SPP1+ TAM Regulates the Metastatic Colonization of CXCR4+ Metastasis-Associated Tumor Cells by Remodeling the Lymph Node Microenvironment

Adv Sci (Weinh). 2024 Nov;11(44):e2400524. doi: 10.1002/advs.202400524. Epub 2024 Sep 5.

Abstract

Lymph node metastasis, the initial step in distant metastasis, represents a primary contributor to mortality in patients diagnosed with oral squamous cell carcinoma (OSCC). However, the underlying mechanisms of lymph node metastasis in OSCC remain incompletely understood. Here, the transcriptomes of 56 383 single cells derived from paired tissues of six OSCC patients are analyzed. This study founds that CXCR4+ epithelial cells, identified as highly malignant disseminated tumor cells (DTCs), exhibited a propensity for lymph node metastasis. Importantly, a distinct subset of tumor-associated macrophages (TAMs) characterized by exclusive expression of phosphoprotein 1 (SPP1) is discovered. These TAMs may remodel the metastatic lymph node microenvironment by potentially activating fibroblasts and promoting T cell exhaustion through SPP1-CD44 and CD155-CD226 ligand-receptor interactions, thereby facilitating colonization and proliferation of disseminated tumor cells. The research advanced the mechanistic understanding of metastatic tumor microenvironment (TME) and provided a foundation for the development of personalized treatments for OSCC patients with metastasis.

Keywords: SPP1; lymph node metastatic microenvironment; macrophage; oral squamous cell carcinoma; single cell RNA sequencing.

MeSH terms

  • Animals
  • Carcinoma, Squamous Cell / genetics
  • Carcinoma, Squamous Cell / metabolism
  • Carcinoma, Squamous Cell / pathology
  • Disease Models, Animal
  • Female
  • Humans
  • Lymph Nodes / metabolism
  • Lymph Nodes / pathology
  • Lymphatic Metastasis*
  • Male
  • Mice
  • Middle Aged
  • Mouth Neoplasms* / genetics
  • Mouth Neoplasms* / metabolism
  • Mouth Neoplasms* / pathology
  • Osteopontin* / genetics
  • Osteopontin* / metabolism
  • Receptors, CXCR4* / genetics
  • Receptors, CXCR4* / metabolism
  • Tumor Microenvironment*
  • Tumor-Associated Macrophages / immunology
  • Tumor-Associated Macrophages / metabolism

Substances

  • Receptors, CXCR4
  • Osteopontin
  • CXCR4 protein, human
  • SPP1 protein, human