Journal Article
. 2015 Apr; 112(19):6140-5.
doi: 10.1073/pnas.1417320112.

Ipilimumab-dependent cell-mediated cytotoxicity of regulatory T cells ex vivo by nonclassical monocytes in melanoma patients

Emanuela Romano 1 Monika Kusio-Kobialka 2 Periklis G Foukas 3 Petra Baumgaertner 4 Christiane Meyer 4 Pierluigi Ballabeni 5 Olivier Michielin 6 Benjamin Weide 7 Pedro Romero 4 Daniel E Speiser 4 
  • PMID: 25918390
  •     30 References
  •     241 citations


Enhancing immune responses with immune-modulatory monoclonal antibodies directed to inhibitory immune receptors is a promising modality in cancer therapy. Clinical efficacy has been demonstrated with antibodies blocking inhibitory immune checkpoints such as cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) or PD-1/PD-L1. Treatment with ipilimumab, a fully human CTLA-4-specific mAb, showed durable clinical efficacy in metastatic melanoma; its mechanism of action is, however, only partially understood. This is a study of 29 patients with advanced cutaneous melanoma treated with ipilimumab. We analyzed peripheral blood mononuclear cells (PBMCs) and matched melanoma metastases from 15 patients responding and 14 not responding to ipilimumab by multicolor flow cytometry, antibody-dependent cell-mediated cytotoxicity (ADCC) assay, and immunohistochemistry. PBMCs and matched tumor biopsies were collected 24 h before (i.e., baseline) and up to 4 wk after ipilimumab. Our findings show, to our knowledge for the first time, that ipilimumab can engage ex vivo FcγRIIIA (CD16)-expressing, nonclassical monocytes resulting in ADCC-mediated lysis of regulatory T cells (Tregs). In contrast, classical CD14(++)CD16(-) monocytes are unable to do so. Moreover, we show that patients responding to ipilimumab display significantly higher baseline peripheral frequencies of nonclassical monocytes compared with nonresponder patients. In the tumor microenvironment, responders have higher CD68(+)/CD163(+) macrophage ratios at baseline and show decreased Treg infiltration after treatment. Together, our results suggest that anti-CTLA-4 therapy may target Tregs in vivo. Larger translational studies are, however, warranted to substantiate this mechanism of action of ipilimumab in patients.

Keywords: ADCC; Tregs; ipilimumab; macrophages; monocytes.

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Front Immunol, 2018 May 01; 9. PMID: 29706961    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.
Sequential immunotherapy in a patient with primary refractory Hodgkin lymphoma and novel mutations.
Richard Greil, Lisa Pleyer, +7 authors, Sigrun Greil-Ressler.
Oncotarget, 2018 May 15; 9(29). PMID: 29755699    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.
Tumor matrix remodeling and novel immunotherapies: the promise of matrix-derived immune biomarkers.
Muhammad Umair Mushtaq, Athanasios Papadas, +4 authors, Fotis Asimakopoulos.
J Immunother Cancer, 2018 Jul 05; 6(1). PMID: 29970158    Free PMC article.
Hide or defend, the two strategies of lymphoma immune evasion: potential implications for immunotherapy.
Marie de Charette, Roch Houot.
Haematologica, 2018 Jul 15; 103(8). PMID: 30006449    Free PMC article.
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.
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.
Neurologic immune-related adverse events associated with adjuvant ipilimumab: report of two cases.
Christine A Garcia, Alex El-Ali, +4 authors, Diwakar Davar.
J Immunother Cancer, 2018 Sep 02; 6(1). PMID: 30170622    Free PMC article.
Endocrine Toxicity of Cancer Immunotherapy Targeting Immune Checkpoints.
Lee-Shing Chang, Romualdo Barroso-Sousa, +3 authors, Le Min.
Endocr Rev, 2018 Sep 06; 40(1). PMID: 30184160    Free PMC article.
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.
Targeting Checkpoint Receptors and Molecules for Therapeutic Modulation of Natural Killer Cells.
Nayoung Kim, Hun Sik Kim.
Front Immunol, 2018 Sep 27; 9. PMID: 30250471    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.

;. PMID: 30345161
Highly Cited.
Targeting macrophages: therapeutic approaches in cancer.
Luca Cassetta, Jeffrey W Pollard.
Nat Rev Drug Discov, 2018 Oct 27; 17(12). PMID: 30361552
Highly Cited. Review.
Recent advances in immunotherapies: from infection and autoimmunity, to cancer, and back again.
Samantha L Bucktrout, Jeffrey A Bluestone, Fred Ramsdell.
Genome Med, 2018 Nov 01; 10(1). PMID: 30376867    Free PMC article.
Effects of tumor grade and dexamethasone on myeloid cells in patients with glioma.
Kara W Moyes, Amira Davis, +14 authors, Courtney A Crane.
Oncoimmunology, 2018 Nov 01; 7(11). PMID: 30377570    Free PMC article.
Preclinical and Clinical Therapeutic Strategies Affecting Tumor-Associated Macrophages in Hepatocellular Carcinoma.
H Degroote, A Van Dierendonck, +2 authors, L Devisscher.
J Immunol Res, 2018 Nov 10; 2018. PMID: 30410942    Free PMC article.
Outcomes of vedolizumab therapy in patients with immune checkpoint inhibitor-induced colitis: a multi-center study.
Hamzah Abu-Sbeih, Faisal S Ali, +6 authors, Yinghong Wang.
J Immunother Cancer, 2018 Dec 07; 6(1). PMID: 30518410    Free PMC article.
PD-L1 expression with immune-infiltrate evaluation and outcome prediction in melanoma patients treated with ipilimumab.
Gabriele Madonna, Carmen Ballesteros-Merino, +10 authors, Paolo A Ascierto.
Oncoimmunology, 2018 Dec 14; 7(12). PMID: 30524879    Free PMC article.
Monocyte heterogeneity and functions in cancer.
Claire E Olingy, Huy Q Dinh, Catherine C Hedrick.
J Leukoc Biol, 2019 Feb 19; 106(2). PMID: 30776148    Free PMC article.
Highly Cited. Review.
Biomarkers, measured during therapy, for response of melanoma patients to immune checkpoint inhibitors: a systematic review.
Wouter Ouwerkerk, Mirjam van den Berg, +2 authors, Rosalie M Luiten.
Melanoma Res, 2019 Mar 12; 29(5). PMID: 30855527    Free PMC article.
Systematic Review.
Efficacy and Adverse Events of Immunotherapy with Checkpoint Inhibitors in Older Patients with Cancer.
Yara van Holstein, Ellen Kapiteijn, +3 authors, Nienke A de Glas.
Drugs Aging, 2019 Jul 19; 36(10). PMID: 31317421    Free PMC article.
Opposing Functions of Interferon Coordinate Adaptive and Innate Immune Responses to Cancer Immune Checkpoint Blockade.
Joseph L Benci, Lexus R Johnson, +14 authors, Andy J Minn.
Cell, 2019 Aug 10; 178(4). PMID: 31398344    Free PMC article.
Highly Cited.
Circulating biomarkers predictive of tumor response to cancer immunotherapy.
Ernest Y Lee, Rajan P Kulkarni.
Expert Rev Mol Diagn, 2019 Aug 31; 19(10). PMID: 31469965    Free PMC article.
6-Sulfo LacNAc (Slan) as a Marker for Non-classical Monocytes.
Thomas P Hofer, Arjan A van de Loosdrecht, +2 authors, Loems Ziegler-Heitbrock.
Front Immunol, 2019 Oct 02; 10. PMID: 31572354    Free PMC article.
Profiles of tumor-infiltrating immune cells in renal cell carcinoma and their clinical implications.
Gongmin Zhu, Lijiao Pei, +5 authors, Xin Gou.
Oncol Lett, 2019 Oct 16; 18(5). PMID: 31612034    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.
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.
Beneficial modulation of the tumor microenvironment and generation of anti-tumor responses by TLR9 agonist lefitolimod alone and in combination with checkpoint inhibitors.
Kerstin Kapp, Barbara Volz, +3 authors, Manuel Schmidt.
Oncoimmunology, 2019 Nov 20; 8(12). PMID: 31741757    Free PMC article.
Gut microbiome and CAR-T therapy.
Muhammad Bilal Abid, Nirav N Shah, Theresa C Maatman, Parameswaran N Hari.
Exp Hematol Oncol, 2019 Dec 13; 8. PMID: 31827982    Free PMC article.
High expression of B7-H3 on stromal cells defines tumor and stromal compartments in epithelial ovarian cancer and is associated with limited immune activation.
Heather L MacGregor, Azin Sayad, +9 authors, Pamela S Ohashi.
J Immunother Cancer, 2020 Jan 02; 7(1). PMID: 31892360    Free PMC article.
Time to dissect the autoimmune etiology of cancer antibody immunotherapy.
Michael Dougan, Massimo Pietropaolo.
J Clin Invest, 2020 Jan 03; 130(1). PMID: 31895048    Free PMC article.
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.
Discovery of tumoricidal DNA oligonucleotides by response-directed in vitro evolution.
Noam Mamet, Yaniv Amir, +15 authors, Ido Bachelet.
Commun Biol, 2020 Jan 17; 3(1). PMID: 31941992    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.
Effect of pembrolizumab on CD4+ CD25+ , CD4+ LAP+ and CD4+ TIM-3+ T cell subsets.
S M Toor, V Sasidharan Nair, G Pfister, E Elkord.
Clin Exp Immunol, 2019 Jan 30; 196(3). PMID: 30693485    Free PMC article.
A functional antibody cross-reactive to both human and murine cytotoxic T-lymphocyte-associated protein 4 via binding to an N-glycosylation epitope.
Dong Li, Jing Li, Huanyu Chu, Zhuozhi Wang.
MAbs, 2020 Feb 15; 12(1). PMID: 32054416    Free PMC article.
NK Cell-Based Immune Checkpoint Inhibition.
Muhammad Khan, Sumbal Arooj, Hua Wang.
Front Immunol, 2020 Mar 03; 11. PMID: 32117298    Free PMC article.
A novel immunogenic mouse model of melanoma for the preclinical assessment of combination targeted and immune-based therapy.
