The immunotoxicity, but not anti-tumor efficacy, of anti-CD40 and anti-CD137 immunotherapies is dependent on the gut microbiota

Cell Rep Med. 2021 Dec 8;2(12):100464. doi: 10.1016/j.xcrm.2021.100464. eCollection 2021 Dec 21.

Abstract

Immune agonist antibodies (IAAs) are promising immunotherapies that target co-stimulatory receptors to induce potent anti-tumor immune responses, particularly when combined with checkpoint inhibitors. Unfortunately, their clinical translation is hampered by serious dose-limiting, immune-mediated toxicities, including high-grade and sometimes fatal liver damage, cytokine release syndrome (CRS), and colitis. We show that the immunotoxicity, induced by the IAAs anti-CD40 and anti-CD137, is dependent on the gut microbiota. Germ-free or antibiotic-treated mice have significantly reduced colitis, CRS, and liver damage following IAA treatment compared with conventional mice or germ-free mice recolonized via fecal microbiota transplant. MyD88 signaling is required for IAA-induced CRS and for anti-CD137-induced, but not anti-CD40-induced, liver damage. Importantly, antibiotic treatment does not impair IAA anti-tumor efficacy, alone or in combination with anti-PD1. Our results suggest that microbiota-targeted therapies could overcome the toxicity induced by IAAs without impairing their anti-tumor activity.

Keywords: anti-CD137; anti-CD40; cytokine release syndrome; gut microbiota; immune agonist antibody; immunotherapy; liver damage.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Bacterial Agents / pharmacology
  • Antineoplastic Agents / pharmacology*
  • Bile Acids and Salts / metabolism
  • CD40 Antigens / immunology*
  • Cytokine Release Syndrome / immunology
  • Cytokine Release Syndrome / pathology
  • Fecal Microbiota Transplantation
  • Gastrointestinal Microbiome* / drug effects
  • Germ-Free Life
  • Immunotherapy / adverse effects*
  • Inflammation / pathology
  • Interferon Type I / metabolism
  • Lipid Metabolism / drug effects
  • Liver / drug effects
  • Liver / immunology
  • Liver / metabolism
  • Liver / pathology
  • Mice
  • Mice, Inbred C57BL
  • Myeloid Differentiation Factor 88 / metabolism
  • Signal Transduction / drug effects
  • Tumor Necrosis Factor Receptor Superfamily, Member 9 / immunology*
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Anti-Bacterial Agents
  • Antineoplastic Agents
  • Bile Acids and Salts
  • CD40 Antigens
  • Interferon Type I
  • Myeloid Differentiation Factor 88
  • Tumor Necrosis Factor Receptor Superfamily, Member 9
  • Tumor Necrosis Factor-alpha