Neddylation modification stabilizes LC3B by antagonizing its ubiquitin-mediated degradation and promoting autophagy in skin

Proc Natl Acad Sci U S A. 2025 Apr 15;122(15):e2411429122. doi: 10.1073/pnas.2411429122. Epub 2025 Apr 10.

Abstract

The Atg8-family proteins, including LC3B (microtubule-associated protein 1 light chain 3 beta), are pivotal for key steps in the autophagy process. Proper regulation of LC3B homeostasis is essential for its function. Although LC3B is modulated by various posttranslational modifications (PTMs), the impact of these modifications on LC3B protein homeostasis remains unclear. Neddylation, a recently identified ubiquitin-like modification, plays diverse biological roles. Here, we identify LC3B as a specific target for neddylation. This modification weakens LC3B's interaction with the ubiquitin E3 ligases VHL and BIRC6, thereby reducing LC3B ubiquitination. Depletion of ubiquitin-conjugating enzyme E2M (UBE2M), the primary E2 enzyme in the neddylation pathway, destabilizes LC3B and suppresses autophagy activity. Heterozygous Ube2m knockout (Ube2m+/-) mice exhibit pronounced aging-like phenotypes, with reduced LC3B expression and impaired autophagy in skin tissues. Our findings demonstrate that LC3B neddylation is vital for maintaining its stability and regulating autophagy flux, offering a potential therapeutic avenue to mitigate aging-related processes.

Keywords: LC3B; UBE2M; autophagy; neddylation; skin aging.

MeSH terms

  • Aging* / genetics
  • Aging* / metabolism
  • Animals
  • Autophagy*
  • Autophagy-Related Proteins* / metabolism
  • Carrier Proteins / metabolism
  • Cullin Proteins / metabolism
  • Female
  • Male
  • Mice
  • Mice, Knockout
  • Microtubule-Associated Proteins* / genetics
  • Microtubule-Associated Proteins* / metabolism
  • NEDD8 Protein* / genetics
  • NEDD8 Protein* / metabolism
  • Protein Processing, Post-Translational*
  • Protein Stability
  • Proteolysis*
  • Skin Aging
  • Skin* / metabolism
  • Ubiquitin* / metabolism
  • Ubiquitin-Conjugating Enzymes* / genetics
  • Ubiquitin-Conjugating Enzymes* / metabolism

Substances

  • Ubiquitin
  • Microtubule-Associated Proteins
  • Map1lc3b protein, mouse
  • Autophagy-Related Proteins
  • Ubiquitin-Conjugating Enzymes
  • Nedd8 protein, mouse
  • NEDD8 Protein
  • Cul2 protein, mouse
  • RBX1 protein, mouse
  • Cullin Proteins
  • Carrier Proteins