Emily J Lelliott, Carleen Cullinane, +14 authors, Karen E Sheppard.
Sci Rep, 2019 Feb 06; 9(1). PMID: 30718660    Free PMC article.
PD-1+ regulatory T cells amplified by PD-1 blockade promote hyperprogression of cancer.
Takahiro Kamada, Yosuke Togashi, +13 authors, Hiroyoshi Nishikawa.
Proc Natl Acad Sci U S A, 2019 Apr 28; 116(20). PMID: 31028147    Free PMC article.
Highly Cited.
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.
A Multi-center Phase I Trial of Ipilimumab in Patients with Myelodysplastic Syndromes following Hypomethylating Agent Failure.
Amer M Zeidan, Hanna A Knaus, +17 authors, B Douglas Smith.
Clin Cancer Res, 2018 May 03; 24(15). PMID: 29716921    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
Anti-CTLA-4 Immunotherapy Does Not Deplete FOXP3+ Regulatory T Cells (Tregs) in Human Cancers.
Anu Sharma, Sumit K Subudhi, +6 authors, Padmanee Sharma.
Clin Cancer Res, 2018 Jul 29; 25(4). PMID: 30054281    Free PMC article.
Highly Cited.
Safety and Efficacy of Durvalumab With or Without Tremelimumab in Patients With PD-L1-Low/Negative Recurrent or Metastatic HNSCC: The Phase 2 CONDOR Randomized Clinical Trial.
Lillian L Siu, Caroline Even, +18 authors, Jérôme Fayette.
JAMA Oncol, 2018 Nov 02; 5(2). PMID: 30383184    Free PMC article.
Highly Cited.
French Endocrine Society Guidance on endocrine side effects of immunotherapy.
F Castinetti, F Albarel, +21 authors, F Borson-Chazot.
Endocr Relat Cancer, 2018 Nov 08; 26(2). PMID: 30400055    Free PMC article.
Tumor-conditional anti-CTLA4 uncouples antitumor efficacy from immunotherapy-related toxicity.
Chien-Chun Steven Pai, Donald M Simons, +22 authors, Lawrence Fong.
J Clin Invest, 2018 Dec 12; 129(1). PMID: 30530991    Free PMC article.
Non-invasive biomarkers derived from the extracellular matrix associate with response to immune checkpoint blockade (anti-CTLA-4) in metastatic melanoma patients.
Christina Jensen, Daniel Hargbøl Madsen, +4 authors, Nicholas Willumsen.
J Immunother Cancer, 2018 Dec 21; 6(1). PMID: 30567561    Free PMC article.
Combination Strategies to Optimize Efficacy of Dendritic Cell-Based Immunotherapy.
Mandy van Gulijk, Floris Dammeijer, Joachim G J V Aerts, Heleen Vroman.
Front Immunol, 2018 Dec 21; 9. PMID: 30568653    Free PMC article.
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.
Arg1 expression defines immunosuppressive subsets of tumor-associated macrophages.
Sean P Arlauckas, Seth B Garren, +4 authors, Ralph Weissleder.
Theranostics, 2019 Jan 08; 8(21). PMID: 30613266    Free PMC article.
Highly Cited.
Genomic correlates of response to immune checkpoint blockade.
Tanya E Keenan, Kelly P Burke, Eliezer M Van Allen.
Nat Med, 2019 Mar 08; 25(3). PMID: 30842677    Free PMC article.
Highly Cited. Review.
The CTLA-4 x OX40 bispecific antibody ATOR-1015 induces anti-tumor effects through tumor-directed immune activation.
Anne Månsson Kvarnhammar, Niina Veitonmäki, +16 authors, Peter Ellmark.
J Immunother Cancer, 2019 Apr 13; 7(1). PMID: 30975201    Free PMC article.
T cell pathology in skin inflammation.
Robert Sabat, Kerstin Wolk, +2 authors, Kamran Ghoreschi.
Semin Immunopathol, 2019 Apr 28; 41(3). PMID: 31028434    Free PMC article.
Anti-CTLA-4 Immunotherapy Does Not Deplete FOXP3+ Regulatory T Cells (Tregs) in Human Cancers-Response.
Anu Sharma, Sumit K Subudhi, +5 authors, Padmanee Sharma.
Clin Cancer Res, 2019 Jun 05; 25(11). PMID: 31160495    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.
Conducting a Virtual Clinical Trial in HER2-Negative Breast Cancer Using a Quantitative Systems Pharmacology Model With an Epigenetic Modulator and Immune Checkpoint Inhibitors.
Hanwen Wang, Richard J Sové, +6 authors, Aleksander S Popel.
Front Bioeng Biotechnol, 2020 Mar 12; 8. PMID: 32158754    Free PMC article.
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.
Combination immunotherapy with anti-PD-L1 antibody and depletion of regulatory T cells during acute viral infections results in improved virus control but lethal immunopathology.
Paul David, Malgorzata Drabczyk-Pluta, +24 authors, Gennadiy Zelinskyy.
PLoS Pathog, 2020 Apr 01; 16(3). PMID: 32226027    Free PMC article.
