Journal Article
. 2012 May; 4(134):134ra62.
doi: 10.1126/scitranslmed.3003330.

CD25 blockade depletes and selectively reprograms regulatory T cells in concert with immunotherapy in cancer patients

Andrew J Rech 1 Rosemarie Mick  Sunil Martin  Adri Recio  Nicole A Aqui  Daniel J Powell  Theresa A Colligon  Jennifer A Trosko  Leah I Leinbach  Charles H Pletcher  Carol K Tweed  Angela DeMichele  Kevin R Fox  Susan M Domchek  James L Riley  Robert H Vonderheide  
Affiliations
  • PMID: 22593175
  •     45 References
  •     133 citations

Abstract

Regulatory T cells (T(regs)) are key mediators of immune tolerance and feature prominently in cancer. Depletion of CD25(+) FoxP3(+) T(regs) in vivo may promote T cell cancer immunosurveillance, but no strategy to do so in humans while preserving immunity and preventing autoimmunity has been validated. We evaluated the Food and Drug Administration-approved CD25-blocking monoclonal antibody daclizumab with regard to human T(reg) survival and function. In vitro, daclizumab did not mediate antibody-dependent or complement-mediated cytotoxicity but rather resulted in the down-regulation of FoxP3 selectively among CD25(high) CD45RA(neg) T(regs). Moreover, daclizumab-treated CD45RA(neg) T(regs) lost suppressive function and regained the ability to produce interferon-γ, consistent with reprogramming. To understand the impact of daclizumab on T(regs) in vivo, we performed a clinical trial of daclizumab in combination with an experimental cancer vaccine in patients with metastatic breast cancer. Daclizumab administration led to a marked and prolonged decrease in T(regs) in patients. Robust CD8 and CD4 T cell priming and boosting to all vaccine antigens were observed in the absence of autoimmunity. We conclude that CD25 blockade depletes and selectively reprograms T(regs) in concert with active immune therapy in cancer patients. These results suggest a mechanism to target cancer-associated T(regs) while avoiding autoimmunity.

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Intratumoral depletion of regulatory T cells using CD25-targeted photodynamic therapy in a mouse melanoma model induces antitumoral immune responses.
Dong Sun Oh, Heegon Kim, +4 authors, Heung Kyu Lee.
Oncotarget, 2017 May 26; 8(29). PMID: 28537894    Free PMC article.
Immunotherapy for Breast Cancer: What Are We Missing?
Robert H Vonderheide, Susan M Domchek, Amy S Clark.
Clin Cancer Res, 2017 Jun 03; 23(11). PMID: 28572258    Free PMC article.
Highly Cited.
Molecular Pathways: Targeting the Microenvironment of Liver Metastases.
Simon Milette, Jason K Sicklick, Andrew M Lowy, Pnina Brodt.
Clin Cancer Res, 2017 Jun 16; 23(21). PMID: 28615370    Free PMC article.
Review.
The regulation of immune tolerance by FOXP3.
Ling Lu, Joseph Barbi, Fan Pan.
Nat Rev Immunol, 2017 Aug 02; 17(11). PMID: 28757603    Free PMC article.
Highly Cited. Review.
Negative Correlation between Circulating CD4+FOXP3+CD127- Regulatory T Cells and Subsequent Antibody Responses to Infant Measles Vaccine but Not Diphtheria-Tetanus-Pertussis Vaccine Implies a Regulatory Role.
Jorjoh Ndure, Fatou Noho-Konteh, +10 authors, Katie L Flanagan.
Front Immunol, 2017 Sep 01; 8. PMID: 28855899    Free PMC article.
CTLA-4/CD80 pathway regulates T cell infiltration into pancreatic cancer.
Fee Bengsch, Dawson M Knoblock, +2 authors, Gregory L Beatty.
Cancer Immunol Immunother, 2017 Sep 01; 66(12). PMID: 28856392    Free PMC article.
Zoledronic acid inhibits NFAT and IL-2 signaling pathways in regulatory T cells and diminishes their suppressive function in patients with metastatic cancer.
Dhifaf Sarhan, Caroline Leijonhufvud, +10 authors, Andreas Lundqvist.
Oncoimmunology, 2017 Sep 19; 6(8). PMID: 28920001    Free PMC article.
Nanomaterials for cancer immunotherapy.
