LRP1 induces anti-PD-1 resistance by modulating the DLL4-NOTCH2-CCL2 axis and redirecting M2-like macrophage polarisation in bladder cancer

Cancer Lett. 2024 Jul 1:593:216807. doi: 10.1016/j.canlet.2024.216807. Epub 2024 Mar 8.

Abstract

The tumour microenvironment (TME) drives bladder cancer (BLCA) progression. Targeting the TME has emerged as a promising strategy for BLCA treatment in recent years. Furthermore, checkpoint blockade therapies are only beneficial for a minority of patients with BLCA, and drug resistance is a barrier to achieving significant clinical effects of anti-programmed cell death protein-1 (PD-1)/programmed death protein ligand-1 (PD-L1) therapy. In this study, higher low-density lipoprotein receptor-related protein 1 (LRP1) levels were related to a poorer prognosis for patients with various cancers, including those with higher grades and later stages of BLCA. Enrichment analysis demonstrated that LRP1 plays a role in the epithelial-mesenchymal transition (EMT), NOTCH signalling pathway, and ubiquitination. LRP1 knockdown in BLCA cells delayed BLCA progression both in vivo and in vitro. Furthermore, LRP1 knockdown suppressed EMT, reduced DLL4-NOTCH2 signalling activity, and downregulated M2-like macrophage polarisation. Patients with BLCA and higher LRP1 levels responded weakly to anti-PD-1 therapy in the IMvigor210 cohort. Moreover, LRP1 knockdown enhanced the therapeutic effects of anti-PD-1 in mice. Taken together, our findings suggest that LRP1 is a potential target for improving the efficacy of anti-PD-1/PD-L1 therapy by preventing EMT and M2-like macrophage polarisation by blocking the DLL4-NOTCH2 axis.

Keywords: DLL4-NOTCH2-CCL2 axis; LRP1; M2-like macrophage polarisation; Tumour microenvironment.

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Calcium-Binding Proteins* / genetics
  • Calcium-Binding Proteins* / metabolism
  • Cell Line, Tumor
  • Chemokine CCL2*
  • Drug Resistance, Neoplasm*
  • Epithelial-Mesenchymal Transition / drug effects
  • Female
  • Humans
  • Immune Checkpoint Inhibitors / pharmacology
  • Immune Checkpoint Inhibitors / therapeutic use
  • Low Density Lipoprotein Receptor-Related Protein-1* / genetics
  • Low Density Lipoprotein Receptor-Related Protein-1* / metabolism
  • Macrophages / immunology
  • Macrophages / metabolism
  • Male
  • Mice
  • Programmed Cell Death 1 Receptor / antagonists & inhibitors
  • Programmed Cell Death 1 Receptor / genetics
  • Programmed Cell Death 1 Receptor / metabolism
  • Receptor, Notch2* / genetics
  • Receptor, Notch2* / metabolism
  • Signal Transduction
  • Tumor Microenvironment
  • Urinary Bladder Neoplasms* / drug therapy
  • Urinary Bladder Neoplasms* / genetics
  • Urinary Bladder Neoplasms* / immunology
  • Urinary Bladder Neoplasms* / metabolism
  • Urinary Bladder Neoplasms* / pathology
  • Xenograft Model Antitumor Assays

Substances

  • Adaptor Proteins, Signal Transducing
  • Calcium-Binding Proteins
  • CCL2 protein, human
  • Chemokine CCL2
  • DLL4 protein, human
  • Immune Checkpoint Inhibitors
  • Low Density Lipoprotein Receptor-Related Protein-1
  • LRP1 protein, human
  • NOTCH2 protein, human
  • PDCD1 protein, human
  • Programmed Cell Death 1 Receptor
  • Receptor, Notch2