Depleting tumor-associated Tregs via nanoparticle-mediated hyperthermia to enhance anti-CTLA-4 immunotherapy.
Hongwei Chen, Xin Luan, +7 authors, Duxin Sun.
Nanomedicine (Lond), 2019 Dec 24; 15(1). PMID: 31868112    Free PMC article.
Development of immune checkpoint therapy for cancer.
Jill M Fritz, Michael J Lenardo.
J Exp Med, 2019 May 10; 216(6). PMID: 31068379    Free PMC article.
Highly Cited. Review.
Combining Immune Checkpoint Inhibitors: Established and Emerging Targets and Strategies to Improve Outcomes in Melanoma.
Duaa O Khair, Heather J Bax, +22 authors, Sophia N Karagiannis.
Front Immunol, 2019 Apr 04; 10. PMID: 30941125    Free PMC article.
Highly Cited. 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.
Context Drives Diversification of Monocytes and Neutrophils in Orchestrating the Tumor Microenvironment.
Juhee Jeong, Yoorock Suh, Keehoon Jung.
Front Immunol, 2019 Sep 03; 10. PMID: 31474975    Free PMC article.
Dawn of Monitoring Regulatory T Cells in (Pre-)clinical Studies: Their Relevance Is Slowly Recognised.
A Charlotte M T de Wolf, Carla A Herberts, Marcel H N Hoefnagel.
Front Med (Lausanne), 2020 Apr 18; 7. PMID: 32300597    Free PMC article.
Systematic Review.
Clinical Pharmacokinetic and Pharmacodynamic Considerations in the (Modern) Treatment of Melanoma.
Hannah Yejin Kim, Parth J Upadhyay, +3 authors, Alan V Boddy.
Clin Pharmacokinet, 2019 Mar 15; 58(8). PMID: 30868471
Systemic Blood Immune Cell Populations as Biomarkers for the Outcome of Immune Checkpoint Inhibitor Therapies.
Carlos Hernandez, Hugo Arasanz, +7 authors, Grazyna Kochan.
Int J Mol Sci, 2020 Apr 05; 21(7). PMID: 32244396    Free PMC article.
Targeting T cell activation in immuno-oncology.
S D Saibil, P S Ohashi.
Curr Oncol, 2020 May 06; 27(Suppl 2). PMID: 32368179    Free PMC article.
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.
Mechanisms of Resistance to NK Cell Immunotherapy.
Christian Sordo-Bahamonde, Massimo Vitale, +2 authors, Segundo Gonzalez.
Cancers (Basel), 2020 Apr 11; 12(4). PMID: 32272610    Free PMC article.
Normalization Cancer Immunotherapy for Melanoma.
Matthew D Vesely, Lieping Chen.
J Invest Dermatol, 2020 Feb 25; 140(6). PMID: 32092349    Free PMC article.
The Tumor Microenvironment in the Response to Immune Checkpoint Blockade Therapies.
Florent Petitprez, Maxime Meylan, +2 authors, Wolf H Fridman.
Front Immunol, 2020 May 28; 11. PMID: 32457745    Free PMC article.
Engineering bionic T cells: signal 1, signal 2, signal 3, reprogramming and the removal of inhibitory mechanisms.
Iñaki Etxeberria, Irene Olivera, +4 authors, Ignacio Melero.
Cell Mol Immunol, 2020 May 21; 17(6). PMID: 32433539    Free PMC article.
Immune-checkpoint molecules on regulatory T-cells as a potential therapeutic target in head and neck squamous cell cancers.
Susumu Suzuki, Tetsuya Ogawa, +7 authors, Toyonori Tsuzuki.
Cancer Sci, 2020 Apr 19; 111(6). PMID: 32304268    Free PMC article.
Tumor-induced neurogenesis and immune evasion as targets of innovative anti-cancer therapies.
Rodolfo Daniel Cervantes-Villagrana, Damaris Albores-García, Alberto Rafael Cervantes-Villagrana, Sara Judit García-Acevez.
Signal Transduct Target Ther, 2020 Jun 20; 5(1). PMID: 32555170    Free PMC article.
A Phase I Study of the Combination of Rituximab and Ipilimumab in Patients with Relapsed/Refractory B-Cell Lymphoma.
Joseph M Tuscano, Emanual Maverakis, +10 authors, Edward M Newman.
Clin Cancer Res, 2019 Sep 05; 25(23). PMID: 31481504    Free PMC article.
The Role of Tumor-Associated Myeloid Cells in Modulating Cancer Therapy.
Christiana M Neophytou, Chryso Pierides, +3 authors, Panagiotis Papageorgis.
Front Oncol, 2020 Jul 14; 10. PMID: 32656079    Free PMC article.
MKL-1 is a coactivator for STAT5b, the regulator of Treg cell development and function.
Yuan Xiang, Jun Wang, +12 authors, Xing Hua Liao.
Cell Commun Signal, 2020 Jul 11; 18(1). PMID: 32646440    Free PMC article.
Dissecting the Tumor-Immune Landscape in Chimeric Antigen Receptor T-cell Therapy: Key Challenges and Opportunities for a Systems Immunology Approach.
Gregory M Chen, Andrew Azzam, +3 authors, Kai Tan.
