4-1BB and CD28 signaling plays a synergistic role in redirecting umbilical cord blood T cells against B-cell malignancies

Hum Gene Ther. 2010 Jan;21(1):75-86. doi: 10.1089/hum.2009.122.

Abstract

Umbilical cord blood (UCB) T cells can be redirected to kill leukemia and lymphoma cells by engineering with a single-chain chimeric antigen receptor (CAR) and thus may have general applications in adoptive cell therapy. However, the role of costimulatory molecules in UCB T-cell activation and effector functions in context with CAR remains elusive. To investigate the effect of costimulatory molecules (4-1BB and CD28) on UCB T cells, we transduced UCB T cells with lentiviral vectors expressing Green Fluorescent Protein (GFP) and CAR for CD19 containing an intracellular domain of the CD3zeta chain and either a 4-1BB (UCB-19BBzeta) or a CD28 intracellular domain (UCB-1928zeta), both (UCB-1928BBzeta), or neither (UCB-19zeta). We found that UCB-19BBzeta and UCB-28BBzeta T cells exhibited more cytotoxicity to CD19(+) leukemia and lymphoma cell lines than UCB-19zeta and UCB-1928zeta, although differences in secretion of interleukin-2 and interferon-gamma by these T cells were not evident. In vivo adoptive transfer of these T cells into intraperitoneal tumor-bearing mice demonstrated that UCB-19BBzeta and UCB-1928BBzeta T cells mounted the most potent antitumor response. The mice adoptively transferred with UCB-1928BBzeta cells survived longer than the mice with UCB-19BBzeta. Moreover, UCB-1928BBzeta T cells mounted a more robust antitumor response than UCB-19BBzeta in a systemic tumor model. Our data suggest a synergistic role of 4-1BB and CD28 costimulation in engineering antileukemia UCB effector cells and implicate a design for redirected UCB T-cell therapy for refractory leukemia.

MeSH terms

  • Animals
  • Antigens, CD19 / metabolism
  • B-Lymphocytes / immunology
  • B-Lymphocytes / pathology*
  • CD28 Antigens / metabolism*
  • Cell Line, Tumor
  • Cytotoxicity, Immunologic
  • Fetal Blood / cytology*
  • Green Fluorescent Proteins / metabolism
  • Humans
  • Immunophenotyping
  • Interferon-gamma / biosynthesis
  • Interleukin-2 / biosynthesis
  • Lentivirus / genetics
  • Leukemia / immunology
  • Leukemia / pathology
  • Leukemia / therapy*
  • Lymphoma / immunology
  • Lymphoma / pathology
  • Mice
  • Mice, SCID
  • Recombinant Proteins / metabolism
  • Signal Transduction*
  • T-Lymphocytes / cytology
  • T-Lymphocytes / immunology*
  • Transduction, Genetic
  • Tumor Necrosis Factor Receptor Superfamily, Member 9 / metabolism*

Substances

  • Antigens, CD19
  • CD28 Antigens
  • Interleukin-2
  • Recombinant Proteins
  • Tumor Necrosis Factor Receptor Superfamily, Member 9
  • Green Fluorescent Proteins
  • Interferon-gamma