Proteomic profiling reveals CEACAM6 function in driving gallbladder cancer aggressiveness through integrin receptor, PRKCD and AKT/ERK signaling

Cell Death Dis. 2024 Oct 28;15(10):780. doi: 10.1038/s41419-024-07171-x.

Abstract

Gallbladder cancer (GBC) presents as an aggressive malignancy with poor patient outcome. Like other epithelial cancers, the mechanisms of GBC cancer progression remain vague and efforts in finding targeted therapies fall below expectations. This study combined proteomic analysis of formalin-fixed paraffin-embedded (FFPE) GBC samples, functional and molecular characterization of potential oncogenes and identification of potential therapeutic strategies for GBC. We identified Carcinoembryonic Antigen-related Cell Adhesion Molecule 6 (CEACAM6) as one of the significantly most upregulated proteins in GBC. CEACAM6 overexpression has been observed in other cancer entities but the molecular function remains unclear. Our functional analyses in vitro and in vivo mouse models revealed that CEACAM6 supported the initial steps of cancer progression and metastasis by decreasing cell adhesion and promoting migration and invasion of GBC cells. Conversely, CEACAM6 knockdown abolished GBC aggressiveness by increasing cell adhesion while reducing cell migration, cell proliferation, and colony formation. BirA-BioID followed by mass-spectrometry revealed Integrin Beta-1 (ITGB1) and Protein Kinase C Delta (PRKCD) as direct molecular and functional partners of CEACAM6 supporting GBC cell migration. ERK and AKT signaling and their downstream target genes were regulated by CEACAM6 and thus the treatment with AKT inhibitor capivasertib or ERK inhibitor ulixertinib mitigated the CEACAM6-induced migration. These findings demonstrate that CEACAM6 is crucially involved in gallbladder cancer progression by promoting migration and inhibiting cell adhesion through ERK and AKT signaling providing specific options for treatment of CEACAM6-positive cancers.

MeSH terms

  • Animals
  • Antigens, CD* / genetics
  • Antigens, CD* / metabolism
  • Cell Adhesion
  • Cell Adhesion Molecules* / genetics
  • Cell Adhesion Molecules* / metabolism
  • Cell Line, Tumor
  • Cell Movement*
  • Cell Proliferation
  • Female
  • GPI-Linked Proteins* / genetics
  • GPI-Linked Proteins* / metabolism
  • Gallbladder Neoplasms* / genetics
  • Gallbladder Neoplasms* / metabolism
  • Gallbladder Neoplasms* / pathology
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Integrin beta1 / genetics
  • Integrin beta1 / metabolism
  • MAP Kinase Signaling System
  • Male
  • Mice
  • Mice, Nude
  • Neoplasm Invasiveness
  • Protein Kinase C-delta* / genetics
  • Protein Kinase C-delta* / metabolism
  • Proteomics* / methods
  • Proto-Oncogene Proteins c-akt* / metabolism
  • Signal Transduction

Substances

  • CEACAM6 protein, human
  • Cell Adhesion Molecules
  • GPI-Linked Proteins
  • Proto-Oncogene Proteins c-akt
  • Antigens, CD
  • Protein Kinase C-delta
  • Integrin beta1
  • Itgb1 protein, human