Antisense oligonucleotide therapy for patients with Friedreich’s ataxia carrying the c.165+5G>C splicing mutation

Friedreich’s ataxia (FRDA) is a multisystem, progressive disease. 96% of patients carry biallelic GAA triplet expansion mutations in intron 1 of the frataxin gene (FXN). The remaining 4% have a pathogenic GAA expansion on one FXN allele and another mutation on the second allele. A point mutation, FX...

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Main Authors: Pouiré Yameogo, Selina Aguilar, Thazha P. Prakash, Frank Rigo, David R. Lynch, Jill S. Napierala, Marek Napierala
Format: Article
Language:English
Published: Elsevier 2025-09-01
Series:Molecular Therapy: Nucleic Acids
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Online Access:http://www.sciencedirect.com/science/article/pii/S2162253125001714
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author Pouiré Yameogo
Selina Aguilar
Thazha P. Prakash
Frank Rigo
David R. Lynch
Jill S. Napierala
Marek Napierala
author_facet Pouiré Yameogo
Selina Aguilar
Thazha P. Prakash
Frank Rigo
David R. Lynch
Jill S. Napierala
Marek Napierala
author_sort Pouiré Yameogo
collection DOAJ
description Friedreich’s ataxia (FRDA) is a multisystem, progressive disease. 96% of patients carry biallelic GAA triplet expansion mutations in intron 1 of the frataxin gene (FXN). The remaining 4% have a pathogenic GAA expansion on one FXN allele and another mutation on the second allele. A point mutation, FXN c.165+5G>C, was identified in intron 1 of a patient with FRDA resulting in a significant decrease of FXN levels. Using patient fibroblasts, we demonstrated that the c.165+5G>C mutation affects canonical splicing of FXN, leading to the generation of an aberrant transcript. A library of antisense oligonucleotides (ASOs) was designed to target potential intronic splicing regulator motifs and tested in patient cells. Selected O-methoxyethyl (MOE)-ASOs increased FXN levels in c.165+5G>C patient cells without affecting FXN splicing in control cells. The leading MOE-ASO increased expression of a miniFXN gene carrying the c.165+5G>C point mutation by splicing repair. To increase efficacy, we simultaneously targeted the GAA-expanded allele in patient cells using a synthetic transcription factor (synthetic transcription elongation factor 1 [Syn-TEF1]). This ASO strategy may be therapeutically feasible for patients with FRDA with other point mutations that cause splicing defects. Success in developing treatments for disorders with only a few known cases will give hope to patients with FRDA carrying these rare point mutations.
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spelling doaj-art-cb5be2a948e34acf9e408603c0b7574a2025-08-20T03:12:01ZengElsevierMolecular Therapy: Nucleic Acids2162-25312025-09-0136310261710.1016/j.omtn.2025.102617Antisense oligonucleotide therapy for patients with Friedreich’s ataxia carrying the c.165+5G>C splicing mutationPouiré Yameogo0Selina Aguilar1Thazha P. Prakash2Frank Rigo3David R. Lynch4Jill S. Napierala5Marek Napierala6Department of Neurology, O’Donnell Brain Institute, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX 75390, USADepartment of Neurology, O’Donnell Brain Institute, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX 75390, USAIonis Pharmaceuticals Inc., 2855 Gazelle Court, Carlsbad, CA 92010, USAIonis Pharmaceuticals Inc., 2855 Gazelle Court, Carlsbad, CA 92010, USADepartment of Pediatrics and Neurology, The Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USADepartment of Neurology, O’Donnell Brain Institute, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX 75390, USA; Corresponding author: Jill S. Napierala, Department of Neurology, O’Donnell Brain Institute, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX 75390, USA.Department of Neurology, O’Donnell Brain Institute, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX 75390, USA; Corresponding author: Marek Napierala, Department of Neurology, O’Donnell Brain Institute, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX 75390, USA.Friedreich’s ataxia (FRDA) is a multisystem, progressive disease. 96% of patients carry biallelic GAA triplet expansion mutations in intron 1 of the frataxin gene (FXN). The remaining 4% have a pathogenic GAA expansion on one FXN allele and another mutation on the second allele. A point mutation, FXN c.165+5G>C, was identified in intron 1 of a patient with FRDA resulting in a significant decrease of FXN levels. Using patient fibroblasts, we demonstrated that the c.165+5G>C mutation affects canonical splicing of FXN, leading to the generation of an aberrant transcript. A library of antisense oligonucleotides (ASOs) was designed to target potential intronic splicing regulator motifs and tested in patient cells. Selected O-methoxyethyl (MOE)-ASOs increased FXN levels in c.165+5G>C patient cells without affecting FXN splicing in control cells. The leading MOE-ASO increased expression of a miniFXN gene carrying the c.165+5G>C point mutation by splicing repair. To increase efficacy, we simultaneously targeted the GAA-expanded allele in patient cells using a synthetic transcription factor (synthetic transcription elongation factor 1 [Syn-TEF1]). This ASO strategy may be therapeutically feasible for patients with FRDA with other point mutations that cause splicing defects. Success in developing treatments for disorders with only a few known cases will give hope to patients with FRDA carrying these rare point mutations.http://www.sciencedirect.com/science/article/pii/S2162253125001714MT: Oligonucleotides: Therapies and ApplicationsFriedreich’s ataxiaantisense oligonucleotidesaberrant splicingfrataxin point mutationcompound heterozygous
spellingShingle Pouiré Yameogo
Selina Aguilar
Thazha P. Prakash
Frank Rigo
David R. Lynch
Jill S. Napierala
Marek Napierala
Antisense oligonucleotide therapy for patients with Friedreich’s ataxia carrying the c.165+5G>C splicing mutation
Molecular Therapy: Nucleic Acids
MT: Oligonucleotides: Therapies and Applications
Friedreich’s ataxia
antisense oligonucleotides
aberrant splicing
frataxin point mutation
compound heterozygous
title Antisense oligonucleotide therapy for patients with Friedreich’s ataxia carrying the c.165+5G>C splicing mutation
title_full Antisense oligonucleotide therapy for patients with Friedreich’s ataxia carrying the c.165+5G>C splicing mutation
title_fullStr Antisense oligonucleotide therapy for patients with Friedreich’s ataxia carrying the c.165+5G>C splicing mutation
title_full_unstemmed Antisense oligonucleotide therapy for patients with Friedreich’s ataxia carrying the c.165+5G>C splicing mutation
title_short Antisense oligonucleotide therapy for patients with Friedreich’s ataxia carrying the c.165+5G>C splicing mutation
title_sort antisense oligonucleotide therapy for patients with friedreich s ataxia carrying the c 165 5g c splicing mutation
topic MT: Oligonucleotides: Therapies and Applications
Friedreich’s ataxia
antisense oligonucleotides
aberrant splicing
frataxin point mutation
compound heterozygous
url http://www.sciencedirect.com/science/article/pii/S2162253125001714
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