Autoimmunity linked protein phosphatase PTPN22 as a target for cancer immunotherapy

Background Cancer immunotherapy has evolved from interferon-alpha (IFNα) and interleukin-2 in the 1980s to CTLA-4 and PD-1/PD-L1 checkpoint inhibitors (CPIs), the latter highlighting the importance of enhancing T-cell functions. While the search for novel immunomodulatory pathways continues, combina...

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Main Authors: Jeanne Cheung, Rafael Cubas, Zia Khan, Qian Gong, Marina Moskalenko, Huizhong Xiong, Qinglin Ou, Christine Pai, Ryan Rodriguez, Andrew C Chan
Format: Article
Language:English
Published: BMJ Publishing Group 2020-10-01
Series:Journal for ImmunoTherapy of Cancer
Online Access:https://jitc.bmj.com/content/8/2/e001439.full
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author Jeanne Cheung
Rafael Cubas
Zia Khan
Qian Gong
Marina Moskalenko
Huizhong Xiong
Qinglin Ou
Christine Pai
Ryan Rodriguez
Andrew C Chan
author_facet Jeanne Cheung
Rafael Cubas
Zia Khan
Qian Gong
Marina Moskalenko
Huizhong Xiong
Qinglin Ou
Christine Pai
Ryan Rodriguez
Andrew C Chan
author_sort Jeanne Cheung
collection DOAJ
description Background Cancer immunotherapy has evolved from interferon-alpha (IFNα) and interleukin-2 in the 1980s to CTLA-4 and PD-1/PD-L1 checkpoint inhibitors (CPIs), the latter highlighting the importance of enhancing T-cell functions. While the search for novel immunomodulatory pathways continues, combination therapies augmenting multiple pathways can also increase efficacy. The association of autoimmune-related adverse events with clinical efficacy following CPI treatment has been inferred and suggests that breaking tolerance thresholds associated with autoimmunity may affect host immune responses for effective cancer immunotherapy.Results Here, we show that loss of autoimmune associated PTPN22, a key desensitization node for multiple signaling pathways, including IFNα receptor (IFNAR) and T-cell receptor, can augment tumor responses. Implantation of syngeneic tumors in Ptpn22-/- mice led to expansion and activation of peripheral and intratumoral T cells and, in turn, spontaneous tumor regression as well as enhanced responses in combination with anti-PD-L1 treatment. Using genetically modified mice expressing a catalytically inactive PTPN22 or the autoimmunity-associated human single-nucleotide polymorphism variant, augmentation of antitumor immunity was dependent on PTPN22 phosphatase activity and partially on its adaptor functions. Further, antitumor responses were dependent on both CD4+ and CD8+T cells and, in part, IFNAR function. Finally, we demonstrate that the autoimmune susceptibility Ptpn22(C1858T) variant is associated with lower risk of developing non-melanoma skin cancers, improved overall survival and increased risk for development of hyperthyroidism or hypothyroidism following atezolizumab (anti-PD-L1) treatment.Conclusions Together, these data suggest that inhibition of PTPN22 phosphatase activity may provide an effective therapeutic option for cancer immunotherapy and that exploring genetic variants that shift immune tolerance thresholds may serve as a paradigm for finding new cancer immunotherapy targets.
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spelling doaj-art-32d03c95b9b246bf87576f6584fcdd1a2025-08-20T02:13:56ZengBMJ Publishing GroupJournal for ImmunoTherapy of Cancer2051-14262020-10-018210.1136/jitc-2020-001439Autoimmunity linked protein phosphatase PTPN22 as a target for cancer immunotherapyJeanne Cheung0Rafael Cubas1Zia Khan2Qian Gong3Marina Moskalenko4Huizhong Xiong5Qinglin Ou6Christine Pai7Ryan Rodriguez8Andrew C Chan9Aff1 grid.418158.10000000405344718Genentech, Inc. South San Francisco CA USA1 Department of Translational Oncology, Genentech Inc, South San Francisco, California, USA2 Department of Human Genetics, Genentech, Inc, South San Francisco, California, USA3 Department of Research- Biology, Genentech, Inc, South San Francisco, California, USA1 Department of Translational Oncology, Genentech Inc, South San Francisco, California, USA1 Department of Translational Oncology, Genentech Inc, South San Francisco, California, USA3 Department of Research- Biology, Genentech, Inc, South San Francisco, California, USA3 Department of Research- Biology, Genentech, Inc, South San Francisco, California, USADepartment of Pharmacy Practice, University of Illinois Chicago College of Pharmacy, Chicago, Illinois, USA3 Department of Research- Biology, Genentech, Inc, South San Francisco, California, USABackground Cancer immunotherapy has evolved from interferon-alpha (IFNα) and interleukin-2 in the 1980s to CTLA-4 and PD-1/PD-L1 checkpoint inhibitors (CPIs), the latter highlighting the importance of enhancing T-cell functions. While the search for novel immunomodulatory pathways continues, combination therapies augmenting multiple pathways can also increase efficacy. The association of autoimmune-related adverse events with clinical efficacy following CPI treatment has been inferred and suggests that breaking tolerance thresholds associated with autoimmunity may affect host immune responses for effective cancer immunotherapy.Results Here, we show that loss of autoimmune associated PTPN22, a key desensitization node for multiple signaling pathways, including IFNα receptor (IFNAR) and T-cell receptor, can augment tumor responses. Implantation of syngeneic tumors in Ptpn22-/- mice led to expansion and activation of peripheral and intratumoral T cells and, in turn, spontaneous tumor regression as well as enhanced responses in combination with anti-PD-L1 treatment. Using genetically modified mice expressing a catalytically inactive PTPN22 or the autoimmunity-associated human single-nucleotide polymorphism variant, augmentation of antitumor immunity was dependent on PTPN22 phosphatase activity and partially on its adaptor functions. Further, antitumor responses were dependent on both CD4+ and CD8+T cells and, in part, IFNAR function. Finally, we demonstrate that the autoimmune susceptibility Ptpn22(C1858T) variant is associated with lower risk of developing non-melanoma skin cancers, improved overall survival and increased risk for development of hyperthyroidism or hypothyroidism following atezolizumab (anti-PD-L1) treatment.Conclusions Together, these data suggest that inhibition of PTPN22 phosphatase activity may provide an effective therapeutic option for cancer immunotherapy and that exploring genetic variants that shift immune tolerance thresholds may serve as a paradigm for finding new cancer immunotherapy targets.https://jitc.bmj.com/content/8/2/e001439.full
spellingShingle Jeanne Cheung
Rafael Cubas
Zia Khan
Qian Gong
Marina Moskalenko
Huizhong Xiong
Qinglin Ou
Christine Pai
Ryan Rodriguez
Andrew C Chan
Autoimmunity linked protein phosphatase PTPN22 as a target for cancer immunotherapy
Journal for ImmunoTherapy of Cancer
title Autoimmunity linked protein phosphatase PTPN22 as a target for cancer immunotherapy
title_full Autoimmunity linked protein phosphatase PTPN22 as a target for cancer immunotherapy
title_fullStr Autoimmunity linked protein phosphatase PTPN22 as a target for cancer immunotherapy
title_full_unstemmed Autoimmunity linked protein phosphatase PTPN22 as a target for cancer immunotherapy
title_short Autoimmunity linked protein phosphatase PTPN22 as a target for cancer immunotherapy
title_sort autoimmunity linked protein phosphatase ptpn22 as a target for cancer immunotherapy
url https://jitc.bmj.com/content/8/2/e001439.full
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