Impaired T cell proliferation by ex vivo BET-inhibition impedes adoptive immunotherapy in a murine melanoma model

Epigenetics. 2020 Jan-Feb;15(1-2):134-144. doi: 10.1080/15592294.2019.1656156. Epub 2019 Aug 26.

Abstract

Activation of naïve CD8+ T cells stimulates proliferation and differentiation into cytotoxic T-lymphocytes (CTLs). Adoptive T Cell Therapy (ACT) involves multiple rounds of ex vivo activation to generate enough CTLs for reinfusion into patients, but this drives differentiation into terminal effector T cells. Less differentiated CTL populations, such as stem cell memory T cells, are more ideal candidates for ACT because of increased self-renewal and persistent properties. Ex vivo targeting of T cell differentiation with epigenetic modifiers is a potential strategy to improve cytotoxic T-lymphocyte (CTL) generation for ACT. We established a pipeline to assess the effects of epigenetic modifiers on CD8+ T cell proliferation, differentiation, and efficacy in a preclinical melanoma model. Single treatment with epigenetic modifiers inhibited T cell proliferation in vitro, producing CD44hiCD62Lhi effector-like T cells rather than a stem cell memory T cell phenotype. Most epigenetic modifying agents had no significant effect on ACT efficacy with the notable exception of the bromodomain and extraterminal (BET)-inhibitor JQ1 which was associated with a decrease in efficacy compared to unmodified T cells. These findings reveal the complexity of epigenetic targeting of T cell differentiation, highlighting the need to precisely define the epigenetic targeting strategies to improve CTL generation for ACT.

Keywords: BET inhibition; Cancer immunotherapy; T cell differentiation; adoptive cell therapy; cytotoxic T lymphocytes; melanoma.

MeSH terms

  • Animals
  • Azepines / pharmacology
  • Benzodiazepines / pharmacology
  • Cell Differentiation
  • Cell Line, Tumor
  • Cell Proliferation*
  • Cells, Cultured
  • Epigenesis, Genetic*
  • Immunotherapy, Adoptive / methods*
  • Indolizines / pharmacology
  • Melanoma, Experimental / therapy*
  • Mice
  • Mice, Inbred C57BL
  • Sulfones / pharmacology
  • T-Lymphocytes / cytology
  • T-Lymphocytes / drug effects*
  • T-Lymphocytes / immunology
  • T-Lymphocytes / physiology
  • Triazoles / pharmacology

Substances

  • (+)-JQ1 compound
  • 1-(1-(3-(methylsulfonyl)phenyl)-7-propoxyindolizin-3-yl)ethanone
  • Azepines
  • Indolizines
  • Sulfones
  • Triazoles
  • Benzodiazepines
  • molibresib

Grants and funding

This work was supported by a project grant and Fellowship from the Children’s Leukaemia and Cancer Research Foundation, Western Australia (to MNC). JC was supported by a Cancer Council Western Australia Suzanne Cavanagh Early Career Investigator Award, and a US Department of Defense Peer Reviewed Cancer Program Cancer Horizon Award. JW was supported by fellowships from the NHMRC and Cancer Council WA.