The immunostimulatory RNA RN7SL1 enables CAR-T cells to enhance autonomous and endogenous immune function

Cell. 2021 Sep 16;184(19):4981-4995.e14. doi: 10.1016/j.cell.2021.08.004. Epub 2021 Aug 30.

Abstract

Poor tumor infiltration, development of exhaustion, and antigen insufficiency are common mechanisms that limit chimeric antigen receptor (CAR)-T cell efficacy. Delivery of pattern recognition receptor agonists is one strategy to improve immune function; however, targeting these agonists to immune cells is challenging, and off-target signaling in cancer cells can be detrimental. Here, we engineer CAR-T cells to deliver RN7SL1, an endogenous RNA that activates RIG-I/MDA5 signaling. RN7SL1 promotes expansion and effector-memory differentiation of CAR-T cells. Moreover, RN7SL1 is deployed in extracellular vesicles and selectively transferred to immune cells. Unlike other RNA agonists, transferred RN7SL1 restricts myeloid-derived suppressor cell (MDSC) development, decreases TGFB in myeloid cells, and fosters dendritic cell (DC) subsets with costimulatory features. Consequently, endogenous effector-memory and tumor-specific T cells also expand, allowing rejection of solid tumors with CAR antigen loss. Supported by improved endogenous immunity, CAR-T cells can now co-deploy peptide antigens with RN7SL1 to enhance efficacy, even when heterogenous CAR antigen tumors lack adequate neoantigens.

Keywords: CAR-T cells, RN7SL1, 7SL, pattern recognition receptors, RIG-I, MDA5, interferon, exosomes, extracellular vesicles.

Publication types

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

MeSH terms

  • Animals
  • Antigens / metabolism
  • CD8-Positive T-Lymphocytes / immunology
  • Cell Line, Tumor
  • DEAD Box Protein 58 / metabolism
  • Dendritic Cells / drug effects
  • Dendritic Cells / metabolism
  • Extracellular Vesicles / metabolism
  • Humans
  • Immunity / drug effects
  • Immunocompetence
  • Immunologic Factors / pharmacology*
  • Immunologic Memory
  • Immunotherapy
  • Interferons / metabolism
  • Melanoma, Experimental / pathology
  • Mice
  • Mice, Inbred C57BL
  • Myeloid Cells / drug effects
  • Myeloid Cells / metabolism
  • Peptides / metabolism
  • RNA / pharmacology*
  • Receptors, Chimeric Antigen / immunology*
  • Receptors, Pattern Recognition / metabolism
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / immunology*

Substances

  • Antigens
  • Immunologic Factors
  • Peptides
  • Receptors, Chimeric Antigen
  • Receptors, Pattern Recognition
  • RNA
  • Interferons
  • Ddx58 protein, mouse
  • DEAD Box Protein 58