Clin Cancer Res, 2020 Mar 05; 26(14). PMID: 32127393    Free PMC article.
Durvalumab and tremelimumab combination therapy versus durvalumab or tremelimumab monotherapy for patients with solid tumors: A systematic review and meta-analysis.
Bi-Cheng Wang, Peng-Cheng Li, +2 authors, Quentin Liu.
Medicine (Baltimore), 2020 Jul 16; 99(28). PMID: 32664183    Free PMC article.
Systematic Review.
Mechanisms of Epstein-Barr virus nuclear antigen 1 favor Tregs accumulation in nasopharyngeal carcinoma.
Jie Wang, Yunfan Luo, +5 authors, Xiangping Li.
Cancer Med, 2020 Jun 24; 9(15). PMID: 32573058    Free PMC article.
Harnessing NK Cell Checkpoint-Modulating Immunotherapies.
Sachin Kumar Singh Chauhan, Ulrike Koehl, Stephan Kloess.
Cancers (Basel), 2020 Jul 10; 12(7). PMID: 32640575    Free PMC article.
Myeloid Cells as Clinical Biomarkers for Immune Checkpoint Blockade.
Elisa Peranzoni, Vincenzo Ingangi, +2 authors, Ilaria Marigo.
Front Immunol, 2020 Aug 15; 11. PMID: 32793228    Free PMC article.
An Immunophenotyping of Ovarian Cancer With Clinical and Immunological Significance.
Kai Yang, Weiwei Zhao, +7 authors, Kang Li.
Front Immunol, 2018 Apr 10; 9. PMID: 32793247    Free PMC article.
Scientifically based combination therapies with immuno-oncology checkpoint inhibitors.
Hui Yi Chew, Riccardo Dolcetti, Fiona Simpson.
Br J Clin Pharmacol, 2020 May 07; 86(9). PMID: 32372470    Free PMC article.
The Great Debate at 'Immunotherapy Bridge', Naples, December 5, 2019.
Paolo A Ascierto, Carlo Bifulco, +12 authors, Igor Puzanov.
J Immunother Cancer, 2020 Aug 28; 8(2). PMID: 32843491    Free PMC article.
PD-L1 in Systemic Immunity: Unraveling Its Contribution to PD-1/PD-L1 Blockade Immunotherapy.
Ana Bocanegra, Ester Blanco, +7 authors, Grazyna Kochan.
Int J Mol Sci, 2020 Aug 23; 21(16). PMID: 32824655    Free PMC article.
Significance of Immunosuppressive Cells as a Target for Immunotherapies in Melanoma and Non-Melanoma Skin Cancers.
Taku Fujimura, Setsuya Aiba.
Biomolecules, 2020 Jul 28; 10(8). PMID: 32707850    Free PMC article.
Isolation of Two Novel Human Anti-CTLA-4 mAbs with Intriguing Biological Properties on Tumor and NK Cells.
Margherita Passariello, Cinzia Vetrei, +7 authors, Claudia De Lorenzo.
Cancers (Basel), 2020 Aug 13; 12(8). PMID: 32781690    Free PMC article.
PD-1 checkpoint blockade in advanced melanoma patients: NK cells, monocytic subsets and host PD-L1 expression as predictive biomarker candidates.
Yago Pico de Coaña, Maria Wolodarski, +6 authors, Rolf Kiessling.
Oncoimmunology, 2020 Sep 18; 9(1). PMID: 32939320    Free PMC article.
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.
Isolated Limb Perfusion With Melphalan Triggers Immune Activation in Melanoma Patients.
Junko Johansson, Roberta Kiffin, +4 authors, Anna Martner.
Front Oncol, 2018 Dec 19; 8. PMID: 30560089    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.
Macrophages in Colorectal Cancer Liver Metastases.
Nina Cortese, Cristiana Soldani, +4 authors, Matteo Donadon.
Cancers (Basel), 2019 May 10; 11(5). PMID: 31067629    Free PMC article.
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.
Biomarkers for Immune Checkpoint Inhibitor-Mediated Tumor Response and Adverse Events.
Yoshiyuki Nakamura.
Front Med (Lausanne), 2019 Jun 14; 6. PMID: 31192215    Free PMC article.
Anti-CD40 mAb enhanced efficacy of anti-PD1 against osteosarcoma.
Jingzhe Zhang, Ye Li, +2 authors, Wenjun Wang.
J Bone Oncol, 2019 Jul 12; 17. PMID: 31293882    Free PMC article.
Hyperprogression: A novel response pattern under immunotherapy.
Xue-Jiao Han, Aqu Alu, +2 authors, Xia-Wei Wei.
Clin Transl Med, 2020 Oct 01; 10(5). PMID: 32997401    Free PMC article.
NKG2D-Fc fusion protein promotes antitumor immunity through the depletion of immunosuppressive cells.
Po-Hao Feng, Brandon Lam, +4 authors, Chien-Fu Hung.
Cancer Immunol Immunother, 2020 May 30; 69(10). PMID: 32468232    Free PMC article.
Micro-environmental cross-talk in an organotypic human melanoma-in-skin model directs M2-like monocyte differentiation via IL-10.
