Ascorbate-and iron-driven redox activity of Dp44mT and Emodin facilitates peroxidation of micelles and bicelles
Iron (Fe)-induced oxidative stress leads to reactive oxygen species that damage biomembranes, with this mechanism being involved in the activity of some anti-cancer chemotherapeutics. Herein, we compared the effect of the ligand, di-2-pyridylketone 4,4-dimethyl-3-thiosemicarbazone (Dp44mT), or the p...
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| Published in | Biochimica et biophysica acta. General subjects Vol. 1866; no. 4; p. 130078 |
|---|---|
| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Netherlands
Elsevier B.V
01.04.2022
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| Abstract | Iron (Fe)-induced oxidative stress leads to reactive oxygen species that damage biomembranes, with this mechanism being involved in the activity of some anti-cancer chemotherapeutics.
Herein, we compared the effect of the ligand, di-2-pyridylketone 4,4-dimethyl-3-thiosemicarbazone (Dp44mT), or the potential ligand, Emodin, on Fe-catalyzed lipid peroxidation in cell membrane models (micelles and bicelles). These studies were performed in the presence of hydrogen peroxide (H2O2) and the absence or presence of ascorbate.
In the absence of ascorbate, Fe(II)/Emodin mixtures incubated with H2O2 demonstrated slight pro-oxidant properties on micelles versus Fe(II) alone, while the Fe(III)-Dp44mT complex exhibited marked antioxidant properties. Examining more physiologically relevant phospholipid-containing bicelles, the Fe(II)- and Fe(III)-Dp44mT complexes demonstrated antioxidant activity without ascorbate. Upon adding ascorbate, there was a significant increase in the peroxidation of micelles and bicelles in the presence of unchelated Fe(II) and H2O2. The addition of ascorbate to Fe(III)-Dp44mT substantially increased the peroxidation of micelles and bicelles, with the Fe(III)-Dp44mT complex being reduced by ascorbate to the Fe(II) state, explaining the increased reactivity. Electron paramagnetic resonance spectroscopy demonstrated ascorbyl radical anion generation after mixing ascorbate and Emodin, with signal intensity being enhanced by H2O2. This finding suggested Emodin semiquinone radical formation that could play a role in its reactivity via ascorbate-driven redox cycling. Examining cultured melanoma cells in vitro, ascorbate at pharmacological levels enhanced the anti-proliferative activity of Dp44mT and Emodin.
Ascorbate-driven redox cycling of Dp44mT and Emodin promotes their anti-proliferative activity.
[Display omitted]
•Iron(III)-Dp44mT complexes suppress lipid peroxidation.•Ascorbate reduces iron(III)-Dp44mT to the redox-active iron(II)-Dp44mT complex.•Iron(II)-Dp44mT complexes enhance lipid peroxidation.•Ascorbate drives redox cycling of iron in the presence of Dp44mT and Emodin.•Ascorbate enhances the in vitro anti-proliferative efficacy of Dp44mT and Emodin |
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| AbstractList | Iron (Fe)-induced oxidative stress leads to reactive oxygen species that damage biomembranes, with this mechanism being involved in the activity of some anti-cancer chemotherapeutics.
Herein, we compared the effect of the ligand, di-2-pyridylketone 4,4-dimethyl-3-thiosemicarbazone (Dp44mT), or the potential ligand, Emodin, on Fe-catalyzed lipid peroxidation in cell membrane models (micelles and bicelles). These studies were performed in the presence of hydrogen peroxide (H
O
) and the absence or presence of ascorbate.
