SLC38A5 Modulates Ferroptosis to Overcome Gemcitabine Resistance in Pancreatic Cancer

Cells. 2023 Oct 23;12(20):2509. doi: 10.3390/cells12202509.

Abstract

Pancreatic cancer is characterized by a poor prognosis, with its five-year survival rate lower than that of any other cancer type. Gemcitabine, a standard treatment for pancreatic cancer, often has poor outcomes for patients as a result of chemoresistance. Therefore, novel therapeutic targets must be identified to overcome gemcitabine resistance. Here, we found that SLC38A5, a glutamine transporter, is more highly overexpressed in gemcitabine-resistant patients than in gemcitabine-sensitive patients. Furthermore, the deletion of SLC38A5 decreased the proliferation and migration of gemcitabine-resistant PDAC cells. We also found that the inhibition of SLC38A5 triggered the ferroptosis signaling pathway via RNA sequencing. Also, silencing SLC38A5 induced mitochondrial dysfunction and reduced glutamine uptake and glutathione (GSH) levels, and downregulated the expressions of GSH-related genes NRF2 and GPX4. The blockade of glutamine uptake negatively modulated the mTOR-SREBP1-SCD1 signaling pathway. Therefore, suppression of SLC38A5 triggers ferroptosis via two pathways that regulate lipid ROS levels. Similarly, we observed that knockdown of SLC38A5 restored gemcitabine sensitivity by hindering tumor growth and metastasis in the orthotopic mouse model. Altogether, our results demonstrate that SLC38A5 could be a novel target to overcome gemcitabine resistance in PDAC therapy.

Keywords: PDAC; SLC38A5; ferroptosis; gemcitabine resistance; lipid ROS.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Transport Systems, Neutral*
  • Animals
  • Cell Line, Tumor
  • Deoxycytidine / pharmacology
  • Deoxycytidine / therapeutic use
  • Drug Resistance, Neoplasm
  • Ferroptosis*
  • Gemcitabine
  • Glutamine
  • Humans
  • Mice
  • Pancreatic Neoplasms* / drug therapy
  • Pancreatic Neoplasms* / genetics
  • Pancreatic Neoplasms* / metabolism

Substances

  • Gemcitabine
  • Deoxycytidine
  • Glutamine
  • SLC38A5 protein, human
  • Amino Acid Transport Systems, Neutral

Grants and funding

This work was supported by a National Research Foundation of Korea (NRF) grant funded by the Korean Government, the Ministry of Science and ICT (MSIT) (NRF 2022R1A2C1004141 and NRF 2022R1A2C1091712), and a faculty research grant from Yonsei University College of Medicine (6-2021-0126).