Versatile strategy for controlling the specificity and activity of engineered T cells

Proc Natl Acad Sci U S A. 2016 Jan 26;113(4):E450-8. doi: 10.1073/pnas.1524193113. Epub 2016 Jan 12.

Abstract

The adoptive transfer of autologous T cells engineered to express a chimeric antigen receptor (CAR) has emerged as a promising cancer therapy. Despite impressive clinical efficacy, the general application of current CAR-T--cell therapy is limited by serious treatment-related toxicities. One approach to improve the safety of CAR-T cells involves making their activation and proliferation dependent upon adaptor molecules that mediate formation of the immunological synapse between the target cancer cell and T-cell. Here, we describe the design and synthesis of structurally defined semisynthetic adaptors we refer to as "switch" molecules, in which anti-CD19 and anti-CD22 antibody fragments are site-specifically modified with FITC using genetically encoded noncanonical amino acids. This approach allows the precise control over the geometry and stoichiometry of complex formation between CD19- or CD22-expressing cancer cells and a "universal" anti-FITC-directed CAR-T cell. Optimization of this CAR-switch combination results in potent, dose-dependent in vivo antitumor activity in xenograft models. The advantage of being able to titrate CAR-T-cell in vivo activity was further evidenced by reduced in vivo toxicity and the elimination of persistent B-cell aplasia in immune-competent mice. The ability to control CAR-T cell and cancer cell interactions using intermediate switch molecules may expand the scope of engineered T-cell therapy to solid tumors, as well as indications beyond cancer therapy.

Keywords: B-cell aplasia; cancer immunotherapy; chimeric antigen receptor T cell; cytokine release syndrome; noncanonical amino acids.

MeSH terms

  • Animals
  • Antigens, CD19 / immunology*
  • Antigens, Neoplasm / immunology*
  • Azides
  • B-Lymphocytes / immunology
  • B-Lymphocytes / pathology
  • Cell Line, Tumor
  • Cytotoxicity, Immunologic
  • Female
  • Fluorescein-5-isothiocyanate
  • Genetic Vectors
  • Humans
  • Immunotherapy, Adoptive / adverse effects
  • Immunotherapy, Adoptive / methods*
  • Lentivirus / genetics
  • Leukemia, B-Cell / therapy*
  • Lymphocyte Activation
  • Lymphopenia / etiology
  • Lymphopenia / prevention & control
  • Mice
  • Mice, Inbred C57BL
  • Mice, Inbred NOD
  • Mice, SCID
  • Models, Molecular
  • Phenylalanine / analogs & derivatives
  • Protein Conformation
  • Protein Engineering / methods*
  • Receptors, Antigen, T-Cell / genetics
  • Receptors, Antigen, T-Cell / immunology*
  • Recombinant Fusion Proteins / immunology
  • Sialic Acid Binding Ig-like Lectin 2 / immunology*
  • Single-Chain Antibodies / genetics
  • Single-Chain Antibodies / immunology
  • T-Cell Antigen Receptor Specificity*
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / transplantation
  • Transduction, Genetic
  • Xenograft Model Antitumor Assays

Substances

  • Antigens, CD19
  • Antigens, Neoplasm
  • Azides
  • CD22 protein, human
  • CTL019 chimeric antigen receptor
  • Receptors, Antigen, T-Cell
  • Recombinant Fusion Proteins
  • Sialic Acid Binding Ig-like Lectin 2
  • Single-Chain Antibodies
  • 4-azidophenylalanine
  • Phenylalanine
  • Fluorescein-5-isothiocyanate