. 2019 Sep;19(3).
doi: 10.1038/s41573-019-0038-z.

Translating gammadelta (γδ) T cells and their receptors into cancer cell therapies

Zsolt Sebestyen 1 Immo Prinz 2 Julie Déchanet-Merville 3 Bruno Silva-Santos 4 Jurgen Kuball 5 
  • PMID: 31492944
  •     165 References
  •     49 citations


Clinical responses to checkpoint inhibitors used for cancer immunotherapy seemingly require the presence of αβT cells that recognize tumour neoantigens, and are therefore primarily restricted to tumours with high mutational load. Approaches that could address this limitation by engineering αβT cells, such as chimeric antigen receptor T (CAR T) cells, are being investigated intensively, but these approaches have other issues, such as a scarcity of appropriate targets for CAR T cells in solid tumours. Consequently, there is renewed interest among translational researchers and commercial partners in the therapeutic use of γδT cells and their receptors. Overall, γδT cells display potent cytotoxicity, which usually does not depend on tumour-associated (neo)antigens, towards a large array of haematological and solid tumours, while preserving normal tissues. However, the precise mechanisms of tumour-specific γδT cells, as well as the mechanisms for self-recognition, remain poorly understood. In this Review, we discuss the challenges and opportunities for the clinical implementation of cancer immunotherapies based on γδT cells and their receptors.

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J Immunol, 2014 Feb 04; 192(5). PMID: 24489097
Heterogeneous yet stable Vδ2(+) T-cell profiles define distinct cytotoxic effector potentials in healthy human individuals.
Paul L Ryan, Nital Sumaria, +6 authors, Daniel J Pennington.
Proc Natl Acad Sci U S A, 2016 Dec 03; 113(50). PMID: 27911793    Free PMC article.
γδ T Cells Support Pancreatic Oncogenesis by Restraining αβ T Cell Activation.
Donnele Daley, Constantinos Pantelis Zambirinis, +17 authors, George Miller.
Cell, 2016 Aug 30; 166(6). PMID: 27569912    Free PMC article.
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Tumor-Infiltrating γδ T Lymphocytes: Pathogenic Role, Clinical Significance, and Differential Programing in the Tumor Microenvironment.
Elena Lo Presti, Franceso Dieli, Serena Meraviglia.
Front Immunol, 2014 Dec 17; 5. PMID: 25505472    Free PMC article.
γδ T Cells: Unexpected Regulators of Cancer Development and Progression.
Christopher Fleming, Samantha Morrissey, Yihua Cai, Jun Yan.
Trends Cancer, 2017 Aug 07; 3(8). PMID: 28780933    Free PMC article.
Murine CD27(-) Vγ6(+) γδ T cells producing IL-17A promote ovarian cancer growth via mobilization of protumor small peritoneal macrophages.
Margarida Rei, Natacha Gonçalves-Sousa, +6 authors, Bruno Silva-Santos.
Proc Natl Acad Sci U S A, 2014 Aug 13; 111(34). PMID: 25114209    Free PMC article.
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Tumor-infiltrating IL-17-producing gammadelta T cells support the progression of tumor by promoting angiogenesis.
Daiko Wakita, Kentaro Sumida, +5 authors, Takashi Nishimura.
Eur J Immunol, 2010 Apr 17; 40(7). PMID: 20397212
Identification of a tumor-specific allo-HLA-restricted γδTCR.
G J J Kierkels, W Scheper, +23 authors, J Kuball.
Blood Adv, 2019 Oct 06; 3(19). PMID: 31585951    Free PMC article.
TEG001 Insert Integrity from Vector Producer Cells until Medicinal Product.
Trudy Straetemans, Anke Janssen, +8 authors, Jurgen Kuball.
Mol Ther, 2019 Dec 29; 28(2). PMID: 31882320    Free PMC article.
Mechanisms of Leukemia Immune Evasion and Their Role in Relapse After Haploidentical Hematopoietic Cell Transplantation.
Pier Edoardo Rovatti, Valentina Gambacorta, +2 authors, Luca Vago.
Front Immunol, 2020 Mar 12; 11. PMID: 32158444    Free PMC article.
ABCA1/ABCB1 Ratio Determines Chemo- and Immune-Sensitivity in Human Osteosarcoma.