Wantong Song, Sara N Musetti, Leaf Huang.
Biomaterials, 2017 Sep 30; 148. PMID: 28961532    Free PMC article.
Review.
Sox2 Communicates with Tregs Through CCL1 to Promote the Stemness Property of Breast Cancer Cells.
Yingxi Xu, Xiaoli Dong, +10 authors, Na Li.
Stem Cells, 2017 Oct 19; 35(12). PMID: 29044882    Free PMC article.
Posttraumatic Stress Disorder: An Immunological Disorder?
Zhewu Wang, Blaine Caughron, M Rita I Young.
Front Psychiatry, 2017 Nov 23; 8. PMID: 29163241    Free PMC article.
Review.
Requirement of Treg-intrinsic CTLA4/PKCη signaling pathway for suppressing tumor immunity.
Christophe Pedros, Ann J Canonigo-Balancio, Kok-Fai Kong, Amnon Altman.
JCI Insight, 2017 Dec 08; 2(23). PMID: 29212947    Free PMC article.
Inflammatory Cytokine Signaling during Development of Pancreatic and Prostate Cancers.
Geou-Yarh Liou.
J Immunol Res, 2018 Jan 31; 2017. PMID: 29379802    Free PMC article.
Review.
Regulatory T cells (Tregs): A major immune checkpoint to consider in combinatorial therapeutic HIV-1 vaccines.
Audrey Hubert, Nabila Seddiki.
Hum Vaccin Immunother, 2018 Jan 31; 14(6). PMID: 29381418    Free PMC article.
Review.
Harnessing the immune system in the battle against breast cancer.
Elizabeth S Nakasone, Sara A Hurvitz, Kelly E McCann.
Drugs Context, 2018 Feb 20; 7. PMID: 29456568    Free PMC article.
Review.
Phenotypic and Functional Properties of Tumor-Infiltrating Regulatory T Cells.
Gap Ryol Lee.
Mediators Inflamm, 2018 Feb 22; 2017. PMID: 29463952    Free PMC article.
Review.
Reinforcing the Functionality of Mononuclear Phagocyte System to Control Tuberculosis.
Susanta Pahari, Gurpreet Kaur, +7 authors, Javed N Agrewala.
Front Immunol, 2018 Feb 27; 9. PMID: 29479353    Free PMC article.
Review.
CAR T-cell therapy for glioblastoma: recent clinical advances and future challenges.
Stephen J Bagley, Arati S Desai, +2 authors, Donald M O'Rourke.
Neuro Oncol, 2018 Mar 07; 20(11). PMID: 29509936    Free PMC article.
Highly Cited. Review.
Immunotherapy for Breast Cancer: Current and Future Strategies.
Austin D Williams, Kyle K Payne, +4 authors, Julia Tchou.
Curr Surg Rep, 2018 Apr 17; 5. PMID: 29657904    Free PMC article.
Targeting EZH2 Reprograms Intratumoral Regulatory T Cells to Enhance Cancer Immunity.
David Wang, Jason Quiros, +12 authors, Michel DuPage.
Cell Rep, 2018 Jun 14; 23(11). PMID: 29898397    Free PMC article.
Highly Cited.
Spotlight on daclizumab: its potential in the treatment of multiple sclerosis.
Ron Milo, Olaf Stüve.
Degener Neurol Neuromuscul Dis, 2016 Nov 17; 6. PMID: 30050372    Free PMC article.
Review.
Treg Destabilization and Reprogramming: Implications for Cancer Immunotherapy.
David H Munn, Madhav D Sharma, Theodore S Johnson.
Cancer Res, 2018 Sep 06; 78(18). PMID: 30181177    Free PMC article.
Review.
Regulatory T cells in the treatment of disease.
Amir Sharabi, Maria G Tsokos, +3 authors, George C Tsokos.
Nat Rev Drug Discov, 2018 Oct 13; 17(11). PMID: 30310234
Highly Cited. Review.
CD25 and TGF-β blockade based on predictive integrated immune ratio inhibits tumor growth in pancreatic cancer.
Ning Pu, Guochao Zhao, +8 authors, Wenchuan Wu.
J Transl Med, 2018 Oct 26; 16(1). PMID: 30359281    Free PMC article.
Differential Roles of IL-2 Signaling in Developing versus Mature Tregs.
