Attenuating homologous recombination stimulates an AID-induced antileukemic effect

J Exp Med. 2013 May 6;210(5):1021-33. doi: 10.1084/jem.20121258.

Abstract

Activation-induced cytidine deaminase (AID) is critical in normal B cells to initiate somatic hypermutation and immunoglobulin class switch recombination. Accumulating evidence suggests that AID is also prooncogenic, inducing cancer-promoting mutations or chromosome rearrangements. In this context, we find that AID is expressed in >40% of primary human chronic lymphocytic leukemia (CLL) cases, consistent with other reports. Using a combination of human B lymphoid leukemia cells and mouse models, we now show that AID expression can be harnessed for antileukemic effect, after inhibition of the RAD51 homologous recombination (HR) factor with 4,4'-diisothiocyanatostilbene-2-2'-disulfonic acid (DIDS). As a proof of principle, we show that DIDS treatment inhibits repair of AID-initiated DNA breaks, induces apoptosis, and promotes cytotoxicity preferentially in AID-expressing human CLL. This reveals a novel antineoplastic role of AID that can be triggered by inhibition of HR, suggesting a potential new paradigm to treat AID-expressing tumors. Given the growing list of tumor types with aberrant AID expression, this novel therapeutic approach has potential to impact a significant patient population.

MeSH terms

  • 4,4'-Diisothiocyanostilbene-2,2'-Disulfonic Acid / pharmacology
  • Active Transport, Cell Nucleus / drug effects
  • Active Transport, Cell Nucleus / radiation effects
  • Animals
  • B-Lymphocytes / drug effects
  • B-Lymphocytes / enzymology
  • B-Lymphocytes / pathology
  • B-Lymphocytes / radiation effects
  • Cell Death / drug effects
  • Cell Death / radiation effects
  • Cell Line, Transformed
  • Cell Line, Tumor
  • Cell Nucleus / drug effects
  • Cell Nucleus / metabolism
  • Cytidine Deaminase / genetics
  • Cytidine Deaminase / metabolism*
  • DNA Breaks, Double-Stranded / drug effects
  • DNA Breaks, Double-Stranded / radiation effects
  • DNA Repair / drug effects
  • DNA Repair / radiation effects
  • Gene Expression Regulation, Leukemic / drug effects
  • Gene Expression Regulation, Leukemic / radiation effects
  • Histones / metabolism
  • Homologous Recombination / drug effects
  • Homologous Recombination / genetics*
  • Homologous Recombination / radiation effects
  • Humans
  • Leukemia, Lymphocytic, Chronic, B-Cell / enzymology*
  • Leukemia, Lymphocytic, Chronic, B-Cell / genetics*
  • Mice
  • Rad51 Recombinase / metabolism
  • Radiation, Ionizing

Substances

  • H2AX protein, human
  • Histones
  • Rad51 Recombinase
  • AICDA (activation-induced cytidine deaminase)
  • Cytidine Deaminase
  • 4,4'-Diisothiocyanostilbene-2,2'-Disulfonic Acid