article
. 2013 Jul; 210(9):1685-93.
doi: 10.1084/jem.20130573.

Activating Fc γ receptors contribute to the antitumor activities of immunoregulatory receptor-targeting antibodies

Yannick Bulliard 1 Rose Jolicoeur  Maurice Windman  Sarah M Rue  Seth Ettenberg  Deborah A Knee  Nicholas S Wilson  Glenn Dranoff  Jennifer L Brogdon  
Affiliations
  • PMID: 23897982
  •     33 References
  •     205 citations

Abstract

Fc γ receptor (FcγR) coengagement can facilitate antibody-mediated receptor activation in target cells. In particular, agonistic antibodies that target tumor necrosis factor receptor (TNFR) family members have shown dependence on expression of the inhibitory FcγR, FcγRIIB. It remains unclear if engagement of FcγRIIB also extends to the activities of antibodies targeting immunoregulatory TNFRs expressed by T cells. We have explored the requirement for activating and inhibitory FcγRs for the antitumor effects of antibodies targeting the TNFR glucocorticoid-induced TNFR-related protein (GITR; TNFRSF18; CD357) expressed on activated and regulatory T cells (T reg cells). We found that although FcγRIIB was dispensable for the in vivo efficacy of anti-GITR antibodies, in contrast, activating FcγRs were essential. Surprisingly, the dependence on activating FcγRs extended to an antibody targeting the non-TNFR receptor CTLA-4 (CD152) that acts as a negative regulator of T cell immunity. We define a common mechanism that correlated with tumor efficacy, whereby antibodies that coengaged activating FcγRs expressed by tumor-associated leukocytes facilitated the selective elimination of intratumoral T cell populations, particularly T reg cells. These findings may have broad implications for antibody engineering efforts aimed at enhancing the therapeutic activity of immunomodulatory antibodies.

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Matthew H Spitzer, Yaron Carmi, +10 authors, Edgar G Engleman.
Cell, 2017 Jan 24; 168(3). PMID: 28111070    Free PMC article.
Highly Cited.
Co-inhibitory blockade while preserving tolerance: checkpoint inhibitors for glioblastoma.
Liliana E Lucca, David A Hafler.
Immunol Rev, 2017 Mar 05; 276(1). PMID: 28258696    Free PMC article.
Review.
The Unique Molecular and Cellular Microenvironment of Ovarian Cancer.
Thomas Worzfeld, Elke Pogge von Strandmann, +4 authors, Rolf Müller.
Front Oncol, 2017 Mar 10; 7. PMID: 28275576    Free PMC article.
Highly Cited. Review.
Combination GITR targeting/PD-1 blockade with vaccination drives robust antigen-specific antitumor immunity.
Daniel O Villarreal, Diana Chin, +2 authors, Linda A Snyder.
Oncotarget, 2017 Apr 08; 8(24). PMID: 28388572    Free PMC article.
MEDI1873, a potent, stabilized hexameric agonist of human GITR with regulatory T-cell targeting potential.
Natalie J Tigue, Lisa Bamber, +24 authors, Ross Stewart.
Oncoimmunology, 2017 Apr 14; 6(3). PMID: 28405505    Free PMC article.
Signaling by Antibodies: Recent Progress.
Stylianos Bournazos, Taia T Wang, +2 authors, Jeffrey V Ravetch.
Annu Rev Immunol, 2017 Apr 28; 35. PMID: 28446061    Free PMC article.
Highly Cited. Review.
Potent antitumour activity of interleukin-2-Fc fusion proteins requires Fc-mediated depletion of regulatory T-cells.
Rodrigo Vazquez-Lombardi, Claudia Loetsch, +8 authors, Daniel Christ.
Nat Commun, 2017 May 13; 8. PMID: 28497796    Free PMC article.
Delivering safer immunotherapies for cancer.
Lauren Milling, Yuan Zhang, Darrell J Irvine.
Adv Drug Deliv Rev, 2017 May 27; 114. PMID: 28545888    Free PMC article.
Highly Cited. Review.
PD-1 Blockade Promotes Emerging Checkpoint Inhibitors in Enhancing T Cell Responses to Allogeneic Dendritic Cells.
Carmen Stecher, Claire Battin, +5 authors, Peter Steinberger.
Front Immunol, 2017 Jun 08; 8. PMID: 28588576    Free PMC article.
Anti-GITR Antibody Treatment Increases TCR Repertoire Diversity of Regulatory but not Effector T Cells Engaged in the Immune Response Against B16 Melanoma.
Bozena Scirka, Edyta Szurek, +4 authors, Arkadiusz Miazek.
Arch Immunol Ther Exp (Warsz), 2017 Jun 24; 65(6). PMID: 28638937    Free PMC article.
Concurrent OX40 and CD30 Ligand Blockade Abrogates the CD4-Driven Autoimmunity Associated with CTLA4 and PD1 Blockade while Preserving Excellent Anti-CD8 Tumor Immunity.
Maher G Nawaf, Maria H Ulvmar, +7 authors, Peter J L Lane.
