Longitudinal phosphoproteomics reveals the PI3K-PAK1 axis as a potential target for recurrent colorectal liver metastases

Cell Rep. 2024 Dec 24;43(12):115061. doi: 10.1016/j.celrep.2024.115061. Epub 2024 Dec 16.

Abstract

The resistance of colorectal cancer liver metastases (CRLMs) to 5-fluorouracil (5-FU) chemotherapy remains a significant global health challenge. We investigated the phosphoproteomic dynamics of serial tissue sections obtained from initial metastases and recurrent tumors collected from 24 patients to address this unmet need for innovative therapeutic strategies for patients with CRLM with a poor prognosis. Our analysis revealed the activation of PAK kinase in patients with CRLM with a poor prognosis. Using an unbiased computational approach, we conducted a correlation analysis between PAK1 kinase activity and 545 drug sensitivity profiles across 35 colorectal cancer cell lines and identified PI3K inhibitors as potential therapeutic candidates. The efficacy of the FDA-approved PI3K inhibitor copanlisib was validated in 5-FU-resistant cell lines with high PAK1 kinase activity both in vitro and in vivo. This study presents an effective strategy for drug target discovery based on kinase activity, and the concept of this approach is widely applicable.

Keywords: CP: Cancer; chemotherapy resistance; colorectal cancer liver metastases; computational approaches; drug repositioning; phosphoproteomic dynamics.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Colorectal Neoplasms* / drug therapy
  • Colorectal Neoplasms* / metabolism
  • Colorectal Neoplasms* / pathology
  • Drug Resistance, Neoplasm / drug effects
  • Female
  • Fluorouracil / pharmacology
  • Humans
  • Liver Neoplasms* / drug therapy
  • Liver Neoplasms* / metabolism
  • Liver Neoplasms* / secondary
  • Male
  • Mice
  • Mice, Nude
  • Neoplasm Recurrence, Local / drug therapy
  • Neoplasm Recurrence, Local / metabolism
  • Neoplasm Recurrence, Local / pathology
  • Phosphatidylinositol 3-Kinases* / metabolism
  • Phosphoproteins / metabolism
  • Proteomics* / methods
  • Signal Transduction / drug effects
  • p21-Activated Kinases* / metabolism

Substances

  • p21-Activated Kinases
  • Phosphatidylinositol 3-Kinases
  • PAK1 protein, human
  • Fluorouracil
  • Phosphoproteins