Microbial short-chain fatty acids modulate CD8+ T cell responses and improve adoptive immunotherapy for cancer

Nat Commun. 2021 Jul 1;12(1):4077. doi: 10.1038/s41467-021-24331-1.

Abstract

Emerging data demonstrate that the activity of immune cells can be modulated by microbial molecules. Here, we show that the short-chain fatty acids (SCFAs) pentanoate and butyrate enhance the anti-tumor activity of cytotoxic T lymphocytes (CTLs) and chimeric antigen receptor (CAR) T cells through metabolic and epigenetic reprograming. We show that in vitro treatment of CTLs and CAR T cells with pentanoate and butyrate increases the function of mTOR as a central cellular metabolic sensor, and inhibits class I histone deacetylase activity. This reprogramming results in elevated production of effector molecules such as CD25, IFN-γ and TNF-α, and significantly enhances the anti-tumor activity of antigen-specific CTLs and ROR1-targeting CAR T cells in syngeneic murine melanoma and pancreatic cancer models. Our data shed light onto microbial molecules that may be used for enhancing cellular anti-tumor immunity. Collectively, we identify pentanoate and butyrate as two SCFAs with therapeutic utility in the context of cellular cancer immunotherapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Butyrates / metabolism
  • CD8-Positive T-Lymphocytes / metabolism*
  • Cell Line, Tumor
  • Cytokines / metabolism
  • Fatty Acids, Volatile / metabolism*
  • Female
  • Immunologic Factors / metabolism*
  • Immunotherapy
  • Immunotherapy, Adoptive / methods*
  • Interferon-gamma
  • Interleukin-2 Receptor alpha Subunit
  • Megasphaera
  • Melanoma / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Microbiota / physiology*
  • Neoplasms / immunology*
  • Peptide Fragments
  • Receptor Tyrosine Kinase-like Orphan Receptors
  • Receptors, G-Protein-Coupled / genetics
  • T-Lymphocytes, Cytotoxic / immunology*
  • Tumor Necrosis Factor-alpha

Substances

  • Butyrates
  • Cytokines
  • FFAR3 protein, mouse
  • Fatty Acids, Volatile
  • Ffar2 protein, mouse
  • Il2ra protein, mouse
  • Immunologic Factors
  • Interleukin-2 Receptor alpha Subunit
  • Peptide Fragments
  • Receptors, G-Protein-Coupled
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma
  • Receptor Tyrosine Kinase-like Orphan Receptors
  • Ror1 protein, mouse

Supplementary concepts

  • Megasphaera massiliensis