J Immunol, 2017 Jun 25; 199(3). PMID: 28646041    Free PMC article.
GITR ligand fusion protein agonist enhances the tumor antigen-specific CD8 T-cell response and leads to long-lasting memory.
Nick M Durham, Nick Holoweckyj, +3 authors, Scott H Robbins.
J Immunother Cancer, 2017 Jun 27; 5. PMID: 28649380    Free PMC article.
Functional optimization of agonistic antibodies to OX40 receptor with novel Fc mutations to promote antibody multimerization.
Di Zhang, Anthony A Armstrong, +4 authors, Mark L Chiu.
MAbs, 2017 Aug 02; 9(7). PMID: 28758875    Free PMC article.
Mechanisms of action and rationale for the use of checkpoint inhibitors in cancer.
Clemence Granier, Eleonore De Guillebon, +7 authors, Eric Tartour.
ESMO Open, 2017 Aug 02; 2(2). PMID: 28761757    Free PMC article.
Highly Cited. Review.
Blockade of surface-bound TGF-β on regulatory T cells abrogates suppression of effector T cell function in the tumor microenvironment.
Sadna Budhu, David A Schaer, +8 authors, Jedd D Wolchok.
Sci Signal, 2017 Aug 31; 10(494). PMID: 28851824    Free PMC article.
Gene expression of NOX family members and their clinical significance in hepatocellular carcinoma.
Hyuk Soo Eun, Sang Yeon Cho, +5 authors, Byung Seok Lee.
Sci Rep, 2017 Sep 13; 7(1). PMID: 28894215    Free PMC article.
Roles for Innate Immunity in Combination Immunotherapies.
Kelly D Moynihan, Darrell J Irvine.
Cancer Res, 2017 Sep 21; 77(19). PMID: 28928130    Free PMC article.
Review.
Immuno-thermal ablations - boosting the anticancer immune response.
Ryan Slovak, Johannes M Ludwig, +2 authors, Hyun S Kim.
J Immunother Cancer, 2017 Oct 19; 5(1). PMID: 29037259    Free PMC article.
Review.
Therapeutic Antibodies: What Have We Learnt from Targeting CD20 and Where Are We Going?
Michael J E Marshall, Richard J Stopforth, Mark S Cragg.
Front Immunol, 2017 Oct 20; 8. PMID: 29046676    Free PMC article.
Review.
Enhanced immunotherapy by combining a vaccine with a novel murine GITR ligand fusion protein.
Y Maurice Morillon, Scott A Hammond, +2 authors, John W Greiner.
Oncotarget, 2017 Nov 02; 8(43). PMID: 29088720    Free PMC article.
CD27-Mediated Regulatory T Cell Depletion and Effector T Cell Costimulation Both Contribute to Antitumor Efficacy.
Anna Wasiuk, James Testa, +9 authors, Li-Zhen He.
J Immunol, 2017 Nov 08; 199(12). PMID: 29109120    Free PMC article.
Immune checkpoint inhibitors: new strategies to checkmate cancer.
R A M Wilson, T R J Evans, A R Fraser, R J B Nibbs.
Clin Exp Immunol, 2017 Nov 16; 191(2). PMID: 29139554    Free PMC article.
Review.
Engineered aglycosylated full-length IgG Fc variants exhibiting improved FcγRIIIa binding and tumor cell clearance.
Migyeong Jo, Hyeong Sun Kwon, +2 authors, Sang Taek Jung.
MAbs, 2017 Nov 28; 10(2). PMID: 29173039    Free PMC article.
Trial Watch: Immunostimulatory monoclonal antibodies for oncological indications.
Mariona Cabo, Rienk Offringa, +3 authors, Lorenzo Galluzzi.
Oncoimmunology, 2017 Dec 07; 6(12). PMID: 29209572    Free PMC article.
Review.
Checkpoint Blockade Toxicity and Immune Homeostasis in the Gastrointestinal Tract.
Michael Dougan.
Front Immunol, 2017 Dec 13; 8. PMID: 29230210    Free PMC article.
Highly Cited. Review.
PD-1/PD-L1 Blockade: Have We Found the Key to Unleash the Antitumor Immune Response?
Zijun Y Xu-Monette, Mingzhi Zhang, Jianyong Li, Ken H Young.
Front Immunol, 2017 Dec 20; 8. PMID: 29255458    Free PMC article.
Highly Cited. Review.
The activity of myeloid cell-specific VHH immunotoxins is target-, epitope-, subset- and organ dependent.
Christopher Bachran, Matthias Schröder, +5 authors, Lee Kim Swee.
Sci Rep, 2017 Dec 22; 7(1). PMID: 29263417    Free PMC article.
Potential effect of tumor-specific Treg-targeted antibodies in the treatment of human cancers: A bioinformatics analysis.
Luigi Cari, Giuseppe Nocentini, Graziella Migliorati, Carlo Riccardi.
Oncoimmunology, 2018 Jan 09; 7(2). PMID: 29308313    Free PMC article.
