Positive Regulation of Interleukin-1β Bioactivity by Physiological ROS-Mediated Cysteine S-Glutathionylation
Reactive oxygen species (ROS)-induced cysteine S-glutathionylation is an important posttranslational modification (PTM) that controls a wide range of intracellular protein activities. However, whether physiological ROS can modulate the function of extracellular components via S-glutathionylation is ...
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Elsevier
2017-07-01
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| Series: | Cell Reports |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124717307271 |
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| author | Xue Zhang Peng Liu Christie Zhang Direkrit Chiewchengchol Fan Zhao Hongbo Yu Jingyu Li Hiroto Kambara Kate Y. Luo Arvind Venkataraman Ziling Zhou Weidong Zhou Haiyan Zhu Li Zhao Jiro Sakai Yuanyuan Chen Ye-Shih Ho Besnik Bajrami Bing Xu Leslie E. Silberstein Tao Cheng Yuanfu Xu Yuehai Ke Hongbo R. Luo |
| author_facet | Xue Zhang Peng Liu Christie Zhang Direkrit Chiewchengchol Fan Zhao Hongbo Yu Jingyu Li Hiroto Kambara Kate Y. Luo Arvind Venkataraman Ziling Zhou Weidong Zhou Haiyan Zhu Li Zhao Jiro Sakai Yuanyuan Chen Ye-Shih Ho Besnik Bajrami Bing Xu Leslie E. Silberstein Tao Cheng Yuanfu Xu Yuehai Ke Hongbo R. Luo |
| author_sort | Xue Zhang |
| collection | DOAJ |
| description | Reactive oxygen species (ROS)-induced cysteine S-glutathionylation is an important posttranslational modification (PTM) that controls a wide range of intracellular protein activities. However, whether physiological ROS can modulate the function of extracellular components via S-glutathionylation is unknown. Using a screening approach, we identified ROS-mediated cysteine S-glutathionylation on several extracellular cytokines. Glutathionylation of the highly conserved Cys-188 in IL-1β positively regulates its bioactivity by preventing its ROS-induced irreversible oxidation, including sulfinic acid and sulfonic acid formation. We show this mechanism protects IL-1β from deactivation by ROS in an in vivo system of irradiation-induced bone marrow (BM) injury. Glutaredoxin 1 (Grx1), an enzyme that catalyzes deglutathionylation, was present and active in the extracellular space in serum and the BM, physiologically regulating IL-1β glutathionylation and bioactivity. Collectively, we identify cysteine S-glutathionylation as a cytokine regulatory mechanism that could be a therapeutic target in the treatment of various infectious and inflammatory diseases. |
| first_indexed | 2024-04-13T23:57:21Z |
| format | Article |
| id | doaj.art-3ed102667e6c4843a6716263d2cc2f0c |
| institution | Directory Open Access Journal |
| issn | 2211-1247 |
| language | English |
| last_indexed | 2024-04-13T23:57:21Z |
| publishDate | 2017-07-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Cell Reports |
| spelling | doaj.art-3ed102667e6c4843a6716263d2cc2f0c2022-12-22T02:23:49ZengElsevierCell Reports2211-12472017-07-0120122423510.1016/j.celrep.2017.05.070Positive Regulation of Interleukin-1β Bioactivity by Physiological ROS-Mediated Cysteine S-GlutathionylationXue Zhang0Peng Liu1Christie Zhang2Direkrit Chiewchengchol3Fan Zhao4Hongbo Yu5Jingyu Li6Hiroto Kambara7Kate Y. Luo8Arvind Venkataraman9Ziling Zhou10Weidong Zhou11Haiyan Zhu12Li Zhao13Jiro Sakai14Yuanyuan Chen15Ye-Shih Ho16Besnik Bajrami17Bing Xu18Leslie E. Silberstein19Tao Cheng20Yuanfu Xu21Yuehai Ke22Hongbo R. Luo23Department of Pathology and Pathophysiology, Program in Molecular Cell Biology, Zhejiang University School of Medicine, Hangzhou 310058, ChinaThe State Key Laboratory of Experimental Hematology, Institute of Hematology and Blood Diseases Hospital, Center for Stem Cell Medicine, Chinese Academy of Medical Sciences and Peking Union Medical College, 288 Nanjing Road, Tianjin 300020, ChinaDepartment of Pathology, Harvard Medical School, Boston, MA 02115, USADepartment of Pathology, Harvard Medical School, Boston, MA 02115, USAThe State Key Laboratory of Experimental Hematology, Institute of Hematology and Blood Diseases Hospital, Center for Stem Cell Medicine, Chinese Academy of Medical Sciences and Peking Union Medical College, 288 Nanjing Road, Tianjin 300020, ChinaHematopathology, Flow Cytometry, Hematology, and Blood Bank Labs, VA Boston Healthcare System, West Roxbury, MA 02132, USADepartment of Pathology, Harvard Medical School, Boston, MA 02115, USADepartment of Pathology, Harvard Medical School, Boston, MA 02115, USADepartment of Pathology, Harvard Medical School, Boston, MA 02115, USADepartment of Pathology, Harvard Medical School, Boston, MA 02115, USADepartment of Pathology, Harvard