Martin Y Fan, Jun Siong Low, +5 authors, Laurence A Turka.
Cell Rep, 2018 Nov 01; 25(5). PMID: 30380412    Free PMC article.
Latest Advances in Targeting the Tumor Microenvironment for Tumor Suppression.
Chloé Laplagne, Marcin Domagala, +7 authors, Mary Poupot.
Int J Mol Sci, 2019 Sep 25; 20(19). PMID: 31547627    Free PMC article.
Review.
The influence of microenvironment on tumor immunotherapy.
Jieying Zhang, Zhaopeng Shi, +2 authors, Jun Mi.
FEBS J, 2019 Aug 01; 286(21). PMID: 31365790    Free PMC article.
Review.
Immunohistochemical distribution of FOXP3+ regulatory T cells in colorectal cancer patients.
Zhi-An Ling, Li-Jie Zhang, +4 authors, Jing-Jing Zeng.
Int J Clin Exp Pathol, 2018 Apr 01; 11(4). PMID: 31938291    Free PMC article.
Cancer Immunotherapies Targeting Tumor-Associated Regulatory T Cells.
Xiaoxu Ge, Yamei Zhao, +2 authors, Lifeng Sun.
Onco Targets Ther, 2020 Jan 31; 12. PMID: 31997881    Free PMC article.
Review.
CD36-mediated metabolic adaptation supports regulatory T cell survival and function in tumors.
Haiping Wang, Fabien Franco, +17 authors, Ping-Chih Ho.
Nat Immunol, 2020 Feb 19; 21(3). PMID: 32066953    Free PMC article.
Age Correlates with Response to Anti-PD1, Reflecting Age-Related Differences in Intratumoral Effector and Regulatory T-Cell Populations.
Curtis H Kugel, Stephen M Douglass, +40 authors, Ashani T Weeraratna.
Clin Cancer Res, 2018 Jun 15; 24(21). PMID: 29898988    Free PMC article.
Highly Cited.
Depletion of regulatory T cells in tumors with an anti-CD25 immunotoxin induces CD8 T cell-mediated systemic antitumor immunity.
Masanori Onda, Kazuto Kobayashi, Ira Pastan.
Proc Natl Acad Sci U S A, 2019 Feb 15; 116(10). PMID: 30760587    Free PMC article.
Treg programming and therapeutic reprogramming in cancer.
Mariela A Moreno Ayala, Zehui Li, Michel DuPage.
Immunology, 2019 Mar 14; 157(3). PMID: 30866047    Free PMC article.
Review.
Novel therapeutic strategies and perspectives for metastatic pancreatic cancer: vaccine therapy is more than just a theory.
Wenhao Luo, Gang Yang, +8 authors, Taiping Zhang.
Cancer Cell Int, 2020 Mar 12; 20. PMID: 32158356    Free PMC article.
Review.
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.
Blocking inflammation to improve immunotherapy of advanced cancer.
Antonio Macciò, Clelia Madeddu.
Immunology, 2019 Dec 11; 159(4). PMID: 31821533    Free PMC article.
Review.
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.
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.
Hypoxia as a barrier to immunotherapy in pancreatic adenocarcinoma.
S K Daniel, K M Sullivan, K P Labadie, V G Pillarisetty.
Clin Transl Med, 2019 Apr 02; 8(1). PMID: 30931508    Free PMC article.
Highly Cited. Review.
Immune Evasion by Head and Neck Cancer: Foundations for Combination Therapy.
Joshua D Horton, Hannah M Knochelmann, +2 authors, David M Neskey.
Trends Cancer, 2019 Apr 10; 5(4). PMID: 30961829    Free PMC article.
Review.
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.
Review.
Therapeutic Strategies for Overcoming Immunotherapy Resistance Mediated by Immunosuppressive Factors of the Glioblastoma Microenvironment.
Tsubasa Miyazaki, Eiichi Ishikawa, Narushi Sugii, Masahide Matsuda.
Cancers (Basel), 2020 Jul 28; 12(7). PMID: 32707672    Free PMC article.
Review.
Daclizumab: Mechanisms of Action, Therapeutic Efficacy, Adverse Events and Its Uncovering the Potential Role of Innate Immune System Recruitment as a Treatment Strategy for Relapsing Multiple Sclerosis.
