Ubiquitin ligase MARCH 8 cooperates with CD83 to control surface MHC II expression in thymic epithelium and CD4 T cell selection

J Exp Med. 2016 Aug 22;213(9):1695-703. doi: 10.1084/jem.20160312. Epub 2016 Aug 8.

Abstract

Major histocompatibility complex class II (MHC II) expression is tightly regulated, being subjected to cell type-specific mechanisms that closely control its levels at the cell surface. Ubiquitination by the E3 ubiquitin ligase MARCH 1 regulates MHC II expression in dendritic cells and B cells. In this study, we demonstrate that the related ligase MARCH 8 is responsible for regulating surface MHC II in thymic epithelial cells (TECs). March8(-/-) mice have elevated MHC II at the surface of cortical TECs and autoimmune regulator (AIRE)(-) medullary TECs (mTECs), but not AIRE(+) mTECs. Despite this, thymic and splenic CD4(+) T cell numbers and repertoires remained unaltered in March8(-/-) mice. Notably, the ubiquitination of MHC II by MARCH 8 is controlled by CD83. Mice expressing a mutated form of CD83 (Cd83(anu/anu) mice) have impaired CD4(+) T cell selection, but deleting March8 in Cd83(anu/anu) mice restored CD4(+) T cell selection to normal levels. Therefore, orchestrated regulation of MHC II surface expression in TECs by MARCH 8 and CD83 plays a major role in CD4(+) T cell selection. Our results also highlight the specialized use of ubiquitinating machinery in distinct antigen-presenting cell types, with important functional consequences and implications for therapeutic manipulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, CD / physiology*
  • CD4-Positive T-Lymphocytes / immunology*
  • CD83 Antigen
  • Epithelial Cells / immunology*
  • Histocompatibility Antigens Class II / metabolism*
  • Immunoglobulins / physiology*
  • Membrane Glycoproteins / physiology*
  • Mice
  • Mice, Inbred C57BL
  • Thymus Gland / diagnostic imaging*
  • Thymus Gland / immunology
  • Ubiquitin-Protein Ligases / physiology*
  • Ubiquitination

Substances

  • Antigens, CD
  • Histocompatibility Antigens Class II
  • Immunoglobulins
  • Membrane Glycoproteins
  • March8 protein, mouse
  • Ubiquitin-Protein Ligases