N6-methyladenosine modified TGFB2 triggers lipid metabolism reprogramming to confer pancreatic ductal adenocarcinoma gemcitabine resistance

Oncogene. 2024 Jul;43(31):2405-2420. doi: 10.1038/s41388-024-03092-3. Epub 2024 Jun 24.

Abstract

Gemcitabine resistance is a major obstacle to the effectiveness of chemotherapy in pancreatic ductal adenocarcinoma (PDAC). Therefore, new strategies are needed to sensitize cancer cells to gemcitabine. Here, we constructed gemcitabine-resistant PDAC cells and analyzed them with RNA-sequence. Employing an integrated approach involving bioinformatic analyses from multiple databases, TGFB2 is identified as a crucial gene in gemcitabine-resistant PDAC and is significantly associated with poor gemcitabine therapeutic response. The patient-derived xenograft (PDX) model further substantiates the gradual upregulation of TGFB2 expression during gemcitabine-induced resistance. Silencing TGFB2 expression can enhance the chemosensitivity of gemcitabine against PDAC. Mechanistically, TGFB2, post-transcriptionally stabilized by METTL14-mediated m6A modification, can promote lipid accumulation and the enhanced triglyceride accumulation drives gemcitabine resistance by lipidomic profiling. TGFB2 upregulates the lipogenesis regulator sterol regulatory element binding factor 1 (SREBF1) and its downstream lipogenic enzymes via PI3K-AKT signaling. Moreover, SREBF1 is responsible for TGFB2-mediated lipogenesis to promote gemcitabine resistance in PDAC. Importantly, TGFB2 inhibitor imperatorin combined with gemcitabine shows synergistic effects in gemcitabine-resistant PDAC PDX model. This study sheds new light on an avenue to mitigate PDAC gemcitabine resistance by targeting TGFB2 and lipid metabolism and develops the potential of imperatorin as a promising chemosensitizer in clinical translation.

MeSH terms

  • Adenosine* / analogs & derivatives
  • Adenosine* / metabolism
  • Adenosine* / pharmacology
  • Animals
  • Carcinoma, Pancreatic Ductal* / drug therapy
  • Carcinoma, Pancreatic Ductal* / genetics
  • Carcinoma, Pancreatic Ductal* / metabolism
  • Carcinoma, Pancreatic Ductal* / pathology
  • Cell Line, Tumor
  • Deoxycytidine* / analogs & derivatives
  • Deoxycytidine* / pharmacology
  • Drug Resistance, Neoplasm* / genetics
  • Gemcitabine*
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Lipid Metabolism* / drug effects
  • Lipid Metabolism* / genetics
  • Metabolic Reprogramming
  • Mice
  • Pancreatic Neoplasms* / drug therapy
  • Pancreatic Neoplasms* / genetics
  • Pancreatic Neoplasms* / metabolism
  • Pancreatic Neoplasms* / pathology
  • Signal Transduction / drug effects
  • Sterol Regulatory Element Binding Protein 1
  • Transforming Growth Factor beta2* / genetics
  • Transforming Growth Factor beta2* / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • Deoxycytidine
  • Gemcitabine
  • Transforming Growth Factor beta2
  • TGFB2 protein, human
  • Adenosine
  • N-methyladenosine
  • SREBF1 protein, human
  • Sterol Regulatory Element Binding Protein 1