Green tea polyphenolic antioxidants oxidize hydrogen sulfide to thiosulfate and polysulfides: A possible new mechanism underpinning their biological action
Matcha and green tea catechins such as (−)-epicatechin (EC), (−)-epigallocatechin (EGC) and (−)-epigallocatechin gallate (EGCG) have long been studied for their antioxidant and health-promoting effects. Using specific fluorophores for H2S (AzMC) and polysulfides (SSP4) as well as IC-MS and UPLC-MS/M...
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| Format: | Article |
| Language: | English |
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Elsevier
2020-10-01
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| Series: | Redox Biology |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213231720309368 |
| _version_ | 1818664016048816128 |
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| author | Kenneth R. Olson Austin Briggs Monesh Devireddy Nicholas A. Iovino Nicole C. Skora Jenna Whelan Brian P. Villa Xiaotong Yuan Varun Mannam Scott Howard Yan Gao Magdalena Minnion Martin Feelisch |
| author_facet | Kenneth R. Olson Austin Briggs Monesh Devireddy Nicholas A. Iovino Nicole C. Skora Jenna Whelan Brian P. Villa Xiaotong Yuan Varun Mannam Scott Howard Yan Gao Magdalena Minnion Martin Feelisch |
| author_sort | Kenneth R. Olson |
| collection | DOAJ |
| description | Matcha and green tea catechins such as (−)-epicatechin (EC), (−)-epigallocatechin (EGC) and (−)-epigallocatechin gallate (EGCG) have long been studied for their antioxidant and health-promoting effects. Using specific fluorophores for H2S (AzMC) and polysulfides (SSP4) as well as IC-MS and UPLC-MS/MS-based techniques we here show that popular Japanese and Chinese green teas and select catechins all catalytically oxidize hydrogen sulfide (H2S) to polysulfides with the potency of EGC > EGCG >> EG. This reaction is accompanied by the formation of sulfite, thiosulfate and sulfate, consumes oxygen and is partially inhibited by the superoxide scavenger, tempol, and superoxide dismutase but not mannitol, trolox, DMPO, or the iron chelator, desferrioxamine. We propose that the reaction proceeds via a one-electron autoxidation process during which one of the OH-groups of the catechin B-ring is autooxidized to a semiquinone radical and oxygen is reduced to superoxide, either of which can then oxidize HS− to thiyl radicals (HS•) which react to form hydrogen persulfide (H2S2). H2S oxidation reduces the B-ring back to the hydroquinone for recycling while the superoxide is reduced to hydrogen peroxide (H2O2). Matcha and catechins also concentration-dependently and rapidly produce polysulfides in HEK293 cells with the potency order EGCG > EGC > EG, an EGCG threshold of ~300 nM, and an EC50 of ~3 μM, suggesting green tea also acts as powerful pro-oxidant in vivo. The resultant polysulfides formed are not only potent antioxidants, but elicit a cascade of secondary cytoprotective effects, and we propose that many of the health benefits of green tea are mediated through these reactions. Remarkably, all green tea leaves constitutively contain small amounts of H2S2. |
| first_indexed | 2024-12-17T05:26:02Z |
| format | Article |
| id | doaj.art-fef26bf76cf14328b53c8e8215713d9b |
| institution | Directory Open Access Journal |
| issn | 2213-2317 |
| language | English |
| last_indexed | 2024-12-17T05:26:02Z |
| publishDate | 2020-10-01 |
| publisher | Elsevier |
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| series | Redox Biology |
| spelling | doaj.art-fef26bf76cf14328b53c8e8215713d9b2022-12-21T22:01:52ZengElsevierRedox Biology2213-23172020-10-0137101731Green tea polyphenolic antioxidants oxidize hydrogen sulfide to thiosulfate and polysulfides: A possible new mechanism underpinning their biological actionKenneth R. Olson0Austin Briggs1Monesh Devireddy2Nicholas A. Iovino3Nicole C. Skora4Jenna Whelan5Brian P. Villa6Xiaotong Yuan7Varun Mannam8Scott Howard9Yan Gao10Magdalena Minnion11Martin Feelisch12Indiana University School of Medicine - South Bend, South Bend, IN, 46617, USA; Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, 46556, USA; Corresponding author. Indiana University School of Medicine -South Bend, Raclin Carmichael Hall, 1234 Notre Dame Avenue, South Bend, IN, 46617, USA.Indiana University School of Medicine - South Bend, South Bend, IN, 46617, USA; Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, 46556, USAIndiana University School of Medicine - South Bend, South Bend, IN, 46617, USAIndiana University School of Medicine - South Bend, South Bend, IN, 46617, USA; Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, 46556, USAIndiana University School of Medicine - South Bend, South Bend, IN, 46617, USA; Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, 46556, USAIndiana University School of Medicine - South Bend, South Bend, IN, 