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Mining for protein S-sulfenylation in Arabidopsis uncovers redox-sensitive sites

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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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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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