Early postnatal expression mitigates immune responses to Cas9 in the murine central nervous system

A barrier in the development of adeno-associated virus (AAV) gene therapy is the immunogenicity of the AAV particles, and in some cases, the expressed transgene. The immunogenic risk is heightened when exogenous proteins, such as prokaryotic Cas9 nucleases, are used in gene editing. We documented th...

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Main Authors: Robert Duba-Kiss, David R. Hampson
Format: Article
Language:English
Published: Elsevier 2025-09-01
Series:Molecular Therapy: Methods & Clinical Development
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Online Access:http://www.sciencedirect.com/science/article/pii/S2329050125001317
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author Robert Duba-Kiss
David R. Hampson
author_facet Robert Duba-Kiss
David R. Hampson
author_sort Robert Duba-Kiss
collection DOAJ
description A barrier in the development of adeno-associated virus (AAV) gene therapy is the immunogenicity of the AAV particles, and in some cases, the expressed transgene. The immunogenic risk is heightened when exogenous proteins, such as prokaryotic Cas9 nucleases, are used in gene editing. We documented the immune responses generated after CNS injections of AAVs encoding Staphylococcus aureus Cas9 in neonatal vs. adult mice. Injection of AAV-Cas9s containing either a neuron-specific synapsin promoter, or a cytomegalovirus promoter, into neonatal mice resulted in robust expression of Cas9 and activation of microglia. Expression of Cas9 was maintained 3 months post-injection while the microglial response dissipated by this time. In contrast, infusion of AAV-Cas9s into the adult brain resulted in the absence of detectable Cas9 protein and reduced neuronal density. Activation of microglia and astrocytes, T cell infiltration into the CNS, and circulating antibodies were also observed. Surprisingly, these effects were not seen in adult mice administered an AAV encoding EGFP. The lack of detectable Cas9 protein in the adult injected mice indicates that Cas9-expressing neurons were eliminated via a cytotoxic immune response. Our findings suggest that very early postnatal administration may enhance safety and efficacy in treatments for pediatric disorders employing CRISPR-Cas9 gene editing.
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spelling doaj-art-83f867a6e5584acfa4acb1b31d8e4e4c2025-08-20T04:00:27ZengElsevierMolecular Therapy: Methods & Clinical Development2329-05012025-09-0133310153610.1016/j.omtm.2025.101536Early postnatal expression mitigates immune responses to Cas9 in the murine central nervous systemRobert Duba-Kiss0David R. Hampson1Department of Pharmacology and Toxicology, University of Toronto, Toronto, ON, CanadaDepartment of Pharmacology and Toxicology, University of Toronto, Toronto, ON, Canada; Department of Pharmaceutical Sciences, University of Toronto, Toronto, ON, Canada; Corresponding author: David R. Hampson, Department of Pharmacology and Toxicology, University of Toronto, Toronto, ON, Canada.A barrier in the development of adeno-associated virus (AAV) gene therapy is the immunogenicity of the AAV particles, and in some cases, the expressed transgene. The immunogenic risk is heightened when exogenous proteins, such as prokaryotic Cas9 nucleases, are used in gene editing. We documented the immune responses generated after CNS injections of AAVs encoding Staphylococcus aureus Cas9 in neonatal vs. adult mice. Injection of AAV-Cas9s containing either a neuron-specific synapsin promoter, or a cytomegalovirus promoter, into neonatal mice resulted in robust expression of Cas9 and activation of microglia. Expression of Cas9 was maintained 3 months post-injection while the microglial response dissipated by this time. In contrast, infusion of AAV-Cas9s into the adult brain resulted in the absence of detectable Cas9 protein and reduced neuronal density. Activation of microglia and astrocytes, T cell infiltration into the CNS, and circulating antibodies were also observed. Surprisingly, these effects were not seen in adult mice administered an AAV encoding EGFP. The lack of detectable Cas9 protein in the adult injected mice indicates that Cas9-expressing neurons were eliminated via a cytotoxic immune response. Our findings suggest that very early postnatal administration may enhance safety and efficacy in treatments for pediatric disorders employing CRISPR-Cas9 gene editing.http://www.sciencedirect.com/science/article/pii/S2329050125001317adeno-associated virusgene editinggreen fluorescent proteinmicroglianeonatalneurodevelopmental disorder
spellingShingle Robert Duba-Kiss
David R. Hampson
Early postnatal expression mitigates immune responses to Cas9 in the murine central nervous system
Molecular Therapy: Methods & Clinical Development
adeno-associated virus
gene editing
green fluorescent protein
microglia
neonatal
neurodevelopmental disorder
title Early postnatal expression mitigates immune responses to Cas9 in the murine central nervous system
title_full Early postnatal expression mitigates immune responses to Cas9 in the murine central nervous system
title_fullStr Early postnatal expression mitigates immune responses to Cas9 in the murine central nervous system
title_full_unstemmed Early postnatal expression mitigates immune responses to Cas9 in the murine central nervous system
title_short Early postnatal expression mitigates immune responses to Cas9 in the murine central nervous system
title_sort early postnatal expression mitigates immune responses to cas9 in the murine central nervous system
topic adeno-associated virus
gene editing
green fluorescent protein
microglia
neonatal
neurodevelopmental disorder
url http://www.sciencedirect.com/science/article/pii/S2329050125001317
work_keys_str_mv AT robertdubakiss earlypostnatalexpressionmitigatesimmuneresponsestocas9inthemurinecentralnervoussystem
AT davidrhampson earlypostnatalexpressionmitigatesimmuneresponsestocas9inthemurinecentralnervoussystem