Dimas Carolina Belisario, Muhlis Akman, +9 authors, Chiara Riganti.
Cells, 2020 Mar 12; 9(3). PMID: 32155954    Free PMC article.
Immunosuppressant indulges EBV reactivation and related lymphoproliferative disease by inhibiting Vδ2+ T cells activities after hematopoietic transplantation for blood malignancies.
Jiangying Liu, Haitao Gao, +10 authors, Xiao-Jun Huang.
J Immunother Cancer, 2020 Mar 30; 8(1). PMID: 32221014    Free PMC article.
Targeting Cancer Stem Cells by Genetically Engineered Chimeric Antigen Receptor T Cells.
Rowa Y Alhabbab.
Front Genet, 2020 May 12; 11. PMID: 32391048    Free PMC article.
Recent advances in understanding the development and function of γδ T cells.
Alejandra V Contreras, David L Wiest.
F1000Res, 2020 May 14; 9. PMID: 32399190    Free PMC article.
Challenges for Immunotherapy in Multiple Myeloma: Bone Marrow Microenvironment-Mediated Immune Suppression and Immune Resistance.
Lisa C Holthof, Tuna Mutis.
Cancers (Basel), 2020 Apr 23; 12(4). PMID: 32316450    Free PMC article.
Electroporation of NKG2D RNA CAR Improves Vγ9Vδ2 T Cell Responses against Human Solid Tumor Xenografts.
Wei Xia Ang, Yu Yang Ng, +8 authors, Shu Wang.
Mol Ther Oncolytics, 2020 May 29; 17. PMID: 32462079    Free PMC article.
Signaling from T cell receptors (TCRs) and chimeric antigen receptors (CARs) on T cells.
Ling Wu, Qianru Wei, Joanna Brzostek, Nicholas R J Gascoigne.
Cell Mol Immunol, 2020 May 27; 17(6). PMID: 32451454    Free PMC article.
Emerging Challenges of Preclinical Models of Anti-tumor Immunotherapeutic Strategies Utilizing Vγ9Vδ2 T Cells.
Noémie Joalland, Emmanuel Scotet.
Front Immunol, 2020 Jun 13; 11. PMID: 32528477    Free PMC article.
The Role of Human γδ T Cells in Anti-Tumor Immunity and Their Potential for Cancer Immunotherapy.
Yuxia Liu, Cai Zhang.
Cells, 2020 May 18; 9(5). PMID: 32413966    Free PMC article.
Immune Signatures and Survival of Patients With Metastatic Melanoma, Renal Cancer, and Breast Cancer.
Kilian Wistuba-Hamprecht, Cécile Gouttefangeas, Benjamin Weide, Graham Pawelec.
Front Immunol, 2020 Jun 26; 11. PMID: 32582215    Free PMC article.
Mistletoe-Extract Drugs Stimulate Anti-Cancer Vγ9Vδ2 T Cells.
Ling Ma, Swati Phalke, +2 authors, David Vermijlen.
Cells, 2020 Jul 02; 9(6). PMID: 32604868    Free PMC article.
γ9δ2T cell diversity and the receptor interface with tumor cells.
Anna Vyborova, Dennis X Beringer, +19 authors, Jürgen Kuball.
J Clin Invest, 2020 Jun 03; 130(9). PMID: 32484803    Free PMC article.
Engineering the Bridge between Innate and Adaptive Immunity for Cancer Immunotherapy: Focus on γδ T and NK Cells.
Fabio Morandi, Mahboubeh Yazdanifar, +2 authors, Irma Airoldi.
Cells, 2020 Jul 28; 9(8). PMID: 32707982    Free PMC article.
Structure-Activity Relationships of Butyrophilin 3 Ligands.
Andrew J Wiemer.
ChemMedChem, 2020 May 27; 15(12). PMID: 32453919    Free PMC article.
Expansion With IL-15 Increases Cytotoxicity of Vγ9Vδ2 T Cells and Is Associated With Higher Levels of Cytotoxic Molecules and T-bet.
Pia Aehnlich, Ana Micaela Carnaz Simões, +2 authors, Per Thor Straten.
Front Immunol, 2020 Sep 29; 11. PMID: 32983105    Free PMC article.
Adoptive transfer of zoledronate-expanded autologous Vγ9Vδ2 T-cells in patients with treatment-refractory non-small-cell lung cancer: a multicenter, open-label, single-arm, phase 2 study.