46617, USA; Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, 46556, USAIndiana University School of Medicine - South Bend, South Bend, IN, 46617, USA; Department of Biological Sciences, University of Notre Dame, Notre Dame, IN, 46556, USADepartment of Electrical Engineering, University of Notre Dame, Notre Dame, IN, 46556, USADepartment of Electrical Engineering, University of Notre Dame, Notre Dame, IN, 46556, USADepartment of Electrical Engineering, University of Notre Dame, Notre Dame, IN, 46556, USAIndiana University School of Medicine - South Bend, South Bend, IN, 46617, USANIHR Southampton Biomedical Research Center, University of Southampton, Southampton, General Hospital, Southampton, SO16 6YD, UK; Clinical & Experimental Sciences, Faculty of Medicine, Southampton General Hospital, University of Southampton, Southampton, SO16 6YD, UKNIHR Southampton Biomedical Research Center, University of Southampton, Southampton, General Hospital, Southampton, SO16 6YD, UK; Clinical & Experimental Sciences, Faculty of Medicine, Southampton General Hospital, University of Southampton, Southampton, SO16 6YD, UK; Corresponding author. NIHR Southampton Biomedical Research Center, University of Southampton, Southampton General Hospital, Southampton, SO16 6YD, UK.Matcha and green tea catechins such as (−)-epicatechin (EC), (−)-epigallocatechin (EGC) and (−)-epigallocatechin gallate (EGCG) have long been studied for their antioxidant and health-promoting effects. Using specific fluorophores for H2S (AzMC) and polysulfides (SSP4) as well as IC-MS and UPLC-MS/MS-based techniques we here show that popular Japanese and Chinese green teas and select catechins all catalytically oxidize hydrogen sulfide (H2S) to polysulfides with the potency of EGC > EGCG >> EG. This reaction is accompanied by the formation of sulfite, thiosulfate and sulfate, consumes oxygen and is partially inhibited by the superoxide scavenger, tempol, and superoxide dismutase but not mannitol, trolox, DMPO, or the iron chelator, desferrioxamine. We propose that the reaction proceeds via a one-electron autoxidation process during which one of the OH-groups of the catechin B-ring is autooxidized to a semiquinone radical and oxygen is reduced to superoxide, either of which can then oxidize HS− to thiyl radicals (HS•) which react to form hydrogen persulfide (H2S2). H2S oxidation reduces the B-ring back to the hydroquinone for recycling while the superoxide is reduced to hydrogen peroxide (H2O2). Matcha and catechins also concentration-dependently and rapidly produce polysulfides in HEK293 cells with the potency order EGCG > EGC > EG, an EGCG threshold of ~300 nM, and an EC50 of ~3 μM, suggesting green tea also acts as powerful pro-oxidant in vivo. The resultant polysulfides formed are not only potent antioxidants, but elicit a cascade of secondary cytoprotective effects, and we propose that many of the health benefits of green tea are mediated through these reactions. Remarkably, all green tea leaves constitutively contain small amounts of H2S2.http://www.sciencedirect.com/science/article/pii/S2213231720309368Reactive sulfide speciesReactive oxygen speciesAntioxidants |
| spellingShingle | Kenneth R. Olson Austin Briggs Monesh Devireddy Nicholas A. Iovino Nicole C. Skora Jenna Whelan Brian P. Villa Xiaotong Yuan Varun Mannam Scott Howard Yan Gao Magdalena Minnion Martin Feelisch Green tea polyphenolic antioxidants oxidize hydrogen sulfide to thiosulfate and polysulfides: A possible new mechanism underpinning their biological action Redox Biology Reactive sulfide species Reactive oxygen species Antioxidants |
| title | Green tea polyphenolic antioxidants oxidize hydrogen sulfide to thiosulfate and polysulfides: A possible new mechanism underpinning their biological action |
| title_full | Green tea polyphenolic antioxidants oxidize hydrogen sulfide to thiosulfate and polysulfides: A possible new mechanism underpinning their biological action |
| title_fullStr | Green tea polyphenolic antioxidants oxidize hydrogen sulfide to thiosulfate and polysulfides: A possible new mechanism underpinning their biological action |
| title_full_unstemmed | Green tea polyphenolic antioxidants oxidize hydrogen sulfide to thiosulfate and polysulfides: A possible new mechanism underpinning their biological action |
| title_short | Green tea polyphenolic antioxidants oxidize hydrogen sulfide to thiosulfate and polysulfides: A possible new mechanism underpinning their biological action |
| title_sort | green tea polyphenolic antioxidants oxidize hydrogen sulfide to thiosulfate and polysulfides a possible new mechanism underpinning their biological action |
| topic | Reactive sulfide species Reactive oxygen species Antioxidants |
| url | http://www.sciencedirect.com/science/article/pii/S2213231720309368 |
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