Unlocking the Complexities of Tumor-Associated Regulatory T Cells.
Jaime L Chao, Peter A Savage.
J Immunol, 2018 Jan 10; 200(2). PMID: 29311383    Free PMC article.
Review.
FcγRII-binding Centyrins mediate agonism and antibody-dependent cellular phagocytosis when fused to an anti-OX40 antibody.
Di Zhang, Brian Whitaker, Mehabaw G Derebe, Mark L Chiu.
MAbs, 2018 Jan 24; 10(3). PMID: 29359992    Free PMC article.
Uncoupling therapeutic from immunotherapy-related adverse effects for safer and effective anti-CTLA-4 antibodies in CTLA4 humanized mice.
Xuexiang Du, Mingyue Liu, +8 authors, Pan Zheng.
Cell Res, 2018 Feb 22; 28(4). PMID: 29463898    Free PMC article.
Highly Cited.
A reappraisal of CTLA-4 checkpoint blockade in cancer immunotherapy.
Xuexiang Du, Fei Tang, +14 authors, Yang Liu.
Cell Res, 2018 Feb 24; 28(4). PMID: 29472691    Free PMC article.
Highly Cited.
The unique antibody suppresses HBV viremia and reduces hepatocarcinogenesis in HBV-transgenic mice.
Xiao-Zhen Kang, Xue-Ran Guo, +5 authors, Ning-Shao Xia.
Hum Vaccin Immunother, 2018 Mar 14; 14(7). PMID: 29533134    Free PMC article.
Fc Effector Function Contributes to the Activity of Human Anti-CTLA-4 Antibodies.
Frederick Arce Vargas, Andrew J S Furness, +32 authors, Sergio A Quezada.
Cancer Cell, 2018 Mar 27; 33(4). PMID: 29576375    Free PMC article.
Highly Cited.
Anti-CTLA-4 therapy requires an Fc domain for efficacy.
Jessica R Ingram, Olga S Blomberg, +15 authors, Michael Dougan.
Proc Natl Acad Sci U S A, 2018 Mar 28; 115(15). PMID: 29581255    Free PMC article.
Highly Cited.
Anti-CTLA-4 immunotherapy: uncoupling toxicity and efficacy.
Jonathan Pol, Guido Kroemer.
Cell Res, 2018 Mar 30; 28(5). PMID: 29593340    Free PMC article.
Toxicological and pharmacological assessment of AGEN1884, a novel human IgG1 anti-CTLA-4 antibody.
Randi B Gombos, Ana Gonzalez, +24 authors, Nicholas S Wilson.
PLoS One, 2018 Apr 05; 13(4). PMID: 29617360    Free PMC article.
Combination Immunotherapy: Taking Cancer Vaccines to the Next Level.
Jeremy M Grenier, Stephen T Yeung, Kamal M Khanna.
Front Immunol, 2018 Apr 07; 9. PMID: 29623082    Free PMC article.
Review.
Anti-CTLA-4 antibodies in cancer immunotherapy: selective depletion of intratumoral regulatory T cells or checkpoint blockade?
Fei Tang, Xuexiang Du, +2 authors, Yang Liu.
Cell Biosci, 2018 May 02; 8. PMID: 29713453    Free PMC article.
Complimentary mechanisms of dual checkpoint blockade expand unique T-cell repertoires and activate adaptive anti-tumor immunity in triple-negative breast tumors.
Erika J Crosby, Junping Wei, +10 authors, Zachary C Hartman.
Oncoimmunology, 2018 May 04; 7(5). PMID: 29721371    Free PMC article.
Selective FcγR Co-engagement on APCs Modulates the Activity of Therapeutic Antibodies Targeting T Cell Antigens.
Jeremy D Waight, Dhan Chand, +14 authors, Nicholas S Wilson.
Cancer Cell, 2018 Jun 13; 33(6). PMID: 29894690    Free PMC article.
The promise and challenges of immune agonist antibody development in cancer.
Patrick A Mayes, Kenneth W Hance, Axel Hoos.
Nat Rev Drug Discov, 2018 Jun 16; 17(7). PMID: 29904196
Highly Cited. Review.
Novel tumour antigens and the development of optimal vaccine design.
Victoria A Brentville, Suha Atabani, Katherine Cook, Lindy G Durrant.
Ther Adv Vaccines Immunother, 2018 Jul 13; 6(2). PMID: 29998219    Free PMC article.
Review.
Glyco-Engineered Anti-Human Programmed Death-Ligand 1 Antibody Mediates Stronger CD8 T Cell Activation Than Its Normal Glycosylated and Non-Glycosylated Counterparts.
Christoph Goletz, Timo Lischke, +4 authors, Steffen Goletz.
Front Immunol, 2018 Aug 01; 9. PMID: 30061887    Free PMC article.
New tricks for old targets: Anti-CTLA-4 antibodies re-envisioned for cancer immunotherapy.
Jeremy D Waight, Dhan Chand, David A Savitsky.