Kazuhiro Kakimi, Hirokazu Matsushita, +17 authors, Jun Nakajima.
J Immunother Cancer, 2020 Sep 20; 8(2). PMID: 32948652    Free PMC article.
Nano-Enhanced Cancer Immunotherapy: Immunology Encounters Nanotechnology.
Ernesto Bockamp, Sebastian Rosigkeit, Dominik Siegl, Detlef Schuppan.
Cells, 2020 Sep 19; 9(9). PMID: 32942725    Free PMC article.
Aiming for the Sweet Spot: Glyco-Immune Checkpoints and γδ T Cells in Targeted Immunotherapy.
Margarita Bartish, Sonia V Del Rincón, Christopher E Rudd, H Uri Saragovi.
Front Immunol, 2020 Nov 03; 11. PMID: 33133075    Free PMC article.
Cancer immunotherapy with γδ T cells: many paths ahead of us.
Dieter Kabelitz, Ruben Serrano, +2 authors, Shirin Kalyan.
Cell Mol Immunol, 2020 Jul 24; 17(9). PMID: 32699351    Free PMC article.
Ligand recognition by the γδ TCR and discrimination between homeostasis and stress conditions.
Malte Deseke, Immo Prinz.
Cell Mol Immunol, 2020 Jul 28; 17(9). PMID: 32709926    Free PMC article.
TEG011 persistence averts extramedullary tumor growth without exerting off-target toxicity against healthy tissues in a humanized HLA-A*24:02 transgenic mice.
Inez Johanna, Patricia Hernández-López, +9 authors, Jürgen Kuball.
J Leukoc Biol, 2020 Feb 06; 107(6). PMID: 32022317    Free PMC article.
Off-the-Shelf Allogeneic T Cell Therapies for Cancer: Opportunities and Challenges Using Naturally Occurring "Universal" Donor T Cells.
Cynthia Perez, Isabelle Gruber, Caroline Arber.
Front Immunol, 2020 Dec 03; 11. PMID: 33262761    Free PMC article.
Editorial: γδ T Cells in Cancer.
Seth B Coffelt, Dieter Kabelitz, +3 authors, Ilan Bank.
Front Immunol, 2020 Dec 18; 11. PMID: 33329597    Free PMC article.
Single-cell RNA sequencing of human breast tumour-infiltrating immune cells reveals a γδ T-cell subtype associated with good clinical outcome.
Katerina Boufea, Víctor González-Huici, +3 authors, Nizar N Batada.
Life Sci Alliance, 2020 Dec 04; 4(1). PMID: 33268347    Free PMC article.
Comparable Vδ2 Cell Functional Characteristics in Virally Suppressed People Living with HIV and Uninfected Individuals.
Matthew L Clohosey, Brendan T Mann, +4 authors, Natalia Soriano-Sarabia.
Cells, 2020 Dec 05; 9(12). PMID: 33271808    Free PMC article.
From thymus to periphery: Molecular basis of effector γδ-T cell differentiation.
Gina J Fiala, Anita Q Gomes, Bruno Silva-Santos.
Immunol Rev, 2020 Nov 17; 298(1). PMID: 33191519    Free PMC article.
Immunobiology and immunotherapy of HCC: spotlight on innate and innate-like immune cells.
Benjamin Ruf, Bernd Heinrich, Tim F Greten.
Cell Mol Immunol, 2020 Nov 26; 18(1). PMID: 33235387    Free PMC article.
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.
Distinct metabolic programs established in the thymus control effector functions of γδ T cell subsets in tumor microenvironments.
Noella Lopes, Claire McIntyre, +19 authors, Lydia Lynch.
Nat Immunol, 2021 Jan 20; 22(2). PMID: 33462452    Free PMC article.
Allogeneic Vγ9Vδ2 T-cell immunotherapy exhibits promising clinical safety and prolongs the survival of patients with late-stage lung or liver cancer.
Yan Xu, Zheng Xiang, +24 authors, Zhinan Yin.
Cell Mol Immunol, 2020 Sep 18; 18(2). PMID: 32939032    Free PMC article.
Functional and metabolic dichotomy of murine γδ T cell subsets in cancer immunity.
Noëlla Lopes, Bruno Silva-Santos.
