Different cytokine and stimulation conditions influence the expansion and immune phenotype of third-generation chimeric antigen receptor T cells specific for tumor antigen GD2

Cytotherapy. 2015 Apr;17(4):487-95. doi: 10.1016/j.jcyt.2014.12.002. Epub 2015 Jan 6.

Abstract

Background aims: Chimeric antigen receptor (CAR) T cells are a novel immunotherapy for cancer. To achieve anti-tumor efficacy, these cells must survive, expand, and persist after infusion into patients, functions that are reportedly best achieved by cells with a stem or central-memory rather than effector-memory phenotype. We have developed third-generation CAR T cells specific for the tumor-associated antigen GD2 for use in a phase I clinical trial. We investigated the optimal cell culture conditions for CAR T-cell production, and here we describe the relative effects of 3 activation and cytokine conditions on CAR T-cell expansion, effector function and phenotype.

Methods: Peripheral blood mononuclear cells were activated by anti-CD3 and anti-CD28 or anti-CD3 and Retronectin. Activated cells were transduced with the CAR-encoding retroviral vector and expanded in either interleukin (IL)-2 or IL-7 and IL-15. Immune phenotype and expansion were tracked throughout the culture, and transduction efficiency, and subsequent GD2-specific effector functions were evaluated by flow cytometry and cytotoxic T lymphocytes assay.

Results: CD3/Retronectin stimulation with IL-2 resulted in poorer activation, expansion and Th1 cytokine secretion of CAR T cells than CD3/CD28 stimulation with either IL-2 or IL-7 and IL-15. However, CAR T cells cultured in CD3/CD28/IL7/IL-15 and CD3/Retronectin/IL-2 had superior cytotoxic T lymphocyte activity and a more stem-like phenotype.

Discussion: The combination of CD3 and CD28 with IL-7 and IL-15 gave the best balance of CAR T-cell expansion and potent GD2-specific effector functions while retaining a stem/memory phenotype, and these growth conditions will therefore be used to manufacture CAR T cells for our phase I clinical trial.

Keywords: IL-15; IL-2; IL-7; Retronectin; anti-CD3 and anti-CD28 stimulation; chimeric antigen receptor T cells; effector function; immune phenotype.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adoptive Transfer
  • Antigens, Neoplasm / immunology*
  • CD28 Antigens / immunology
  • CD3 Complex / immunology
  • Cell Culture Techniques
  • Cell Line, Tumor
  • Fibronectins / pharmacology
  • Humans
  • Interleukin-15 / pharmacology
  • Interleukin-2 / pharmacology
  • Interleukin-7 / pharmacology
  • Leukocytes, Mononuclear / immunology
  • Lymphocyte Activation / immunology*
  • Phenotype
  • Receptors, Antigen, T-Cell / genetics
  • Receptors, Antigen, T-Cell / immunology*
  • Recombinant Fusion Proteins / immunology
  • Recombinant Proteins / pharmacology
  • T-Lymphocytes, Cytotoxic / immunology*
  • T-Lymphocytes, Cytotoxic / transplantation
  • Th1 Cells / immunology

Substances

  • Antigens, Neoplasm
  • CD28 Antigens
  • CD3 Complex
  • Fibronectins
  • IL15 protein, human
  • IL2 protein, human
  • IL7 protein, human
  • Interleukin-15
  • Interleukin-2
  • Interleukin-7
  • Receptors, Antigen, T-Cell
  • Recombinant Fusion Proteins
  • Recombinant Proteins
  • retronectin