
Mining for protein S-sulfenylation in Arabidopsis uncovers redox-sensitive sites
(2019)
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA.
116(42).
p.21256-21261
- Author
- Jingjing Huang (UGent) , Patrick Willems (UGent) , Bo Wei (UGent) , Caiping Tian, Renan B Ferreira, Nandita Bodra (UGent) , Santiago Agustín Martínez Gache, Khadija Wahni, Keke Liu, Didier Vertommen, Kris Gevaert (UGent) , Kate S Carroll, Marc Van Montagu (UGent) , Jing Yang, Frank Van Breusegem (UGent) and Joris Messens
- Organization
- Abstract
- Hydrogen peroxide (H2O2) is an important messenger molecule for diverse cellular processes. H2O2 oxidizes proteinaceous cysteinyl thiols to sulfenic acid, also known as S-sulfenylation, thereby affecting the protein conformation and functionality. Although many proteins have been identified as S-sulfenylation targets in plants, site-specific mapping and quantification remain largely unexplored. By means of a peptide-centric chemoproteomics approach, we mapped 1,537 S-sulfenylated sites on more than 1,000 proteins in Arabidopsis thaliana cells. Proteins involved in RNA homeostasis and metabolism were identified as hotspots for S-sulfenylation. Moreover, S-sulfenylation frequently occurred on cysteines located at catalytic sites of enzymes or on cysteines involved in metal binding, hinting at a direct mode of action for redox regulation. Comparison of human and Arabidopsis S-sulfenylation datasets provided 155 conserved S-sulfenylated cysteines, including Cys181 of the Arabidopsis MITOGEN-ACTIVATED PROTEIN KINASE4 (AtMAPK4) that corresponds to Cys161 in the human MAPK1, which has been identified previously as being S-sulfenylated. We show that, by replacing Cys181 of recombinant AtMAPK4 by a redox-insensitive serine residue, the kinase activity decreased, indicating the importance of this noncatalytic cysteine for the kinase mechanism. Altogether, we quantitatively mapped the S-sulfenylated cysteines in Arabidopsis cells under H2O2 stress and thereby generated a comprehensive view on the S-sulfenylation landscape that will facilitate downstream plant redox studies.
- Keywords
- S-sulfenylation, redox regulation, posttranslational modification, Arabidopsis, chemoproteomics, OXIDATIVE STRESS, CYSTEINE SULFENYLATION, HYDROGEN-PEROXIDE, TARGET PROTEIN, MAP KINASES, NITROSYLATION, THALIANA, IDENTIFICATION, DEHYDROGENASE, GLUTAREDOXINS
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Citation
Please use this url to cite or link to this publication: http://hdl.handle.net/1854/LU-8631988
- MLA
- Huang, Jingjing, et al. “Mining for Protein S-Sulfenylation in Arabidopsis Uncovers Redox-Sensitive Sites.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 116, no. 42, 2019, pp. 21256–61, doi:10.1073/pnas.1906768116.
- APA
- Huang, J., Willems, P., Wei, B., Tian, C., Ferreira, R. B., Bodra, N., … Messens, J. (2019). Mining for protein S-sulfenylation in Arabidopsis uncovers redox-sensitive sites. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 116(42), 21256–21261. https://doi.org/10.1073/pnas.1906768116
- Chicago author-date
- Huang, Jingjing, Patrick Willems, Bo Wei, Caiping Tian, Renan B Ferreira, Nandita Bodra, Santiago Agustín Martínez Gache, et al. 2019. “Mining for Protein S-Sulfenylation in Arabidopsis Uncovers Redox-Sensitive Sites.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 116 (42): 21256–61. https://doi.org/10.1073/pnas.1906768116.
- Chicago author-date (all authors)
- Huang, Jingjing, Patrick Willems, Bo Wei, Caiping Tian, Renan B Ferreira, Nandita Bodra, Santiago Agustín Martínez Gache, Khadija Wahni, Keke Liu, Didier Vertommen, Kris Gevaert, Kate S Carroll, Marc Van Montagu, Jing Yang, Frank Van Breusegem, and Joris Messens. 2019. “Mining for Protein S-Sulfenylation in Arabidopsis Uncovers Redox-Sensitive Sites.” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 116 (42): 21256–21261. doi:10.1073/pnas.1906768116.
- Vancouver
- 1.Huang J, Willems P, Wei B, Tian C, Ferreira RB, Bodra N, et al. Mining for protein S-sulfenylation in Arabidopsis uncovers redox-sensitive sites. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA. 2019;116(42):21256–61.
- IEEE
- [1]J. Huang et al., “Mining for protein S-sulfenylation in Arabidopsis uncovers redox-sensitive sites,” PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, vol. 116, no. 42, pp. 21256–21261, 2019.
@article{8631988, abstract = {{Hydrogen peroxide (H2O2) is an important messenger molecule for diverse cellular processes. H2O2 oxidizes proteinaceous cysteinyl thiols to sulfenic acid, also known as S-sulfenylation, thereby affecting the protein conformation and functionality. Although many proteins have been identified as S-sulfenylation targets in plants, site-specific mapping and quantification remain largely unexplored. By means of a peptide-centric chemoproteomics approach, we mapped 1,537 S-sulfenylated sites on more than 1,000 proteins in Arabidopsis thaliana cells. Proteins involved in RNA homeostasis and metabolism were identified as hotspots for S-sulfenylation. Moreover, S-sulfenylation frequently occurred on cysteines located at catalytic sites of enzymes or on cysteines involved in metal binding, hinting at a direct mode of action for redox regulation. Comparison of human and Arabidopsis S-sulfenylation datasets provided 155 conserved S-sulfenylated cysteines, including Cys181 of the Arabidopsis MITOGEN-ACTIVATED PROTEIN KINASE4 (AtMAPK4) that corresponds to Cys161 in the human MAPK1, which has been identified previously as being S-sulfenylated. We show that, by replacing Cys181 of recombinant AtMAPK4 by a redox-insensitive serine residue, the kinase activity decreased, indicating the importance of this noncatalytic cysteine for the kinase mechanism. Altogether, we quantitatively mapped the S-sulfenylated cysteines in Arabidopsis cells under H2O2 stress and thereby generated a comprehensive view on the S-sulfenylation landscape that will facilitate downstream plant redox studies.}}, author = {{Huang, Jingjing and Willems, Patrick and Wei, Bo and Tian, Caiping and Ferreira, Renan B and Bodra, Nandita and Martínez Gache, Santiago Agustín and Wahni, Khadija and Liu, Keke and Vertommen, Didier and Gevaert, Kris and Carroll, Kate S and Van Montagu, Marc and Yang, Jing and Van Breusegem, Frank and Messens, Joris}}, issn = {{0027-8424}}, journal = {{PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA}}, keywords = {{S-sulfenylation,redox regulation,posttranslational modification,Arabidopsis,chemoproteomics,OXIDATIVE STRESS,CYSTEINE SULFENYLATION,HYDROGEN-PEROXIDE,TARGET PROTEIN,MAP KINASES,NITROSYLATION,THALIANA,IDENTIFICATION,DEHYDROGENASE,GLUTAREDOXINS}}, language = {{eng}}, number = {{42}}, pages = {{21256--21261}}, title = {{Mining for protein S-sulfenylation in Arabidopsis uncovers redox-sensitive sites}}, url = {{http://dx.doi.org/10.1073/pnas.1906768116}}, volume = {{116}}, year = {{2019}}, }
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