Improving CRISPR-Cas9 directed faithful transgene integration outcomes by reducing unwanted random DNA integration

J Biomed Sci. 2024 Mar 26;31(1):32. doi: 10.1186/s12929-024-01020-x.

Abstract

Background: The field of genome editing has been revolutionized by the development of an easily programmable editing tool, the CRISPR-Cas9. Despite its promise, off-target activity of Cas9 posed a great disadvantage for genome editing purposes by causing DNA double strand breaks at off-target locations and causing unwanted editing outcomes. Furthermore, for gene integration applications, which introduce transgene sequences, integration of transgenes to off-target sites could be harmful, hard to detect, and reduce faithful genome editing efficiency.

Method: Here we report the development of a multicolour fluorescence assay for studying CRISPR-Cas9-directed gene integration at an endogenous locus in human cell lines. We examine genetic integration of reporter genes in transiently transfected cells as well as puromycin-selected stable cell lines to determine the fidelity of multiple CRISPR-Cas9 strategies.

Result: We found that there is a high occurrence of unwanted DNA integration which tarnished faithful knock-in efficiency. Integration outcomes are influenced by the type of DNA DSBs, donor design, the use of enhanced specificity Cas9 variants, with S-phase regulated Cas9 activity. Moreover, restricting Cas9 expression with a self-cleaving system greatly improves knock-in outcomes by substantially reducing the percentage of cells with unwanted DNA integration.

Conclusion: Our results highlight the need for a more stringent assessment of CRISPR-Cas9-mediated knock-in outcomes, and the importance of careful strategy design to maximise efficient and faithful transgene integration.

Keywords: CRISPR–Cas9; Faithful genome editing; Homology arms; Knock-in; Off-target; Self-cleaving.

MeSH terms

  • CRISPR-Cas Systems*
  • DNA
  • DNA Breaks, Double-Stranded
  • Gene Editing* / methods
  • Humans
  • Transgenes

Substances

  • DNA