Medical School, Boston, MA 02115, USACenter for Applied Proteomics and Molecular Medicine, George Mason University, Manassas, VA 20110, USAThe State Key Laboratory of Experimental Hematology, Institute of Hematology and Blood Diseases Hospital, Center for Stem Cell Medicine, Chinese Academy of Medical Sciences and Peking Union Medical College, 288 Nanjing Road, Tianjin 300020, ChinaDepartment of Pathology, Harvard Medical School, Boston, MA 02115, USADepartment of Pathology, Harvard Medical School, Boston, MA 02115, USADepartment of Pathology and Pathophysiology, Program in Molecular Cell Biology, Zhejiang University School of Medicine, Hangzhou 310058, ChinaInstitute of Environmental Health Sciences and Department of Biochemistry and Molecular Biology, Wayne State University, Detroit, MI 48201, USAMass Spectrometry Unit, Waters Corporation, Milford, MA 01757, USADepartment of Chemistry, Brandeis University, 415 South Street MS015, Waltham, MA 02454, USADepartment of Pathology, Harvard Medical School, Boston, MA 02115, USAThe State Key Laboratory of Experimental Hematology, Institute of Hematology and Blood Diseases Hospital, Center for Stem Cell Medicine, Chinese Academy of Medical Sciences and Peking Union Medical College, 288 Nanjing Road, Tianjin 300020, ChinaThe State Key Laboratory of Experimental Hematology, Institute of Hematology and Blood Diseases Hospital, Center for Stem Cell Medicine, Chinese Academy of Medical Sciences and Peking Union Medical College, 288 Nanjing Road, Tianjin 300020, ChinaDepartment of Pathology, Harvard Medical School, Boston, MA 02115, USADepartment of Pathology, Harvard Medical School, Boston, MA 02115, USAReactive oxygen species (ROS)-induced cysteine S-glutathionylation is an important posttranslational modification (PTM) that controls a wide range of intracellular protein activities. However, whether physiological ROS can modulate the function of extracellular components via S-glutathionylation is unknown. Using a screening approach, we identified ROS-mediated cysteine S-glutathionylation on several extracellular cytokines. Glutathionylation of the highly conserved Cys-188 in IL-1β positively regulates its bioactivity by preventing its ROS-induced irreversible oxidation, including sulfinic acid and sulfonic acid formation. We show this mechanism protects IL-1β from deactivation by ROS in an in vivo system of irradiation-induced bone marrow (BM) injury. Glutaredoxin 1 (Grx1), an enzyme that catalyzes deglutathionylation, was present and active in the extracellular space in serum and the BM, physiologically regulating IL-1β glutathionylation and bioactivity. Collectively, we identify cysteine S-glutathionylation as a cytokine regulatory mechanism that could be a therapeutic target in the treatment of various infectious and inflammatory diseases.http://www.sciencedirect.com/science/article/pii/S2211124717307271cytokinesinterleukin-1oxidationinfection and inflammationreactive oxygen speciesposttranslational modificationcysteine S-glutathionylation |
| spellingShingle | Xue Zhang Peng Liu Christie Zhang Direkrit Chiewchengchol Fan Zhao Hongbo Yu Jingyu Li Hiroto Kambara Kate Y. Luo Arvind Venkataraman Ziling Zhou Weidong Zhou Haiyan Zhu Li Zhao Jiro Sakai Yuanyuan Chen Ye-Shih Ho Besnik Bajrami Bing Xu Leslie E. Silberstein Tao Cheng Yuanfu Xu Yuehai Ke Hongbo R. Luo Positive Regulation of Interleukin-1β Bioactivity by Physiological ROS-Mediated Cysteine S-Glutathionylation Cell Reports cytokines interleukin-1 oxidation infection and inflammation reactive oxygen species posttranslational modification cysteine S-glutathionylation |
| title | Positive Regulation of Interleukin-1β Bioactivity by Physiological ROS-Mediated Cysteine S-Glutathionylation |
| title_full | Positive Regulation of Interleukin-1β Bioactivity by Physiological ROS-Mediated Cysteine S-Glutathionylation |
| title_fullStr | Positive Regulation of Interleukin-1β Bioactivity by Physiological ROS-Mediated Cysteine S-Glutathionylation |
| title_full_unstemmed | Positive Regulation of Interleukin-1β Bioactivity by Physiological ROS-Mediated Cysteine S-Glutathionylation |
| title_short | Positive Regulation of Interleukin-1β Bioactivity by Physiological ROS-Mediated Cysteine S-Glutathionylation |
| title_sort | positive regulation of interleukin 1β bioactivity by physiological ros mediated cysteine s glutathionylation |
| topic | cytokines interleukin-1 oxidation infection and inflammation reactive oxygen species posttranslational modification cysteine S-glutathionylation |
| url | http://www.sciencedirect.com/science/article/pii/S2211124717307271 |
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