A CLIC1 network coordinates matrix stiffness and the Warburg effect to promote tumor growth in pancreatic cancer

Cell Rep. 2024 Aug 27;43(8):114633. doi: 10.1016/j.celrep.2024.114633. Epub 2024 Aug 17.

Abstract

Pancreatic ductal adenocarcinoma (PDAC) features substantial matrix stiffening and reprogrammed glucose metabolism, particularly the Warburg effect. However, the complex interplay between these traits and their impact on tumor advancement remains inadequately explored. Here, we integrated clinical, cellular, and bioinformatics approaches to explore the connection between matrix stiffness and the Warburg effect in PDAC, identifying CLIC1 as a key mediator. Elevated CLIC1 expression, induced by matrix stiffness through Wnt/β-catenin/TCF4 signaling, signifies poorer prognostic outcomes in PDAC. Functionally, CLIC1 serves as a catalyst for glycolytic metabolism, propelling tumor proliferation. Mechanistically, CLIC1 fortifies HIF1α stability by curbing hydroxylation via reactive oxygen species (ROS). Collectively, PDAC cells elevate CLIC1 levels in a matrix-stiffness-responsive manner, bolstering the Warburg effect to drive tumor growth via ROS/HIF1α signaling. Our insights highlight opportunities for targeted therapies that concurrently address matrix properties and metabolic rewiring, with CLIC1 emerging as a promising intervention point.

Keywords: CP: Cancer; CP: Metabolism; chloride intracellular channel 1; extracellular matrix stiffness; pancreatic ductal adenocarcinoma; the Warburg effect.

MeSH terms

  • Animals
  • Carcinoma, Pancreatic Ductal* / genetics
  • Carcinoma, Pancreatic Ductal* / metabolism
  • Carcinoma, Pancreatic Ductal* / pathology
  • Cell Line, Tumor
  • Cell Proliferation*
  • Chloride Channels* / genetics
  • Chloride Channels* / metabolism
  • Extracellular Matrix / metabolism
  • Gene Expression Regulation, Neoplastic
  • Glycolysis
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit* / metabolism
  • Mice
  • Mice, Nude
  • Pancreatic Neoplasms* / genetics
  • Pancreatic Neoplasms* / metabolism
  • Pancreatic Neoplasms* / pathology
  • Reactive Oxygen Species / metabolism
  • Warburg Effect, Oncologic*

Substances

  • Chloride Channels
  • CLIC1 protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Reactive Oxygen Species
  • HIF1A protein, human