TBK1-Zyxin signaling controls tumor-associated macrophage recruitment to mitigate antitumor immunity

EMBO J. 2024 Nov;43(21):4984-5017. doi: 10.1038/s44318-024-00244-9. Epub 2024 Sep 20.

Abstract

Mechanical control is fundamental for cellular localization within a tissue, including for tumor-associated macrophages (TAMs). While the innate immune sensing pathways cGAS-STING and RLR-MAVS impact the pathogenesis and therapeutics of malignant diseases, their effects on cell residency and motility remain incompletely understood. Here, we uncovered that TBK1 kinase, activated by cGAS-STING or RLR-MAVS signaling in macrophages, directly phosphorylates and mobilizes Zyxin, a key regulator of actin dynamics. Under pathological conditions and in STING or MAVS signalosomes, TBK1-mediated Zyxin phosphorylation at S143 facilitates rapid recruitment of phospho-Zyxin to focal adhesions, leading to subsequent F-actin reorganization and reduced macrophage migration. Intratumoral STING-TBK1-Zyxin signaling was evident in TAMs and critical in antitumor immunity. Furthermore, myeloid-specific or global disruption of this signaling decreased the population of CD11b+ F4/80+ TAMs and promoted PD-1-mediated antitumor immunotherapy. Thus, our findings identify a new biological function of innate immune sensing pathways by regulating macrophage tissue localization, thus providing insights into context-dependent mitigation of antitumor immunity.

Keywords: Antitumor Immunity; Cell Motility; TBK1; Tumor-associated Macrophages; cGAS-STING.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Cell Movement
  • Humans
  • Immunity, Innate
  • Macrophages / immunology
  • Macrophages / metabolism
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Neoplasms / immunology
  • Neoplasms / metabolism
  • Neoplasms / pathology
  • Phosphorylation
  • Protein Serine-Threonine Kinases* / genetics
  • Protein Serine-Threonine Kinases* / metabolism
  • Signal Transduction*
  • Tumor-Associated Macrophages* / immunology
  • Tumor-Associated Macrophages* / metabolism

Substances

  • Protein Serine-Threonine Kinases
  • Tbk1 protein, mouse
  • Membrane Proteins
  • Sting1 protein, mouse