Review
. 2020 Jan; 11:10731-10747.
doi: 10.2147/CMAR.S228887.

T-Regulatory Cells In Tumor Progression And Therapy

Amit Verma 1 Rohit Mathur 2 Abdullah Farooque 3 Vandana Kaul 4 Seema Gupta 5 Bilikere S Dwarakanath 6 
Affiliations
  • PMID: 31920383
  •     174 References
  •     16 citations

Abstract

Regulatory T cells (Tregs) are important members of the immune system regulating the host responses to infection and neoplasms. Tregs prevent autoimmune disorders by protecting the host-cells from an immune response, related to the peripheral tolerance. However, tumor cells use Tregs as a shield to protect themselves against anti-tumor immune response. Thus, Tregs are a hurdle in achieving the complete potential of anti-cancer therapies including immunotherapy. This has prompted the development of novel adjuvant therapies that obviate their negative effects thereby enhancing the therapeutic efficacy. Our earlier studies have shown the efficacy of the glycolytic inhibitor, 2-deoxy-D-glucose (2-DG) by reducing the induced Tregs pool and enhance immune stimulation as well as local tumor control. These findings have suggested its potential for enhancing the efficacy of immunotherapy, besides radiotherapy and chemotherapy. This review provides a brief account of the current status of Tregs as a component of the immune-biology of tumors and various preclinical and clinical strategies pursued to obviate the limitations imposed by them in achieving therapeutic efficacy.

Keywords: 2-deoxy-D-glucose; T-regulatory cells; cyclophosphamide; dendritic cells; immune enhancement; metabolic inhibitor; targeted cancer therapy.

