CRISPR-SKIP: Programmable gene splicing with single base editors

Genome Biology

Volumn 19, Issue 1, 2018, Pages

  Gapinske, Michael ^a   Luu, Alan ^a,b   Winter, Jackson ^a   Woods, Wendy S ^a   Kostan, Kurt A ^a   Shiva, Nikhil ^a   Song, Jun S ^a,b   Perez Pinera, Pablo ^a,b,c  

^a University of Illinois at Urbana Champaign   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Alternative splicing; Base editing; BRCA2; CRISPR Cas9; Exon skipping; Gene editing; Gene isoform; PIK3CA; RELA; Synthetic biology

Indexed keywords

CELL DNA; CYTIDINE DEAMINASE; ISOPROTEIN;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CRISPR-CAS9 SYSTEM; DNA REPAIR; DOUBLE STRANDED DNA BREAK; EMBRYO; EXON; EXON SKIPPING; GENE CONTROL; GENE EDITING; GENE MUTATION; GENE TARGETING; GENE THERAPY; GENETIC REGULATION; HUMAN; HUMAN CELL; INTRON; MOUSE; NONHUMAN; PILOT STUDY; RNA SPLICE SITE; RNA SPLICING; RNA TRANSCRIPTION; SYNTHETIC BIOLOGY; BASE PAIRING; CELL LINE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CONSENSUS SEQUENCE; GENETICS; GENOME; HIGH THROUGHPUT SEQUENCING; NUCLEOTIDE SEQUENCE;

BASE PAIRING; BASE SEQUENCE; CELL LINE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEATS; CONSENSUS SEQUENCE; EXONS; GENE EDITING; GENOME; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; RNA SPLICE SITES;

EID: 85051582903     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-018-1482-5     Document Type: Article

References (44)

