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Fine tuning of phosphorothioate inclusion in 2'-O-methyl oligonucleotides contributes to specific cell targeting for splice-switching modulation

Abstract:
Splice-switching antisense oligonucleotide- (SSO-) mediated correction of framedisrupting mutation-containing premessenger RNA (mRNA) transcripts using exon skipping is a highly promising treatment method for muscular diseases such as Duchenne muscular dystrophy (DMD). Phosphorothioate (PS) chemistry, a commonly used oligonucleotide modification, has been shown to increase the stability of and improve the pharmacokinetics of SSOs. However, the effect of PS inclusion in 2'-O-methyl SSOs (2OMe) on cellular uptake and splice switching is less well-understood. At present, we demonstrate that the modification of PS facilitates the uptake of 2OMe in H2k-<i>mdx</i> myoblasts. Furthermore, we found a dependency of SSO nuclear accumulation and high splice-switching activity on PS inclusion in 2OMe (2OMePS), as tested in various reporter cell lines carrying pLuc/705. Increased exon-inclusion activity was observed in muscle, neuronal, liver, and bone cell lineages <i>via</i> both the gymnotic uptake and lipofection of 2OMePS. Using the photoactivatable ribonucleoside-enhanced crosslinking and a subsequent proteomic approach, we identified several 2OMePS-binding proteins, which are likely to play a role in the trafficking of 2OMePS to the nucleus. Ablation of one of them, <i>Ncl</i> by small-interfering RNA (siRNA) enhanced 2OMePS uptake in C2C12 myoblasts and upregulated luciferase RNA splicing in the HeLa Luc/705 reporter cell line. Overall, we demonstrate that PS inclusion increases nuclear delivery and splice switching in muscle, neuronal, liver, and bone cell lineages and that the modulation of 2OMePS-binding partners may improve SSO delivery.
Publication status:
Published
Peer review status:
Peer reviewed

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Publisher copy:
10.3389/fphys.2021.689179

Authors


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Institution:
University of Oxford
Division:
MSD
Department:
Clinical Neurosciences
Role:
Author
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Role:
Author
ORCID:
0000-0002-7131-2998
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Role:
Author
ORCID:
0000-0003-4729-4205


Publisher:
Frontiers Media
Journal:
Frontiers in Physiology More from this journal
Volume:
12
Article number:
689179
Place of publication:
Switzerland
Publication date:
2021-10-13
Acceptance date:
2021-09-06
DOI:
EISSN:
1664-042X
ISSN:
1664-042X
Pmid:
34721051


Language:
English
Keywords:
Pubs id:
1207792
Local pid:
pubs:1207792
Deposit date:
2023-09-21

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