Ascorbyl stearate and ionizing radiation potentiate apoptosis through intracellular thiols and oxidative stress in murine T lymphoma cells

Chem Biol Interact. 2018 Feb 1:281:37-50. doi: 10.1016/j.cbi.2017.12.028. Epub 2017 Dec 19.

Abstract

Ascorbyl stearate (Asc-s) is a derivative of ascorbic acid with better anti-tumour efficacy compared to its parent compound ascorbic acid. In this study, we have examined radio-sensitizing effect of Asc-s in murine T cell lymphoma (EL4) cells at 4 Gy. Asc-s and radiation treatment reduced cell proliferation, induced apoptosis in a dose dependent manner by arresting the cells at S/G2-M phase of cell cycle. It also decreased the frequency of cancer stem cells per se, with significantly higher decrease in combination with radiation treatment./Further, Asc-s and radiation treatment increased the level of reactive oxygen species (ROS), drop in mitochondrial membrane potential (MMP) and increased caspase-3 activity resulting in apoptosis of EL4 cells. Further it also significantly decreased GSH/GSSG ratio due to binding of Asc-s with thiols. The increase in oxidative stress induced by Asc-s and radiation treatment was abrogated by thiol antioxidants in EL4 cells. Interestingly, this redox modulation triggered significant increase in protein glutathionylation in a time dependent manner. Asc-s treatment resulted in glutathionylation of IKK, p50-NF-kB and mutated p53, thereby inhibiting cancer progression during oxidative stress. Asc-s quenches GSH ensuing Asc-s + GSH adduct thereby further modulating GSH/GSSG ratio as evident from HPLC and docking studies. The anti-tumour effect of Asc-s along with radiation was studied by injecting EL4 cells in synegenicC57/BL6 male mice. Intraperitoneal injection of Asc-s followed by radiation exposure at 4 Gy to the tumour bearing mice resulted in radio-sensitization which is evident from significant regression of tumour as evident from tumour burden index. The survival study supports the data that Asc-s pre-treatment enhances radio-sensitization in murine lymphoma. Our data, suggest that Asc-s and ionizing radiation induced cell cycle arrest and apoptosis by perturbing redox balance through irreversible complexes of thiols with Asc-s, disturbed mitochondrial membrane permeability and activation of caspase-3 in EL4 cells.

Keywords: Ascorbyl stearate; Glutathionylation; Ionizing radiation; MMP; Mouse lymphoma EL4 cells; ROS.

MeSH terms

  • Animals
  • Antioxidants / metabolism
  • Antioxidants / pharmacology
  • Apoptosis / drug effects*
  • Apoptosis / radiation effects
  • Ascorbic Acid / analogs & derivatives*
  • Ascorbic Acid / pharmacology
  • Binding Sites
  • Biomarkers, Tumor / metabolism
  • Caspase 3 / metabolism
  • Cell Cycle Checkpoints / drug effects
  • Cell Cycle Checkpoints / radiation effects
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Proliferation / radiation effects
  • Glutathione / chemistry
  • Lymphoma / drug therapy
  • Lymphoma / pathology
  • Lymphoma / radiotherapy
  • Male
  • Membrane Potential, Mitochondrial / drug effects
  • Mice
  • Mice, Inbred C57BL
  • Neoplastic Stem Cells / cytology
  • Neoplastic Stem Cells / drug effects
  • Neoplastic Stem Cells / metabolism
  • Oxidative Stress / drug effects*
  • Oxidative Stress / radiation effects
  • Radiation, Ionizing*
  • Reactive Oxygen Species / metabolism
  • Sulfhydryl Compounds / metabolism*

Substances

  • Antioxidants
  • Biomarkers, Tumor
  • Reactive Oxygen Species
  • Sulfhydryl Compounds
  • ascorbyl monostearate
  • Caspase 3
  • Glutathione
  • Ascorbic Acid