CD137 (4-1BB) stimulation leads to metabolic and functional reprogramming of human monocytes/macrophages enhancing their tumoricidal activity

Leukemia. 2021 Dec;35(12):3482-3496. doi: 10.1038/s41375-021-01287-1. Epub 2021 May 21.

Abstract

Immunotherapies have heralded a new era in the cancer treatment. In addition to checkpoint inhibitors, agonistic antibodies against co-stimulatory immune receptors hold the potential to invoke efficient antitumor immunity. Targeting CD137 has gained momentum based on its ability to drive NK- and T-cell-based responses. CD137-engaging mAbs have already entered clinical trials for different types of tumors showing promising results. Despite the efforts to translate CD137-mediated immunotherapy into clinical practice, little remains known regarding the role of CD137 in human monocytes/macrophages.We found CD137 being expressed on monocytes of healthy controls and at even higher levels in patients with multiple myeloma or CLL. CD137HI(GH) monocytes displayed a distinct phenotypic, transcriptomic, and metabolic profile. They possessed an increased phagocytic capacity enabling superior antibody-dependent phagocytosis (ADPC) of multiple myeloma and lymphoma cells that were treated with anti-CD38 or anti-CD20 mAbs. Triggering CD137 promoted both metabolic and tumoricidal activity in an extracellular signal-regulated kinase (ERK)-dependent fashion. In addition, we observed a phenotypic, transcriptomic, and functional skewing towards a M1-like phenotype.Overall, we introduce CD137 as a positive immune checkpoint on human monocytes/macrophages, which can have therapeutic implications especially in view of synergistic effects when combining CD137 agonists with tumor-targeting antibodies.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antibodies, Monoclonal / pharmacology
  • Antibody-Dependent Cell Cytotoxicity
  • Cells, Cultured
  • Cellular Reprogramming / immunology
  • Humans
  • Immunotherapy / methods*
  • Killer Cells, Natural / immunology
  • Macrophages / immunology*
  • Macrophages / metabolism
  • Monocytes / immunology*
  • Monocytes / metabolism
  • Multiple Myeloma / blood
  • Multiple Myeloma / drug therapy*
  • Multiple Myeloma / immunology*
  • Multiple Myeloma / metabolism
  • Phagocytosis
  • T-Lymphocytes / immunology
  • Tumor Necrosis Factor Receptor Superfamily, Member 9 / immunology*
  • Tumor Necrosis Factor Receptor Superfamily, Member 9 / metabolism

Substances

  • Antibodies, Monoclonal
  • TNFRSF9 protein, human
  • Tumor Necrosis Factor Receptor Superfamily, Member 9