Oncotarget, 2018 Aug 23; 9(58). PMID: 30131845    Free PMC article.
Hapten-mediated recruitment of polyclonal antibodies to tumors engenders antitumor immunity.
Brett Schrand, Emily Clark, +5 authors, Eli Gilboa.
Nat Commun, 2018 Aug 24; 9(1). PMID: 30135425    Free PMC article.
Strategies for Predicting Response to Checkpoint Inhibitors.
Roberta Zappasodi, Jedd D Wolchok, Taha Merghoub.
Curr Hematol Malig Rep, 2018 Aug 31; 13(5). PMID: 30159703    Free PMC article.
Review.
A comprehensive review on the role of co-signaling receptors and Treg homeostasis in autoimmunity and tumor immunity.
Prabhakaran Kumar, Palash Bhattacharya, Bellur S Prabhakar.
J Autoimmun, 2018 Sep 04; 95. PMID: 30174217    Free PMC article.
Review.
PD-1 has a unique capacity to inhibit allergen-specific human CD4+ T cell responses.
Sandra Rosskopf, Beatrice Jahn-Schmid, +2 authors, Peter Steinberger.
Sci Rep, 2018 Sep 12; 8(1). PMID: 30201974    Free PMC article.
Not All Immune Checkpoints Are Created Equal.
Annika De Sousa Linhares, Judith Leitner, Katharina Grabmeier-Pfistershammer, Peter Steinberger.
Front Immunol, 2018 Sep 21; 9. PMID: 30233564    Free PMC article.
Highly Cited. Review.
Dose escalation results from a first-in-human, phase 1 study of glucocorticoid-induced TNF receptor-related protein agonist AMG 228 in patients with advanced solid tumors.
Ben Tran, Richard D Carvajal, +8 authors, Patrick Schöffski.
J Immunother Cancer, 2018 Sep 27; 6(1). PMID: 30253804    Free PMC article.
Characterization and Comparison of GITR Expression in Solid Tumors.
Luis Vence, Samantha L Bucktrout, +17 authors, Padmanee Sharma.
Clin Cancer Res, 2019 Jul 31; 25(21). PMID: 31358539    Free PMC article.
NK Cell-Fc Receptors Advance Tumor Immunotherapy.
Emilio Sanseviero.
J Clin Med, 2019 Oct 17; 8(10). PMID: 31614774    Free PMC article.
Review.
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.
T Regulatory Cells and Priming the Suppressive Tumor Microenvironment.
Christina M Paluskievicz, Xuefang Cao, +3 authors, Jonathan S Bromberg.
Front Immunol, 2019 Nov 05; 10. PMID: 31681327    Free PMC article.
Review.
Hijacking antibody-induced CTLA-4 lysosomal degradation for safer and more effective cancer immunotherapy.
Yan Zhang, Xuexiang Du, +9 authors, Yang Liu.
Cell Res, 2019 Jul 04; 29(8). PMID: 31267017    Free PMC article.
Anti-CTLA-4 Activates Intratumoral NK Cells and Combined with IL15/IL15Rα Complexes Enhances Tumor Control.
Emilio Sanseviero, Erin M O'Brien, +16 authors, Erica L Stone.
Cancer Immunol Res, 2019 Jun 27; 7(8). PMID: 31239316    Free PMC article.
Amplifying Outcomes: Checkpoint Inhibitor Combinations in First-Line Non-Small Cell Lung Cancer.
Barbara Melosky, Rosalyn Juergens, +5 authors, Quincy Chu.
Oncologist, 2019 May 30; 25(1). PMID: 31138727    Free PMC article.
Construction of a risk score prognosis model based on hepatocellular carcinoma microenvironment.
Fa-Peng Zhang, Yi-Pei Huang, +4 authors, Chao Liu.
World J Gastroenterol, 2020 Jan 24; 26(2). PMID: 31969776    Free PMC article.
Antibody Structure and Function: The Basis for Engineering Therapeutics.
Mark L Chiu, Dennis R Goulet, Alexey Teplyakov, Gary L Gilliland.
Antibodies (Basel), 2019 Dec 11; 8(4). PMID: 31816964    Free PMC article.
Review.
TLR1/2 ligand enhances antitumor efficacy of CTLA-4 blockade by increasing intratumoral Treg depletion.
Naveen Sharma, Jean Vacher, James P Allison.
Proc Natl Acad Sci U S A, 2019 May 12; 116(21). PMID: 31076558    Free PMC article.
Acquired resistance to cancer immunotherapy.
Arianna Draghi, Christopher Aled Chamberlain, Andrew Furness, Marco Donia.
Semin Immunopathol, 2018 Jul 04; 41(1). PMID: 29968044
Review.
Therapeutic cancer vaccine: building the future from lessons of the past.
T Tran, C Blanc, +3 authors, Eric Tartour.
Semin Immunopathol, 2018 Jul 07; 41(1). PMID: 29978248
Review.
Sensitizing the Tumor Microenvironment to Immune Checkpoint Therapy.
