Elements between the IgH variable (V) and diversity (D) clusters influence antisense transcription and lineage-specific V(D)J recombination

Proc Natl Acad Sci U S A. 2010 Dec 21;107(51):22207-12. doi: 10.1073/pnas.1015954107. Epub 2010 Dec 1.

Abstract

Ig and T-cell receptor (TCR) variable-region gene exons are assembled from component variable (V), diversity (D) and joining (J) gene segments during early B and T cell development. The RAG1/2 endonuclease initiates V(D)J recombination by introducing DNA double-strand breaks at borders of the germ-line segments. In mice, the Ig heavy-chain (IgH) locus contains, from 5' to 3', several hundred V(H) gene segments, 13 D segments, and 4 J(H) segments within a several megabase region. In developing B cells, IgH variable-region exon assembly is ordered with D to J(H) rearrangement occurring on both alleles before appendage of a V(H) segment. Also, IgH V(H) to DJ(H) rearrangement does not occur in T cells, even though DJ(H) rearrangements occur at low levels. In these contexts, V(D)J recombination is controlled by modulating substrate gene segment accessibility to RAG1/2 activity. To elucidate control elements, we deleted the 100-kb intergenic region that separates the V(H) and D clusters (generating ΔV(H)-D alleles). In both B and T cells, ΔV(H)-D alleles initiated high-level antisense and, at lower levels, sense transcription from within the downstream D cluster, with antisense transcripts extending into proximal V(H) segments. In developing T lymphocytes, activated germ-line antisense transcription was accompanied by markedly increased IgH D-to-J(H) rearrangement and substantial V(H) to DJ(H) rearrangement of proximal IgH V(H) segments. Thus, the V(H)-D intergenic region, and likely elements within it, can influence silencing of sense and antisense germ-line transcription from the IgH D cluster and thereby influence targeting of V(D)J recombination.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Animals
  • B-Lymphocytes / metabolism*
  • DNA, Intergenic / genetics
  • DNA, Intergenic / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Gene Rearrangement, B-Lymphocyte, Heavy Chain / physiology*
  • Genetic Loci / physiology
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism
  • Immunoglobulin Heavy Chains / biosynthesis*
  • Immunoglobulin Heavy Chains / genetics
  • Immunoglobulin Variable Region / biosynthesis*
  • Immunoglobulin Variable Region / genetics
  • Mice
  • Mice, Mutant Strains
  • RNA, Antisense / biosynthesis*
  • RNA, Antisense / genetics
  • T-Lymphocytes / metabolism
  • Transcription, Genetic / physiology*

Substances

  • DNA, Intergenic
  • DNA-Binding Proteins
  • Homeodomain Proteins
  • Immunoglobulin Heavy Chains
  • Immunoglobulin Variable Region
  • RNA, Antisense
  • Rag2 protein, mouse
  • RAG-1 protein