Publication Information
Huang et al., 2019
Abstract
Proc Natl Acad Sci U S A. 2019 Oct 15;116(42):21256-21261. doi:
10.1073/pnas.1906768116. Epub 2019 Oct 2.
Mining for protein S-sulfenylation in Arabidopsis uncovers redox-sensitive
sites.
Huang J(1)(2)(3)(4)(5), Willems P(1)(2)(6)(7), Wei B(1)(2)(3)(4)(5), Tian C(8),
Ferreira RB(9), Bodra N(1)(2)(3)(4)(5), Martínez Gache SA(3)(4)(5), Wahni
K(3)(4)(5), Liu K(8), Vertommen D(10), Gevaert K(6)(7), Carroll KS(9), Van
Montagu M(11)(2), Yang J(12), Van Breusegem F(11)(2), Messens J(13)(4)(5).
Author information:
(1)Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052
Ghent, Belgium.
(2)Center for Plant Systems Biology, VIB, 9052 Ghent, Belgium.
(3)Center for Structural Biology, VIB, 1050 Brussels, Belgium.
(4)Brussels Center for Redox Biology, Vrije Universiteit Brussel, 1050 Brussels,
Belgium.
(5)Structural Biology Brussels, Vrije Universiteit Brussel, 1050 Brussels,
Belgium.
(6)Department of Biomolecular Medicine, Ghent University, 9000 Ghent, Belgium.
(7)Center for Medical Biotechnology, VIB, 9000 Ghent, Belgium.
(8)State Key Laboratory of Proteomics, Beijing Proteome Research Center,
National Center for Protein Sciences, Beijing Institute of Lifeomics, 102206
Beijing, China.
(9)Department of Chemistry, The Scripps Research Institute, Jupiter, FL 33458.
(10)de Duve Institute, Université Catholique de Louvain, 1200 Brussels, Belgium.
(11)Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052
Ghent, Belgium; marc.vanmontagu@ugent.be yangjing54@hotmail.com
frank.vanbreusegem@psb.vib-ugent.be joris.messens@vub.vib.be.
(12)State Key Laboratory of Proteomics, Beijing Proteome Research Center,
National Center for Protein Sciences, Beijing Institute of Lifeomics, 102206
Beijing, China; marc.vanmontagu@ugent.be yangjing54@hotmail.com
frank.vanbreusegem@psb.vib-ugent.be joris.messens@vub.vib.be.
(13)Center for Structural Biology, VIB, 1050 Brussels, Belgium;
marc.vanmontagu@ugent.be yangjing54@hotmail.com
frank.vanbreusegem@psb.vib-ugent.be joris.messens@vub.vib.be.
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.
DOI: 10.1073/pnas.1906768116
PMCID: PMC6800386
PMID: 31578252 [Indexed for MEDLINE]
Conflict of interest statement: The authors declare no competing interest.
