The ASCIZ-DYNLL1 Axis Is Essential for TLR4-Mediated Antibody Responses and NF-κB Pathway Activation

Mol Cell Biol. 2021 Nov 22;41(12):e0025121. doi: 10.1128/MCB.00251-21. Epub 2021 Sep 20.

Abstract

Toll-like receptors (TLRs) and interleukin-1 (IL-1) receptors regulate immune and inflammatory responses by activating the NF-κB pathway. Here, we report that B-cell-specific loss of dynein light chain 1 (DYNLL1, LC8) or its designated transcription factor ASCIZ (ATMIN) leads to severely reduced in vivo antibody responses to TLR4-dependent but not T-cell-dependent antigens in mice. This defect was independent of DYNLL1's established roles in modulating BIM-dependent apoptosis and 53BP1-dependent antibody class-switch recombination. In B cells and fibroblasts, the ASCIZ-DYNLL1 axis was required for TLR4-, IL-1-, and CD40-mediated NF-κB pathway activation but dispensable for antigen receptor and tumor necrosis factor α (TNF-α) signaling. In contrast to previous reports that overexpressed DYNLL1 directly inhibits the phosphorylation and degradation of the NF-κB inhibitor IκBα, we found here that under physiological conditions, DYNLL1 is required for signal-specific activation of the NF-κB pathway upstream of IκBα. Our data identify DYNLL1 as a signal-specific regulator of the NF-κB pathway and indicate that it may act as a universal modulator of TLR4 (and IL-1) signaling with wide-ranging roles in inflammation and immunity.

Keywords: B-cell responses; BIM; DYNLL1; NF-κB; cell proliferation; immunization.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibody Formation / immunology*
  • B-Lymphocytes / immunology
  • CD40 Antigens / metabolism
  • Cells, Cultured
  • Cytoplasmic Dyneins / genetics
  • Cytoplasmic Dyneins / metabolism*
  • Immunoglobulin Class Switching / immunology
  • Mice
  • Mice, Inbred C57BL
  • NF-KappaB Inhibitor alpha / metabolism
  • NF-kappa B / metabolism*
  • T-Lymphocytes / immunology
  • Toll-Like Receptor 4 / immunology*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Tumor Necrosis Factor-alpha / metabolism
  • Tumor Suppressor p53-Binding Protein 1 / immunology

Substances

  • ATMIN protein, mouse
  • CD40 Antigens
  • NF-kappa B
  • Tlr4 protein, mouse
  • Tnf protein, mouse
  • Toll-Like Receptor 4
  • Transcription Factors
  • Trp53bp1 protein, mouse
  • Tumor Necrosis Factor-alpha
  • Tumor Suppressor p53-Binding Protein 1
  • NF-KappaB Inhibitor alpha
  • Cytoplasmic Dyneins
  • DYNLL1 protein, mouse