Stanley L Cohan, Elisabeth B Lucassen, Meghan C Romba, Stefanie N Linch.
Biomedicines, 2019 Mar 14; 7(1). PMID: 30862055    Free PMC article.
Review.
Depleting T regulatory cells by targeting intracellular Foxp3 with a TCR mimic antibody.
Tao Dao, Sung Soo Mun, +11 authors, David A Scheinberg.
Oncoimmunology, 2019 May 31; 8(7). PMID: 31143508    Free PMC article.
Tumor Infiltrating Regulatory T Cells in Sporadic and Colitis-Associated Colorectal Cancer: The Red Little Riding Hood and the Wolf.
Massimo Claudio Fantini, Agnese Favale, Sara Onali, Federica Facciotti.
Int J Mol Sci, 2020 Sep 18; 21(18). PMID: 32937953    Free PMC article.
Review.
The Role of the Tumor Microenvironment in Developing Successful Therapeutic and Secondary Prophylactic Breast Cancer Vaccines.
Benjamin Gordon, Vijayakrishna K Gadi.
Vaccines (Basel), 2020 Sep 18; 8(3). PMID: 32937885    Free PMC article.
Review.
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.
Review.
Reprogramming the Tumor Microenvironment to Improve Immunotherapy: Emerging Strategies and Combination Therapies.
Meenal Datta, Lisa M Coussens, +2 authors, Rakesh K Jain.
Am Soc Clin Oncol Educ Book, 2019 May 18; 39. PMID: 31099649    Free PMC article.
Review.
Metaplastic breast cancers frequently express immune checkpoint markers FOXP3 and PD-L1.
Emarene Kalaw, Malcolm Lim, +21 authors, Amy E McCart Reed.
Br J Cancer, 2020 Sep 18; 123(11). PMID: 32939056    Free PMC article.
Modulating the Crosstalk between the Tumor and the Microenvironment Using SiRNA: A Flexible Strategy for Breast Cancer Treatment.
Giuseppina Roscigno, Iolanda Scognamiglio, +4 authors, Gerolama Condorelli.
Cancers (Basel), 2020 Dec 17; 12(12). PMID: 33322132    Free PMC article.
Review.
Emerging immunotherapies for metastasis.
Sarah C Edwards, Wilma H M Hoevenaar, Seth B Coffelt.
Br J Cancer, 2020 Dec 03; 124(1). PMID: 33262520    Free PMC article.
Review.
Regulation of Treg Functions by the Ubiquitin Pathway.
Elena Montauti, Deyu Fang.
Adv Exp Med Biol, 2021 Feb 02; 1278. PMID: 33523442
Therapeutic depletion of CCR8+ tumor-infiltrating regulatory T cells elicits antitumor immunity and synergizes with anti-PD-1 therapy.
Helena Van Damme, Bruno Dombrecht, +26 authors, Jo Agnes Van Ginderachter.
J Immunother Cancer, 2021 Feb 17; 9(2). PMID: 33589525    Free PMC article.
Investigating T Cell Immunity in Cancer: Achievements and Prospects.
Zhen Zeng, Hui Yi Chew, +2 authors, James W Wells.
Int J Mol Sci, 2021 Apr 04; 22(6). PMID: 33809369    Free PMC article.
Review.
Blockade of TNFR2 signaling enhances the immunotherapeutic effect of CpG ODN in a mouse model of colon cancer.
Yingjie Nie, Jiang He, +5 authors, Xin Chen.
Sci Signal, 2018 Jan 04; 11(511). PMID: 29295954    Free PMC article.
Hyperprogressive Disease: Main Features and Key Controversies.
Hugo Arasanz, Miren Zuazo, +15 authors, Ruth Vera.
Int J Mol Sci, 2021 May 01; 22(7). PMID: 33916696    Free PMC article.
Review.
Reprogramming Immune Cells for Enhanced Cancer Immunotherapy: Targets and Strategies.
Yan Dong, Zhuo Wan, +2 authors, Li Liu.
Front Immunol, 2021 May 11; 12. PMID: 33968014    Free PMC article.
Review.
IL-21 Is an Accomplice of PD-L1 in the Induction of PD-1-Dependent Treg Generation in Head and Neck Cancer.
Yi Zhao, Zhiyu Zhang, +11 authors, Wei Sun.
Front Oncol, 2021 May 25; 11. PMID: 34026621    Free PMC article.
