Multifunctional thiosemicarbazones targeting sigma receptors: in vitro and in vivo antitumor activities in pancreatic cancer models

Cell Oncol (Dordr). 2021 Dec;44(6):1307-1323. doi: 10.1007/s13402-021-00638-5. Epub 2021 Sep 29.

Abstract

Purpose: Association of the metal chelating portion of thiosemicarbazone with the cytotoxic activity of sigma-2 receptors appears a promising strategy for the treatment of pancreatic tumors. Here, we developed a novel sigma-2 receptor targeting thiosemicarbazone (FA4) that incorporates a moiety associated with lysosome destabilization and ROS increase in order to design more efficient antitumor agents.

Methods: The density of sigma receptors in pancreatic cancer cells was evaluated by flow cytometry. In these cells, cytotoxicity (MTT assay) and activation of ER- and mitochondria-dependent cell death pathways (mRNA expression of GRP78, ATF6, IRE1, PERK; ROS levels by MitoSOX and DCFDA-AM; JC-1 staining) induced by the thiosemicarbazones FA4, MLP44, PS3 and ACthio-1, were evaluated. The expression of autophagic proteins (ATG5, ATG7, ATG12, beclin, p62 and LC3-I) was also studied. In addition, the in vivo effect of FA4 in xenograft models with and without gemcitabine challenge was investigated.

Results: We found that FA4 exerted a more potent cytotoxicity than previously studied thiosemicarbazones (MLP44, PS3 and ACthio-1), which were found to display variable effects on the ER or the mitochondria-dependent pro-apoptotic axis. By contrast, FA4 activated pro-apoptotic pathways and decreased autophagy, except in MiaPaCa2 cells, in which autophagic proteins were expressed at lower levels and remained unmodified by FA4. FA4 treatment of PANC-1 xenografted mouse models, poorly responsive to conventional chemotherapy, significantly reduced tumor volumes and increased intratumor apoptosis compared to gemcitabine, with no signs of toxicity.

Conclusions: Our data indicate that FA4 exhibits encouraging activity in pancreatic cancer cells unresponsive to gemcitabine. These results warrant further investigation in patient-derived pancreatic cancers, and hold promise for the development of therapies that can more efficiently target the specific characteristics of individual tumor types.

Keywords: Autophagy; Caspase 3/7/9; PANC-1 xenograft; Pancreatic cancer; Sigma receptors; Thiosemicarbazone.

MeSH terms

  • Animals
  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / pharmacology
  • Antineoplastic Agents / therapeutic use*
  • Apoptosis / drug effects
  • Autophagy / drug effects
  • Biomarkers, Tumor / genetics
  • Biomarkers, Tumor / metabolism
  • Caspases / metabolism
  • Cell Death / drug effects
  • Cell Line, Tumor
  • Disease Models, Animal
  • Endoplasmic Reticulum Stress / drug effects
  • Enzyme Activation / drug effects
  • Female
  • Gene Expression Regulation, Neoplastic / drug effects
  • Mice
  • Mice, Inbred C57BL
  • Mice, Nude
  • Mitochondria / drug effects
  • Mitochondria / pathology
  • Pancreatic Neoplasms / drug therapy*
  • Pancreatic Neoplasms / genetics
  • Pancreatic Neoplasms / pathology*
  • Reactive Oxygen Species / metabolism
  • Receptors, sigma / metabolism*
  • Thiosemicarbazones / chemistry
  • Thiosemicarbazones / pharmacology
  • Thiosemicarbazones / therapeutic use*

Substances

  • Antineoplastic Agents
  • Biomarkers, Tumor
  • Reactive Oxygen Species
  • Receptors, sigma
  • Thiosemicarbazones
  • Caspases