Elisabetta Michielon, Marta López González, +4 authors, Susan Gibbs.
Cancer Immunol Immunother, 2020 Jun 09; 69(11). PMID: 32507967    Free PMC article.
Managing Ipilimumab-Induced Hypophysitis: Challenges and Current Therapeutic Strategies.
Marina Tsoli, Gregory Kaltsas, +3 authors, Eva Kassi.
Cancer Manag Res, 2020 Oct 17; 12. PMID: 33061641    Free PMC article.
Uncoupling Therapeutic Efficacy from Immune-Related Adverse Events in Immune Checkpoint Blockade.
Weilei Hu, Guosheng Wang, +2 authors, Ming You.
iScience, 2020 Oct 22; 23(10). PMID: 33083746    Free PMC article.
Regulatory T Cells in Cancer Immunotherapy: Basic Research Outcomes and Clinical Directions.
Guoming Zeng, Libo Jin, +9 authors, Da Sun.
Cancer Manag Res, 2020 Oct 30; 12. PMID: 33116895    Free PMC article.
CTLA4 has a profound impact on the landscape of tumor-infiltrating lymphocytes with a high prognosis value in clear cell renal cell carcinoma (ccRCC).
Shiyi Liu, Feiyan Wang, +10 authors, Yanxiang Cheng.
Cancer Cell Int, 2020 Oct 30; 20. PMID: 33117084    Free PMC article.
Transcriptional regulation of Treg homeostasis and functional specification.
Ke Wang, Wenxian Fu.
Cell Mol Life Sci, 2020 May 01; 77(21). PMID: 32350553    Free PMC article.
Differential association of CD68+ and CD163+ macrophages with macrophage enzymes, whole tumour gene expression and overall survival in advanced melanoma.
Liam Friel Tremble, Mark McCabe, +8 authors, Cynthia C B B Heffron.
Br J Cancer, 2020 Aug 28; 123(10). PMID: 32843682    Free PMC article.
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.
Synergistic effect of immune checkpoint blockade and anti-angiogenesis in cancer treatment.
Ming Yi, Dechao Jiao, +3 authors, Anping Li.
Mol Cancer, 2019 Mar 31; 18(1). PMID: 30925919    Free PMC article.
Highly Cited. Review.
<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.
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.
Overcoming Immune Evasion in Melanoma.
Kevinn Eddy, Suzie Chen.
Int J Mol Sci, 2020 Dec 02; 21(23). PMID: 33256089    Free PMC article.
Advanced drug delivery 2020 and beyond: Perspectives on the future.
You Han Bae, Kinam Park.
Adv Drug Deliv Rev, 2020 Jun 28; 158. PMID: 32592727    Free PMC article.
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.
Highly Cited.
The Therapeutic Potential of Regulatory T Cells: Challenges and Opportunities.
Fatemeh Bayati, Mahsa Mohammadi, +3 authors, Ehsan Sharif-Paghaleh.
Front Immunol, 2021 Feb 02; 11. PMID: 33519807    Free PMC article.
Activity of murine surrogate antibodies for durvalumab and tremelimumab lacking effector function and the ability to deplete regulatory T cells in mouse models of cancer.
Darren J Schofield, Jennifer Percival-Alwyn, +18 authors, Michael Oberst.
MAbs, 2021 Jan 06; 13(1). PMID: 33397194    Free PMC article.
Harnessing NK cells for cancer immunotherapy: immune checkpoint receptors and chimeric antigen receptors.
Nayoung Kim, Dong-Hee Lee, +5 authors, Hun Sik Kim.
BMB Rep, 2020 Dec 11; 54(1). PMID: 33298244    Free PMC article.
HDAC inhibition potentiates anti-tumor activity of macrophages and enhances anti-PD-L1-mediated tumor suppression.
Xiaolei Li, Xiao Su, +8 authors, Yufang Shi.
Oncogene, 2021 Feb 11; 40(10). PMID: 33564072    Free PMC article.
Emerging dynamics pathways of response and resistance to PD-1 and CTLA-4 blockade: tackling uncertainty by confronting complexity.
Allan Relecom, Maysaloun Merhi, +4 authors, Said Dermime.
J Exp Clin Cancer Res, 2021 Feb 20; 40(1). PMID: 33602280    Free PMC article.
Regulatory T lymphocyte infiltration in metastatic breast cancer-an independent prognostic factor that changes with tumor progression.
Jenny Stenström, Ingrid Hedenfalk, Catharina Hagerling.
Breast Cancer Res, 2021 Feb 20; 23(1). PMID: 33602289    Free PMC article.
Case Report: Neoadjuvant PD-1 Blockade Plus Concurrent Chemoradiotherapy in Unresectable Locally Advanced Gastric Cancer Patients.
Jia Wei, Xiaofeng Lu, +10 authors, Baorui Liu.
Front Oncol, 2021 Feb 27; 10. PMID: 33634011    Free PMC article.
CD4+ T Cells: Multitasking Cells in the Duty of Cancer Immunotherapy.
Jennifer R Richardson, Anna Schöllhorn, Cécile Gouttefangeas, Juliane Schuhmacher.
