VAMP2 controls murine epidermal differentiation and carcinogenesis by regulation of nucleophagy

Dev Cell. 2024 Aug 5;59(15):2005-2016.e4. doi: 10.1016/j.devcel.2024.05.004. Epub 2024 May 28.

Abstract

Differentiation of murine epidermal stem/progenitor cells involves the permanent withdrawal from the cell cycle, the synthesis of various protein and lipid components for the cornified envelope, and the controlled dissolution of cellular organelles and nuclei. Deregulated epidermal differentiation contributes to the development of various skin diseases, including skin cancers. With a genome-wide shRNA screen, we identified vesicle-associated membrane protein 2 (VAMP2) as a critical factor involved in skin differentiation. Deletion of VAMP2 leads to aberrant skin stratification and enucleation in vivo. With quantitative proteomics, we further identified an autophagy protein, focal adhesion kinase family interacting protein of 200 kDa (FIP200), as a binding partner of VAMP2. Additionally, we showed that both VAMP2 and FIP200 are critical for murine keratinocyte enucleation and epidermal differentiation. Loss of VAMP2 or FIP200 enhances cutaneous carcinogenesis in vivo. Together, our findings identify important molecular mechanisms underlying epidermal differentiation and skin tumorigenesis.

Keywords: autophagy; differentiation; epidermal progenitor cells; skin; squamous cell carcinoma.

MeSH terms

  • Animals
  • Autophagy*
  • Autophagy-Related Proteins* / genetics
  • Autophagy-Related Proteins* / metabolism
  • Carcinogenesis* / genetics
  • Carcinogenesis* / metabolism
  • Carcinogenesis* / pathology
  • Cell Differentiation*
  • Cell Nucleus / metabolism
  • Epidermal Cells / metabolism
  • Epidermis* / metabolism
  • Epidermis* / pathology
  • Keratinocytes* / cytology
  • Keratinocytes* / metabolism
  • Mice
  • Mice, Knockout
  • Skin Neoplasms / genetics
  • Skin Neoplasms / metabolism
  • Skin Neoplasms / pathology
  • Vesicle-Associated Membrane Protein 2* / genetics
  • Vesicle-Associated Membrane Protein 2* / metabolism

Substances

  • Autophagy-Related Proteins
  • Rb1cc1 protein, mouse
  • Vesicle-Associated Membrane Protein 2
  • vesicle-associated membrane protein 2, mouse