TSC2 Interacts with HDLBP/Vigilin and Regulates Stress Granule Formation

Mol Cancer Res. 2021 Aug;19(8):1389-1397. doi: 10.1158/1541-7786.MCR-20-1046. Epub 2021 Apr 22.

Abstract

Tuberous sclerosis complex (TSC) is caused by mutations of either the TSC1 or TSC2 tumor suppressor gene. TSC causes tumors of the brain, heart, kidney, skin and lymphangioleiomyomatosis (LAM). Here we report that the TSC2 protein physically binds to high-density lipoprotein binding protein (HDLBP), also called vigilin, a core stress granule (SG) protein, and that TSC2 localizes to SGs. SGs contain mRNAs and translation initiation complexes, and regulate gene expression by sequestering specific transcripts, thereby serving a cytoprotective role. TSC2 has never before been shown to localize to SGs and knocking down vigilin impacts SG translocation of TSC2. TSC2-deficient cells showed a striking increase in the number of SGs after thermal shock and arsenite treatment relative to Tsc2-expressing cells. Our findings also show that murine kidney lysates from a model of TSC have increased levels of SG components including G3BP1 and Caprin1. G3BP1 and Caprin are elevated in renal angiomyolipomas (a renal tumor common in patients with TSC) compared with control normal kidney. G3BP1 is also elevated in TSC-associated subependymal giant cell astrocytomas. We found that genetic inhibition of G3BP1 inhibits the proliferation of TSC2-deficient cells in vitro. Finally, in a mouse model of TSC, genetic inhibition of SGs suppresses cell growth, suggesting that targeting SGs may have efficacy in the therapy of TSC. IMPLICATIONS: This study demonstrates that TSC2 physically interacts with HDLBP/vigilin, a component of SGs, that TSC2 localizes to SG and that TSC2-deficient cells have more SGs, suggesting that SGs represent a novel therapeutic target in TSC.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiomyolipoma / metabolism
  • Angiomyolipoma / pathology
  • Animals
  • Cell Line
  • Cell Line, Tumor
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • Kidney Neoplasms / metabolism
  • Kidney Neoplasms / pathology
  • Lymphangioleiomyomatosis / metabolism
  • Lymphangioleiomyomatosis / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • RNA Recognition Motif Proteins / metabolism
  • RNA, Messenger / metabolism
  • RNA-Binding Proteins / metabolism*
  • Stress Granules / metabolism*
  • Stress Granules / pathology
  • Tuberous Sclerosis Complex 2 Protein / metabolism*
  • Tumor Suppressor Proteins / metabolism

Substances

  • RNA Recognition Motif Proteins
  • RNA, Messenger
  • RNA-Binding Proteins
  • TSC2 protein, human
  • Tuberous Sclerosis Complex 2 Protein
  • Tumor Suppressor Proteins
  • high density lipoprotein binding protein