Ikaros regulation of the BCL6/BACH2 axis and its clinical relevance in acute lymphoblastic leukemia

Oncotarget. 2017 Jan 31;8(5):8022-8034. doi: 10.18632/oncotarget.14038.

Abstract

B-Cell CLL/Lymphoma 6 (BCL6) is a proto-oncogene that is highly expressed in acute lymphoblastic leukemia (ALL). BTB and CNC Homology 1 Basic Leucine Zipper Transcription Factor 2 (BACH2) is a suppressor of transcription. The BACH2-BCL6 balance controls selection at the pre-B cell receptor checkpoint by regulating p53 expression. However, the underlying mechanism and the clinical relevance of the BCL6/BACH2 axis are unknown. Here, we found that Ikaros, a tumor suppressor encoded by IKZF1, directly binds to both the BCL6 and BACH2 promoters where it suppresses BCL6 and promotes BACH2 expression in B-cell ALL (B-ALL) cells. Casein kinase 2 (CK2) inhibitors increase Ikaros function thereby inhibiting BCL6 and promoting BACH2 expression in an Ikaros-dependent manner. We also found that the expression of BCL6 is higher while BACH2 expression is lower in patients with B-ALL than normal bone marrow control. High BCL6 and low BACH2 expression is associated with high leukemic cell proliferation, unfavorable clinical and laboratory features, and inferior outcomes. Moreover, IKZF1 deletion is associated with high BCL6 and low BACH2 expression in B-ALL patients. CK2 inhibitors increase Ikaros binding to the promoter of BCL6 and BACH2 and suppress BCL6 while promoting BACH2 expression in the primary B-ALL cells. Our data indicates that Ikaros regulates expression of the BCL6/BACH2 axis in B-ALL. High BCL6 and low BACH2 expression are associated with Ikaros dysregulation and have a potential effect on the development of B-ALL.

Keywords: BACH2; BCL6; IKZF1; acute lymphoblastic leukemia.

MeSH terms

  • Adolescent
  • Adult
  • Aged
  • Basic-Leucine Zipper Transcription Factors / genetics
  • Basic-Leucine Zipper Transcription Factors / metabolism*
  • Binding Sites
  • Casein Kinase II / antagonists & inhibitors
  • Casein Kinase II / metabolism
  • Cell Line, Tumor
  • Female
  • Gene Expression Regulation, Leukemic
  • Humans
  • Ikaros Transcription Factor / genetics
  • Ikaros Transcription Factor / metabolism*
  • Kaplan-Meier Estimate
  • Male
  • Middle Aged
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / genetics
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / metabolism*
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / mortality
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / pathology
  • Prognosis
  • Promoter Regions, Genetic
  • Protein Kinase Inhibitors / pharmacology
  • Proto-Oncogene Mas
  • Proto-Oncogene Proteins c-bcl-6 / genetics
  • Proto-Oncogene Proteins c-bcl-6 / metabolism*
  • Signal Transduction
  • Time Factors
  • Transfection
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism*
  • Young Adult

Substances

  • BACH2 protein, human
  • BCL6 protein, human
  • Basic-Leucine Zipper Transcription Factors
  • IKZF1 protein, human
  • MAS1 protein, human
  • Protein Kinase Inhibitors
  • Proto-Oncogene Mas
  • Proto-Oncogene Proteins c-bcl-6
  • Tumor Suppressor Proteins
  • Ikaros Transcription Factor
  • Casein Kinase II