Regulation of B cell receptor-dependent NF-κB signaling by the tumor suppressor KLHL14

Proc Natl Acad Sci U S A. 2020 Mar 17;117(11):6092-6102. doi: 10.1073/pnas.1921187117. Epub 2020 Mar 3.

Abstract

The KLHL14 gene acquires frequent inactivating mutations in mature B cell malignancies, especially in the MYD88L265P, CD79B mutant (MCD) genetic subtype of diffuse large B cell lymphoma (DLBCL), which relies on B cell receptor (BCR) signaling for survival. However, the pathogenic role of KLHL14 in DLBCL and its molecular function are largely unknown. Here, we report that KLHL14 is in close proximity to the BCR in the endoplasmic reticulum of MCD cell line models and promotes the turnover of immature glycoforms of BCR subunits, reducing total cellular BCR levels. Loss of KLHL14 confers relative resistance to the Bruton tyrosine kinase (BTK) inhibitor ibrutinib and promotes assembly of the MYD88-TLR9-BCR (My-T-BCR) supercomplex, which initiates prosurvival NF-κB activation. Consequently, KLHL14 inactivation allows MCD cells to maintain NF-κB signaling in the presence of ibrutinib. These findings reinforce the central role of My-T-BCR-dependent NF-κB signaling in MCD DLBCL and suggest that the genetic status of KLHL14 should be considered in clinical trials testing inhibitors of BTK and BCR signaling mediators in DLBCL.

Keywords: B cell receptor; DLBCL; KLHL14; NF-κB.

Publication types

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

MeSH terms

  • Adenine / analogs & derivatives
  • CD79 Antigens / genetics
  • Carrier Proteins / genetics*
  • Carrier Proteins / metabolism
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm / genetics
  • Endoplasmic Reticulum / metabolism
  • Genes, Tumor Suppressor*
  • HEK293 Cells
  • Humans
  • Intracellular Signaling Peptides and Proteins
  • Lymphoma, Large B-Cell, Diffuse / genetics*
  • Lymphoma, Large B-Cell, Diffuse / pathology
  • Mutagenesis, Site-Directed
  • Myeloid Differentiation Factor 88 / metabolism
  • NF-kappa B / metabolism
  • Piperidines
  • Proteolysis
  • Pyrazoles / pharmacology
  • Pyrazoles / therapeutic use
  • Pyrimidines / pharmacology
  • Pyrimidines / therapeutic use
  • Receptors, Antigen, B-Cell / metabolism*
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Ubiquitin-Protein Ligase Complexes / metabolism*

Substances

  • CD79 Antigens
  • CD79B protein, human
  • Carrier Proteins
  • Intracellular Signaling Peptides and Proteins
  • KLHL14 protein, human
  • MYD88 protein, human
  • Myeloid Differentiation Factor 88
  • NF-kappa B
  • Piperidines
  • Pyrazoles
  • Pyrimidines
  • Receptors, Antigen, B-Cell
  • ibrutinib
  • Ubiquitin-Protein Ligase Complexes
  • Adenine