Hydrogen Peroxide Mediates Artemisinin-Derived C-16 Carba-Dimer-Induced Toxicity of Human Cancer Cells
Identifieur interne : 000140 ( an2020/Analysis ); précédent : 000139; suivant : 000141Hydrogen Peroxide Mediates Artemisinin-Derived C-16 Carba-Dimer-Induced Toxicity of Human Cancer Cells
Auteurs : Amanda L. Kalen ; Brett A. Wagner ; Ehab H. Sarsour ; Maneesh G. Kumar ; Jessica L. Reedy ; Garry R. Buettner ; Nabin C. Barua ; Prabhat C. GoswamiSource :
- Antioxidants [ 2076-3921 ] ; 2020.
Abstract
This study used a nitroaliphatic chemistry approach to synthesize a novel artemisinin-derived carba-dimer (AG-1) and determined its anti-proliferative effects in human normal and cancer cells. AG-1 treatments selectively inhibit proliferation of cancer cells compared to normal human fibroblasts. Compared to artemisinin, AG-1 is more toxic to human breast, prostate, head–neck, pancreas and skin cancer cells; 50% inhibition (IC50) 123 µM in AG-1 vs. 290 µM in artemisinin-treated breast cancer cells. AG-1 treatment decreased (~5 folds) cyclin D1 protein expression that correlated with an increase in the percentage of cells in the G1-phase, suggesting a G1 delay. AG-1-induced toxicity was independent of the DNA damage at 72 h post-treatment, as measured by micronuclei frequency and γH2AX protein levels. Results from electron paramagnetic resonance spectroscopy showed Fe-catalyzed formation of AG-1 carbon-centered radicals in a cell-free system. Flow cytometry analysis of H2DCF-DA oxidation showed a significant increase in the steady-state levels of reactive oxygen species (ROS) in AG-1-treated cells. Pre-treatment with
Url:
DOI: 10.3390/antiox9020108
PubMed: 31991904
PubMed Central: 7070254
Affiliations:
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Hydrogen Peroxide Mediates Artemisinin-Derived C-16 Carba-Dimer-Induced Toxicity of Human Cancer Cells</title><author><name sortKey="Kalen, Amanda L" sort="Kalen, Amanda L" uniqKey="Kalen A" first="Amanda L." last="Kalen">Amanda L. Kalen</name><affiliation><nlm:aff id="af1-antioxidants-09-00108">Free Radical and Radiation Biology Division, Department of Radiation Oncology, The University of Iowa, Iowa City, IA 52242, USA;<email>amanda-kalen@uiowa.edu</email> (A.L.K.);<email>brett-wagner@uiowa.edu</email> (B.A.W.);<email>mgkumar@gmail.com</email> (M.G.K.);<email>garry-buettner@uiowa.edu</email> (G.R.B.)</nlm:aff></affiliation></author><author><name sortKey="Wagner, Brett A" sort="Wagner, Brett A" uniqKey="Wagner B" first="Brett A." last="Wagner">Brett A. Wagner</name><affiliation><nlm:aff id="af1-antioxidants-09-00108">Free Radical and Radiation Biology Division, Department of Radiation Oncology, The University of Iowa, Iowa City, IA 52242, USA;<email>amanda-kalen@uiowa.edu</email> (A.L.K.);<email>brett-wagner@uiowa.edu</email> (B.A.W.);<email>mgkumar@gmail.com</email> (M.G.K.);<email>garry-buettner@uiowa.edu</email> (G.R.B.)</nlm:aff></affiliation></author><author><name sortKey="Sarsour, Ehab H" sort="Sarsour, Ehab H" uniqKey="Sarsour E" first="Ehab H." last="Sarsour">Ehab H. Sarsour</name><affiliation><nlm:aff id="af2-antioxidants-09-00108">Department of Basic Sciences, Kansas City University of Medicine and Biosciences, Kansas City, MO 64106, USA;<email>esarsour@kcumb.edu</email></nlm:aff></affiliation></author><author><name sortKey="Kumar, Maneesh G" sort="Kumar, Maneesh G" uniqKey="Kumar M" first="Maneesh G." last="Kumar">Maneesh G. Kumar</name><affiliation><nlm:aff id="af1-antioxidants-09-00108">Free Radical and Radiation Biology Division, Department of Radiation Oncology, The University of Iowa, Iowa City, IA 52242, USA;<email>amanda-kalen@uiowa.edu</email> (A.L.K.);<email>brett-wagner@uiowa.edu</email> (B.A.W.);<email>mgkumar@gmail.com</email> (M.G.K.);<email>garry-buettner@uiowa.edu</email> (G.R.B.)