Metabolism of hydrogen sulfide (H2S) and Production of Reactive Sulfur Species (RSS) by superoxide dismutase
Reactive sulfur species (RSS) such as H2S, HS•, H2Sn, (n = 2–7) and HS2•- are chemically similar to H2O and the reactive oxygen species (ROS) HO•, H2O2, O2•- and act on common biological effectors. RSS were present in evolution long before ROS, and because both are metabolized by catalase it has bee...
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| Format: | Article |
| Language: | English |
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Elsevier
2018-05-01
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| Series: | Redox Biology |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213231717306730 |
| _version_ | 1818297971385565184 |
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| author | Kenneth R. Olson Yan Gao Faihaan Arif Kanika Arora Shivali Patel Eric. R. DeLeon Thomas R. Sutton Martin Feelisch Miriam M. Cortese-Krott Karl D. Straub |
| author_facet | Kenneth R. Olson Yan Gao Faihaan Arif Kanika Arora Shivali Patel Eric. R. DeLeon Thomas R. Sutton Martin Feelisch Miriam M. Cortese-Krott Karl D. Straub |
| author_sort | Kenneth R. Olson |
| collection | DOAJ |
| description | Reactive sulfur species (RSS) such as H2S, HS•, H2Sn, (n = 2–7) and HS2•- are chemically similar to H2O and the reactive oxygen species (ROS) HO•, H2O2, O2•- and act on common biological effectors. RSS were present in evolution long before ROS, and because both are metabolized by catalase it has been suggested that “antioxidant” enzymes originally evolved to regulate RSS and may continue to do so today. Here we examined RSS metabolism by Cu/Zn superoxide dismutase (SOD) using amperometric electrodes for dissolved H2S, a polysulfide-specific fluorescent probe (SSP4), and mass spectrometry to identify specific polysulfides (H2S2-H2S5). H2S was concentration- and oxygen-dependently oxidized by 1 μM SOD to polysulfides (mainly H2S2, and to a lesser extent H2S3 and H2S5) with an EC50 of approximately 380 μM H2S. H2S concentrations > 750 μM inhibited SOD oxidation (IC50 = 1.25 mM) with complete inhibition when H2S > 1.75 mM. Polysulfides were not metabolized by SOD. SOD oxidation preferred dissolved H2S over hydrosulfide anion (HS-), whereas HS- inhibited polysulfide production. In hypoxia, other possible electron donors such as nitrate, nitrite, sulfite, sulfate, thiosulfate and metabisulfite were ineffective. Manganese SOD also catalyzed H2S oxidation to form polysulfides, but did not metabolize polysulfides indicating common attributes of these SODs. These experiments suggest that, unlike the well-known SOD-mediated dismutation of two O2•- to form H2O2 and O2, SOD catalyzes a reaction using H2S and O2 to form persulfide. These can then combine in various ways to form polysulfides and sulfur oxides. It is also possible that H2S (or polysulfides) interact/react with SOD cysteines to affect catalytic activity or to directly contribute to sulfide metabolism. Our studies suggest that H2S metabolism by SOD may have been an ancient mechanism to detoxify sulfide or to regulate RSS and along with catalase may continue to do so in contemporary organisms. |
| first_indexed | 2024-12-13T04:27:54Z |
| format | Article |
| id | doaj.art-7d8b8a728e6b4f398e04fa1feaaf6c3d |
| institution | Directory Open Access Journal |
| issn | 2213-2317 |
| language | English |
| last_indexed | 2024-12-13T04:27:54Z |
| publishDate | 2018-05-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Redox Biology |
| spelling | doaj.art-7d8b8a728e6b4f398e04fa1feaaf6c3d2022-12-21T23:59:39ZengElsevierRedox Biology2213-23172018-05-0115C748510.1016/j.redox.2017.11.009Metabolism of hydrogen sulfide (H2S) and Production of Reactive Sulfur Species (RSS) by superoxide dismutaseKenneth R. Olson0Yan Gao1Faihaan Arif2Kanika Arora3Shivali Patel4Eric. R. DeLeon5Thomas R. Sutton6Martin Feelisch7Miriam M. Cortese-Krott8Karl D. Straub9Indiana University School of Medicine - South Bend Center, South Bend, IN 46617, USAIndiana University School of Medicine - South Bend Center, South Bend, IN 46617, USAIndiana University School of Medicine - South Bend Center, South Bend, IN 46617, USAIndiana University School of Medicine - South Bend Center, South