Blockade of the CD47/SIRPα checkpoint axis potentiates the macrophage-mediated antitumor efficacy of tafasitamab

Haematologica. 2024 Dec 1;109(12):3928-3940. doi: 10.3324/haematol.2023.284795.

Abstract

Macrophages are one of the key mediators of the therapeutic effects exerted by monoclonal antibodies, such as the anti-CD19 antibody tafasitamab, approved in combination with lenalidomide for the treatment of relapsed or refractory diffuse large B-cell lymphoma (DLBCL). However, antibody-dependent cellular phagocytosis (ADCP) in the tumor microenvironment can be counteracted by increased expression of the inhibitory receptor SIRPα on macrophages and its ligand, the immune checkpoint molecule CD47, on tumor cells. The aim of this study was to investigate the impact of the CD47-SIRPα axis on tafasitamab- mediated phagocytosis and explore the potential of anti-CD47 blockade to enhance its antitumor activity. Elevated expression of both SIRPα and CD47 was observed in DLBCL patient-derived lymph node biopsies compared to healthy control lymph nodes. CRISPR-mediated CD47 overexpression affected tafasitamab-mediated ADCP in vitro and increased expression of SIRPα on macrophages correlated with decreased ADCP activity of tafasitamab against DLBCL cell lines. A combination of tafasitamab and an anti-CD47 blocking antibody enhanced ADCP activity of in vitro-generated macrophages. Importantly, tafasitamab-mediated phagocytosis was elevated in combination with CD47 blockade using primary DLBCL cells and patient-derived lymphoma-associated macrophages in an autologous setting. Furthermore, lymphoma cells with low CD19 expression were efficiently eliminated by the combination treatment. Finally, combined treatment of tafasitamab and an anti-CD47 antibody resulted in enhanced tumor volume reduction and survival benefit in lymphoma xenograft mouse models. These findings provide evidence that CD47 blockade can enhance the phagocytic potential of tumor-targeting immunotherapies such as tafasitamab and suggest that there is value in exploring the combination in the clinic.

MeSH terms

  • Animals
  • Antibodies, Monoclonal, Humanized / pharmacology
  • Antibodies, Monoclonal, Humanized / therapeutic use
  • Antigens, Differentiation* / metabolism
  • CD47 Antigen* / antagonists & inhibitors
  • CD47 Antigen* / metabolism
  • Cell Line, Tumor
  • Humans
  • Lymphoma, Large B-Cell, Diffuse* / drug therapy
  • Lymphoma, Large B-Cell, Diffuse* / metabolism
  • Lymphoma, Large B-Cell, Diffuse* / pathology
  • Macrophages* / drug effects
  • Macrophages* / immunology
  • Macrophages* / metabolism
  • Mice
  • Phagocytosis / drug effects
  • Receptors, Immunologic* / antagonists & inhibitors
  • Receptors, Immunologic* / metabolism
  • Tumor Microenvironment / drug effects
  • Xenograft Model Antitumor Assays*

Substances

  • CD47 Antigen
  • Receptors, Immunologic
  • SIRPA protein, human
  • Antigens, Differentiation
  • CD47 protein, human
  • Antibodies, Monoclonal, Humanized

Grants and funding

Funding: HB was supported by the Wilhelm-Sander Foundation, by the Research Training Group 2740 “Immunomicrotope” (project B3), by the German Cancer Foundation (grant n. 70114489) and by the SFB TR 221 (project B12). MB-H was supported by the SFB TR 221 (project Z01). AL was supported by the Research Training Group 2740 “Immunomicrotope” (project A3).