Altered Peptide Ligands Impact the Diversity of Polyfunctional Phenotypes in T Cell Receptor Gene-Modified T Cells

Mol Ther. 2018 Apr 4;26(4):996-1007. doi: 10.1016/j.ymthe.2018.01.015. Epub 2018 Feb 2.

Abstract

The use of T cell receptor (TCR) gene-modified T cells in adoptive cell transfer has had promising clinical success, but often, simple preclinical evaluation does not necessarily accurately predict treatment efficacy or safety. Preclinical studies generally evaluate one or a limited number of type 1 cytokines to assess antigen recognition. However, recent studies have implicated other "typed" T cells in effective anti-tumor/viral immunity, and limited functional evaluations may underestimate cross-reactivity. In this study, we use an altered peptide ligand (APL) model and multi-dimensional flow cytometry to evaluate polyfunctionality of TCR gene-modified T cells. Evaluating six cytokines and the lytic marker CD107a on a per cell basis revealed remarkably diverse polyfunctional phenotypes within a single T cell culture and among peripheral blood lymphocyte (PBL) donors. This polyfunctional assessment identified unexpected phenotypes, including cells producing both type 1 and type 2 cytokines, and highlighted interferon γneg (IFNγneg) antigen-reactive populations overlooked in our previous studies. Additionally, APLs skewed functional phenotypes to be less polyfunctional, which was not necessarily related to changes in TCR-peptide-major histocompatibility complex (pMHC) affinity. A better understanding of gene-modified T cell functional diversity may help identify optimal therapeutic phenotypes, predict clinical responses, anticipate off-target recognition, and improve the design and delivery of TCR gene-modified T cells.

Keywords: T cell; T cell receptor; adoptive cell therapy; affinity; altered peptide ligand; gene-modified T cells; multi-dimensional flow cytometry; polyfunctionality.

Publication types

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

MeSH terms

  • Biomarkers
  • Cells, Cultured
  • Cytokines / metabolism
  • Cytotoxicity, Immunologic
  • Histocompatibility Antigens / chemistry
  • Histocompatibility Antigens / immunology
  • Histocompatibility Antigens / metabolism
  • Humans
  • Immunophenotyping
  • Immunotherapy, Adoptive / methods
  • Ligands
  • Lymphocyte Activation
  • Models, Molecular
  • Peptides / chemistry
  • Peptides / metabolism*
  • Phenotype*
  • Protein Binding
  • Protein Conformation
  • Receptors, Antigen, T-Cell / chemistry
  • Receptors, Antigen, T-Cell / genetics*
  • Receptors, Antigen, T-Cell / metabolism*
  • Receptors, Chimeric Antigen / genetics*
  • Receptors, Chimeric Antigen / metabolism*
  • Structure-Activity Relationship
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism*

Substances

  • Biomarkers
  • Cytokines
  • Histocompatibility Antigens
  • Ligands
  • Peptides
  • Receptors, Antigen, T-Cell
  • Receptors, Chimeric Antigen