Active immunotherapy reduces NOTCH3 deposition in brain capillaries in a CADASIL mouse model

Abstract Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL) is the most common monogenic form of familial small vessel disease; no preventive or curative therapy is available. CADASIL is caused by mutations in the NOTCH3 gene, resulting in a mutated...

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Main Authors: Daniel V Oliveira, Kirsten G Coupland, Wenchao Shao, Shaobo Jin, Francesca Del Gaudio, Sailan Wang, Rhys Fox, Julie W Rutten, Johan Sandin, Henrik Zetterberg, Johan Lundkvist, Saskia AJ Lesnik Oberstein, Urban Lendahl, Helena Karlström
Format: Article
Language:English
Published: Springer Nature 2022-12-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.202216556
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author Daniel V Oliveira
Kirsten G Coupland
Wenchao Shao
Shaobo Jin
Francesca Del Gaudio
Sailan Wang
Rhys Fox
Julie W Rutten
Johan Sandin
Henrik Zetterberg
Johan Lundkvist
Saskia AJ Lesnik Oberstein
Urban Lendahl
Helena Karlström
author_facet Daniel V Oliveira
Kirsten G Coupland
Wenchao Shao
Shaobo Jin
Francesca Del Gaudio
Sailan Wang
Rhys Fox
Julie W Rutten
Johan Sandin
Henrik Zetterberg
Johan Lundkvist
Saskia AJ Lesnik Oberstein
Urban Lendahl
Helena Karlström
author_sort Daniel V Oliveira
collection DOAJ
description Abstract Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL) is the most common monogenic form of familial small vessel disease; no preventive or curative therapy is available. CADASIL is caused by mutations in the NOTCH3 gene, resulting in a mutated NOTCH3 receptor, with aggregation of the NOTCH3 extracellular domain (ECD) around vascular smooth muscle cells. In this study, we have developed a novel active immunization therapy specifically targeting CADASIL‐like aggregated NOTCH3 ECD. Immunizing CADASIL TgN3R182C150 mice with aggregates composed of CADASIL‐R133C mutated and wild‐type EGF1–5 repeats for a total of 4 months resulted in a marked reduction (38–48%) in NOTCH3 deposition around brain capillaries, increased microglia activation and lowered serum levels of NOTCH3 ECD. Active immunization did not impact body weight, general behavior, the number and integrity of vascular smooth muscle cells in the retina, neuronal survival, or inflammation or the renal system, suggesting that the therapy is tolerable. This is the first therapeutic study reporting a successful reduction of NOTCH3 accumulation in a CADASIL mouse model supporting further development towards clinical application for the benefit of CADASIL patients.
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spelling doaj-art-68d5b97efac9440abb6b6bcfdeb077ea2025-08-24T11:43:55ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842022-12-0115212010.15252/emmm.202216556Active immunotherapy reduces NOTCH3 deposition in brain capillaries in a CADASIL mouse modelDaniel V Oliveira0Kirsten G Coupland1Wenchao Shao2Shaobo Jin3Francesca Del Gaudio4Sailan Wang5Rhys Fox6Julie W Rutten7Johan Sandin8Henrik Zetterberg9Johan Lundkvist10Saskia AJ Lesnik Oberstein11Urban Lendahl12Helena Karlström13Department of Neurobiology, Care Sciences and Society, Karolinska InstitutetDepartment of Neurobiology, Care Sciences and Society, Karolinska InstitutetDepartment of Neurobiology, Care Sciences and Society, Karolinska InstitutetDepartment of Neurobiology, Care Sciences and Society, Karolinska InstitutetDepartment of Cell and Molecular Biology, Karolinska InstitutetDepartment of Neurobiology, Care Sciences and Society, Karolinska InstitutetDepartment of Neurobiology, Care Sciences and Society, Karolinska InstitutetDepartment of Clinical Genetics, Leiden University Medical CenterDepartment of Neurobiology, Care Sciences and Society, Karolinska InstitutetDepartment of Psychiatry and Neurochemistry, Institute of Neuroscience and Physiology, The Sahlgrenska Academy at the University of GothenburgDepartment of Neurobiology, Care Sciences and Society, Karolinska InstitutetDepartment of Clinical Genetics, Leiden University Medical CenterDepartment of Neurobiology, Care Sciences and Society, Karolinska InstitutetDepartment of Neurobiology, Care Sciences and Society, Karolinska InstitutetAbstract Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL) is the most common monogenic form of familial small vessel disease; no preventive or curative therapy is available. CADASIL is caused by mutations in the NOTCH3 gene, resulting in a mutated NOTCH3 receptor, with aggregation of the NOTCH3 extracellular domain (ECD) around vascular smooth muscle cells. In this study, we have developed a novel active immunization therapy specifically targeting CADASIL‐like aggregated NOTCH3 ECD. Immunizing CADASIL TgN3R182C150 mice with aggregates composed of CADASIL‐R133C mutated and wild‐type EGF1–5 repeats for a total of 4 months resulted in a marked reduction (38–48%) in NOTCH3 deposition around brain capillaries, increased microglia activation and lowered serum levels of NOTCH3 ECD. Active immunization did not impact body weight, general behavior, the number and integrity of vascular smooth muscle cells in the retina, neuronal survival, or inflammation or the renal system, suggesting that the therapy is tolerable. This is the first therapeutic study reporting a successful reduction of NOTCH3 accumulation in a CADASIL mouse model supporting further development towards clinical application for the benefit of CADASIL patients.https://doi.org/10.15252/emmm.202216556CADASILimmunizationNOTCH3small vessel diseasetherapy
spellingShingle Daniel V Oliveira
Kirsten G Coupland
Wenchao Shao
Shaobo Jin
Francesca Del Gaudio
Sailan Wang
Rhys Fox
Julie W Rutten
Johan Sandin
Henrik Zetterberg
Johan Lundkvist
Saskia AJ Lesnik Oberstein
Urban Lendahl
Helena Karlström
Active immunotherapy reduces NOTCH3 deposition in brain capillaries in a CADASIL mouse model
EMBO Molecular Medicine
CADASIL
immunization
NOTCH3
small vessel disease
therapy
title Active immunotherapy reduces NOTCH3 deposition in brain capillaries in a CADASIL mouse model
title_full Active immunotherapy reduces NOTCH3 deposition in brain capillaries in a CADASIL mouse model
title_fullStr Active immunotherapy reduces NOTCH3 deposition in brain capillaries in a CADASIL mouse model
title_full_unstemmed Active immunotherapy reduces NOTCH3 deposition in brain capillaries in a CADASIL mouse model
title_short Active immunotherapy reduces NOTCH3 deposition in brain capillaries in a CADASIL mouse model
title_sort active immunotherapy reduces notch3 deposition in brain capillaries in a cadasil mouse model
topic CADASIL
immunization
NOTCH3
small vessel disease
therapy
url https://doi.org/10.15252/emmm.202216556
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