Developmental partitioning of SYK and ZAP70 prevents autoimmunity and cancer

Mol Cell. 2021 May 20;81(10):2094-2111.e9. doi: 10.1016/j.molcel.2021.03.043. Epub 2021 Apr 19.

Abstract

Even though SYK and ZAP70 kinases share high sequence homology and serve analogous functions, their expression in B and T cells is strictly segregated throughout evolution. Here, we identified aberrant ZAP70 expression as a common feature in a broad range of B cell malignancies. We validated SYK as the kinase that sets the thresholds for negative selection of autoreactive and premalignant clones. When aberrantly expressed in B cells, ZAP70 competes with SYK at the BCR signalosome and redirects SYK from negative selection to tonic PI3K signaling, thereby promoting B cell survival. In genetic mouse models for B-ALL and B-CLL, conditional expression of Zap70 accelerated disease onset, while genetic deletion impaired malignant transformation. Inducible activation of Zap70 during B cell development compromised negative selection of autoreactive B cells, resulting in pervasive autoantibody production. Strict segregation of the two kinases is critical for normal B cell selection and represents a central safeguard against the development of autoimmune disease and B cell malignancies.

Keywords: Anergy; B cell selection; Kinases; Leukemia; NFAT; Tolerance.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, CD19 / metabolism
  • Autoimmunity*
  • B-Lymphocytes
  • Calcium / metabolism
  • Cell Differentiation
  • Cell Transformation, Neoplastic
  • Enzyme Activation
  • Humans
  • Immune Tolerance
  • Lymphoma, B-Cell / enzymology
  • Lymphoma, B-Cell / pathology
  • Mice
  • Models, Genetic
  • NFATC Transcription Factors / metabolism
  • Neoplasm Proteins
  • Neoplasms / enzymology*
  • Neoplasms / prevention & control*
  • Phosphatidylinositol 3-Kinases / metabolism
  • Protein Binding
  • Receptors, Antigen, B-Cell / metabolism
  • Signal Transduction
  • Syk Kinase / metabolism*
  • ZAP-70 Protein-Tyrosine Kinase / metabolism*

Substances

  • Antigens, CD19
  • NFATC Transcription Factors
  • Neoplasm Proteins
  • Receptors, Antigen, B-Cell
  • Syk Kinase
  • ZAP-70 Protein-Tyrosine Kinase
  • Calcium