Podoplanin-Expressing Macrophages Promote Lymphangiogenesis and Lymphoinvasion in Breast Cancer

Cell Metab. 2019 Nov 5;30(5):917-936.e10. doi: 10.1016/j.cmet.2019.07.015. Epub 2019 Aug 22.

Abstract

Among mammary tumor-infiltrating immune cells, the highest expression of podoplanin (PDPN) is found in a subset of tumor-associated macrophages (TAMs). We hereby demonstrate that PDPN is involved in the attachment of this TAM subset to lymphatic endothelial cells (LECs). Mechanistically, the binding of PDPN to LEC-derived galectin 8 (GAL8) in a glycosylation-dependent manner promotes the activation of pro-migratory integrin β1. When proximal to lymphatics, PDPN-expressing macrophages (PoEMs) stimulate local matrix remodeling and promote vessel growth and lymphoinvasion. Anti-integrin β1 blockade, macrophage-specific Pdpn knockout, or GAL8 inhibition impairs TAM adhesion to LECs, restraining lymphangiogenesis and reducing lymphatic cancer spread. In breast cancer patients, association of PoEMs with tumor lymphatic vessels correlates with incidences of lymph node and distant organ metastasis.

Keywords: breast cancer; lymph nodes; lymphangiogenesis; lymphoinvasion; metastasis; podoplanin; tumor-associated macrophages.

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Animals
  • Breast Neoplasms / metabolism*
  • Breast Neoplasms / pathology
  • Cell Line, Tumor
  • Endothelial Cells / metabolism
  • Extracellular Matrix / metabolism
  • Female
  • Humans
  • Lymph Nodes / pathology*
  • Lymphangiogenesis / genetics*
  • Lymphatic Metastasis / genetics*
  • Lymphatic Vessels / metabolism
  • Macrophages / metabolism*
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Middle Aged

Substances

  • Gp38 protein, mouse
  • Membrane Glycoproteins
  • PDPN protein, human