Deltex1 promotes protein kinase Cθ degradation and sustains Casitas B-lineage lymphoma expression

J Immunol. 2014 Aug 15;193(4):1672-80. doi: 10.4049/jimmunol.1301416. Epub 2014 Jul 7.

Abstract

The generation of T cell anergy is associated with upregulation of ubiquitin E3 ligases including Casitas B-lineage lymphoma (Cbl-b), Itch, gene related to anergy in lymphocyte, and deltex1 (DTX1). These E3 ligases attenuate T cell activation by targeting to signaling molecules. For example, Cbl-b and Itch promote the degradation of protein kinase Cθ (PKCθ) and phospholipase C-γ1 (PLC-γ1) in anergic Th1 cells. How these anergy-associated E3 ligases coordinate during T cell anergy remains largely unknown. In the current study, we found that PKCθ and PLC-γ1 are also downregulated by DTX1. DTX1 interacted with PKCθ and PLC-γ1 and stimulated the degradation of PKCθ and PLC-γ1. T cell anergy-induced proteolysis of PKCθ was prevented in Dtx1(-/-) T cells, supporting the essential role of DTX1 in PKCθ downregulation. Similar to Cbl-b and Itch, DTX1 promoted monoubiquitination of PKCθ. Proteasome inhibitor did not inhibit DTX1-directed PKCθ degradation, but instead DTX1 directed the relocalization of PKCθ into the lysosomal pathway. In addition, DTX1 interacted with Cbl-b and increased the protein levels of Cbl-b. We further demonstrated the possibility that, through the downregulation of PKCθ, DTX1 prevented PKCθ-induced Cbl-b degradation and increased Cbl-b protein stability. Our results suggest the coordination between E3 ligases during T cell anergy; DTX1 acts with Cbl-b to assure a more extensive silencing of PKCθ, whereas DTX1-mediated PKCθ degradation further stabilizes Cbl-b.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcimycin / pharmacology
  • Cell Line
  • Clonal Anergy
  • DNA-Binding Proteins / biosynthesis
  • DNA-Binding Proteins / genetics*
  • Down-Regulation
  • HEK293 Cells
  • Humans
  • Isoenzymes / biosynthesis
  • Isoenzymes / genetics
  • Isoenzymes / metabolism*
  • Jurkat Cells
  • Lymphocyte Activation / immunology
  • Lysosomes / immunology
  • Mice
  • Mice, Knockout
  • Oncogene Protein v-cbl / biosynthesis*
  • Oncogene Protein v-cbl / genetics
  • Phospholipase C gamma / biosynthesis
  • Phospholipase C gamma / metabolism
  • Proteasome Inhibitors / pharmacology
  • Protein Kinase C / biosynthesis
  • Protein Kinase C / genetics
  • Protein Kinase C / metabolism*
  • Protein Kinase C-theta
  • Proteolysis*
  • RNA Interference
  • RNA, Small Interfering
  • Th1 Cells / immunology*
  • Ubiquitin-Protein Ligases / biosynthesis
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitination
  • ZAP-70 Protein-Tyrosine Kinase / biosynthesis

Substances

  • DNA-Binding Proteins
  • Isoenzymes
  • Oncogene Protein v-cbl
  • Proteasome Inhibitors
  • RNA, Small Interfering
  • Calcimycin
  • Itch protein, mouse
  • Dtx1 protein, mouse
  • Ubiquitin-Protein Ligases
  • ZAP-70 Protein-Tyrosine Kinase
  • ZAP70 protein, human
  • Prkcq protein, mouse
  • Protein Kinase C
  • Protein Kinase C-theta
  • Phospholipase C gamma