RNA 2'-O-methylation promotes persistent R-loop formation and AID-mediated IgH class switch recombination

BMC Biol. 2024 Jul 8;22(1):151. doi: 10.1186/s12915-024-01947-5.

Abstract

Background: RNA-DNA hybrids or R-loops are associated with deleterious genomic instability and protective immunoglobulin class switch recombination (CSR). However, the underlying phenomenon regulating the two contrasting functions of R-loops is unknown. Notably, the underlying mechanism that protects R-loops from classic RNase H-mediated digestion thereby promoting persistence of CSR-associated R-loops during CSR remains elusive.

Results: Here, we report that during CSR, R-loops formed at the immunoglobulin heavy (IgH) chain are modified by ribose 2'-O-methylation (2'-OMe). Moreover, we find that 2'-O-methyltransferase fibrillarin (FBL) interacts with activation-induced cytidine deaminase (AID) associated snoRNA aSNORD1C to facilitate the 2'-OMe. Moreover, deleting AID C-terminal tail impairs its association with aSNORD1C and FBL. Disrupting FBL, AID or aSNORD1C expression severely impairs 2'-OMe, R-loop stability and CSR. Surprisingly, FBL, AID's interaction partner and aSNORD1C promoted AID targeting to the IgH locus.

Conclusion: Taken together, our results suggest that 2'-OMe stabilizes IgH-associated R-loops to enable productive CSR. These results would shed light on AID-mediated CSR and explain the mechanism of R-loop-associated genomic instability.

Keywords: 2'-O-methylation (2'-OMe); Activation-induced cytidine deaminase (AID); Class switching recombination (CSR); R-loop.

MeSH terms

  • AICDA (Activation-Induced Cytidine Deaminase)
  • Animals
  • Cytidine Deaminase* / chemistry
  • Cytidine Deaminase* / genetics
  • Cytidine Deaminase* / metabolism
  • Immunoglobulin Class Switching* / genetics
  • Immunoglobulin Heavy Chains / genetics
  • Immunoglobulin Heavy Chains / metabolism
  • Methylation
  • Mice
  • R-Loop Structures*
  • RNA / genetics
  • RNA / metabolism
  • Recombination, Genetic

Substances

  • Cytidine Deaminase
  • AICDA (Activation-Induced Cytidine Deaminase)
  • Immunoglobulin Heavy Chains
  • RNA