Rachael M Zemek, Wee Loong Chin, +3 authors, W Joost Lesterhuis.
Front Immunol, 2020 Mar 07; 11. PMID: 32133005    Free PMC article.
Review.
Differential control of human Treg and effector T cells in tumor immunity by Fc-engineered anti-CTLA-4 antibody.
Danbee Ha, Atsushi Tanaka, +10 authors, Shimon Sakaguchi.
Proc Natl Acad Sci U S A, 2018 Dec 28; 116(2). PMID: 30587582    Free PMC article.
Antigen delivery targeted to tumor-associated macrophages overcomes tumor immune resistance.
Daisuke Muraoka, Naohiro Seo, +17 authors, Hiroshi Shiku.
J Clin Invest, 2019 Jan 11; 129(3). PMID: 30628894    Free PMC article.
GITR ligation enhances functionality of tumor-infiltrating T cells in hepatocellular carcinoma.
Adriaan A van Beek, Guoying Zhou, +14 authors, Jaap Kwekkeboom.
Int J Cancer, 2019 Feb 06; 145(4). PMID: 30719701    Free PMC article.
Functional diversification of hybridoma-produced antibodies by CRISPR/HDR genomic engineering.
Johan M S van der Schoot, Felix L Fennemann, +18 authors, Ferenc A Scheeren.
Sci Adv, 2019 Sep 07; 5(8). PMID: 31489367    Free PMC article.
Regulatory T Cells in Tumor Microenvironment and Approach for Anticancer Immunotherapy.
Jung-Ho Kim, Beom Seok Kim, Sang-Kyou Lee.
Immune Netw, 2020 Mar 12; 20(1). PMID: 32158592    Free PMC article.
Review.
Mechanisms of human FoxP3+ Treg cell development and function in health and disease.
M Attias, T Al-Aubodah, C A Piccirillo.
Clin Exp Immunol, 2019 Mar 14; 197(1). PMID: 30864147    Free PMC article.
Review.
Mechanism- and Immune Landscape-Based Ranking of Therapeutic Responsiveness of 22 Major Human Cancers to Next Generation Anti-CTLA-4 Antibodies.
Peng Zhang, Xinxin Xiong, +8 authors, Pan Zheng.
Cancers (Basel), 2020 Jan 30; 12(2). PMID: 31991588    Free PMC article.
Targeting the Antibody Checkpoints to Enhance Cancer Immunotherapy-Focus on FcγRIIB.
Ingrid Teige, Linda Mårtensson, Björn L Frendéus.
Front Immunol, 2019 Apr 02; 10. PMID: 30930905    Free PMC article.
Review.
FcγR-Binding Is an Important Functional Attribute for Immune Checkpoint Antibodies in Cancer Immunotherapy.
Xin Chen, Xiaomin Song, Kang Li, Tong Zhang.
Front Immunol, 2019 Mar 14; 10. PMID: 30863404    Free PMC article.
Highly Cited. Review.
Immunometabolic Checkpoints of Treg Dynamics: Adaptation to Microenvironmental Opportunities and Challenges.
Ilenia Pacella, Silvia Piconese.
Front Immunol, 2019 Sep 12; 10. PMID: 31507585    Free PMC article.
Review.
Regulatory T (Treg) cells in cancer: Can Treg cells be a new therapeutic target?
Yoshihiro Ohue, Hiroyoshi Nishikawa.
Cancer Sci, 2019 May 19; 110(7). PMID: 31102428    Free PMC article.
Highly Cited. Review.
T Cell Dysfunction in Cancer Immunity and Immunotherapy.
Anliang Xia, Yan Zhang, +2 authors, Xiao-Jie Lu.
Front Immunol, 2019 Aug 06; 10. PMID: 31379886    Free PMC article.
Highly Cited. Review.
HERA-GITRL activates T cells and promotes anti-tumor efficacy independent of FcγR-binding functionality.
David M Richards, Viola Marschall, +10 authors, Meinolf Thiemann.
J Immunother Cancer, 2019 Jul 22; 7(1). PMID: 31324216    Free PMC article.
Current issues and perspectives in PD-1 blockade cancer immunotherapy.
Kenji Chamoto, Ryusuke Hatae, Tasuku Honjo.
Int J Clin Oncol, 2020 Jan 05; 25(5). PMID: 31900651    Free PMC article.
Review.
Preserving the CTLA-4 Checkpoint for Safer and More Effective Cancer Immunotherapy.
Yang Liu, Pan Zheng.
Trends Pharmacol Sci, 2019 Dec 15; 41(1). PMID: 31836191    Free PMC article.
Review.
Bcl6 Preserves the Suppressive Function of Regulatory T Cells During Tumorigenesis.
Yiding Li, Zhiming Wang, +16 authors, Lifan Xu.
Front Immunol, 2020 Jun 02; 11. PMID: 32477338    Free PMC article.
Tumor necrosis factor receptor family costimulation increases regulatory T-cell activation and function via NF-κB.
Martina Lubrano di Ricco, Emilie Ronin, +8 authors, Benoît L Salomon.