In the absence of ascorbate, Fe(II)/Emodin mixtures incubated with H
O
demonstrated slight pro-oxidant properties on micelles versus Fe(II) alone, while the Fe(III)-Dp44mT complex exhibited marked antioxidant properties. Examining more physiologically relevant phospholipid-containing bicelles, the Fe(II)- and Fe(III)-Dp44mT complexes demonstrated antioxidant activity without ascorbate. Upon adding ascorbate, there was a significant increase in the peroxidation of micelles and bicelles in the presence of unchelated Fe(II) and H
O
. The addition of ascorbate to Fe(III)-Dp44mT substantially increased the peroxidation of micelles and bicelles, with the Fe(III)-Dp44mT complex being reduced by ascorbate to the Fe(II) state, explaining the increased reactivity. Electron paramagnetic resonance spectroscopy demonstrated ascorbyl radical anion generation after mixing ascorbate and Emodin, with signal intensity being enhanced by H
O
. This finding suggested Emodin semiquinone radical formation that could play a role in its reactivity via ascorbate-driven redox cycling. Examining cultured melanoma cells in vitro, ascorbate at pharmacological levels enhanced the anti-proliferative activity of Dp44mT and Emodin.
Ascorbate-driven redox cycling of Dp44mT and Emodin promotes their anti-proliferative activity. Iron (Fe)-induced oxidative stress leads to reactive oxygen species that damage biomembranes, with this mechanism being involved in the activity of some anti-cancer chemotherapeutics.BACKGROUNDIron (Fe)-induced oxidative stress leads to reactive oxygen species that damage biomembranes, with this mechanism being involved in the activity of some anti-cancer chemotherapeutics.Herein, we compared the effect of the ligand, di-2-pyridylketone 4,4-dimethyl-3-thiosemicarbazone (Dp44mT), or the potential ligand, Emodin, on Fe-catalyzed lipid peroxidation in cell membrane models (micelles and bicelles). These studies were performed in the presence of hydrogen peroxide (H2O2) and the absence or presence of ascorbate.METHODSHerein, we compared the effect of the ligand, di-2-pyridylketone 4,4-dimethyl-3-thiosemicarbazone (Dp44mT), or the potential ligand, Emodin, on Fe-catalyzed lipid peroxidation in cell membrane models (micelles and bicelles). These studies were performed in the presence of hydrogen peroxide (H2O2) and the absence or presence of ascorbate.In the absence of ascorbate, Fe(II)/Emodin mixtures incubated with H2O2 demonstrated slight pro-oxidant properties on micelles versus Fe(II) alone, while the Fe(III)-Dp44mT complex exhibited marked antioxidant properties. Examining more physiologically relevant phospholipid-containing bicelles, the Fe(II)- and Fe(III)-Dp44mT complexes demonstrated antioxidant activity without ascorbate. Upon adding ascorbate, there was a significant increase in the peroxidation of micelles and bicelles in the presence of unchelated Fe(II) and H2O2. The addition of ascorbate to Fe(III)-Dp44mT substantially increased the peroxidation of micelles and bicelles, with the Fe(III)-Dp44mT complex being reduced by ascorbate to the Fe(II) state, explaining the increased reactivity. Electron paramagnetic resonance spectroscopy demonstrated ascorbyl radical anion generation after mixing ascorbate and Emodin, with signal intensity being enhanced by H2O2. This finding suggested Emodin semiquinone radical formation that could play a role in its reactivity via ascorbate-driven redox cycling. Examining cultured melanoma cells in vitro, ascorbate at pharmacological levels enhanced the anti-proliferative activity of Dp44mT and Emodin.RESULTSIn the absence of ascorbate, Fe(II)/Emodin mixtures incubated with H2O2 demonstrated slight pro-oxidant properties on micelles versus Fe(II) alone, while the Fe(III)-Dp44mT complex exhibited marked antioxidant properties. Examining more physiologically relevant phospholipid-containing bicelles, the Fe(II)- and Fe(III)-Dp44mT complexes demonstrated antioxidant activity without ascorbate. Upon adding ascorbate, there was a significant increase in the peroxidation of micelles and bicelles in the