Hybridization-mediated off-target effects of splice-switching antisense oligonucleotides.


Journal

Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011

Informations de publication

Date de publication:
24 01 2020
Historique:
accepted: 03 12 2019
revised: 03 10 2019
received: 17 04 2019
pubmed: 6 12 2019
medline: 19 3 2020
entrez: 6 12 2019
Statut: ppublish

Résumé

Splice-switching antisense oligonucleotides (ASOs), which bind specific RNA-target sequences and modulate pre-mRNA splicing by sterically blocking the binding of splicing factors to the pre-mRNA, are a promising therapeutic modality to treat a range of genetic diseases. ASOs are typically 15-25 nt long and considered to be highly specific towards their intended target sequence, typically elements that control exon definition and/or splice-site recognition. However, whether or not splice-modulating ASOs also induce hybridization-dependent mis-splicing of unintended targets has not been systematically studied. Here, we tested the in vitro effects of splice-modulating ASOs on 108 potential off-targets predicted on the basis of sequence complementarity, and identified 17 mis-splicing events for one of the ASOs tested. Based on analysis of data from two overlapping ASO sequences, we conclude that off-target effects are difficult to predict, and the choice of ASO chemistry influences the extent of off-target activity. The off-target events caused by the uniformly modified ASOs tested in this study were significantly reduced with mixed-chemistry ASOs of the same sequence. Furthermore, using shorter ASOs, combining two ASOs, and delivering ASOs by free uptake also reduced off-target activity. Finally, ASOs with strategically placed mismatches can be used to reduce unwanted off-target splicing events.

Identifiants

pubmed: 31802121
pii: 5658446
doi: 10.1093/nar/gkz1132
pmc: PMC6954394
doi:

Substances chimiques

Oligonucleotides, Antisense 0
RNA Precursors 0
RNA Splice Sites 0
RNA, Messenger 0

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

802-816

Subventions

Organisme : NCI NIH HHS
ID : P01 CA013106
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA045508
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM042699
Pays : United States
Organisme : NIGMS NIH HHS
ID : R37 GM042699
Pays : United States

Informations de copyright

© The Author(s) 2019. Published by Oxford University Press on behalf of Nucleic Acids Research.

Références

RNA. 2004 Oct;10(10):1507-17
pubmed: 15383676
EMBO Mol Med. 2016 Mar 31;8(4):328-45
pubmed: 26902204
J Anal Methods Chem. 2016;2016:5318935
pubmed: 27833775
Sci Rep. 2017 Jun 16;7(1):3672
pubmed: 28623256
Nature. 2010 Jan 21;463(7279):364-8
pubmed: 20010808
Mol Ther Nucleic Acids. 2019 Jun 7;16:313-325
pubmed: 30965276
Nucleic Acids Res. 2014 Jul;42(Web Server issue):W361-7
pubmed: 24829458
Nat Biotechnol. 2012 Oct;30(10):920-3
pubmed: 23051805
Nucleic Acids Res. 2016 Mar 18;44(5):2093-109
pubmed: 26553810
Nucleic Acid Ther. 2017 Jun;27(3):144-158
pubmed: 28375678
Science. 2015 Jan 23;347(6220):1260419
pubmed: 25613900
Adv Drug Deliv Rev. 2015 Jun 29;87:46-51
pubmed: 25666165
RNA Biol. 2009 Jul-Aug;6(3):341-50
pubmed: 19430205
J Biol Chem. 1997 May 2;272(18):11994-2000
pubmed: 9115264
Nucleic Acids Res. 2015 Oct 15;43(18):8638-50
pubmed: 26338776
Development. 2008 May;135(10):1735-43
pubmed: 18403413
PLoS Biol. 2007 Apr;5(4):e73
pubmed: 17355180
Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7305-9
pubmed: 1380154
Nucleic Acids Res. 2018 Jan 4;46(D1):D213-D217
pubmed: 29069475
Nucleic Acids Res. 2017 Sep 19;45(16):9528-9546
pubmed: 28934489
Mol Ther Nucleic Acids. 2014 Jul 08;3:e174
pubmed: 25004100
Nat Genet. 2011 Mar 20;43(4):371-8
pubmed: 21423181
Gene Ther. 2015 Jun;22(6):503-15
pubmed: 25832542
Open Biol. 2012 Oct;2(10):120133
pubmed: 23155487
Sci Rep. 2017 Oct 2;7(1):12532
pubmed: 28970564
Nat Rev Drug Discov. 2012 Jan 20;11(2):125-40
pubmed: 22262036
PLoS One. 2014 Jul 29;9(7):e101752
pubmed: 25072142
J Mol Cell Biol. 2012 Apr;4(2):79-87
pubmed: 22044881
BMC Bioinformatics. 2012 Jun 18;13:134
pubmed: 22708584
Annu Rev Pharmacol Toxicol. 2010;50:259-93
pubmed: 20055705
Nat Biotechnol. 2016 Feb;34(2):164-6
pubmed: 26655495
J Org Chem. 2010 Mar 5;75(5):1569-81
pubmed: 20136157
Mol Pharmacol. 2007 Jan;71(1):83-91
pubmed: 17028158
J Biol Chem. 1999 Oct 1;274(40):28270-8
pubmed: 10497183
Nucleic Acids Res. 2018 Jun 1;46(10):4833-4844
pubmed: 29672717
Nat Genet. 2000 Oct;26(2):216-20
pubmed: 11017081
Nucleic Acid Ther. 2019 Jun;29(3):116-122
pubmed: 30907681
Nucleic Acids Res. 2010 Jan;38(1):e3
pubmed: 19854938
EMBO Rep. 2000 Jul;1(1):18-23
pubmed: 11256617
Proc Natl Acad Sci U S A. 1991 Sep 15;88(18):8237-41
pubmed: 1896475
Nat Biotechnol. 2017 Mar;35(3):230-237
pubmed: 28244996

Auteurs

Juergen Scharner (J)

Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA.

Wai Kit Ma (WK)

Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA.

Qian Zhang (Q)

Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA.

Kuan-Ting Lin (KT)

Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA.

Frank Rigo (F)

Ionis Pharmaceuticals, Carlsbad, CA, USA.

C Frank Bennett (CF)

Ionis Pharmaceuticals, Carlsbad, CA, USA.

Adrian R Krainer (AR)

Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH