Engineered CD47 protects T cells for enhanced antitumour immunity

Nature. 2024 Jun;630(8016):457-465. doi: 10.1038/s41586-024-07443-8. Epub 2024 May 15.

Abstract

Adoptively transferred T cells and agents designed to block the CD47-SIRPα axis are promising cancer therapeutics that activate distinct arms of the immune system1,2. Here we administered anti-CD47 antibodies in combination with adoptively transferred T cells with the goal of enhancing antitumour efficacy but observed abrogated therapeutic benefit due to rapid macrophage-mediated clearance of T cells expressing chimeric antigen receptors (CARs) or engineered T cell receptors. Anti-CD47-antibody-mediated CAR T cell clearance was potent and rapid enough to serve as an effective safety switch. To overcome this challenge, we engineered the CD47 variant CD47(Q31P) (47E), which engages SIRPα and provides a 'don't eat me' signal that is not blocked by anti-CD47 antibodies. TCR or CAR T cells expressing 47E are resistant to clearance by macrophages after treatment with anti-CD47 antibodies, and mediate substantial, sustained macrophage recruitment to the tumour microenvironment. Although many of the recruited macrophages manifested an M2-like profile3, the combined therapy synergistically enhanced antitumour efficacy. Our study identifies macrophages as major regulators of T cell persistence and illustrates the fundamental challenge of combining T-cell-directed therapeutics with those designed to activate macrophages. It delivers a therapeutic approach that is capable of simultaneously harnessing the antitumour effects of T cells and macrophages, offering enhanced potency against solid tumours.

MeSH terms

  • Animals
  • Antibodies / immunology
  • Antibodies / therapeutic use
  • Antigens, Differentiation / immunology
  • Antigens, Differentiation / metabolism
  • CD47 Antigen* / genetics
  • CD47 Antigen* / immunology
  • CD47 Antigen* / metabolism
  • Cell Line, Tumor
  • Female
  • Humans
  • Immunotherapy, Adoptive* / methods
  • Macrophage Activation
  • Macrophages / cytology
  • Macrophages / immunology
  • Male
  • Mice
  • Neoplasms* / immunology
  • Neoplasms* / metabolism
  • Neoplasms* / therapy
  • Receptors, Antigen, T-Cell / genetics
  • Receptors, Antigen, T-Cell / immunology
  • Receptors, Antigen, T-Cell / metabolism
  • Receptors, Chimeric Antigen / genetics
  • Receptors, Chimeric Antigen / immunology
  • Receptors, Chimeric Antigen / metabolism
  • Receptors, Immunologic / immunology
  • Receptors, Immunologic / metabolism
  • T-Lymphocytes* / immunology
  • T-Lymphocytes* / metabolism
  • T-Lymphocytes* / transplantation
  • Tumor Microenvironment / immunology

Substances

  • Antigens, Differentiation
  • CD47 Antigen
  • CD47 protein, human
  • Receptors, Antigen, T-Cell
  • Receptors, Chimeric Antigen
  • Receptors, Immunologic
  • SIRPA protein, human
  • Antibodies