</nlm:aff></affiliation></author><author><name sortKey="Reedy, Jessica L" sort="Reedy, Jessica L" uniqKey="Reedy J" first="Jessica L." last="Reedy">Jessica L. Reedy</name><affiliation><nlm:aff id="af3-antioxidants-09-00108">Radiation Oncology Branch, Center for Cancer Research, National Cancer Institutes of Health, Bethesda, MD 20892, USA;<email>jess.reedy@nih.gov</email></nlm:aff></affiliation></author><author><name sortKey="Buettner, Garry R" sort="Buettner, Garry R" uniqKey="Buettner G" first="Garry R." last="Buettner">Garry R. Buettner</name><affiliation><nlm:aff id="af1-antioxidants-09-00108">Free Radical and Radiation Biology Division, Department of Radiation Oncology, The University of Iowa, Iowa City, IA 52242, USA;<email>amanda-kalen@uiowa.edu</email> (A.L.K.);<email>brett-wagner@uiowa.edu</email> (B.A.W.);<email>mgkumar@gmail.com</email> (M.G.K.);<email>garry-buettner@uiowa.edu</email> (G.R.B.)</nlm:aff></affiliation></author><author><name sortKey="Barua, Nabin C" sort="Barua, Nabin C" uniqKey="Barua N" first="Nabin C." last="Barua">Nabin C. Barua</name><affiliation><nlm:aff id="af4-antioxidants-09-00108">Natural Products Chemistry Division, CSIR-North East Institute of Science and Technology, Jorhat, 785006 Assam, India;<email>ncbarua2000@yahoo.co.in</email></nlm:aff></affiliation></author><author><name sortKey="Goswami, Prabhat C" sort="Goswami, Prabhat C" uniqKey="Goswami P" first="Prabhat C." last="Goswami">Prabhat C. Goswami</name><affiliation><nlm:aff id="af1-antioxidants-09-00108">Free Radical and Radiation Biology Division, Department of Radiation Oncology, The University of Iowa, Iowa City, IA 52242, USA;<email>amanda-kalen@uiowa.edu</email> (A.L.K.);<email>brett-wagner@uiowa.edu</email> (B.A.W.);<email>mgkumar@gmail.com</email> (M.G.K.);<email>garry-buettner@uiowa.edu</email> (G.R.B.)</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31991904</idno><idno type="pmc">7070254</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7070254</idno><idno type="RBID">PMC:7070254</idno><idno type="doi">10.3390/antiox9020108</idno><date when="2020">2020</date><idno type="wicri:Area/Pmc/Corpus">000411</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000411</idno><idno type="wicri:Area/Pmc/Curation">000411</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000411</idno><idno type="wicri:Area/Pmc/Checkpoint">000131</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000131</idno><idno type="wicri:Area/Ncbi/Merge">000E73</idno><idno type="wicri:Area/Ncbi/Curation">000E73</idno><idno type="wicri:Area/Ncbi/Checkpoint">000E73</idno><idno type="wicri:Area/Main/Merge">000140</idno><idno type="wicri:Area/Main/Curation">000140</idno><idno type="wicri:Area/Main/Exploration">000140</idno><idno type="wicri:Area/an2020/Extraction">000140</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Hydrogen Peroxide Mediates Artemisinin-Derived C-16 Carba-Dimer-Induced Toxicity of Human Cancer Cells</title><author><name sortKey="Kalen, Amanda L" sort="Kalen, Amanda L" uniqKey="Kalen A" first="Amanda L." last="Kalen">Amanda L. Kalen</name><affiliation><nlm:aff id="af1-antioxidants-09-00108">Free Radical and Radiation Biology Division, Department of Radiation Oncology, The University of Iowa, Iowa City, IA 52242, USA;<email>amanda-kalen@uiowa.edu</email> (A.L.K.);<email>brett-wagner@uiowa.edu</email> (B.A.W.);<email>mgkumar@gmail.com</email> (M.G.K.);<email>garry-buettner@uiowa.edu</email> (G.R.B.)