Efficient CRISPR/Cas9-mediated editing of trinucleotide repeat expansion in myotonic dystrophy patient-derived iPS and myogenic cells.

Authors:
Dastidar S, Ardui S, Singh K, Majumdar D, Nair N, Fu Y, Reyon D, Samara E, Gerli MFM, Klein AF, De Schrijver W, Tipanee J, Seneca S, Tulalamba W, Wang H, Chai YC, In't Veld P, Furling D, Tedesco FS, Vermeesch JR, Joung JK, Chuah MK, VandenDriessche T. 
In:
Source: Nucleic Acids Res
Publication Date: (2018)
Issue: 46(16): 8275-8298
Research Area:
Stem Cells
Gene Expression
Cells used in publication:
Induced Pluripotent Stem Cell (iPS), human
Species: human
Tissue Origin:
Platform:
4D-Nucleofector® X-Unit
Experiment

The nucleofection of DM1-iPSCs were carried out using Lonza P3 primary cell 4D nucleofection kit according to manufacturer’s protocol (Lonza). Prior to nucleofection, the DM1 –iPSCs were maintained in feeder free culture
condition as described previously. For the nucleofection reaction mix, a ribonucleoprotein (RNP) complex was prepared by mixing 60 pmol Cas9 protein (Integrated DNA Technologies) and 150 pmol of each sgRNA (5-CTGrepeatsgRNA, 3-CTGrepeat-sgRNA) (Synthego) followed by a 10
min incubation at room temperature (control conditions comprised the following: 60 pmol Cas9 and 300 pmol scrambled gRNA; 150 pmol 5-CTGrepeat-sgRNA, 150 pmol 3-CTGrepeat-sgRNA and no Cas9) mixes. Thereafter, DM1– iPSCs were dissociated into single cells with TrypLE express
(Thermo Scientific). Post dissociation, 5 × 105 DM1– iPSCs were resuspended in 20 l P3 nucleofection buffer and mixed with previously prepared RNP complexes and nucleofected using the ‘CA137’ program (using the Nucleofector 4D). Post-nucleofection, the cells were plated on geltrex-coated surface, in Essential 8™ medium (Thermo Scientific) with 10M rock inhibitor (Y-27632, Stem cell Technologies). A day post-nucleofection, cells were supplemented
with fresh Essential 8™ medium (Thermo Scientific) and cultured for further downstream experiments. DM1– iPSCs treated with Cas9 protein and sgRNA (5-CTGrepeatsgRNA, 3-CTGrepeat-sgRNA) were cloned by limiting dilution.
Dissociated DM1–iPSCs were plated as single cells on vitronectin (Stemcell Technologies) coated 96-well plate with Clone R supplement and mTeSR culturing medium (Stemcell Technologies). After 10–15 days of culturing with regular media change, single clones were established. These
DM1-iPSC clones obtained were transferred to larger surface area and maintained as iPSCs clonal lines until further analysis.

Abstract

CRISPR/Cas9 is an attractive platform to potentially correct dominant genetic diseases by gene editing with unprecedented precision. In the current proof-of-principle study, we explored the use of CRISPR/Cas9 for gene-editing in myotonic dystrophy type-1 (DM1), an autosomal-dominant muscle disorder, by excising the CTG-repeat expansion in the 3'-untranslated-region (UTR) of the human myotonic dystrophy protein kinase (DMPK) gene in DM1 patient-specific induced pluripotent stem cells (DM1-iPSC), DM1-iPSC-derived myogenic cells and DM1 patient-specific myoblasts. To eliminate the pathogenic gain-of-function mutant DMPK transcript, we designed a dual guide RNA based strategy that excises the CTG-repeat expansion with high efficiency, as confirmed by Southern blot and single molecule real-time (SMRT) sequencing. Correction efficiencies up to 90% could be attained in DM1-iPSC as confirmed at the clonal level, following ribonucleoprotein (RNP) transfection of CRISPR/Cas9 components without the need for selective enrichment. Expanded CTG repeat excision resulted in the disappearance of ribonuclear foci, a quintessential cellular phenotype of DM1, in the corrected DM1-iPSC, DM1-iPSC-derived myogenic cells and DM1 myoblasts. Consequently, the normal intracellular localization of the muscleblind-like splicing regulator 1 (MBNL1) was restored, resulting in the normalization of splicing pattern of SERCA1. This study validates the use of CRISPR/Cas9 for gene editing of repeat expansions.