1. Gaj T, Gersbach CA, Barbas CF 3rd. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol. 2013;31:397-405.
2. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F. Multiplex genome engineering using CRISPR/Cas systems. Science. 2013;339:819-23.
3. Jinek M, East A, Cheng A, Lin S, Ma E, Doudna J. RNA-programmed genome editing in human cells. Elife. 2013;2:e00471.
4. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM. RNA-guided human genome engineering via Cas9. Science. 2013;339:823-6.
5. Nelson CE, Gersbach CA. Cas9 loosens its grip on off-target sites. Nat Biotechnol. 2016;34:298-9.
6. Kleinstiver BP, Pattanayak V, Prew MS, Tsai SQ, Nguyen NT, Zheng Z, Joung JK. High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature. 2016;529:490-5.
7. Liang X, Potter J, Kumar S, Zou Y, Quintanilla R, Sridharan M, Carte J, Chen W, Roark N, Ranganathan S, et al. Rapid and highly efficient mammalian cell engineering via Cas9 protein transfection. J Biotechnol. 2015;208:44-53.
8. Slaymaker IM, Gao L, Zetsche B, Scott DA, Yan WX, Zhang F. Rationally engineered Cas9 nucleases with improved specificity. Science. 2016;351:84-8.
9. Gaudelli NM, Komor AC, Rees HA, Packer MS, Badran AH, Bryson DI, Liu DR. Programmable base editing of a*T to G*C in genomic DNA without DNA cleavage. Nature. 2017;551:464-71.
10. Kim YB, Komor AC, Levy JM, Packer MS, Zhao KT, Liu DR. Increasing the genome-targeting scope and precision of base editing with engineered Cas9-cytidine deaminase fusions. Nat Biotechnol. 2017;35(4):371-6.
11. Komor AC, Kim YB, Packer MS, Zuris JA, Liu DR. Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature. 2016;533:420-4.
12. Ma Y, Zhang J, Yin W, Zhang Z, Song Y, Chang X. Targeted AID-mediated mutagenesis (TAM) enables efficient genomic diversification in mammalian cells. Nat Methods. 2016;13:1029-35.
13. Nishida K, Arazoe T, Yachie N, Banno S, Kakimoto M, Tabata M, Mochizuki M, Miyabe A, Araki M, Hara KY, et al. Targeted nucleotide editing using hybrid prokaryotic and vertebrate adaptive immune systems. Science. 2016;353(6305):aaf8729. https://doi.org/10.1126/science.aaf8729.
14. Hess GT, Fresard L, Han K, Lee CH, Li A, Cimprich KA, Montgomery SB, Bassik MC. Directed evolution using dCas9-targeted somatic hypermutation in mammalian cells. Nat Methods. 2016;13:1036-42.
15. Kuscu C, Parlak M, Tufan T, Yang J, Szlachta K, Wei X, Mammadov R, Adli M. CRISPR-STOP: gene silencing through base-editing-induced nonsense mutations. Nat Methods. 2017;14:710-2.
16. Graveley BR. Alternative splicing: increasing diversity in the proteomic world. Trends Genet. 2001;17:100-7.
17. Crooke ST. Molecular mechanisms of action of antisense drugs. Biochim Biophys Acta. 1999;1489:31-44.
18. Brown A, Woods WS, Perez-Pinera P. Multiplexed targeted genome engineering using a universal nuclease-assisted vector integration system. ACS Synth Biol. 2016;5(7):582-8.
19. Langmead B, Salzberg SL. Fast gapped-read alignment with bowtie 2. Nat Methods. 2012;9:357-9.
20. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013;14:R36.
21. Hsu PD, Scott DA, Weinstein JA, Ran FA, Konermann S, Agarwala V, Li Y, Fine EJ, Wu X, Shalem O, et al. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol. 2013;31:827-32.
22. Mou H, Smith JL, Peng L, Yin H, Moore J, Zhang XO, Song CQ, Sheel A, Wu Q, Ozata DM, et al. CRISPR/Cas9-mediated genome editing induces exon skipping by alternative splicing or exon deletion. Genome Biol. 2017;18:108.
23. Baralle FE, Giudice J. Alternative splicing as a regulator of development and tissue identity. Nat Rev Mol Cell Biol. 2017;18:437-51.
24. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, et al. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res. 2012;22:1775-89.
25. Goyal A, Myacheva K, Groß M, Klingenberg M, Duran Arqué B, Diederichs S. Challenges of CRISPR/Cas9 applications for long non-coding RNA genes. Nucleic Acids Res. 2017;45(3):e12.
26. Gerard X, Perrault I, Hanein S, Silva E, Bigot K, Defoort-Delhemmes S, Rio M, Munnich A, Scherman D, Kaplan J, et al. AON-mediated exon skipping restores Ciliation in fibroblasts harboring the common Leber congenital Amaurosis CEP290 mutation. Mol Ther Nucleic Acids. 2012;1:e29.
27. Khoo B, Roca X, Chew SL, Krainer AR. Antisense oligonucleotide-induced alternative splicing of the APOB mRNA generates a novel isoform of APOB. BMC Mol Biol. 2007;8:3.
28. Kalbfuss B, Mabon SA, Misteli T. Correction of alternative splicing of tau in frontotemporal dementia and parkinsonism linked to chromosome 17. J Biol Chem. 2001;276:42986-93.
29. Mercatante DR, Mohler JL, Kole R. Cellular response to an antisense-mediated shift of Bcl-x pre-mRNA splicing and antineoplastic agents. J Biol Chem. 2002;277:49374-82.
30. Karras JG, McKay RA, Dean NM, Monia BP. Deletion of individual exons and induction of soluble murine interleukin-5 receptor-alpha chain expression through antisense oligonucleotide-mediated redirection of pre-mRNA splicing. Mol Pharmacol. 2000;58:380-7.
31. Goto M, Sawamura D, Nishie W, Sakai K, McMillan JR, Akiyama M, Shimizu H. Targeted skipping of a single exon harboring a premature termination codon mutation: implications and potential for gene correction therapy for selective dystrophic epidermolysis bullosa patients. J Invest Dermatol. 2006;126:2614-20.
32. Aartsma-Rus A, van Ommen GJB. Antisense-mediated exon skipping: a versatile tool with therapeutic and research applications. Rna. 2007;13:1609-24.
33. Aartsma-Rus A, Fokkema I, Verschuuren J, Ginjaar I, van Deutekom J, van Ommen GJ, den Dunnen JT. Theoretic applicability of antisense-mediated exon skipping for Duchenne muscular dystrophy mutations. Hum Mutat. 2009;30:293-9.
34. van Putten M, Hulsker M, Young C, Nadarajah VD, Heemskerk H, van der Weerd L, t Hoen PAC, van Ommen G-JB, Aartsma-Rus AM. Low dystrophin levels increase survival and improve muscle pathology and function in dystrophin/utrophin double-knockout mice. FASEB J. 2013;27:2484-95.
35. Dawson TM, Li D, Yue Y, Duan D. Marginal level dystrophin expression improves clinical outcome in a strain of dystrophin/Utrophin double knockout mice. PLoS One. 2010;5:e15286.
36. Long C, Li H, Tiburcy M, Rodriguez-Caycedo C, Kyrychenko V, Zhou H, Zhang Y, Min YL, Shelton JM, Mammen PPA, et al. Correction of diverse muscular dystrophy mutations in human engineered heart muscle by single-site genome editing. Sci Adv. 2018;4:eaap9004.
37. Hu JH, Miller SM, Geurts MH, Tang W, Chen L, Sun N, Zeina CM, Gao X, Rees HA, Lin Z, Liu DR. Evolved Cas9 variants with broad PAM compatibility and high DNA specificity. Nature. 2018;556:57-63.
38. Kwak H, Fuda NJ, Core LJ, Lis JT. Precise maps of RNA polymerase reveal how promoters direct initiation and pausing. Science. 2013;339:950-3.
39. Fuchs G, Voichek Y, Benjamin S, Gilad S, Amit I, Oren M. 4sUDRB-seq: measuring genomewide transcriptional elongation rates and initiation frequencies within cells. Genome Biol. 2014;15(5):R69.
40. Veloso A, Kirkconnell KS, Magnuson B, Biewen B, Paulsen MT, Wilson TE, Ljungman M. Rate of elongation by RNA polymerase II is associated with specific gene features and epigenetic modifications. Genome Res. 2014;24:896-905.
41. Alexander RD, Innocente SA, Barrass JD, Beggs JD. Splicing-dependent RNA polymerase pausing in yeast. Mol Cell. 2010;40:582-93.
42. Rees HA, Komor AC, Yeh W-H, Caetano-Lopes J, Warman M, Edge ASB, Liu DR. Improving the DNA specificity and applicability of base editing through protein engineering and protein delivery. Nat Commun. 2017;8:15790.
43. Komor AC, Zhao KT, Packer MS, Gaudelli NM, Waterbury AL, Koblan LW, Kim YB, Badran AH, Liu DR. Improved base excision repair inhibition and bacteriophage mu gam protein yields C:G-to-T:a base editors with higher efficiency and product purity. Sci Adv. 2017;3(8):eaao4774.
44. Gapinske M, Luu A, Winter J, Kostan K, Shiva N, Song JS, Perez-Pinera P. CRISPR-SKIP: programmable gene splicing with single base editors Data sets. Gene Expression Omnibus. https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE111646.