presence of unchelated Fe(II) and H2O2. The addition of ascorbate to Fe(III)-Dp44mT substantially increased the peroxidation of micelles and bicelles, with the Fe(III)-Dp44mT complex being reduced by ascorbate to the Fe(II) state, explaining the increased reactivity. Electron paramagnetic resonance spectroscopy demonstrated ascorbyl radical anion generation after mixing ascorbate and Emodin, with signal intensity being enhanced by H2O2. This finding suggested Emodin semiquinone radical formation that could play a role in its reactivity via ascorbate-driven redox cycling. Examining cultured melanoma cells in vitro, ascorbate at pharmacological levels enhanced the anti-proliferative activity of Dp44mT and Emodin.Ascorbate-driven redox cycling of Dp44mT and Emodin promotes their anti-proliferative activity.CONCLUSIONS AND GENERAL SIGNIFICANCEAscorbate-driven redox cycling of Dp44mT and Emodin promotes their anti-proliferative activity. Iron (Fe)-induced oxidative stress leads to reactive oxygen species that damage biomembranes, with this mechanism being involved in the activity of some anti-cancer chemotherapeutics. Herein, we compared the effect of the ligand, di-2-pyridylketone 4,4-dimethyl-3-thiosemicarbazone (Dp44mT), or the potential ligand, Emodin, on Fe-catalyzed lipid peroxidation in cell membrane models (micelles and bicelles). These studies were performed in the presence of hydrogen peroxide (H₂O₂) and the absence or presence of ascorbate. In the absence of ascorbate, Fe(II)/Emodin mixtures incubated with H₂O₂ demonstrated slight pro-oxidant properties on micelles versus Fe(II) alone, while the Fe(III)-Dp44mT complex exhibited marked antioxidant properties. Examining more physiologically relevant phospholipid-containing bicelles, the Fe(II)- and Fe(III)-Dp44mT complexes demonstrated antioxidant activity without ascorbate. Upon adding ascorbate, there was a significant increase in the peroxidation of micelles and bicelles in the presence of unchelated Fe(II) and H₂O₂. The addition of ascorbate to Fe(III)-Dp44mT substantially increased the peroxidation of micelles and bicelles, with the Fe(III)-Dp44mT complex being reduced by ascorbate to the Fe(II) state, explaining the increased reactivity. Electron paramagnetic resonance spectroscopy demonstrated ascorbyl radical anion generation after mixing ascorbate and Emodin, with signal intensity being enhanced by H₂O₂. This finding suggested Emodin semiquinone radical formation that could play a role in its reactivity via ascorbate-driven redox cycling. Examining cultured melanoma cells in vitro, ascorbate at pharmacological levels enhanced the anti-proliferative activity of Dp44mT and Emodin. Ascorbate-driven redox cycling of Dp44mT and Emodin promotes their anti-proliferative activity. Iron (Fe)-induced oxidative stress leads to reactive oxygen species that damage biomembranes, with this mechanism being involved in the activity of some anti-cancer chemotherapeutics. Herein, we compared the effect of the ligand, di-2-pyridylketone 4,4-dimethyl-3-thiosemicarbazone (Dp44mT), or the potential ligand, Emodin, on Fe-catalyzed lipid peroxidation in cell membrane models (micelles and bicelles). These studies were performed in the presence of hydrogen peroxide (H2O2) and the absence or presence of ascorbate. In the absence of ascorbate, Fe(II)/Emodin mixtures incubated with H2O2 demonstrated slight pro-oxidant properties on micelles versus Fe(II) alone, while the Fe(III)-Dp44mT complex exhibited marked antioxidant properties. Examining more physiologically relevant phospholipid-containing bicelles, the Fe(II)- and Fe(III)-Dp44mT complexes demonstrated antioxidant activity without ascorbate. Upon adding ascorbate, there was a significant increase in the peroxidation of micelles and bicelles in the presence of unchelated Fe(II) and H2O2. The addition of ascorbate to Fe(III)-Dp44mT substantially increased the peroxidation of micelles and bicelles, with the Fe(III)-Dp44mT complex being reduced by ascorbate to the Fe(II) state, explaining the increased reactivity. Electron paramagnetic resonance spectroscopy demonstrated ascorbyl radical anion generation after mixing ascorbate and Emodin, with signal intensity being enhanced by H2O2. This finding suggested Emodin semiquinone radical formation that could play a role in its reactivity via ascorbate-driven redox cycling. Examining cultured melanoma cells in vitro, ascorbate at pharmacological levels enhanced the anti-proliferative activity of Dp44mT and Emodin. Ascorbate-driven redox cycling of Dp44mT and Emodin promotes their anti-proliferative activity. [Display omitted] •Iron(III)-Dp44mT complexes suppress lipid peroxidation.