R-Loop Depletion by Over-expressed RNase H1 in Mouse B Cells Increases Activation-Induced Deaminase Access to the Transcribed Strand without Altering Frequency of Isotype Switching

J Mol Biol. 2017 Oct 27;429(21):3255-3263. doi: 10.1016/j.jmb.2016.12.020. Epub 2017 Jan 6.

Abstract

R-loops, three-strand structures consisting of mRNA hybridized to the complementary DNA and a single-stranded DNA loop, are formed in switch regions on the heavy-chain immunoglobulin locus. To determine if R-loops have a direct effect on any of the steps involved in isotype switching, we generated a transgenic mouse that over-expressed RNase H1, an enzyme that cleaves the RNA of RNA/DNA hybrids in B cells. R-loops in the switch μ region were depleted by 70% in ex vivo activated splenic B cells. Frequencies of isotype switching to IgG1, IgG2b, IgG2c, and IgG3 were the same as C57BL/6 control cells. However, somatic hypermutation was increased specifically on the transcribed strand from μ-γ joins, indicating that R-loops limit activation-induced (cytosine) deaminase access to the transcribed DNA strand. Our data suggest that, in the normal G+C-rich context of mammalian class switch recombination regions, R-loops are obligatory intermediates. Processing of the R-loops is needed to remove RNA allowing activation-induced (cytosine) deaminase to promote somatic hypermutation on both DNA strands to generate double-strand DNA breaks for efficient class switch recombination. One of the two cellular RNases H may assist in this process.

Keywords: R-loops; RNase H1; class switch recombination; somatic hypermutation; transgenic mouse.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Animals
  • B-Lymphocytes / metabolism*
  • Cytidine Deaminase / genetics
  • Cytidine Deaminase / metabolism*
  • DNA Breaks, Double-Stranded
  • Female
  • Immunoglobulin Class Switching / genetics*
  • Immunoglobulin Isotypes / genetics*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Nucleic Acid Conformation*
  • Recombination, Genetic*
  • Ribonuclease H / physiology*
  • Somatic Hypermutation, Immunoglobulin

Substances

  • Immunoglobulin Isotypes
  • Ribonuclease H
  • ribonuclease HI
  • AICDA (activation-induced cytidine deaminase)
  • Cytidine Deaminase