Antisense oligonucleotides reverse SPTLC1-related hereditary sensory neuropathy in a mouse model
Hereditary sensory neuropathy type IA (HSN1A) is a rare neurodegenerative condition caused by dominant mutations in the Serine Palmitoyl Transferase Long Chain base subunit 1 (SPTLC1) gene. There is no treatment available. Allele-specific silencing by antisense oligonucleotides (ASOs) to preferentially silence the mutant transcripts has shown therapeutic promise for dominant gain-of-function genetic disorders. In this study, we validated an allele-specific ASO therapy to selectively silence mutant SPTLC1 (p.S331F) in a disease mouse model carrying heterozygous p.S331F mutation (S331F mice). Gapmer ASOs, targeting the S331F variant in either 2'-O-Methyl (2'-OMe), locked nucleic acid (LNA) or 2'-O-methoxy ethyl (MOE) chemistries, were firstly studied in cultured mouse skin fibroblasts. The candidate ASOs in LNA or MOE were further evaluated in vivo. Single subcutaneous injection of ASOs in neonatal or adult S331F mice achieved over 90% mutant transcripts silencing in the liver and dorsal root ganglia (DRG). Weekly subcutaneous injections of LNA-ASOs of either unconjugated or conjugated with N-acetylgalactosamine (GalNAc) in S331F mice showed that GalNAc-LNA-ASO presented higher efficiency than the unconjugated LNA-ASO in reducing the mutant transcripts in the liver, DRG and sciatic nerve, without affecting the wild-type transcripts. GalNAc-LNA-ASO also achieved significant reduction in the blood levels of the neurotoxic metabolites 1-deoxysphingoidbases (1-deoxySL), a biomarker used in HSN1A patients. Transcriptomic studies in DRGs demonstrated the involvement of the mitochondrial pathway in pathological changes of the S331F mice. Quantitative RT-PCR analysis confirmed the differentially expressed genes between the S331F and wildtype mice. Furthermore, these aberrantly expressed genes in S331F mice were reversed by the GalNAc-LNA-ASO treatment. Our data provides necessary in vivo evidence as proof-of-concept for ASO-mediated mutant allele-specific silencing as a therapeutic approach for SPTLC1-related HSN1.
Authors
- Shuang‐Gang Ma (ORCID: https://orcid.org/0000-0002-1065-154X)
- Charalambos Demetriou (ORCID: https://orcid.org/0000-0001-6630-1322)
- David Bennett (ORCID: https://orcid.org/0000-0002-7996-2696)
- Mary M. Reilly (ORCID: https://orcid.org/0000-0003-0686-905X)
- Emma Graham
- Thorsten Hornemann (ORCID: https://orcid.org/0000-0002-4218-1087)
- Stephanie C. Koch (ORCID: https://orcid.org/0000-0002-7131-4141)
- Jinhong Meng (ORCID: https://orcid.org/0000-0002-8405-8140)
- Laura Andréoli (ORCID: https://orcid.org/0000-0002-9107-3218)
- Francesco Muntoni
- Simon Beggs (ORCID: https://orcid.org/0000-0002-1582-8391)
- Alex Clark (ORCID: https://orcid.org/0000-0002-0836-6328)
- Museer A. Lone (ORCID: https://orcid.org/0000-0001-9710-775X)
- Shona Mackie
- Qiang Zhang (ORCID: https://orcid.org/0000-0002-5923-2696)
- Shuzhi Cheng
- Hou Wang Lam
- Nicole Ziak
- Hanna Kedzior
Institutions
- Queen Mary University of London (GB)
- Great Ormond Street Hospital (GB)
- John Radcliffe Hospital (GB)
- University Hospital of Zurich (CH)
- MRC Prion Unit (GB)
- Institute of Child Health (IN)
- National Hospital for Neurology and Neurosurgery (GB)
- University College London (GB)
Publication Details
- Journal
- Brain
- Published
- 2025-10-21
- DOI
- https://doi.org/10.1093/brain/awaf403
- Primary Topic
- Hereditary Neurological Disorders
- Type
- article
- Field-Weighted Citation Impact
- 0.00
Funders
- INFRAFRONTIER
- Rosetrees Trust
- Medical Research Council