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CTCF-Binding Elements Mediate Accessibility of RAG Substrates During Chromatin Scanning.

Suvi Jain1, Zhaoqing Ba1, Yu Zhang1

  • 1Howard Hughes Medical Institute; Program in Cellular and Molecular Medicine, Boston Children's Hospital, and Department of Genetics, Harvard Medical School, Boston, MA 02115, USA.

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Summary

CTCF-binding elements (CBEs) near antibody V(D)J recombination sites enhance V(D)J recombination efficiency. This occurs through an unexpected chromatin accessibility function, particularly when the IGCR1 control region is inactive.

Keywords:
3C-HTGTSCBE orientationCTCF-binding elementsHTGTS-Rep-seqRAG chromatin scanningV(D)J recombinationV(H) accessibilityV(H)81Xintergenic control region 1loop extrusion

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Area of Science:

  • Immunology
  • Molecular Biology
  • Genetics

Background:

  • Antibody heavy chain variable region (V(D)J) exon assembly is initiated by RAG endonuclease at a V(D)J recombination center (RC).
  • The IGCR1 control region facilitates DJ(H) intermediate formation by sequestering D, J(H), and RC elements from upstream V(H) segments via a chromatin loop anchored by CTCF-binding elements (CBEs).

Purpose of the Study:

  • To investigate the mechanism by which V(H) segments access the DJ(H)RC for V(H) to DJ(H) rearrangement.
  • To elucidate the role of CBEs in V(H) segment accessibility and recombination potential.

Main Methods:

  • Investigated the function of CBEs located downstream of V(H)-recombination signal sequences (RSSs).
  • Analyzed V(H) to DJ(H) rearrangement efficiency in the presence and absence of functional IGCR1.
  • Utilized a model of RAG endonuclease-mediated chromatin scanning and loop extrusion.

Main Results:

  • CBEs downstream of V(H)-RSSs significantly enhance the recombination potential of associated V(H) segments beyond RSS function alone.
  • This CBE-mediated enhancement is particularly pronounced upon IGCR1 inactivation, revealing an unanticipated chromatin accessibility-enhancing function.
  • In the absence of IGCR1, CBEs stabilize interactions between D-proximal V(H) segments encountered during linear RAG scanning, promoting their preferential rearrangement.

Conclusions:

  • CBEs play a critical role in promoting V(H) segment accessibility and enhancing V(D)J recombination.
  • The findings reveal a novel mechanism where CBEs facilitate V(H) access to the DJ(H)RC, particularly under conditions of compromised IGCR1 function.
  • This highlights an unexpected role for CBEs in regulating antibody gene rearrangement through chromatin accessibility modulation.