Bend, IN 46617, USAIndiana University School of Medicine - South Bend Center, South Bend, IN 46617, USAIndiana University School of Medicine - South Bend Center, South Bend, IN 46617, USANIHR Southampton Biomedical Research Center, University of Southampton, Southampton, General Hospital, Southampton SO16 6YD, UKNIHR Southampton Biomedical Research Center, University of Southampton, Southampton, General Hospital, Southampton SO16 6YD, UKCardiovascular Research Laboratory, Department of Cardiology, Pneumology and Angiology,Medical Faculty, Heinrich Heine University of Düsseldorf, Universitätstrasse 1, 40225 Düsseldorf, GermanyCentral Arkansas Veteran's Healthcare System, Little Rock, AR 72205 USAReactive sulfur species (RSS) such as H2S, HS•, H2Sn, (n = 2–7) and HS2•- are chemically similar to H2O and the reactive oxygen species (ROS) HO•, H2O2, O2•- and act on common biological effectors. RSS were present in evolution long before ROS, and because both are metabolized by catalase it has been suggested that “antioxidant” enzymes originally evolved to regulate RSS and may continue to do so today. Here we examined RSS metabolism by Cu/Zn superoxide dismutase (SOD) using amperometric electrodes for dissolved H2S, a polysulfide-specific fluorescent probe (SSP4), and mass spectrometry to identify specific polysulfides (H2S2-H2S5). H2S was concentration- and oxygen-dependently oxidized by 1 μM SOD to polysulfides (mainly H2S2, and to a lesser extent H2S3 and H2S5) with an EC50 of approximately 380 μM H2S. H2S concentrations > 750 μM inhibited SOD oxidation (IC50 = 1.25 mM) with complete inhibition when H2S > 1.75 mM. Polysulfides were not metabolized by SOD. SOD oxidation preferred dissolved H2S over hydrosulfide anion (HS-), whereas HS- inhibited polysulfide production. In hypoxia, other possible electron donors such as nitrate, nitrite, sulfite, sulfate, thiosulfate and metabisulfite were ineffective. Manganese SOD also catalyzed H2S oxidation to form polysulfides, but did not metabolize polysulfides indicating common attributes of these SODs. These experiments suggest that, unlike the well-known SOD-mediated dismutation of two O2•- to form H2O2 and O2, SOD catalyzes a reaction using H2S and O2 to form persulfide. These can then combine in various ways to form polysulfides and sulfur oxides. It is also possible that H2S (or polysulfides) interact/react with SOD cysteines to affect catalytic activity or to directly contribute to sulfide metabolism. Our studies suggest that H2S metabolism by SOD may have been an ancient mechanism to detoxify sulfide or to regulate RSS and along with catalase may continue to do so in contemporary organisms.http://www.sciencedirect.com/science/article/pii/S2213231717306730AntioxidantsOxidantsRedoxReactive oxygen speciesSuperoxideHydrogen peroxideReactive Species Interactome |
| spellingShingle | Kenneth R. Olson Yan Gao Faihaan Arif Kanika Arora Shivali Patel Eric. R. DeLeon Thomas R. Sutton Martin Feelisch Miriam M. Cortese-Krott Karl D. Straub Metabolism of hydrogen sulfide (H2S) and Production of Reactive Sulfur Species (RSS) by superoxide dismutase Redox Biology Antioxidants Oxidants Redox Reactive oxygen species Superoxide Hydrogen peroxide Reactive Species Interactome |
| title | Metabolism of hydrogen sulfide (H2S) and Production of Reactive Sulfur Species (RSS) by superoxide dismutase |
| title_full | Metabolism of hydrogen sulfide (H2S) and Production of Reactive Sulfur Species (RSS) by superoxide dismutase |
| title_fullStr | Metabolism of hydrogen sulfide (H2S) and Production of Reactive Sulfur Species (RSS) by superoxide dismutase |
| title_full_unstemmed | Metabolism of hydrogen sulfide (H2S) and Production of Reactive Sulfur Species (RSS) by superoxide dismutase |
| title_short | Metabolism of hydrogen sulfide (H2S) and Production of Reactive Sulfur Species (RSS) by superoxide dismutase |
| title_sort | metabolism of hydrogen sulfide h2s and production of reactive sulfur species rss by superoxide dismutase |
| topic | Antioxidants Oxidants Redox Reactive oxygen species Superoxide Hydrogen peroxide Reactive Species Interactome |
| url | http://www.sciencedirect.com/science/article/pii/S2213231717306730 |
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