Eur J Immunol, 2020 Feb 06; 50(7). PMID: 32012260    Free PMC article.
Endocrinopathies Associated with Immune Checkpoint Inhibitor Cancer Treatment: A Review.
Naoko Okura, Mai Asano, +6 authors, Koichi Takayama.
J Clin Med, 2020 Jul 03; 9(7). PMID: 32610470    Free PMC article.
Review.
New emerging targets in cancer immunotherapy: the role of GITR.
Giulia Buzzatti, Chiara Dellepiane, Lucia Del Mastro.
ESMO Open, 2020 Aug 21; 4(Suppl 3). PMID: 32817129    Free PMC article.
Review.
Human regulatory T cells (Treg) and their response to cancer.
Theresa L Whiteside.
Expert Rev Precis Med Drug Dev, 2019 Jan 01; 4(4). PMID: 32953989    Free PMC article.
Tregs, Helios and tumor immunity: the sun has not yet risen.
Angela M Thornton, Ethan M Shevach.
Transl Cancer Res, 2016 Oct 01; 5(Suppl 4). PMID: 30637198    Free PMC article.
Turning the Tide Against Regulatory T Cells.
SeongJun Han, Aras Toker, Zhe Qi Liu, Pamela S Ohashi.
Front Oncol, 2019 May 07; 9. PMID: 31058083    Free PMC article.
Review.
Monoclonal antibody therapy of solid tumors: clinical limitations and novel strategies to enhance treatment efficacy.
Esteban Cruz, Veysel Kayser.
Biologics, 2019 May 24; 13. PMID: 31118560    Free PMC article.
Highly Cited. Review.
A novel combination of chemotherapy and immunotherapy controls tumor growth in mice with a human immune system.
Aude Burlion, Rodrigo N Ramos, +7 authors, Gilles Marodon.
Oncoimmunology, 2019 May 31; 8(7). PMID: 31143518    Free PMC article.
Effective Anti-tumor Response by TIGIT Blockade Associated With FcγR Engagement and Myeloid Cell Activation.
Jin-Hwan Han, Mingmei Cai, +9 authors, Sybil M Genther Williams.
Front Immunol, 2020 Oct 30; 11. PMID: 33117369    Free PMC article.
Mechanisms of Resistance to Immune Checkpoint Blockade.
David Liu, Russell W Jenkins, Ryan J Sullivan.
Am J Clin Dermatol, 2018 Sep 28; 20(1). PMID: 30259383    Free PMC article.
Review.
A Paradigm Shift in Cancer Immunotherapy: From Enhancement to Normalization.
Miguel F Sanmamed, Lieping Chen.
Cell, 2018 Oct 06; 175(2). PMID: 30290139    Free PMC article.
Highly Cited. Review.
How Does an Anti-CTLA-4 Antibody Promote Cancer Immunity?
Yang Liu, Pan Zheng.
Trends Immunol, 2018 Dec 01; 39(12). PMID: 30497614    Free PMC article.
Review.
Development and validation of a TP53-associated immune prognostic model for hepatocellular carcinoma.
Junyu Long, Anqiang Wang, +6 authors, Haitao Zhao.
EBioMedicine, 2019 Mar 20; 42. PMID: 30885723    Free PMC article.
Highly Cited.
<Editors' Choice> Meddling with meddlers: curbing regulatory T cells and augmenting antitumor immunity.
Vitaly Kochin, Hiroyoshi Nishikawa.
Nagoya J Med Sci, 2019 Apr 10; 81(1). PMID: 30962651    Free PMC article.
Review.
CTLA-4 antibody ipilimumab negatively affects CD4+ T-cell responses in vitro.
Sandra Rosskopf, Judith Leitner, Gerhard J Zlabinger, Peter Steinberger.
Cancer Immunol Immunother, 2019 Jul 25; 68(8). PMID: 31332464    Free PMC article.
Cyclophosphamide Enhances Cancer Antibody Immunotherapy in the Resistant Bone Marrow Niche by Modulating Macrophage FcγR Expression.
Ali Roghanian, Guangan Hu, +12 authors, Jianzhu Chen.
Cancer Immunol Res, 2019 Aug 28; 7(11). PMID: 31451483    Free PMC article.
The Current Landscape of Antibody-based Therapies in Solid Malignancies.
Ashu Shah, Sanchita Rauth, +6 authors, Surinder K Batra.
Theranostics, 2021 Jan 05; 11(3). PMID: 33391547    Free PMC article.
Review.
The Role of Antigen Processing and Presentation in Cancer and the Efficacy of Immune Checkpoint Inhibitor Immunotherapy.
Anastasia Mpakali, Efstratios Stratikos.
Cancers (Basel), 2021 Jan 08; 13(1). PMID: 33406696    Free PMC article.
Review.
Domain binding and isotype dictate the activity of anti-human OX40 antibodies.
Jordana Griffiths, Khiyam Hussain, +18 authors, Mark S Cragg.