•Ascorbate reduces iron(III)-Dp44mT to the redox-active iron(II)-Dp44mT complex.•Iron(II)-Dp44mT complexes enhance lipid peroxidation.•Ascorbate drives redox cycling of iron in the presence of Dp44mT and Emodin.•Ascorbate enhances the in vitro anti-proliferative efficacy of Dp44mT and Emodin |
| ArticleNumber | 130078 |
| Author | Richardson, D.R. Dharmasivam, M. Shelepova, E.A. Selyutina, O.Yu Kononova, P.A. Koshman, V.E. Bernhardt, Paul V. Afroz, R. Azad, M. Gholam Polyakov, N.E. |
| Author_xml | – sequence: 1 givenname: O.Yu surname: Selyutina fullname: Selyutina, O.Yu email: olga.gluschenko@gmail.com organization: Institute of Chemical Kinetics and Combustion, Institutskaya St., 3, 630090 Novosibirsk, Russia – sequence: 2 givenname: P.A. surname: Kononova fullname: Kononova, P.A. organization: Institute of Chemical Kinetics and Combustion, Institutskaya St., 3, 630090 Novosibirsk, Russia – sequence: 3 givenname: V.E. surname: Koshman fullname: Koshman, V.E. organization: Institute of Chemical Kinetics and Combustion, Institutskaya St., 3, 630090 Novosibirsk, Russia – sequence: 4 givenname: E.A. surname: Shelepova fullname: Shelepova, E.A. organization: Institute of Chemical Kinetics and Combustion, Institutskaya St., 3, 630090 Novosibirsk, Russia – sequence: 5 givenname: M. Gholam surname: Azad fullname: Azad, M. Gholam organization: Centre for Cancer Cell Biology and Drug Discovery, Griffith Institute for Drug Discovery, Griffith University, Nathan, Brisbane, Queensland 4111, Australia – sequence: 6 givenname: R. surname: Afroz fullname: Afroz, R. organization: Centre for Cancer Cell Biology and Drug Discovery, Griffith Institute for Drug Discovery, Griffith University, Nathan, Brisbane, Queensland 4111, Australia – sequence: 7 givenname: M. surname: Dharmasivam fullname: Dharmasivam, M. organization: Centre for Cancer Cell Biology and Drug Discovery, Griffith Institute for Drug Discovery, Griffith University, Nathan, Brisbane, Queensland 4111, Australia – sequence: 8 givenname: Paul V. surname: Bernhardt fullname: Bernhardt, Paul V. organization: School of Chemistry and Molecular Biosciences, University of Queensland, Brisbane, Queensland 4072, Australia – sequence: 9 givenname: N.E. surname: Polyakov fullname: Polyakov, N.E. organization: Institute of Chemical Kinetics and Combustion, Institutskaya St., 3, 630090 Novosibirsk, Russia – sequence: 10 givenname: D.R. surname: Richardson fullname: Richardson, D.R. email: d.richardson@griffith.edu.au organization: Centre for Cancer Cell Biology and Drug Discovery, Griffith Institute for Drug Discovery, Griffith University, Nathan, Brisbane, Queensland 4111, Australia |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34974127$$D View this record in MEDLINE/PubMed |
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| Keywords | Iron chelators Iron Ascorbate Dp44mT |
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| SubjectTerms | antioxidant activity Ascorbate Ascorbic Acid - chemistry cell membranes Dp44mT drug therapy electron paramagnetic resonance spectroscopy emodin Emodin - pharmacology Ferrous Compounds Hydrogen Peroxide Iron Iron - metabolism Iron chelators Ligands lipid peroxidation melanoma Micelles Oxidation-Reduction oxidative stress Reactive Oxygen Species Thiosemicarbazones - pharmacology |
| Title | Ascorbate-and iron-driven redox activity of Dp44mT and Emodin facilitates peroxidation of micelles and bicelles |
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