Switch-mediated activation and retargeting of CAR-T cells for B-cell malignancies

Proc Natl Acad Sci U S A. 2016 Jan 26;113(4):E459-68. doi: 10.1073/pnas.1524155113. Epub 2016 Jan 12.

Abstract

Chimeric antigen receptor T (CAR-T) cell therapy has produced impressive results in clinical trials for B-cell malignancies. However, safety concerns related to the inability to control CAR-T cells once infused into the patient remain a significant challenge. Here we report the engineering of recombinant antibody-based bifunctional switches that consist of a tumor antigen-specific Fab molecule engrafted with a peptide neo-epitope, which is bound exclusively by a peptide-specific switchable CAR-T cell (sCAR-T). The switch redirects the activity of the bio-orthogonal sCAR-T cells through the selective formation of immunological synapses, in which the sCAR-T cell, switch, and target cell interact in a structurally defined and temporally controlled manner. Optimized switches specific for CD19 controlled the activity, tissue-homing, cytokine release, and phenotype of sCAR-T cells in a dose-titratable manner in a Nalm-6 xenograft rodent model of B-cell leukemia. The sCAR-T-cell dosing regimen could be tuned to provide efficacy comparable to the corresponding conventional CART-19, but with lower cytokine levels, thereby offering a method of mitigating cytokine release syndrome in clinical translation. Furthermore, we demonstrate that this methodology is readily adaptable to targeting CD20 on cancer cells using the same sCAR-T cell, suggesting that this approach may be broadly applicable to heterogeneous and resistant tumor populations, as well as other liquid and solid tumor antigens.

Keywords: antibody engineering; autologous cell therapy; cancer; chimeric antigen receptor T cell; leukemia.

Publication types

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

MeSH terms

  • Animals
  • Antigens, CD19 / immunology*
  • Antigens, Neoplasm / immunology*
  • Azides
  • B-Lymphocytes / immunology
  • B-Lymphocytes / pathology
  • Basic-Leucine Zipper Transcription Factors / immunology
  • Cell Line, Tumor
  • Cytokines / metabolism
  • Cytotoxicity, Immunologic
  • Dose-Response Relationship, Immunologic
  • Female
  • Genes, Reporter
  • Genetic Vectors
  • Humans
  • Immunotherapy, Adoptive / adverse effects
  • Immunotherapy, Adoptive / methods*
  • Leukemia, B-Cell / therapy*
  • Lymphocyte Activation
  • Lymphopenia / etiology
  • Lymphopenia / prevention & control
  • Mice
  • Mice, Inbred C57BL
  • Mice, Inbred NOD
  • Mice, SCID
  • Phenylalanine / analogs & derivatives
  • Protein Engineering / methods
  • Receptors, Antigen, T-Cell / genetics
  • Receptors, Antigen, T-Cell / immunology*
  • Recombinant Fusion Proteins / immunology
  • Saccharomyces cerevisiae Proteins / immunology
  • Sialic Acid Binding Ig-like Lectin 2 / immunology*
  • Single-Chain Antibodies / genetics
  • Single-Chain Antibodies / immunology
  • Structure-Activity Relationship
  • T-Cell Antigen Receptor Specificity*
  • T-Lymphocyte Subsets / immunology*
  • T-Lymphocyte Subsets / transplantation
  • Xenograft Model Antitumor Assays

Substances

  • Antigens, CD19
  • Antigens, Neoplasm
  • Azides
  • Basic-Leucine Zipper Transcription Factors
  • CD22 protein, human
  • Cytokines
  • GCN4 protein, S cerevisiae
  • Receptors, Antigen, T-Cell
  • Recombinant Fusion Proteins
  • Saccharomyces cerevisiae Proteins
  • Sialic Acid Binding Ig-like Lectin 2
  • Single-Chain Antibodies
  • 4-azidophenylalanine
  • Phenylalanine