Cancers (Basel), 2021 Feb 07; 13(4). PMID: 33546283    Free PMC article.
Natural Killer Cells and Anti-Cancer Therapies: Reciprocal Effects on Immune Function and Therapeutic Response.
Elisa C Toffoli, Abdolkarim Sheikhi, +6 authors, Tanja D de Gruijl.
Cancers (Basel), 2021 Feb 13; 13(4). PMID: 33572396    Free PMC article.
Inflammatory B cells correlate with failure to checkpoint blockade in melanoma patients.
Kaat de Jonge, Laure Tillé, +8 authors, Daniel E Speiser.
Oncoimmunology, 2021 Mar 02; 10(1). PMID: 33643691    Free PMC article.
Beyond immune checkpoint blockade: emerging immunological strategies.
Shawn P Kubli, Thorsten Berger, +2 authors, Tak W Mak.
Nat Rev Drug Discov, 2021 Mar 10; 20(12). PMID: 33686237
Precision Medicine Approaches to Overcome Resistance to Therapy in Head and Neck Cancers.
Sandra Ortiz-Cuaran, Jebrane Bouaoud, +2 authors, Pierre Saintigny.
Front Oncol, 2021 Mar 16; 11. PMID: 33718169    Free PMC article.
Hyperprogressive disease after radiotherapy combined with anti-PD-1 therapy in renal cell carcinoma: a case report and review of the literature.
Chao Liu, Jingjing Piao, Zhiyang Shang.
BMC Urol, 2021 Mar 22; 21(1). PMID: 33743675    Free PMC article.
MMP9 and IGFBP1 Regulate Tumor Immune and Drive Tumor Progression in Clear Cell Renal Cell Carcinoma.
Tianbo Xu, Su Gao, +3 authors, Xiaoping Zhang.
J Cancer, 2021 Mar 25; 12(8). PMID: 33758602    Free PMC article.
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.
Specific Patterns of Blood ILCs in Metastatic Melanoma Patients and Their Modulations in Response to Immunotherapy.
Louise Rethacker, Marie Roelens, +3 authors, Anne Caignard.
Cancers (Basel), 2021 Apr 04; 13(6). PMID: 33810032    Free PMC article.
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.
Recruitment and Expansion of Tregs Cells in the Tumor Environment-How to Target Them?
Justine Cinier, Margaux Hubert, +5 authors, Christine Ménétrier-Caux.
Cancers (Basel), 2021 May 01; 13(8). PMID: 33924428    Free PMC article.
Impact of Immunotherapy on CD4 T Cell Phenotypes and Function in Cancer.
Margaux Saillard, Mara Cenerenti, Pedro Romero, Camilla Jandus.
Vaccines (Basel), 2021 Jun 03; 9(5). PMID: 34064410    Free PMC article.
High Monocyte Count and Expression of S100A9 and S100A12 in Peripheral Blood Mononuclear Cells Are Associated with Poor Outcome in Patients with Metastatic Prostate Cancer.
Anna-Maja Åberg, Sofia Halin Bergström, +7 authors, Marie Lundholm.
Cancers (Basel), 2021 Jun 03; 13(10). PMID: 34067757    Free PMC article.
DLL1 orchestrates CD8+ T cells to induce long-term vascular normalization and tumor regression.
Naidong Zhang, Rongping Yin, +13 authors, Yuhui Huang.
Proc Natl Acad Sci U S A, 2021 May 27; 118(22). PMID: 34035167    Free PMC article.
Immune Checkpoint Inhibitors-Related Thyroid Dysfunction: Epidemiology, Clinical Presentation, Possible Pathogenesis, and Management.
Ling Zhan, Hong-Fang Feng, +4 authors, Sheng-Rong Sun.
Front Endocrinol (Lausanne), 2021 Jun 29; 12. PMID: 34177799    Free PMC article.
Systematic Review.
Construction of a five-gene prognostic model based on immune-related genes for the prediction of survival in pancreatic cancer.
Bo Liu, Tingting Fu, +2 authors, Ke Xu.
Biosci Rep, 2021 Jun 19; 41(7). PMID: 34143198    Free PMC article.
Immune checkpoint inhibitors in lymphoma: challenges and opportunities.
Haris Hatic, Devi Sampat, Gaurav Goyal.
Ann Transl Med, 2021 Jul 20; 9(12). PMID: 34277837    Free PMC article.
Heterogeneous Myeloid Cells in Tumors.
Aixia Dou, Jing Fang.
Cancers (Basel), 2021 Aug 08; 13(15). PMID: 34359674    Free PMC article.
Immune suppressive checkpoint interactions in the tumour microenvironment of primary liver cancers.
Guoying Zhou, Patrick P C Boor, +2 authors, Jaap Kwekkeboom.
Br J Cancer, 2021 Aug 18; 126(1). PMID: 34400801    Free PMC article.
Inhibitory Receptors and Immune Checkpoints Regulating Natural Killer Cell Responses to Cancer.
Irina Buckle, Camille Guillerey.
Cancers (Basel), 2021 Sep 11; 13(17). PMID: 34503073    Free PMC article.
