In vivo macrophage engineering reshapes the tumor microenvironment leading to eradication of liver metastases

Cancer Cell. 2023 Nov 13;41(11):1892-1910.e10. doi: 10.1016/j.ccell.2023.09.014. Epub 2023 Oct 19.

Abstract

Liver metastases are associated with poor response to current pharmacological treatments, including immunotherapy. We describe a lentiviral vector (LV) platform to selectively engineer liver macrophages, including Kupffer cells and tumor-associated macrophages (TAMs), to deliver type I interferon (IFNα) to liver metastases. Gene-based IFNα delivery delays the growth of colorectal and pancreatic ductal adenocarcinoma liver metastases in mice. Response to IFNα is associated with TAM immune activation, enhanced MHC-II-restricted antigen presentation and reduced exhaustion of CD8+ T cells. Conversely, increased IL-10 signaling, expansion of Eomes CD4+ T cells, a cell type displaying features of type I regulatory T (Tr1) cells, and CTLA-4 expression are associated with resistance to therapy. Targeting regulatory T cell functions by combinatorial CTLA-4 immune checkpoint blockade and IFNα LV delivery expands tumor-reactive T cells, attaining complete response in most mice. These findings support a promising therapeutic strategy with feasible translation to patients with unmet medical need.

Keywords: Colorectal cancer (CRC); EOMES; Gene therapy; Immunotherapy; Interferon-alpha; Interleukin-10 (IL-10); Liver metastases; Pancreatic cancer; Tumor-associated macrophages (TAMs); Type 1 regulatory T cells (Tr1).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD8-Positive T-Lymphocytes*
  • CTLA-4 Antigen / metabolism
  • Humans
  • Liver Neoplasms* / genetics
  • Liver Neoplasms* / pathology
  • Liver Neoplasms* / therapy
  • Macrophages
  • Mice
  • Tumor Microenvironment / genetics

Substances

  • CTLA-4 Antigen