A Novel CAR Expressing NK Cell Targeting CD25 With the Prospect of Overcoming Immune Escape Mechanism in Cancers.
Moein Dehbashi, Zohreh Hojati, +5 authors, Mazdak Ganjalikhani-Hakemi.
Front Oncol, 2021 Jun 01; 11. PMID: 34055618    Free PMC article.
Therapeutic Targets and Tumor Microenvironment in Colorectal Cancer.
Gaetano Gallo, Giuseppina Vescio, Gilda De Paola, Giuseppe Sammarco.
J Clin Med, 2021 Jun 03; 10(11). PMID: 34070480    Free PMC article.
Review.
TRP Channels Interactome as a Novel Therapeutic Target in Breast Cancer.
María Paz Saldías, Diego Maureira, +6 authors, Oscar Cerda.
Front Oncol, 2021 Jun 29; 11. PMID: 34178620    Free PMC article.
Systematic Review.
Phase 1 study of safety, tolerability and immunogenicity of the human telomerase (hTERT)-encoded DNA plasmids INO-1400 and INO-1401 with or without IL-12 DNA plasmid INO-9012 in adult patients with solid tumors.
Robert H Vonderheide, Kimberly A Kraynyak, +14 authors, Jeffrey M Skolnik.
J Immunother Cancer, 2021 Jul 08; 9(7). PMID: 34230114    Free PMC article.
Immunopeptidomics-Guided Warehouse Design for Peptide-Based Immunotherapy in Chronic Lymphocytic Leukemia.
Annika Nelde, Yacine Maringer, +11 authors, Juliane S Walz.
Front Immunol, 2021 Jul 27; 12. PMID: 34305947    Free PMC article.
Mogamulizumab in Combination with Durvalumab or Tremelimumab in Patients with Advanced Solid Tumors: A Phase I Study.
Dmitriy Zamarin, Omid Hamid, +6 authors, David S Hong.
Clin Cancer Res, 2020 Jun 27; 26(17). PMID: 32586937    Free PMC article.
Prognostic and therapeutic role of tumor-infiltrating lymphocyte subtypes in breast cancer.
Molly A Nelson, Worapol Ngamcherdtrakul, Shiuh-Wen Luoh, Wassana Yantasee.
Cancer Metastasis Rev, 2021 May 09; 40(2). PMID: 33963482    Free PMC article.
Review.
Regulatory T Cells in Autoimmunity and Cancer: A Duplicitous Lifestyle.
Aikaterini Hatzioannou, Athina Boumpas, +4 authors, Panayotis Verginis.
Front Immunol, 2021 Sep 21; 12. PMID: 34539668    Free PMC article.
Review.
The Multifaceted Role of Regulatory T Cells in Breast Cancer.
Kevin Kos, Karin E de Visser.
Annu Rev Cancer Biol, 2021 Oct 12; 5. PMID: 34632244    Free PMC article.
The Breast Tumor Microenvironment: A Key Player in Metastatic Spread.
Lucas E L Terceiro, Chidalu A Edechi, +5 authors, Yvonne Myal.
Cancers (Basel), 2021 Oct 14; 13(19). PMID: 34638283    Free PMC article.
Review.
Cell-Based Regeneration and Treatment of Liver Diseases.
Julia Hofmann, Verena Hackl, +6 authors, Theresa Hautz.
Int J Mol Sci, 2021 Oct 14; 22(19). PMID: 34638617    Free PMC article.
Review.
Connecting blood and intratumoral Treg cell activity in predicting future relapse in breast cancer.
Lei Wang, Diana L Simons, +9 authors, Peter P Lee.
Nat Immunol, 2019 Jul 10; 20(9). PMID: 31285626    Free PMC article.
Highly Cited.
Functional Diversities of Regulatory T Cells in the Context of Cancer Immunotherapy.
Ran Gao, Guo-Ping Shi, Jing Wang.
Front Immunol, 2022 Apr 05; 13. PMID: 35371055    Free PMC article.
Review.
Tumor-Associated Regulatory T Cells in Non-Small-Cell Lung Cancer: Current Advances and Future Perspectives.
Jiaqi Liang, Guoshu Bi, +3 authors, Qun Wang.
J Immunol Res, 2022 May 03; 2022. PMID: 35497874    Free PMC article.
Review.