Tumor-Infiltrating Neutrophils and Non-Classical Monocytes May Be Potential Therapeutic Targets for HER2negative Gastric Cancer.
Juhee Jeong, Duk Ki Kim, +5 authors, Keehoon Jung.
Immune Netw, 2021 Sep 16; 21(4). PMID: 34522444    Free PMC article.
Dermatologic infections in cancer patients treated with checkpoint inhibitors.
Mytrang H Do, Dulce M Barrios, +6 authors, Mario E Lacouture.
J Am Acad Dermatol, 2021 Mar 22; 85(6). PMID: 33744355    Free PMC article.
Diagnosis and Management of Immune Checkpoint Inhibitor Colitis.
Jana G Hashash, Fadi F Francis, Francis A Farraye.
Gastroenterol Hepatol (N Y), 2021 Oct 05; 17(8). PMID: 34602898    Free PMC article.
Remodeling the Tumor Myeloid Landscape to Enhance Antitumor Antibody Immunotherapies.
Khiyam Hussain, Mark S Cragg, Stephen A Beers.
Cancers (Basel), 2021 Oct 14; 13(19). PMID: 34638388    Free PMC article.
Trial watch: intratumoral immunotherapy.
Juliette Humeau, Julie Le Naour, +2 authors, Jonathan G Pol.
Oncoimmunology, 2021 Oct 23; 10(1). PMID: 34676147    Free PMC article.
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.
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.
T cell receptor (TCR) signaling in health and disease.
Kinjal Shah, Amr Al-Haidari, Jianmin Sun, Julhash U Kazi.
Signal Transduct Target Ther, 2021 Dec 14; 6(1). PMID: 34897277    Free PMC article.
Current Progress and Future Perspectives of Immune Checkpoint in Cancer and Infectious Diseases.
Xin Cai, Huajie Zhan, +4 authors, Yuan Zhuang.
Front Genet, 2021 Dec 18; 12. PMID: 34917131    Free PMC article.
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
Barriers to Immunotherapy in Ovarian Cancer: Metabolic, Genomic, and Immune Perturbations in the Tumour Microenvironment.
Racheal Louise Johnson, Michele Cummings, +3 authors, Nicolas Michel Orsi.
Cancers (Basel), 2021 Dec 25; 13(24). PMID: 34944851    Free PMC article.
Combination strategies with PD-1/PD-L1 blockade: current advances and future directions.
Ming Yi, Xiaoli Zheng, +3 authors, Kongming Wu.
Mol Cancer, 2022 Jan 23; 21(1). PMID: 35062949    Free PMC article.
T Cell Memory in Infection, Cancer, and Autoimmunity.
Vincenzo Barnaba.
Front Immunol, 2022 Jan 25; 12. PMID: 35069600    Free PMC article.
A Novel Prognostic Signature for Survival Prediction and Immune Implication Based on SARS-CoV-2-Related Genes in Kidney Renal Clear Cell Carcinoma.
Yongbiao Huang, Sheng Chen, +5 authors, Xianglin Yuan.
Front Bioeng Biotechnol, 2022 Feb 11; 9. PMID: 35141213    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
A Review of Emerging Biomarkers for Immune Checkpoint Inhibitors in Tumors of the Gastrointestinal Tract.
Xuqiang Liao, Gao Li, Renzhong Cai, Ru Chen.
Med Sci Monit, 2022 Feb 06; 28. PMID: 35121724    Free PMC article.
A decade of checkpoint blockade immunotherapy in melanoma: understanding the molecular basis for immune sensitivity and resistance.
Alexander C Huang, Roberta Zappasodi.
Nat Immunol, 2022 Mar 05; 23(5). PMID: 35241833    Free PMC article.
Addressing the Elephant in the Immunotherapy Room: Effector T-Cell Priming versus Depletion of Regulatory T-Cells by Anti-CTLA-4 Therapy.
Megan M Y Hong, Saman Maleki Vareki.
Cancers (Basel), 2022 Mar 26; 14(6). PMID: 35326731    Free PMC article.
HIF activation enhances FcγRIIb expression on mononuclear phagocytes impeding tumor targeting antibody immunotherapy.
Khiyam Hussain, Rena Liu, +28 authors, Mark S Cragg.
J Exp Clin Cancer Res, 2022 Apr 09; 41(1). PMID: 35392965    Free PMC article.
The Role of Myeloid Cells in Hepatotoxicity Related to Cancer Immunotherapy.
Cathrin L C Gudd, Lucia A Possamai.
Cancers (Basel), 2022 Apr 24; 14(8). PMID: 35454819    Free PMC article.
Exploring the Mechanisms Underlying the Cardiotoxic Effects of Immune Checkpoint Inhibitor Therapies.
Daniel Ronen, Aseel Bsoul, +4 authors, Rabea Asleh.
Vaccines (Basel), 2022 Apr 24; 10(4). PMID: 35455289    Free PMC article.
The immune checkpoint B7x expands tumor-infiltrating Tregs and promotes resistance to anti-CTLA-4 therapy.
Peter John, Marc C Pulanco, +4 authors, Xingxing Zang.
Nat Commun, 2022 May 07; 13(1). PMID: 35523809    Free PMC article.