Constitutive reduction in the checkpoint inhibitor, CTLA-4, does not accelerate SLE in NZM 2328 mice

Background/objective Treatment with immune checkpoint inhibitors (ICIs) in oncology patients is increasing. Although ICIs trigger rheumatic immune-related adverse events, development of SLE features has been rare. Whether long-term treatment with ICIs would promote SLE features remains unknown. To b...

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Main Authors: William Stohl, Chaim Putterman, Ning Yu, Samantha A Chalmers, Chaim O Jacob
Format: Article
Language:English
Published: BMJ Publishing Group 2019-12-01
Series:Lupus Science and Medicine
Online Access:https://lupus.bmj.com/content/6/1/e000313.full
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author William Stohl
Chaim Putterman
Ning Yu
Samantha A Chalmers
Chaim O Jacob
author_facet William Stohl
Chaim Putterman
Ning Yu
Samantha A Chalmers
Chaim O Jacob
author_sort William Stohl
collection DOAJ
description Background/objective Treatment with immune checkpoint inhibitors (ICIs) in oncology patients is increasing. Although ICIs trigger rheumatic immune-related adverse events, development of SLE features has been rare. Whether long-term treatment with ICIs would promote SLE features remains unknown. To begin to address this, we generated SLE-prone NZM 2328 mice with lifelong reduction in CTLA-4 expression.Methods Since CTLA-4-deficient (Ctla4−/−) NZM mice developed a lethal lymphoproliferative disorder by 3–6 weeks of age, development of SLE in these mice could not be studied. Ctla4 haploinsufficient NZM.Ctla4+/− mice were assessed in parallel with littermate female NZM.Ctla4+/+ mice. Evaluations included CTLA-4 expression and lymphocyte profiles, assessed by fluorescence-activated cell sorting; serological profiles, assessed by ELISA; renal immunopathology, assessed by histology and immunofluorescence; and clinical courses, assessed by mortality.Results CTLA-4 expression was lower in NZM.Ctla4+/− mice than in NZM.Ctla4+/+ mice. Spleen mononuclear cells, B cells, plasma cells, CD4+ cells, recently activated CD4+ cells and CD4+ T regulatory (Treg) cells were increased in NZM.Ctla4+/− mice (p≤0.042). The serological profile, degree of renal immunopathology and mortality in NZM.Ctla4+/− mice remained unaffected.Conclusion Lifelong reduction in CTLA-4 expression in NZM mice neither accelerated nor aggravated SLE. Expansion in Treg cells may have played a protective role. Our observations raise the hope that long-term treatment of patients with SLE with an anti-CTLA-4 agent, should the need arise, would not adversely affect SLE disease activity.
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spelling doaj-art-a1d8e02464494d6fa06e7561ad5b1ec22025-08-20T01:56:48ZengBMJ Publishing GroupLupus Science and Medicine2053-87902019-12-016110.1136/lupus-2018-000313Constitutive reduction in the checkpoint inhibitor, CTLA-4, does not accelerate SLE in NZM 2328 miceWilliam Stohl0Chaim Putterman1Ning Yu2Samantha A Chalmers3Chaim O Jacob46 University of Southern California Keck School of Medicine, Los Angeles, California, USA3 Department of Microbiology and Immunology, Albert Einstein College of Medicine, Bronx, New York, USA1 Division of Rheumatology, University of Southern California, Los Angeles, California, USA2 Division of Rheumatology, Albert Einstein College of Medicine, Bronx, New York, USA1 Division of Rheumatology, University of Southern California, Los Angeles, California, USABackground/objective Treatment with immune checkpoint inhibitors (ICIs) in oncology patients is increasing. Although ICIs trigger rheumatic immune-related adverse events, development of SLE features has been rare. Whether long-term treatment with ICIs would promote SLE features remains unknown. To begin to address this, we generated SLE-prone NZM 2328 mice with lifelong reduction in CTLA-4 expression.Methods Since CTLA-4-deficient (Ctla4−/−) NZM mice developed a lethal lymphoproliferative disorder by 3–6 weeks of age, development of SLE in these mice could not be studied. Ctla4 haploinsufficient NZM.Ctla4+/− mice were assessed in parallel with littermate female NZM.Ctla4+/+ mice. Evaluations included CTLA-4 expression and lymphocyte profiles, assessed by fluorescence-activated cell sorting; serological profiles, assessed by ELISA; renal immunopathology, assessed by histology and immunofluorescence; and clinical courses, assessed by mortality.Results CTLA-4 expression was lower in NZM.Ctla4+/− mice than in NZM.Ctla4+/+ mice. Spleen mononuclear cells, B cells, plasma cells, CD4+ cells, recently activated CD4+ cells and CD4+ T regulatory (Treg) cells were increased in NZM.Ctla4+/− mice (p≤0.042). The serological profile, degree of renal immunopathology and mortality in NZM.Ctla4+/− mice remained unaffected.Conclusion Lifelong reduction in CTLA-4 expression in NZM mice neither accelerated nor aggravated SLE. Expansion in Treg cells may have played a protective role. Our observations raise the hope that long-term treatment of patients with SLE with an anti-CTLA-4 agent, should the need arise, would not adversely affect SLE disease activity.https://lupus.bmj.com/content/6/1/e000313.full
spellingShingle William Stohl
Chaim Putterman
Ning Yu
Samantha A Chalmers
Chaim O Jacob
Constitutive reduction in the checkpoint inhibitor, CTLA-4, does not accelerate SLE in NZM 2328 mice
Lupus Science and Medicine
title Constitutive reduction in the checkpoint inhibitor, CTLA-4, does not accelerate SLE in NZM 2328 mice
title_full Constitutive reduction in the checkpoint inhibitor, CTLA-4, does not accelerate SLE in NZM 2328 mice
title_fullStr Constitutive reduction in the checkpoint inhibitor, CTLA-4, does not accelerate SLE in NZM 2328 mice
title_full_unstemmed Constitutive reduction in the checkpoint inhibitor, CTLA-4, does not accelerate SLE in NZM 2328 mice
title_short Constitutive reduction in the checkpoint inhibitor, CTLA-4, does not accelerate SLE in NZM 2328 mice
title_sort constitutive reduction in the checkpoint inhibitor ctla 4 does not accelerate sle in nzm 2328 mice
url https://lupus.bmj.com/content/6/1/e000313.full
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