A biomimetic five-module chimeric antigen receptor (5MCAR) designed to target and eliminate antigen-specific T cells

Proc Natl Acad Sci U S A. 2020 Nov 17;117(46):28950-28959. doi: 10.1073/pnas.2012495117. Epub 2020 Nov 2.

Abstract

T cells express clonotypic T cell receptors (TCRs) that recognize peptide antigens in the context of class I or II MHC molecules (pMHCI/II). These receptor modules associate with three signaling modules (CD3γε, δε, and ζζ) and work in concert with a coreceptor module (either CD8 or CD4) to drive T cell activation in response to pMHCI/II. Here, we describe a first-generation biomimetic five-module chimeric antigen receptor (5MCAR). We show that 1) chimeric receptor modules built with the ectodomains of pMHCII assemble with CD3 signaling modules into complexes that redirect cytotoxic T lymphocyte (CTL) specificity and function in response to the clonotypic TCRs of pMHCII-specific CD4+ T cells, and 2) surrogate coreceptor modules enhance the function of these complexes. Furthermore, we demonstrate that adoptively transferred 5MCAR-CTLs can mitigate type I diabetes by targeting autoimmune CD4+ T cells in NOD mice. This work provides a framework for the construction of biomimetic 5MCARs that can be used as tools to study the impact of particular antigen-specific T cells in immune responses, and may hold potential for ameliorating diseases mediated by pathogenic T cells.

Keywords: 5M-CAR; CAR; T1D; TCR; pMHC.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens / immunology
  • Antigens / metabolism*
  • Biomimetics / methods*
  • CD4-Positive T-Lymphocytes
  • CD8-Positive T-Lymphocytes
  • Female
  • Lymphocyte Activation / immunology
  • Male
  • Mice
  • Mice, Inbred NOD
  • Mice, SCID
  • Pancreas / immunology
  • Pancreas / pathology
  • Receptors, Antigen, T-Cell
  • Receptors, Chimeric Antigen / metabolism*
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism*
  • T-Lymphocytes, Cytotoxic / immunology

Substances

  • Antigens
  • Receptors, Antigen, T-Cell
  • Receptors, Chimeric Antigen