CCL19-producing fibroblasts promote tertiary lymphoid structure formation enhancing anti-tumor IgG response in colorectal cancer liver metastasis

Cancer Cell. 2024 Aug 12;42(8):1370-1385.e9. doi: 10.1016/j.ccell.2024.07.006.

Abstract

Tertiary lymphoid structures (TLSs) are associated with enhanced immunity in tumors. However, their formation and functions in colorectal cancer liver metastasis (CRLM) remain unclear. Here, we reveal that intra- and peri-tumor mature TLSs (TLS+) are associated with improved clinical outcomes than TLS- tumors. Using single-cell-RNA-sequencing and spatial-enhanced-resolution-omics-sequencing (Stereo-seq), we reveal that TLS+ tumors are enriched with IgG+ plasma cells (PCs), while TLS- tumors are characterized with IgA+ PCs. By generating TLS-associated PC-derived monoclonal antibodies in vitro, we show that TLS-PCs secrete tumor-targeting antibodies. As the proof-of-concept, we demonstrate the anti-tumor activities of TLS-PC-mAb6 antibody in humanized mouse model of colorectal cancer. We identify a fibroblast lineage secreting CCL19 that facilitates lymphocyte trafficking to TLSs. CCL19 treatment promotes TLS neogenesis and prevents tumor growth in mice. Our data uncover the central role of CCL19+ fibroblasts in TLS formation, which in turn generates therapeutic antibodies to restrict CRLM.

Keywords: CCL19; IgG plasma cell; Tertiary lymphoid structures; colorectal cancer liver metastasis; humanized mouse; monoclonal antibody; single-cell RNA sequencing; spatial transcriptomics.

MeSH terms

  • Animals
  • Antibodies, Monoclonal / pharmacology
  • Cell Line, Tumor
  • Chemokine CCL19* / genetics
  • Chemokine CCL19* / metabolism
  • Colorectal Neoplasms* / immunology
  • Colorectal Neoplasms* / metabolism
  • Colorectal Neoplasms* / pathology
  • Female
  • Fibroblasts / immunology
  • Fibroblasts / metabolism
  • Humans
  • Immunoglobulin G* / immunology
  • Liver Neoplasms* / immunology
  • Liver Neoplasms* / metabolism
  • Liver Neoplasms* / pathology
  • Liver Neoplasms* / secondary
  • Mice
  • Plasma Cells / immunology
  • Plasma Cells / metabolism
  • Tertiary Lymphoid Structures* / immunology
  • Tertiary Lymphoid Structures* / pathology

Substances

  • Immunoglobulin G
  • Chemokine CCL19
  • CCL19 protein, human
  • Antibodies, Monoclonal