</nlm:aff></affiliation></author><author><name sortKey="Wagner, Brett A" sort="Wagner, Brett A" uniqKey="Wagner B" first="Brett A." last="Wagner">Brett A. Wagner</name><affiliation><nlm:aff id="af1-antioxidants-09-00108">Free Radical and Radiation Biology Division, Department of Radiation Oncology, The University of Iowa, Iowa City, IA 52242, USA;<email>amanda-kalen@uiowa.edu</email> (A.L.K.);<email>brett-wagner@uiowa.edu</email> (B.A.W.);<email>mgkumar@gmail.com</email> (M.G.K.);<email>garry-buettner@uiowa.edu</email> (G.R.B.)</nlm:aff></affiliation></author><author><name sortKey="Sarsour, Ehab H" sort="Sarsour, Ehab H" uniqKey="Sarsour E" first="Ehab H." last="Sarsour">Ehab H. Sarsour</name><affiliation><nlm:aff id="af2-antioxidants-09-00108">Department of Basic Sciences, Kansas City University of Medicine and Biosciences, Kansas City, MO 64106, USA;<email>esarsour@kcumb.edu</email></nlm:aff></affiliation></author><author><name sortKey="Kumar, Maneesh G" sort="Kumar, Maneesh G" uniqKey="Kumar M" first="Maneesh G." last="Kumar">Maneesh G. Kumar</name><affiliation><nlm:aff id="af1-antioxidants-09-00108">Free Radical and Radiation Biology Division, Department of Radiation Oncology, The University of Iowa, Iowa City, IA 52242, USA;<email>amanda-kalen@uiowa.edu</email> (A.L.K.);<email>brett-wagner@uiowa.edu</email> (B.A.W.);<email>mgkumar@gmail.com</email> (M.G.K.);<email>garry-buettner@uiowa.edu</email> (G.R.B.)</nlm:aff></affiliation></author><author><name sortKey="Reedy, Jessica L" sort="Reedy, Jessica L" uniqKey="Reedy J" first="Jessica L." last="Reedy">Jessica L. Reedy</name><affiliation><nlm:aff id="af3-antioxidants-09-00108">Radiation Oncology Branch, Center for Cancer Research, National Cancer Institutes of Health, Bethesda, MD 20892, USA;<email>jess.reedy@nih.gov</email></nlm:aff></affiliation></author><author><name sortKey="Buettner, Garry R" sort="Buettner, Garry R" uniqKey="Buettner G" first="Garry R." last="Buettner">Garry R. Buettner</name><affiliation><nlm:aff id="af1-antioxidants-09-00108">Free Radical and Radiation Biology Division, Department of Radiation Oncology, The University of Iowa, Iowa City, IA 52242, USA;<email>amanda-kalen@uiowa.edu</email> (A.L.K.);<email>brett-wagner@uiowa.edu</email> (B.A.W.);<email>mgkumar@gmail.com</email> (M.G.K.);<email>garry-buettner@uiowa.edu</email> (G.R.B.)</nlm:aff></affiliation></author><author><name sortKey="Barua, Nabin C" sort="Barua, Nabin C" uniqKey="Barua N" first="Nabin C." last="Barua">Nabin C. Barua</name><affiliation><nlm:aff id="af4-antioxidants-09-00108">Natural Products Chemistry Division, CSIR-North East Institute of Science and Technology, Jorhat, 785006 Assam, India;<email>ncbarua2000@yahoo.co.in</email></nlm:aff></affiliation></author><author><name sortKey="Goswami, Prabhat C" sort="Goswami, Prabhat C" uniqKey="Goswami P" first="Prabhat C." last="Goswami">Prabhat C. Goswami</name><affiliation><nlm:aff id="af1-antioxidants-09-00108">Free Radical and Radiation Biology Division, Department of Radiation Oncology, The University of Iowa, Iowa City, IA 52242, USA;<email>amanda-kalen@uiowa.edu</email> (A.L.K.);<email>brett-wagner@uiowa.edu</email> (B.A.W.);<email>mgkumar@gmail.com</email> (M.G.K.);<email>garry-buettner@uiowa.edu</email> (G.R.B.)