Chemotherapy Coupled to Macrophage Inhibition Induces T-cell and B-cell Infiltration and Durable Regression in Triple-Negative Breast Cancer

Abstract

Immunosuppressive elements within the tumor microenvironment, such as tumor-associated macrophages (TAM), can present a barrier to successful antitumor responses by cytolytic T cells. Here we employed preclinical syngeneic p53 null mouse models of triple-negative breast cancer (TNBC) to develop a treatment regimen that harnessed the immunostimulatory effects of low-dose cyclophosphamide coupled with the pharmacologic inhibition of TAMs using either a small-molecule CSF1R inhibitor or an anti-CSF1R antibody. This therapeutic combination was effective in treating several highly aggressive TNBC murine mammary tumor and lung metastasis models. Single-cell RNA sequencing characterized tumor-infiltrating lymphocytes including Th cells and antigen-presenting B cells that were highly enriched in responders to combination therapy. In one model that exhibited long-term posttreatment tumor regression, high-dimensional imaging techniques identified the close spatial localization of B220+/CD86+-activated B cells and CD4+ T cells in tertiary lymphoid structures that were present up to 6 weeks posttreatment. The transcriptional and metabolic heterogeneity of TAMs was also characterized in two closely related claudin-low/mesenchymal subtype tumor models with differential treatment responses. A murine TAM signature derived from the T12 model was highly conserved in human claudin-low breast cancers, and high expression of the TAM signature correlated with reduced overall survival in patients with breast cancer. This TAM signature may help identify human patients with claudin-low breast cancer that will benefit from the combination of cyclophosphamide and anti-CSF1R therapy. These studies illustrate the complexity of the tumor immune microenvironment and highlight different immune responses that result from rational immunotherapy combinations.

Document Details

Document Type
Pub Defense Publication
Publication Date
Apr 20, 2022
Source ID
10.1158/0008-5472.can-21-3714

Entities

People

  • Charles M. Perou
  • Clark Hamor
  • Daniel Hollern
  • Diego A Pedroza
  • Igor Bado
  • Jeffrey M. Rosen
  • Jeffrey T. Chang
  • Jingyuan Hu
  • Licheng Zhang
  • Na Zhao
  • Nigel Lee
  • Sergio Aguirre
  • Shu-hsia Chen
  • Swarnima Singh
  • Xiang H-F Zhang
  • Yang Gao
  • Yichao Shen
  • Ying‐Wooi Wan
  • Yitian Xu
  • Zhandong Liu

Organizations

  • Baylor College of Medicine
  • Cancer Prevention and Research Institute of Texas
  • His Majesty's Railway Inspectorate
  • National Cancer Institute
  • National Institutes of Health
  • The Breast Cancer Research Foundation
  • United States Department of Defense
  • University of North Carolina
  • University of Texas Health Science Center at Houston

Tags

Fields of Study

  • Biology
  • Medicine

Readers

  • Immunology
  • Oncology
  • Oncology (Cancer Research).

Technology Areas

  • Biotechnology
  • Biotechnology - Cancer Biotech