RNA-Modified T Cells Mediate Effective Delivery of Immunomodulatory Cytokines to Brain Tumors

Mol Ther. 2019 Apr 10;27(4):837-849. doi: 10.1016/j.ymthe.2018.10.007. Epub 2018 Oct 17.

Abstract

With the presence of the blood-brain barrier (BBB), successful immunotherapeutic drug delivery to CNS malignancies remains a challenge. Immunomodulatory agents, such as cytokines, can reprogram the intratumoral microenvironment; however, systemic cytokine delivery has limited access to the CNS. To bypass the limitations of systemically administered cytokines, we investigated if RNA-modified T cells could deliver macromolecules directly to brain tumors. The abilities of T cells to cross the BBB and mediate direct cytotoxic killing of intracranial tumors make them an attractive tool as biological carriers. Using T cell mRNA electroporation, we demonstrated that activated T cells can be modified to secrete granulocyte macrophage colony-stimulating factor (GM-CSF) protein while retaining their inherent effector functions in vitro. GM-CSF RNA-modified T cells effectively delivered GM-CSF to intracranial tumors in vivo and significantly extended overall survival in an orthotopic treatment model. Importantly, GM-CSF RNA-modified T cells demonstrated superior anti-tumor efficacy as compared to unmodified T cells alone or in combination with systemic administration of recombinant GM-CSF. Anti-tumor effects were associated with increased IFN-γ secretion locally within the tumor microenvironment and systemic antigen-specific T cell expansion. These findings demonstrate that RNA-modified T cells may serve as a versatile platform for the effective delivery of biological agents to CNS tumors.

Keywords: RNA; T cells; adoptive cellular therapy; brain tumor; immunotherapy.

Publication types

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

MeSH terms

  • Animals
  • Blood-Brain Barrier / metabolism
  • Brain Neoplasms / mortality
  • Brain Neoplasms / therapy*
  • Cell Line, Tumor
  • Cell Survival / genetics
  • Cell- and Tissue-Based Therapy / methods*
  • Disease Models, Animal
  • Granulocyte-Macrophage Colony-Stimulating Factor / biosynthesis*
  • Granulocyte-Macrophage Colony-Stimulating Factor / therapeutic use
  • Green Fluorescent Proteins / metabolism
  • Immunotherapy, Adoptive / methods*
  • Interferon-gamma / biosynthesis
  • Lymphocyte Activation
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • RNA / genetics*
  • T-Lymphocytes / metabolism*
  • Transfection / methods
  • Tumor Microenvironment / genetics

Substances

  • IFNG protein, mouse
  • Green Fluorescent Proteins
  • RNA
  • Interferon-gamma
  • Granulocyte-Macrophage Colony-Stimulating Factor