A novel mechanistic framework for precise sequence replacement using reverse transcriptase and diverse CRISPR-Cas systems

CRISPR/Cas systems coupled with reverse transcriptase (RT), such as the recently described Prime editing, allow for site-specific replacement of DNA sequences. Despite widespread testing of Prime editing, it is currently only compatible with type II CRISPR/Cas proteins such as Streptococcus pyogenes and Staphylococcus aureus Cas9. Enabling RT compatibility with other CRISPR/Cas domains, such as type V enzymes with orthogonal protospacer adjacent motif specificities and smaller protein size would expand the range of edits that can be made in therapeutic and industrial applications. We achieve this with a novel mode of DNA editing at CRISPR-targeted sites that reverse transcribes the edit into the target strand DNA (e.g., the complement of the PAM-containing strand), rather than the non-target strand DNA, as in Prime editing. We term this technology RNA encoded DNA replacement of alleles with CRISPR (hereafter, REDRAW). We show that REDRAW extends the utility of RT-mediated editing beyond type II to include multiple type V CRISPR domains. REDRAW features a broad (8-10 bases) targeting window, at which all types of substitutions, insertions and deletions are possible. REDRAW combines the advantages of type V CRISPR domains with the extensive range of genetic variation enabled by RT-mediated, templated sequence replacement strategies.

[1]  Matthew S. McNeill,et al.  Optimized design parameters for CRISPR Cas9 and Cas12a homology-directed repair , 2021, Scientific Reports.

[2]  Simon P. Shen,et al.  Engineered pegRNAs improve prime editing efficiency , 2021, Nature Biotechnology.

[3]  Y. E. Chen,et al.  MiCas9 increases large size gene knock-in rates and reduces undesirable on-target and off-target indel edits , 2020, Nature Communications.

[4]  Yiliang Zhang,et al.  A Cas12a ortholog with stringent PAM recognition followed by low off-target editing rates for genome editing , 2020, Genome Biology.

[5]  G. Montoya,et al.  CRISPR-Cas12a: Functional overview and applications , 2020, Biomedical journal.

[6]  David R. Liu,et al.  Search-and-replace genome editing without double-strand breaks or donor DNA , 2019, Nature.

[7]  Huiqing Zhou,et al.  Programmable RNA-Guided RNA Effector Proteins Built from Human Parts , 2019, Cell.

[8]  Matthew C. Canver,et al.  CRISPResso2 provides accurate and rapid genome editing sequence analysis , 2019, Nature Biotechnology.

[9]  Jonathan L. Schmid-Burgk,et al.  Engineering of CRISPR-Cas12b for human genome editing , 2019, Nature Communications.

[10]  Luca Pinello,et al.  Engineered CRISPR-Cas12a variants with increased activities and improved targeting ranges for gene, epigenetic and base editing , 2018, Nature Biotechnology.

[11]  Li Yang,et al.  Base editing with a Cpf1–cytidine deaminase fusion , 2018, Nature Biotechnology.

[12]  Feng Zhang,et al.  Engineered Cpf1 variants with altered PAM specificities increase genome targeting range , 2017, Nature Biotechnology.

[13]  Lei S. Qi,et al.  CRISPR/Cas9 in Genome Editing and Beyond. , 2016, Annual review of biochemistry.

[14]  Martin J. Aryee,et al.  Genome-wide specificities of CRISPR-Cas Cpf1 nucleases in human cells , 2016, Nature Biotechnology.

[15]  Kira S. Makarova,et al.  Crystal Structure of Cpf1 in Complex with Guide RNA and Target DNA , 2016, Cell.

[16]  Ines Fonfara,et al.  The CRISPR-associated DNA-cleaving enzyme Cpf1 also processes precursor CRISPR RNA , 2016, Nature.

[17]  David R. Liu,et al.  Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage , 2016, Nature.

[18]  J. Doudna,et al.  The new frontier of genome engineering with CRISPR-Cas9 , 2014, Science.

[19]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[20]  A. Das,et al.  Opening of the TAR hairpin in the HIV-1 genome causes aberrant RNA dimerization and packaging , 2012, Retrovirology.

[21]  T. Ha,et al.  Human Rad52 binds and wraps single-stranded DNA and mediates annealing via two hRad52–ssDNA complexes , 2010, Nucleic acids research.

[22]  N. Pavletich,et al.  Mechanism of homologous recombination from the RecA–ssDNA/dsDNA structures , 2008, Nature.

[23]  H. Puchta The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution. , 2004, Journal of experimental botany.

[24]  J. D. Bendtsen,et al.  Identification and Characterization of the Single-Stranded DNA-Binding Protein of Bacteriophage P1 , 1999, Journal of bacteriology.

[25]  E. Blackburn,et al.  The telomerase RNA pseudoknot is critical for the stable assembly of a catalytically active ribonucleoprotein. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[26]  S. Salzberg,et al.  FLASH: fast length adjustment of short reads to improve genome assemblies , 2011, Bioinform..

[27]  Guo-Min Li,et al.  Mechanisms and functions of DNA mismatch repair , 2008, Cell Research.