CIGAR-seq, a CRISPR/Cas-based method for unbiased screening of novel mRNA modification regulators

Mol Syst Biol. 2020 Nov;16(11):e10025. doi: 10.15252/msb.202010025.

Abstract

Cellular RNA is decorated with over 170 types of chemical modifications. Many modifications in mRNA, including m6 A and m5 C, have been associated with critical cellular functions under physiological and/or pathological conditions. To understand the biological functions of these modifications, it is vital to identify the regulators that modulate the modification rate. However, a high-throughput method for unbiased screening of these regulators is so far lacking. Here, we report such a method combining pooled CRISPR screen and reporters with RNA modification readout, termed CRISPR integrated gRNA and reporter sequencing (CIGAR-seq). Using CIGAR-seq, we discovered NSUN6 as a novel mRNA m5 C methyltransferase. Subsequent mRNA bisulfite sequencing in HAP1 cells without or with NSUN6 and/or NSUN2 knockout showed that NSUN6 and NSUN2 worked on non-overlapping subsets of mRNA m5 C sites and together contributed to almost all the m5 C modification in mRNA. Finally, using m1 A as an example, we demonstrated that CIGAR-seq can be easily adapted for identifying regulators of other mRNA modification.

Keywords: CIGAR-seq; NSUN6; m5C modification; mRNA modification; pooled CRISPR screen.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • CRISPR-Cas Systems / genetics*
  • Cells, Cultured
  • Clustered Regularly Interspaced Short Palindromic Repeats / genetics
  • Gene Expression Regulation
  • Gene Regulatory Networks
  • Genetic Vectors / genetics
  • HEK293 Cells
  • Humans
  • Methylation
  • Methyltransferases / genetics*
  • Methyltransferases / metabolism
  • RNA Processing, Post-Transcriptional / genetics*
  • RNA, Guide, CRISPR-Cas Systems / genetics
  • RNA, Messenger / analysis
  • RNA, Messenger / metabolism*
  • Sequence Analysis, RNA / methods*
  • tRNA Methyltransferases / genetics

Substances

  • RNA, Guide, CRISPR-Cas Systems
  • RNA, Messenger
  • Methyltransferases
  • NSUN6 protein, human
  • tRNA Methyltransferases

Associated data

  • GEO/GSE157368