Epigenetic Activation of the CMTM6-IGF2BP1-EP300 Positive Feedback Loop Drives Gemcitabine Resistance in Pancreatic Ductal Adenocarcinoma

Adv Sci (Weinh). 2024 Dec;11(47):e2406714. doi: 10.1002/advs.202406714. Epub 2024 Nov 3.

Abstract

Pancreatic ductal adenocarcinoma (PDAC) is a highly malignant tumor with a dismal prognosis. Gemcitabine-based chemotherapy has emerged as a first-line treatment for PDAC. However, the development of gemcitabine resistance often results in therapeutic failure. In order to uncover the underlying mechanisms of gemcitabine resistance, gemcitabine-resistant PDAC cell lines and patient-derived xenograft (PDX) models are established and subjected to RNA sequencing. It is found that CMTM6 is closely related to gemcitabine resistance in PDAC. Multi-omics analysis revealed that EP300-mediated H3K27ac modification is involved in the transcriptional activation of CMTM6, which maintains IGF2BP1 expression by preventing its ubiquitination. The m6A reader IGF2BP1 stabilizes the EP300 and MYC mRNAs by recognizing m6A modifications, forming a positive feedback loop that enhances tumor stemness and ultimately contributes to PDAC resistance. The combined application of the EP300 inhibitor inobrodib and gemcitabine exerts a synergistic effect on PDAC. Overall, these findings reveal that the EP300-CMTM6-IGF2BP1 positive feedback loop facilitates gemcitabine resistance via epigenetic reprogramming and the combined use of inobrodib and gemcitabine represents a promising strategy for overcoming chemoresistance in PDAC, warranting further investigation in clinical trials.

Keywords: CMTM6; N6‐methyladenosine; chemoresistance; epigenetic modification; pancreatic ductal adenocarcinoma.

MeSH terms

  • Animals
  • Antimetabolites, Antineoplastic / pharmacology
  • Antimetabolites, Antineoplastic / therapeutic use
  • Carcinoma, Pancreatic Ductal* / drug therapy
  • Carcinoma, Pancreatic Ductal* / genetics
  • Carcinoma, Pancreatic Ductal* / metabolism
  • Cell Line, Tumor
  • Deoxycytidine* / analogs & derivatives
  • Deoxycytidine* / pharmacology
  • Disease Models, Animal
  • Drug Resistance, Neoplasm* / drug effects
  • Drug Resistance, Neoplasm* / genetics
  • E1A-Associated p300 Protein* / genetics
  • E1A-Associated p300 Protein* / metabolism
  • Epigenesis, Genetic* / drug effects
  • Epigenesis, Genetic* / genetics
  • Feedback, Physiological / drug effects
  • Gemcitabine*
  • Humans
  • Mice
  • Pancreatic Neoplasms* / drug therapy
  • Pancreatic Neoplasms* / genetics
  • Pancreatic Neoplasms* / metabolism
  • RNA-Binding Proteins* / genetics
  • RNA-Binding Proteins* / metabolism

Substances

  • Deoxycytidine
  • Gemcitabine
  • RNA-Binding Proteins
  • E1A-Associated p300 Protein
  • IGF2BP1 protein, human
  • EP300 protein, human
  • Antimetabolites, Antineoplastic