</nlm:aff></affiliation></author></analytic><series><title level="j">Antioxidants</title><idno type="eISSN">2076-3921</idno><imprint><date when="2020">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>This study used a nitroaliphatic chemistry approach to synthesize a novel artemisinin-derived carba-dimer (AG-1) and determined its anti-proliferative effects in human normal and cancer cells. AG-1 treatments selectively inhibit proliferation of cancer cells compared to normal human fibroblasts. Compared to artemisinin, AG-1 is more toxic to human breast, prostate, head–neck, pancreas and skin cancer cells; 50% inhibition (IC<sub>50</sub>) 123 µM in AG-1 vs. 290 µM in artemisinin-treated breast cancer cells. AG-1 treatment decreased (~5 folds) cyclin D1 protein expression that correlated with an increase in the percentage of cells in the G<sub>1</sub>-phase, suggesting a G<sub>1</sub> delay. AG-1-induced toxicity was independent of the DNA damage at 72 h post-treatment, as measured by micronuclei frequency and γH2AX protein levels. Results from electron paramagnetic resonance spectroscopy showed Fe-catalyzed formation of AG-1 carbon-centered radicals in a cell-free system. Flow cytometry analysis of H<sub>2</sub>DCF-DA oxidation showed a significant increase in the steady-state levels of reactive oxygen species (ROS) in AG-1-treated cells. Pre-treatment with <italic>N</italic>-acetyl-<sc>l</sc>-cysteine and antioxidant enzymes (superoxide dismutase and catalase) significantly suppressed AG-1-induced toxicity, suggesting that superoxide and hydrogen peroxide contribute to AG-1-induced toxicity in human cancer cells. AG-1 represents a novel class of anti-cancer drug that is more potent than its parent compound, artemisinin. </p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Tu, Y" uniqKey="Tu Y">Y. Tu</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Chaturvedi, D" uniqKey="Chaturvedi D">D. Chaturvedi</name></author><author><name sortKey="Goswami, A" uniqKey="Goswami A">A. Goswami</name></author><author><name sortKey="Saikia, P P" uniqKey="Saikia P">P.P. Saikia</name></author><author><name sortKey="Barua, N C" uniqKey="Barua N">N.C. Barua</name></author><author><name sortKey="Rao, P G" uniqKey="Rao P">P.G. 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Barua</name><name sortKey="Buettner, Garry R" sort="Buettner, Garry R" uniqKey="Buettner G" first="Garry R." last="Buettner">Garry R. Buettner</name><name sortKey="Goswami, Prabhat C" sort="Goswami, Prabhat C" uniqKey="Goswami P" first="Prabhat C." last="Goswami">Prabhat C. Goswami</name><name sortKey="Kalen, Amanda L" sort="Kalen, Amanda L" uniqKey="Kalen A" first="Amanda L." last="Kalen">Amanda L. Kalen</name><name sortKey="Kumar, Maneesh G" sort="Kumar, Maneesh G" uniqKey="Kumar M" first="Maneesh G." last="Kumar">Maneesh G. Kumar</name><name sortKey="Reedy, Jessica L" sort="Reedy, Jessica L" uniqKey="Reedy J" first="Jessica L." last="Reedy">Jessica L. Reedy</name><name sortKey="Sarsour, Ehab H" sort="Sarsour, Ehab H" uniqKey="Sarsour E" first="Ehab H." last="Sarsour">Ehab H. Sarsour</name><name sortKey="Wagner, Brett A" sort="Wagner, Brett A" uniqKey="Wagner B" first="Brett A." last="Wagner">Brett A. 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