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Turning the Tide Against Regulatory T Cells.
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J Immunol, 2004 Dec 22; 174(1). PMID: 15611231
Estrogen-mediated immunomodulation involves reduced activation of effector T cells, potentiation of Treg cells, and enhanced expression of the PD-1 costimulatory pathway.
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Administration of a CD25-directed immunotoxin, LMB-2, to patients with metastatic melanoma induces a selective partial reduction in regulatory T cells in vivo.
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J Immunol, 2007 Sep 20; 179(7). PMID: 17878392    Free PMC article.
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Roles of regulatory T cells in cancer immunity.
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Enhancement of anti-tumor immunity through local modulation of CTLA-4 and GITR by dendritic cells.
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CD25+ cell depletion hastens the onset of severe disease in collagen-induced arthritis.
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Enhancing immunotherapy using chemotherapy and radiation to modify the tumor microenvironment.
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Optimization of tumour radiotherapy: Part V--Radiosensitization by 2-deoxy-D-glucose and DNA ligand Hoechst-33342 in a murine tumour.
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Increased regulatory versus effector T cell development is associated with thymus atrophy in mouse models of multiple myeloma.
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J Immunol, 2004 Jun 10; 172(12). PMID: 15187106
PD-1+ regulatory T cells amplified by PD-1 blockade promote hyperprogression of cancer.
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CD4+CD25+ regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of established tumors to be curative.
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Eur J Immunol, 2004 Feb 10; 34(2). PMID: 14768038
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Alterations in radiation induced cell cycle perturbations by 2-deoxy-D-glucose in human tumor cell lines.
J S Adhikari, B S Dwarakanath, Rohit Mathur, T Ravindranath.
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T regulatory type 1 cells in squamous cell carcinoma of the head and neck: mechanisms of suppression and expansion in advanced disease.
Christoph Bergmann, Laura Strauss, +4 authors, Theresa L Whiteside.
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OX40 triggering blocks suppression by regulatory T cells and facilitates tumor rejection.
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J Exp Med, 2008 Mar 26; 205(4). PMID: 18362171    Free PMC article.
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PD-L1 regulates the development, maintenance, and function of induced regulatory T cells.
Loise M Francisco, Victor H Salinas, +4 authors, Arlene H Sharpe.
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Prevalence of regulatory T cells is increased in peripheral blood and tumor microenvironment of patients with pancreas or breast adenocarcinoma.
Udaya K Liyanage, Todd T Moore, +8 authors, David C Linehan.
J Immunol, 2002 Aug 24; 169(5). PMID: 12193750
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Radiation enhances regulatory T cell representation.
Evelyn L Kachikwu, Keisuke S Iwamoto, +5 authors, Dörthe Schaue.
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The infusion of ex vivo activated and expanded CD4(+)CD25(+) immune regulatory cells inhibits graft-versus-host disease lethality.
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Blood, 2002 May 03; 99(10). PMID: 11986199
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Immunologic self-tolerance maintained by CD25(+)CD4(+) regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4.
T Takahashi, T Tagami, +5 authors, S Sakaguchi.
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Different mechanisms for anti-tumor effects of low- and high-dose cyclophosphamide.
Yasuhide Motoyoshi, Kazuhisa Kaminoda, +5 authors, Katsumi Eguchi.
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Immunity and immune suppression in human ovarian cancer.
Claudia C Preston, Ellen L Goode, +2 authors, Keith L Knutson.
Immunotherapy, 2011 Apr 06; 3(4). PMID: 21463194    Free PMC article.
Immunosuppressive regulatory T cells are abundant in the reactive lymphocytes of Hodgkin lymphoma.
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Blood, 2003 Nov 08; 103(5). PMID: 14604957
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Treg depletion inhibits efficacy of cancer immunotherapy: implications for clinical trials.
James F Curtin, Marianela Candolfi, +5 authors, Maria G Castro.
PLoS One, 2008 Apr 24; 3(4). PMID: 18431473    Free PMC article.
Surface-bound TGF-beta1 on effusion-derived exosomes participates in maintenance of number and suppressive function of regulatory T-cells in malignant effusions.
Junji Wada, Hideya Onishi, +4 authors, Mitsuo Katano.
Anticancer Res, 2010 Oct 15; 30(9). PMID: 20944164
Regulatory T cells: a potential target in cancer immunotherapy.
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The effect of ionizing radiation on regulatory T cells in health and disease.
Eszter Persa, Andrea Balogh, Géza Sáfrány, Katalin Lumniczky.
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Monoclonal antibody blockade of IL-2 receptor α during lymphopenia selectively depletes regulatory T cells in mice and humans.
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Advanced stage melanoma therapies: Detailing the present and exploring the future.
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Enhancement of radiation and chemotherapeutic drug responses by 2-deoxy-D-glucose in animal tumors.
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J Cancer Res Ther, 2009 Dec 17; 5 Suppl 1. PMID: 20009287
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Low-dose cyclophosphamide treatment impairs regulatory T cells and unmasks AFP-specific CD4+ T-cell responses in patients with advanced HCC.
