Inhibition of B cell receptor signaling induced by the human adenovirus species D E3/49K protein

Front Immunol. 2024 Jul 30:15:1432226. doi: 10.3389/fimmu.2024.1432226. eCollection 2024.

Abstract

Introduction: The early transcription unit 3 (E3) of human adenoviruses (HAdVs) encodes several immunoevasins, including the E3/49K protein, which is unique for species D of HAdVs. It is expressed as surface transmembrane protein and shed. E3/49K of HAdV-D64 binds to the protein tyrosine phosphatase surface receptor CD45, thereby modulating activation of T and NK cells.

Methods: Considering that E3/49K represents the most polymorphic viral protein among species D HAdVs, we demonstrate here that all tested E3/49K orthologs bind to the immunologically important regulator CD45. Thus, this feature is conserved regardless of the pathological associations of the respective HAdV types.

Results: It appeared that modulation of CD45 is a unique property restricted to HAdVs of species D. Moreover, E3/49K treatment inhibited B cell receptor (BCR) signaling and impaired BCR signal phenotypes. The latter were highly comparable to B cells having defects in the expression of CD45, suggesting E3/49K as a potential tool to investigate CD45 specific functions.

Conclusion: We identified B cells as new direct target of E3/49K-mediated immune modulation, representing a novel viral immunosubversive mechanism.

Keywords: BCR signaling; CD45; E3/49K; adenovirus; immunoevasion.

MeSH terms

  • Adenovirus E3 Proteins* / genetics
  • Adenovirus E3 Proteins* / immunology
  • Adenovirus E3 Proteins* / metabolism
  • Adenovirus Infections, Human / immunology
  • Adenovirus Infections, Human / metabolism
  • Adenovirus Infections, Human / virology
  • Adenoviruses, Human* / immunology
  • B-Lymphocytes* / immunology
  • B-Lymphocytes* / metabolism
  • HEK293 Cells
  • Humans
  • Leukocyte Common Antigens* / immunology
  • Leukocyte Common Antigens* / metabolism
  • Receptors, Antigen, B-Cell* / immunology
  • Receptors, Antigen, B-Cell* / metabolism
  • Signal Transduction* / immunology

Substances

  • Receptors, Antigen, B-Cell
  • Leukocyte Common Antigens
  • Adenovirus E3 Proteins
  • PTPRC protein, human

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This work was supported by grants from the German Ministry of Education and Research (BMBF) via projects VIRASTORM 03VNE1059C and ADENOTHECA 16LW0230. The project was also supported by the Excellence Initiative of the German Research Foundation (GSC-35 4, Spemann Graduate School), the Ministry for Science, Research and Arts of the State of Baden-Wuerttemberg to PC, by the Alexander von Humboldt Foundation through a research fellowship to MB and the Deutsche Forschungsgemeinschaft through HE2526/9–2 to HH.