J Immunother Cancer, 2021 Jan 12; 8(2). PMID: 33428585    Free PMC article.
Tumor-associated myeloid cells: diversity and therapeutic targeting.
Alberto Mantovani, Federica Marchesi, +2 authors, Paola Allavena.
Cell Mol Immunol, 2021 Jan 22; 18(3). PMID: 33473192    Free PMC article.
Review.
Understanding and Targeting Human Cancer Regulatory T Cells to Improve Therapy.
H Ryan Kolb, Nicholas Borcherding, Weizhou Zhang.
Adv Exp Med Biol, 2021 Feb 02; 1278. PMID: 33523451
Galectin-9 interacts with PD-1 and TIM-3 to regulate T cell death and is a target for cancer immunotherapy.
Riyao Yang, Linlin Sun, +14 authors, Mien-Chie Hung.
Nat Commun, 2021 Feb 07; 12(1). PMID: 33547304    Free PMC article.
Therapy of Established Tumors with Rationally Designed Multiple Agents Targeting Diverse Immune-Tumor Interactions: Engage, Expand, Enable.
Kellsye P Fabian, Anthony S Malamas, +6 authors, James W Hodge.
Cancer Immunol Res, 2020 Dec 24; 9(2). PMID: 33355290    Free PMC article.
Evaluation of glucocorticoid-induced TNF receptor (GITR) expression in breast cancer and across multiple tumor types.
Mayanne M T Zhu, Samantha Burugu, +5 authors, Torsten O Nielsen.
Mod Pathol, 2020 May 01; 33(9). PMID: 32350416
Modulation of regulatory T cell function and stability by co-inhibitory receptors.
Liliana E Lucca, Margarita Dominguez-Villar.
Nat Rev Immunol, 2020 Apr 10; 20(11). PMID: 32269380
Review.
Isotype selection for antibody-based cancer therapy.
N Vukovic, A van Elsas, J S Verbeek, D M W Zaiss.
Clin Exp Immunol, 2020 Nov 07; 203(3). PMID: 33155272    Free PMC article.
Review.
CD25-Treg-depleting antibodies preserving IL-2 signaling on effector T cells enhance effector activation and antitumor immunity.
Isabelle Solomon, Maria Amann, +29 authors, Sergio A Quezada.
Nat Cancer, 2021 Mar 02; 1(12). PMID: 33644766    Free PMC article.
The Impact of Tregs on the Anticancer Immunity and the Efficacy of Immune Checkpoint Inhibitor Therapies.
Jose M González-Navajas, Dengxia Denise Fan, +4 authors, Jongdae Lee.
Front Immunol, 2021 Mar 16; 12. PMID: 33717139    Free PMC article.
Review.
Enhancing CAR-T cell efficacy in solid tumors by targeting the tumor microenvironment.
Guangna Liu, Wei Rui, Xueqiang Zhao, Xin Lin.
Cell Mol Immunol, 2021 Apr 01; 18(5). PMID: 33785843    Free PMC article.
Review.
OX40 as a novel target for the reversal of immune escape in colorectal cancer.
Lin-Hai Yan, Xiao-Liang Liu, +3 authors, Wei-Zhong Tang.
Am J Transl Res, 2021 Apr 13; 13(3). PMID: 33841630    Free PMC article.
Review.
ImmunoPET Imaging of TIM-3 in Murine Melanoma Models.
Weijun Wei, Dawei Jiang, +4 authors, Weibo Cai.
Adv Ther (Weinh), 2021 Apr 24; 3(7). PMID: 33889713    Free PMC article.
Dendritic Cell Tumor Vaccination via Fc Gamma Receptor Targeting: Lessons Learned from Pre-Clinical and Translational Studies.
Enrique Gómez Alcaide, Sinduya Krishnarajah, Fabian Junker.
Vaccines (Basel), 2021 May 01; 9(4). PMID: 33924183    Free PMC article.
Review.
Intratumoural administration and tumour tissue targeting of cancer immunotherapies.
Ignacio Melero, Eduardo Castanon, +2 authors, Aurelien Marabelle.
Nat Rev Clin Oncol, 2021 May 20; 18(9). PMID: 34006998    Free PMC article.
Review.
Pouring petrol on the flames: Using oncolytic virotherapies to enhance tumour immunogenicity.
Alicia Teijeira Crespo, Stephanie Burnell, +7 authors, Alan L Parker.
Immunology, 2021 Feb 28; 163(4). PMID: 33638871    Free PMC article.
Review.
Blockade of immune checkpoints in lymph nodes through locoregional delivery augments cancer immunotherapy.
David M Francis, Margaret P Manspeaker, +6 authors, Susan N Thomas.
Sci Transl Med, 2020 Oct 02; 12(563). PMID: 32998971    Free PMC article.
Tissue-specific Tregs in cancer metastasis: opportunities for precision immunotherapy.
Laura A Huppert, Michael D Green, +4 authors, James C Lee.
Cell Mol Immunol, 2021 Aug 22; 19(1). PMID: 34417572    Free PMC article.
