A major isoform of the E3 ubiquitin ligase March-I in antigen-presenting cells has regulatory sequences within its gene

J Biol Chem. 2018 Mar 23;293(12):4478-4485. doi: 10.1074/jbc.RA118.001775. Epub 2018 Jan 29.

Abstract

Regulation of major histocompatibility complex class II (MHC-II) expression is important not only to maintain a diverse pool of MHC-II-peptide complexes but also to prevent development of autoimmunity. The membrane-associated RING-CH (March) E3 ubiquitin ligase March-I regulates ubiquitination and turnover of MHC-II-peptide complexes in resting dendritic cells (DCs) and B cells. However, activation of either cell type terminates March-I expression, thereby stabilizing MHC-II-peptide complexes. Despite March-I's important role in the biology of antigen-presenting cells (APCs), how expression of March-I mRNA is regulated remains unknown. We now show that both DCs and B cells possess a distinct isoform of March-I whose expression is regulated by a promoter located within the March-I gene. Using March-I promoter fragments to drive expression of GFP, we also identified a core promoter for expression of March-I in DCs and B cells, but not in fibroblasts, kidney cells, or epithelial cells, that contains regulatory regions that down-regulate March-I expression upon activation of DCs. Curiously, we found downstream sequence elements, present in the first coding exon of March-I in APCs, that confer regulation of March-I expression in activated APCs. In summary, our study identifies regulatory regions of the March-I gene that confer APC-specific expression and activation-induced modulation of March-I expression in DCs and B cells.

Keywords: antigen presentation; dendritic cell; gene regulation; intragenic promoter; major histocompatibility complex (MHC); ubiquitin ligase.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Animals
  • Antigen-Presenting Cells / cytology
  • Antigen-Presenting Cells / immunology*
  • Antigen-Presenting Cells / metabolism
  • B-Lymphocytes / cytology
  • B-Lymphocytes / immunology
  • B-Lymphocytes / metabolism
  • Cells, Cultured
  • Dendritic Cells / cytology
  • Dendritic Cells / immunology*
  • Dendritic Cells / metabolism
  • Epithelial Cells / cytology
  • Epithelial Cells / immunology
  • Epithelial Cells / metabolism
  • Gene Expression Regulation*
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Promoter Regions, Genetic
  • Protein Isoforms
  • RNA Stability
  • Regulatory Sequences, Nucleic Acid*
  • Ubiquitin-Protein Ligases / genetics*
  • Ubiquitin-Protein Ligases / immunology
  • Ubiquitin-Protein Ligases / metabolism

Substances

  • Protein Isoforms
  • MARCH1 protein, mouse
  • MARCHF1 protein, human
  • Ubiquitin-Protein Ligases