Eur J Immunol, 2020 Nov 15; 51(1). PMID: 33188652    Free PMC article.
The BTLA and PD-1 signaling pathways independently regulate the proliferation and cytotoxicity of human peripheral blood γδ T cells.
Hyun J Hwang, Jae J Lee, +7 authors, Nayoung Kim.
Immun Inflamm Dis, 2020 Dec 18; 9(1). PMID: 33332777    Free PMC article.
Chimeric Antigen Receptor beyond CAR-T Cells.
Vicky Mengfei Qin, Criselle D'Souza, Paul J Neeson, Joe Jiang Zhu.
Cancers (Basel), 2021 Jan 28; 13(3). PMID: 33499101    Free PMC article.
Brain Tumor Microenvironment and Angiogenesis in Melanoma Brain Metastases.
Dimitri G Trembath, Eric S Davis, +15 authors, Stergios J Moschos.
Front Oncol, 2021 Feb 09; 10. PMID: 33552976    Free PMC article.
αβ T-cell graft depletion for allogeneic HSCT in adults with hematological malignancies.
Moniek A de Witte, Anke Janssen, +13 authors, Jürgen Kuball.
Blood Adv, 2021 Feb 12; 5(1). PMID: 33570642    Free PMC article.
Vγ9Vδ2 T cells strengthen cisplatin inhibition activity against breast cancer MDA-MB-231 cells by disrupting mitochondrial function and cell ultrastructure.
Xin Huang, Cunchuan Wang, Ningxia Wang.
Cancer Cell Int, 2021 Feb 18; 21(1). PMID: 33593340    Free PMC article.
Adoptive cell therapy of patient-derived renal cell carcinoma xenograft model with IL-15-induced γδT cells.
Baofu Zhang, Huizhong Li, +4 authors, Junnian Zheng.
Med Oncol, 2021 Feb 19; 38(3). PMID: 33598783
Phase II Trial of Maintenance Treatment With IL2 and Zoledronate in Multiple Myeloma After Bone Marrow Transplantation: Biological and Clinical Results.
Rita Fazzi, Iacopo Petrini, +6 authors, Gabriele Buda.
Front Immunol, 2021 Feb 23; 11. PMID: 33613510    Free PMC article.
Taking T-Cell Oncotherapy Off-the-Shelf.
Feiyan Mo, Maksim Mamonkin, Malcolm K Brenner, Helen E Heslop.
Trends Immunol, 2021 Feb 05; 42(3). PMID: 33536140    Free PMC article.
The Dual Roles of Human γδ T Cells: Anti-Tumor or Tumor-Promoting.
Yang Li, Gen Li, +2 authors, Xi Chen.
Front Immunol, 2021 Mar 06; 11. PMID: 33664732    Free PMC article.
An Unconventional View of T Cell Reconstitution After Allogeneic Hematopoietic Cell Transplantation.
Hana Andrlová, Marcel R M van den Brink, Kate A Markey.
Front Oncol, 2021 Mar 09; 10. PMID: 33680931    Free PMC article.
Function of γδ T cells in tumor immunology and their application to cancer therapy.
Jang Hyun Park, Heung Kyu Lee.
Exp Mol Med, 2021 Mar 13; 53(3). PMID: 33707742
γδ T cells in tissue physiology and surveillance.
Julie C Ribot, Noëlla Lopes, Bruno Silva-Santos.
Nat Rev Immunol, 2020 Oct 16; 21(4). PMID: 33057185
Cellular Immunotherapy Targeting Cancer Stem Cells: Preclinical Evidence and Clinical Perspective.
Chiara Donini, Ramona Rotolo, +3 authors, Valeria Leuci.
Cells, 2021 Apr 04; 10(3). PMID: 33806296    Free PMC article.
Epigenetic modulation of immune synaptic-cytoskeletal networks potentiates γδ T cell-mediated cytotoxicity in lung cancer.
Rueyhung R Weng, Hsuan-Hsuan Lu, +17 authors, Hsing-Chen Tsai.
Nat Commun, 2021 Apr 14; 12(1). PMID: 33846331
γδ T Cells Participating in Nervous Systems: A Story of Jekyll and Hyde.
Yunxuan Li, Yixi Zhang, Xun Zeng.
Front Immunol, 2021 Apr 20; 12. PMID: 33868300    Free PMC article.