Review.
Strategies to Improve the Antitumor Effect of γδ T Cell Immunotherapy for Clinical Application.
Masatsugu Miyashita, Teruki Shimizu, Eishi Ashihara, Osamu Ukimura.
Int J Mol Sci, 2021 Aug 28; 22(16). PMID: 34445615    Free PMC article.
Review.
Soluble B7-CD28 Family Inhibitory Immune Checkpoint Proteins and Anti-Cancer Immunotherapy.
Muhammad Khan, Sumbal Arooj, Hua Wang.
Front Immunol, 2021 Sep 18; 12. PMID: 34531847    Free PMC article.
Review.
Motility Dynamics of T Cells in Tumor-Draining Lymph Nodes: A Rational Indicator of Antitumor Response and Immune Checkpoint Blockade.
Yasuhiro Kanda, Taku Okazaki, Tomoya Katakai.
Cancers (Basel), 2021 Sep 29; 13(18). PMID: 34572844    Free PMC article.
Review.
Regulatory T-Cells and Multiple Myeloma: Implications in Tumor Immune Biology and Treatment.
Christina Hadjiaggelidou, Eirini Katodritou.
J Clin Med, 2021 Oct 14; 10(19). PMID: 34640606    Free PMC article.
Review.
Crosstalk Between the Tumor Microenvironment and Cancer Cells: A Promising Predictive Biomarker for Immune Checkpoint Inhibitors.
Xiaoying Li, Yueyao Yang, +4 authors, Ming Liu.
Front Cell Dev Biol, 2021 Oct 26; 9. PMID: 34692696    Free PMC article.
Review.
Tumor-immune profiling of CT-26 and Colon 26 syngeneic mouse models reveals mechanism of anti-PD-1 response.
Yosuke Sato, Yu Fu, +2 authors, Michael H Shaw.
BMC Cancer, 2021 Nov 15; 21(1). PMID: 34774008    Free PMC article.
Biological Bases of Immune-Related Adverse Events and Potential Crosslinks With Immunogenic Effects of Radiation.
Lilia Bardoscia, Nadia Pasinetti, +2 authors, Angela Sardaro.
Front Pharmacol, 2021 Nov 19; 12. PMID: 34790123    Free PMC article.
Review.
Targeting regulatory T cells for immunotherapy in melanoma.
Lili Huang, Yeye Guo, +4 authors, Xiaowei Xu.
Mol Biomed, 2021 Nov 23; 2(1). PMID: 34806028    Free PMC article.
Review.
Two novel human anti-CD25 antibodies with antitumor activity inversely related to their affinity and in vitro activity.
Deyong Song, Xiu Liu, +12 authors, Changlin Dou.
Sci Rep, 2021 Nov 27; 11(1). PMID: 34824364    Free PMC article.
Research Progress on the Role of Regulatory T Cell in Tumor Microenvironment in the Treatment of Breast Cancer.
Jianyu Liu, Xueying Wang, +3 authors, Zhigao Li.
Front Oncol, 2021 Dec 07; 11. PMID: 34868991    Free PMC article.
Review.
Expansion of tumor-associated Treg cells upon disruption of a CTLA-4-dependent feedback loop.
Francesco Marangoni, Ademi Zhakyp, +10 authors, Thorsten R Mempel.
Cell, 2021 Jun 23; 184(15). PMID: 34157302    Free PMC article.
The foundations of immune checkpoint blockade and the ipilimumab approval decennial.
Alan J Korman, Sarah C Garrett-Thomson, Nils Lonberg.
Nat Rev Drug Discov, 2021 Dec 24;. PMID: 34937915
Review.

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Immune Checkpoint Blockade Augments Changes Within Oncolytic Virus-induced Cancer MHC-I Peptidome, Creating Novel Antitumor CD8 T Cell Reactivities.
Youra Kim, Prathyusha Konda, +3 authors, Shashi Gujar.
Mol Cell Proteomics, 2021 Dec 19; 21(2). PMID: 34922008    Free PMC article.
Fc-independent functions of anti-CTLA-4 antibodies contribute to anti-tumor efficacy.
Yosuke Sato, Cierra N Casson, +14 authors, Michael H Shaw.
Cancer Immunol Immunother, 2022 Mar 04;. PMID: 35237846
An Fc-Competent Anti-Human TIGIT Blocking Antibody Ociperlimab (BGB-A1217) Elicits Strong Immune Responses and Potent Anti-Tumor Efficacy in Pre-Clinical Models.
Xin Chen, Liu Xue, +23 authors, Tong Zhang.
Front Immunol, 2022 Mar 12; 13. PMID: 35273608    Free PMC article.
Single-Cell RNA-Seq and Bulk RNA-Seq Reveal Intratumoral Heterogeneity and Tumor Microenvironment Characteristics in Diffuse Large B-Cell Lymphoma.
Yang Zhao, Hui Xu, Mingzhi Zhang, Ling Li.
Front Genet, 2022 May 24; 13. PMID: 35601491    Free PMC article.