CD154 Resistant to Cleavage from Intracellular Milieu and Cell Surface Induces More Potent CD40-Mediated Responses

J Immunol. 2021 Apr 15;206(8):1793-1805. doi: 10.4049/jimmunol.2001340. Epub 2021 Mar 24.

Abstract

In addition to the membrane-bound form, CD154 also exists as a soluble molecule originating from an intracellular and membrane cleavage. We have previously shown that CD154 cleavage from T cell surface is mediated by CD40 and involves the action of ADAM10/ADAM17 enzymes. In the aim of defining the importance of CD154 maintained on cell surface, we generated a CD154 mutated at the cleavage site. Our data show that the double mutation of E112 and M113 residues of CD154 abolishes its spontaneous release and the CD40-mediated cleavage from cell surface but does not affect its binding to CD40. We also demonstrated that both the release of CD154 from the intracellular milieu and its CD40-mediated cleavage from cell surface are highly dependent on ADAM10/ADAM17 enzymes. The CD154-EM mutant was shown capable of inducing a more prominent apoptotic response in susceptible B cell lines than the wild-type (WT) form of the molecule. In addition, human B cells cultured in the presence of the CD154-EM mutant exhibited upregulated proliferative responses compared with the CD154-WT. The CD154-EM mutant was also shown to trigger differentiation of human B cells, reflected by an increased Ig production, more significantly than CD154-WT. Thus, our data strongly suggest that cleavage-resistant CD154 is a more prominent stimulant than the cleavable form of the molecule. Therefore, a maintained expression of CD154 on cell membrane and a disturbed cleavage of the molecule could be a mechanism by which CD154 is involved in some pathological conditions and should be revisited.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADAM10 Protein / metabolism
  • ADAM17 Protein / metabolism
  • Apoptosis
  • B-Lymphocytes / metabolism*
  • CD40 Antigens / metabolism*
  • CD40 Ligand / genetics
  • CD40 Ligand / metabolism*
  • Cell Differentiation
  • Cell Membrane / metabolism*
  • HEK293 Cells
  • Humans
  • Immunoglobulins / metabolism
  • Intracellular Space / metabolism*
  • Mutagenesis, Site-Directed
  • Mutation / genetics
  • Protein Binding
  • Proteolysis
  • Signal Transduction
  • T-Lymphocytes / metabolism*

Substances

  • CD40 Antigens
  • Immunoglobulins
  • CD40 Ligand
  • ADAM10 Protein
  • ADAM17 Protein