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CD8+ T cell immunity against a tumor/self-antigen is augmented by CD4+ T helper cells and hindered by naturally occurring T regulatory cells.
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Concomitant tumor immunity to a poorly immunogenic melanoma is prevented by regulatory T cells.
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Targeting the PD-1/B7-H1(PD-L1) pathway to activate anti-tumor immunity.
Suzanne L Topalian, Charles G Drake, Drew M Pardoll.
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T regulatory cells in allergy: novel concepts in the pathogenesis, prevention, and treatment of allergic diseases.
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J Allergy Clin Immunol, 2005 Nov 09; 116(5). PMID: 16275361
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Chemo-immunotherapy of metastatic colorectal carcinoma with gemcitabine plus FOLFOX 4 followed by subcutaneous granulocyte macrophage colony-stimulating factor and interleukin-2 induces strong immunologic and antitumor activity in metastatic colon cancer patients.
Pierpaolo Correale, Maria Grazia Cusi, +11 authors, Guido Francini.
J Clin Oncol, 2005 Aug 03; 23(35). PMID: 16061910
CD4(+)CD25(+) immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor.
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Regulatory T cells: Folate receptor 4: a new handle on regulation and memory?
Lucy S K Walker.
Immunol Cell Biol, 2007 Aug 22; 85(7). PMID: 17710105
Enhancement of antitumor immunity by CTLA-4 blockade.
D R Leach, M F Krummel, J P Allison.
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Phase I/II trial of tremelimumab in patients with metastatic melanoma.
Luis H Camacho, Scott Antonia, +8 authors, Antoni Ribas.
J Clin Oncol, 2009 Jan 14; 27(7). PMID: 19139427
Radiation Dose Escalation is Crucial in Anti-CTLA-4 Antibody Therapy to Enhance Local and Distant Antitumor Effect in Murine Osteosarcoma.
Wataru Takenaka, Yutaka Takahashi, +6 authors, Kazuhiko Ogawa.
Cancers (Basel), 2020 Jun 18; 12(6). PMID: 32545427    Free PMC article.
Resisting Resistance to Immune Checkpoint Therapy: A Systematic Review.
Yolla Haibe, Ziad El Husseini, Rola El Sayed, Ali Shamseddine.
Int J Mol Sci, 2020 Sep 02; 21(17). PMID: 32867025    Free PMC article.
Systematic Review.
SARS-CoV-2 cell receptor gene ACE2 -mediated immunomodulation in breast cancer subtypes.
Vikas Kumar Bhari, Durgesh Kumar, Surendra Kumar, Rajeev Mishra.
Biochem Biophys Rep, 2020 Nov 13; 24. PMID: 33178900    Free PMC article.
Obesity and Cancer Metastasis: Molecular and Translational Perspectives.
Stephanie Annett, Gillian Moore, Tracy Robson.
Cancers (Basel), 2020 Dec 20; 12(12). PMID: 33339340    Free PMC article.
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An overview of the tumor microenvironment, from cells to complex networks (Review).
Ovidiu Farc, Victor Cristea.
Exp Ther Med, 2020 Dec 29; 21(1). PMID: 33363607    Free PMC article.
Review.
Simultaneous targeting of primary tumor, draining lymph node, and distant metastases through high endothelial venule-targeted delivery.
Liwei Jiang, Sungwook Jung, +13 authors, Reza Abdi.
Nano Today, 2021 Jan 05; 36. PMID: 33391389    Free PMC article.
Cell by cell immuno- and cancer marker profiling of non-small cell lung cancer tissue: Checkpoint marker expression on CD103+, CD4+ T-cells predicts circulating tumor cells.
Xiaoyang Wang, Maria Jaimes, +7 authors, Bruce K Patterson.
Transl Oncol, 2020 Nov 21; 14(1). PMID: 33217647    Free PMC article.
Metabolic reprogramming of T regulatory cells in the hypoxic tumor microenvironment.
Varun Sasidharan Nair, Reem Saleh, +2 authors, Eyad Elkord.
Cancer Immunol Immunother, 2021 Feb 04; 70(8). PMID: 33532902    Free PMC article.
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Recent Advancements on Immunomodulatory Mechanisms of Resveratrol in Tumor Microenvironment.
Gagan Chhabra, Chandra K Singh, +2 authors, Nihal Ahmad.
Molecules, 2021 Apr 04; 26(5). PMID: 33802331    Free PMC article.
Review.
Radiotherapy planning parameters correlate with changes in the peripheral immune status of patients undergoing curative radiotherapy for localized prostate cancer.
Elgin Hoffmann, Frank Paulsen, +5 authors, Franziska Eckert.
Cancer Immunol Immunother, 2021 Jul 17; 71(3). PMID: 34269847    Free PMC article.
The Right Partner in Crime: Unlocking the Potential of the Anti-EGFR Antibody Cetuximab via Combination With Natural Killer Cell Chartering Immunotherapeutic Strategies.
Hasan Baysal, Ines De Pauw, +5 authors, An Wouters.
Front Immunol, 2021 Sep 25; 12. PMID: 34557197    Free PMC article.
Review.
Regulatory T-Cells and Multiple Myeloma: Implications in Tumor Immune Biology and Treatment.
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J Clin Med, 2021 Oct 14; 10(19). PMID: 34640606    Free PMC article.
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Cyclophosphamide enhances the antitumor potency of GITR engagement by increasing oligoclonal cytotoxic T cell fitness.
Daniel Hirschhorn, Allison Betof Warner, +11 authors, Jedd D Wolchok.
JCI Insight, 2021 Oct 23; 6(20). PMID: 34676831    Free PMC article.
A radioenhancing nanoparticle mediated immunoradiation improves survival and generates long-term antitumor immune memory in an anti-PD1-resistant murine lung cancer model.
Yun Hu, Sébastien Paris, +12 authors, James W Welsh.
J Nanobiotechnology, 2021 Dec 14; 19(1). PMID: 34895262    Free PMC article.
Can Immune Suppression and Epigenome Regulation in Placenta Offer Novel Insights into Cancer Immune Evasion and Immunotherapy Resistance?
Sultana Mehbuba Hossain, Chiemi F Lynch-Sutherland, +2 authors, Michael R Eccles.
Epigenomes, 2021 Dec 31; 5(3). PMID: 34968365    Free PMC article.
Review.
Naringenin and cryptotanshinone shift the immune response towards Th1 and modulate T regulatory cells via JAK2/STAT3 pathway in breast cancer.
Shokoofe Noori, Mitra Nourbakhsh, +3 authors, Zohreh Abdolvahabi.
BMC Complement Med Ther, 2022 May 24; 22(1). PMID: 35606804