IFNγ-induced Chemokines Are Required for CXCR3-mediated T-Cell Recruitment and Antitumor Efficacy of Anti-HER2/CD3 Bispecific Antibody

Clin Cancer Res. 2018 Dec 15;24(24):6447-6458. doi: 10.1158/1078-0432.CCR-18-1139. Epub 2018 Jun 27.

Abstract

Purpose: The response to cancer immune therapy is dependent on endogenous tumor-reactive T cells. To bypass this requirement, CD3-bispecific antibodies have been developed to induce a polyclonal T-cell response against the tumor. Anti-HER2/CD3 T-cell-dependent bispecific (TDB) antibody is highly efficacious in the treatment of HER2-overexpressing tumors in mice. Efficacy and immunologic effects of anti-HER2/CD3 TDB were investigated in mammary tumor model with very few T cells prior treatment. We further describe the mechanism for TDB-induced T-cell recruitment to tumors.

Experimental design: The immunologic effects and the mechanism of CD3-bispecific antibody-induced T-cell recruitment into spontaneous HER2-overexpressing mammary tumors was studied using human HER2 transgenic, immunocompetent mouse models.

Results: Anti-HER2/CD3 TDB treatment induced an inflammatory response in tumors converting them from poorly infiltrated to an inflamed, T-cell abundant, phenotype. Multiple mechanisms accounted for the TDB-induced increase in T cells within tumors. TDB treatment induced CD8+ T-cell proliferation. T cells were also actively recruited post-TDB treatment by IFNγ-dependent T-cell chemokines mediated via CXCR3. This active T-cell recruitment by TDB-induced chemokine signaling was the dominant mechanism and necessary for the therapeutic activity of anti-HER2/CD3 TDB.

Conclusions: In summary, we demonstrate that the activity of anti-HER2/CD3 TDB was not dependent on high-level baseline T-cell infiltration. Our results suggest that anti-HER2/CD3 TDB may be efficacious in patients and indications that respond poorly to checkpoint inhibitors. An active T-cell recruitment mediated by TDB-induced chemokine signaling was the major mechanism for T-cell recruitment.

MeSH terms

  • Adoptive Transfer
  • Animals
  • Antibodies, Bispecific / pharmacology*
  • CD3 Complex / antagonists & inhibitors*
  • CD8-Positive T-Lymphocytes / drug effects
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / metabolism
  • Cell Line, Tumor
  • Chemokines / metabolism*
  • Cytokines / metabolism
  • Disease Models, Animal
  • Female
  • Humans
  • Inflammation Mediators / metabolism
  • Interferon-gamma / metabolism*
  • Lymphocyte Activation / immunology
  • Lymphocytes, Tumor-Infiltrating / drug effects
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Lymphocytes, Tumor-Infiltrating / metabolism
  • Mice
  • Neoplasms / drug therapy
  • Neoplasms / etiology
  • Neoplasms / metabolism*
  • Neoplasms / pathology
  • Receptor, ErbB-2 / antagonists & inhibitors*
  • Receptors, CXCR3 / metabolism*
  • Signal Transduction
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism*
  • Xenograft Model Antitumor Assays

Substances

  • Antibodies, Bispecific
  • CD3 Complex
  • Chemokines
  • Cytokines
  • Inflammation Mediators
  • Receptors, CXCR3
  • Interferon-gamma
  • Receptor, ErbB-2