Systematic screening identifies therapeutic antisense oligonucleotides for Hutchinson-Gilford progeria syndrome.


Journal

Nature medicine
ISSN: 1546-170X
Titre abrégé: Nat Med
Pays: United States
ID NLM: 9502015

Informations de publication

Date de publication:
03 2021
Historique:
received: 08 07 2020
accepted: 25 01 2021
pubmed: 13 3 2021
medline: 17 4 2021
entrez: 12 3 2021
Statut: ppublish

Résumé

Hutchinson-Gilford progeria syndrome (HGPS) is a rare, invariably fatal childhood premature aging disorder caused by a pre-messenger RNA (mRNA) splicing defect in the LMNA gene. We used combined in vitro screening and in vivo validation to systematically explore the effects of target sequence, backbone chemistry and mechanism of action to identify optimized antisense oligonucleotides (ASOs) for therapeutic use in HGPS. In a library of 198 ASOs, the most potent ASOs targeted the LMNA exon 12 junction and acted via non-RNase H-mediated mechanisms. Treatment with an optimized lead candidate resulted in extension of lifespan in a mouse model of HGPS. Progerin mRNA levels were robustly reduced in vivo, but the extent of progerin protein reduction differed between tissues, suggesting a long half-life and tissue-specific turnover of progerin in vivo. These results identify a novel therapeutic agent for HGPS and provide insight into the HGPS disease mechanism.

Identifiants

pubmed: 33707772
doi: 10.1038/s41591-021-01262-4
pii: 10.1038/s41591-021-01262-4
pmc: PMC10167920
mid: NIHMS1883464
doi:

Substances chimiques

LMNA protein, human 0
Lamin Type A 0
Oligonucleotides, Antisense 0

Types de publication

Journal Article Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

526-535

Subventions

Organisme : Intramural NIH HHS
ID : ZIA BC010309
Pays : United States

Commentaires et corrections

Type : CommentIn
Type : CommentIn
Type : ErratumIn

Références

Cell. 2013 Aug 29;154(5):971-982
pubmed: 23993091
Nat Rev Mol Cell Biol. 2013 Jan;14(1):55-61
pubmed: 23258296
Cell. 2014 Jan 30;156(3):400-7
pubmed: 24485450
Hum Mol Genet. 2009 Jul 1;18(13):2462-71
pubmed: 19376814
Nat Commun. 2017 Aug 30;8(1):328
pubmed: 28855503
Proc Natl Acad Sci U S A. 2006 Feb 28;103(9):3250-5
pubmed: 16492728
Sci Rep. 2016 Oct 14;6:34798
pubmed: 27739443
Proc Natl Acad Sci U S A. 2012 Oct 9;109(41):16666-71
pubmed: 23012407
Proc Natl Acad Sci U S A. 2020 Jun 2;117(22):12029-12040
pubmed: 32404427
PLoS One. 2014 Sep 10;9(9):e107434
pubmed: 25207939
Methods. 2021 Jun;190:3-12
pubmed: 32278808
Oncotarget. 2016 May 24;7(21):30018-31
pubmed: 27145372
Nat Med. 2021 Mar;27(3):536-545
pubmed: 33707773
Oncotarget. 2017 Jul 18;8(39):64809-64826
pubmed: 29029393
Nucleic Acids Res. 1985 Dec 20;13(24):8927-38
pubmed: 4080553
J Clin Invest. 2016 Apr 1;126(4):1592-602
pubmed: 26999604
Nature. 2003 May 15;423(6937):293-8
pubmed: 12714972
J Clin Invest. 2016 Oct 3;126(10):3879-3893
pubmed: 27617860
Nucleic Acids Res. 2020 May 7;48(8):4382-4395
pubmed: 32182359
PLoS Biol. 2007 Apr;5(4):e73
pubmed: 17355180
Oncotarget. 2015 Oct 6;6(30):29914-28
pubmed: 26359359
Nucleic Acids Res. 2019 Jun 20;47(11):5922-5935
pubmed: 31006814
Proc Natl Acad Sci U S A. 2018 Apr 17;115(16):4206-4211
pubmed: 29581305
JAMA. 2018 Apr 24;319(16):1687-1695
pubmed: 29710166
Proc Natl Acad Sci U S A. 2001 Jan 2;98(1):42-7
pubmed: 11120883
Nucleic Acids Res. 2019 Jul 9;47(12):6045-6058
pubmed: 31076766
Sci Transl Med. 2011 Mar 2;3(72):72ra18
pubmed: 21368223
Aging Cell. 2015 Feb;14(1):78-91
pubmed: 25510262
Annu Rev Med. 2019 Jan 27;70:307-321
pubmed: 30691367
EMBO Mol Med. 2016 Jul 01;8(7):685-7
pubmed: 27234439
Nat Med. 2005 Apr;11(4):440-5
pubmed: 15750600
Nucleic Acids Res. 2007;35(13):4562-72
pubmed: 17586818
J Clin Invest. 2006 Mar;116(3):743-52
pubmed: 16511604
Biogerontology. 2019 Jun;20(3):337-358
pubmed: 31041622
Sci Transl Med. 2011 Oct 26;3(106):106ra107
pubmed: 22030750
Science. 2003 Jun 27;300(5628):2055
pubmed: 12702809
Science. 2014 May 2;344(6183):527-32
pubmed: 24786082
Sci Rep. 2017 May 30;7(1):2475
pubmed: 28559565
Handb Clin Neurol. 2015;132:249-64
pubmed: 26564085
Nat Chem Biol. 2012 Apr 15;8(6):555-61
pubmed: 22504300
Cell Death Dis. 2016 Feb 18;7:e2105
pubmed: 26890144
Methods. 2016 Mar 1;96:46-58
pubmed: 26341717

Auteurs

Madaiah Puttaraju (M)

National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

Michaela Jackson (M)

Ionis Pharmaceuticals, Carlsbad, CA, USA.

Stephanie Klein (S)

Ionis Pharmaceuticals, Carlsbad, CA, USA.

Asaf Shilo (A)

National Cancer Institute, National Institutes of Health, Bethesda, MD, USA.

C Frank Bennett (CF)

Ionis Pharmaceuticals, Carlsbad, CA, USA.

Leslie Gordon (L)

Division of Genetics, Department of Pediatrics, Hasbro Children's Hospital and Warren Alpert Medical School of Brown University, Providence, RI, USA.
Department of Anesthesiology, Perioperative and Pain Medicine, Boston Children's Hospital and Harvard Medical School, Boston, MA, USA.

Frank Rigo (F)

Ionis Pharmaceuticals, Carlsbad, CA, USA.

Tom Misteli (T)

National Cancer Institute, National Institutes of Health, Bethesda, MD, USA. mistelit@mail.nih.gov.

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