Ovalbumin Antigen-Specific Activation of Human T Cell Receptor Closely Resembles Soluble Antibody Stimulation as Revealed by BOOST Phosphotyrosine Proteomics

J Proteome Res. 2021 Jun 4;20(6):3330-3344. doi: 10.1021/acs.jproteome.1c00239. Epub 2021 May 21.

Abstract

Activation of the T cell receptor (TCR) leads to a network of early signaling predominantly orchestrated by tyrosine phosphorylation in T cells. The TCR is commonly activated using soluble anti-TCR antibodies, but this approach is not antigen-specific. Alternatively, activating the TCR using specific antigens of a range of binding affinities in the form of a peptide-major histocompatibility complex (pMHC) is presumed to be more physiological. However, due to the lack of wide-scale phosphotyrosine (pTyr) proteomic studies directly comparing anti-TCR antibodies and pMHC, a comprehensive definition of these activated states remains enigmatic. Elucidation of the tyrosine phosphoproteome using quantitative pTyr proteomics enables a better understanding of the unique features of these activating agents and the role of ligand binding affinity on signaling. Here, we apply the recently established Broad-spectrum Optimization Of Selective Triggering (BOOST) to examine perturbations in tyrosine phosphorylation of human TCR triggered by anti-TCR antibodies and pMHC. Our data reveal that high-affinity ovalbumin (OVA) pMHC activation of the human TCR triggers a largely similar, albeit potentially stronger, pTyr-mediated signaling regulatory axis compared to the anti-TCR antibody. The signaling output resulting from OVA pMHC variants correlates well with their weaker affinities, enabling affinity-tunable control of signaling strength. Collectively, we provide a framework for applying BOOST to compare pTyr-mediated signaling pathways of human T cells activated in an antigen-independent and antigen-specific manner.

Keywords: BOOST; OT-1; OVA; T cell receptor; T cell signaling; TMT; pMHC; phosphotyrosine proteomics.

Publication types

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

MeSH terms

  • Antigens
  • Humans
  • Lymphocyte Activation
  • Ovalbumin
  • Phosphotyrosine
  • Protein Binding
  • Proteomics*
  • Receptors, Antigen, T-Cell*

Substances

  • Antigens
  • Receptors, Antigen, T-Cell
  • Phosphotyrosine
  • Ovalbumin