PRKAA2, MTOR, and TFEB in the regulation of lysosomal damage response and autophagy

J Mol Med (Berl). 2024 Mar;102(3):287-311. doi: 10.1007/s00109-023-02411-7. Epub 2024 Jan 6.

Abstract

Lysosomes function as critical signaling hubs that govern essential enzyme complexes. LGALS proteins (LGALS3, LGALS8, and LGALS9) are integral to the endomembrane damage response. If ESCRT fails to rectify damage, LGALS-mediated ubiquitination occurs, recruiting autophagy receptors (CALCOCO2, TRIM16, and SQSTM1) and VCP/p97 complex containing UBXN6, PLAA, and YOD1, initiating selective autophagy. Lysosome replenishment through biogenesis is regulated by TFEB. LGALS3 interacts with TFRC and TRIM16, aiding ESCRT-mediated repair and autophagy-mediated removal of damaged lysosomes. LGALS8 inhibits MTOR and activates TFEB for ATG and lysosomal gene transcription. LGALS9 inhibits USP9X, activates PRKAA2, MAP3K7, ubiquitination, and autophagy. Conjugation of ATG8 to single membranes (CASM) initiates damage repair mediated by ATP6V1A, ATG16L1, ATG12, ATG5, ATG3, and TECPR1. ATG8ylation or CASM activates the MERIT system (ESCRT-mediated repair, autophagy-mediated clearance, MCOLN1 activation, Ca2+ release, RRAG-GTPase regulation, MTOR modulation, TFEB activation, and activation of GTPase IRGM). Annexins ANAX1 and ANAX2 aid damage repair. Stress granules stabilize damaged membranes, recruiting FLCN-FNIP1/2, G3BP1, and NUFIP1 to inhibit MTOR and activate TFEB. Lysosomes coordinate the synergistic response to endomembrane damage and are vital for innate and adaptive immunity. Future research should unveil the collaborative actions of ATG proteins, LGALSs, TRIMs, autophagy receptors, and lysosomal proteins in lysosomal damage response.

Keywords: Autophagy receptors; LGALS; Lysosomal damage response; MTOR; PRKAA2; TFEB.

Publication types

  • Review

MeSH terms

  • Autophagy / genetics
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / metabolism
  • DNA Helicases*
  • Endosomal Sorting Complexes Required for Transport / metabolism
  • GTP Phosphohydrolases / metabolism
  • Galectin 3* / metabolism
  • Lysosomes / metabolism
  • Poly-ADP-Ribose Binding Proteins / metabolism
  • RNA Helicases / metabolism
  • RNA Recognition Motif Proteins / metabolism
  • TOR Serine-Threonine Kinases / metabolism

Substances

  • Galectin 3
  • DNA Helicases
  • Poly-ADP-Ribose Binding Proteins
  • RNA Helicases
  • RNA Recognition Motif Proteins
  • TOR Serine-Threonine Kinases
  • GTP Phosphohydrolases
  • Endosomal Sorting Complexes Required for Transport
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors