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

[en] 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. © 2019 National Academy of Sciences. All rights reserved.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Huang, Jingjing ; Université de Liège - ULiège > Département des sciences de la vie > Génétique et physiologie des microalgues

Willems, P.; Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, 9052, Belgium, Center for Plant Systems Biology, VIB, Ghent, 9052, Belgium, Department of Biomolecular Medicine, Ghent University, Ghent, 9000, Belgium, Center for Medical Biotechnology, VIB, Ghent, 9000, Belgium

Wei, B.; Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, 9052, Belgium, Center for Plant Systems Biology, VIB, Ghent, 9052, Belgium, Center for Structural Biology, VIB, Brussels, 1050, Belgium, Brussels Center for Redox Biology, Vrije Universiteit Brussel, Brussels, 1050, Belgium, Structural Biology Brussels, Vrije Universiteit Brussel, Brussels, 1050, Belgium

Tian, C.; State Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences, Beijing Institute of Lifeomics, Beijing, 102206, China

Ferreira, R. B.; Department of Chemistry, Scripps Research Institute, Jupiter, FL 33458, United States

Bodra, N.; Department of Plant Biotechnology and Bioinformatics, Ghent University, Ghent, 9052, Belgium, Center for Plant Systems Biology, VIB, Ghent, 9052, Belgium, Center for Structural Biology, VIB, Brussels, 1050, Belgium, Brussels Center for Redox Biology, Vrije Universiteit Brussel, Brussels, 1050, Belgium, Structural Biology Brussels, Vrije Universiteit Brussel, Brussels, 1050, Belgium

Martínez Gache, S. A.; Center for Structural Biology, VIB, Brussels, 1050, Belgium, Brussels Center for Redox Biology, Vrije Universiteit Brussel, Brussels, 1050, Belgium, Structural Biology Brussels, Vrije Universiteit Brussel, Brussels, 1050, Belgium

Wahni, K.; Center for Structural Biology, VIB, Brussels, 1050, Belgium, Brussels Center for Redox Biology, Vrije Universiteit Brussel, Brussels, 1050, Belgium, Structural Biology Brussels, Vrije Universiteit Brussel, Brussels, 1050, Belgium

Liu, K.; State Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences, Beijing Institute of Lifeomics, Beijing, 102206, China

Vertommen, D.; de Duve Institute, Université Catholique de Louvain, Brussels, 1200, Belgium

More authors (6 more)

Language :

English

Title :

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

Publication date :

2019

Journal title :

Proceedings of the National Academy of Sciences of the United States of America

ISSN :

0027-8424

eISSN :

1091-6490

Publisher :

National Academy of Sciences

Volume :

116

Issue :

Pages :

20256-20261

Peer reviewed :

Peer Reviewed verified by ORBi

Funders :

BOF - Bijzonder Onderzoeksfonds
CSC - China Scholarship Council [CN]
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]

Available on ORBi :

since 30 May 2020

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Bibliography

C. E. Paulsen, K. S. Carroll, Cysteine-mediated redox signaling: Chemistry, biology, and tools for discovery. Chem. Rev. 113, 4633–4679 (2013).
J. Huang, P. Willems, F. Van Breusegem, J. Messens, Pathways crossing mammalian and plant sulfenomic landscapes. Free Radic. Biol. Med. 122, 193–201 (2018).
L. Tarrago et al., Regeneration mechanisms of Arabidopsis thaliana methionine sulfoxide reductases B by glutaredoxins and thioredoxins. J. Biol. Chem. 284, 18963–18971 (2009).
L. N. Sokolov, J. R. Dominguez-Solis, A.-L. Allary, B. B. Buchanan, S. Luan, A redox-regulated chloroplast protein phosphatase binds to starch diurnally and functions in its accumulation. Proc. Natl. Acad. Sci. U.S.A. 103, 9732–9737 (2006).
Y. Tada et al., Plant immunity requires conformational changes [corrected] of NPR1 via S-nitrosylation and thioredoxins. Science 321, 952–956 (2008). Erratum in: Science 325, 1072 (2009).
Y. Tian et al., Hydrogen peroxide positively regulates brassinosteroid signaling through oxidation of the BRASSINAZOLE-RESISTANT1 transcription factor. Nat. Commun. 9, 1063 (2018).
H.-M. Yuan, W.-C. Liu, Y.-T. Lu, CATALASE2 coordinates SA-mediated repression of both auxin accumulation and JA biosynthesis in plant defenses. Cell Host Microbe 21, 143–155 (2017).
M. Bedhomme et al., Glutathionylation of cytosolic glyceraldehyde-3-phosphate dehydrogenase from the model plant Arabidopsis thaliana is reversed by both glutaredoxins and thioredoxins in vitro. Biochem. J. 445, 337–347 (2012).
B.-W. Yun et al., S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478, 264–268 (2011).
D. Peralta et al., A proton relay enhances H2O2 sensitivity of GAPDH to facilitate metabolic adaptation. Nat. Chem. Biol. 11, 156–163 (2015).
G. Kim, R. L. Levine, A methionine residue promotes hyperoxidation of the catalytic cysteine of mouse methionine sulfoxide reductase A. Biochemistry 55, 3586–3593 (2016).
J. M. Hourihan, L. E. Moronetti Mazzeo, L. P. Fernández-Cárdenas, T. K. Blackwell, Cysteine sulfenylation directs IRE-1 to activate the SKN-1/Nrf2 antioxidant response. Mol. Cell 63, 553–566 (2016).
F. K. Choudhury, R. M. Rivero, E. Blumwald, R. Mittler, Reactive oxygen species, abi-otic stress and stress combination. Plant J. 90, 856–867 (2017).
A. Mhamdi, F. Van Breusegem, Reactive oxygen species in plant development. Development 145, dev164376 (2018).
F. Van Breusegem, J. F. Dat, Reactive oxygen species in plant cell death. Plant Physiol. 141, 384–390 (2006).
C. R. Guadagno, B. E. Ewers, C. Weinig, Circadian rhythms and redox state in plants: Till stress do us part. Front. Plant Sci. 9, 247 (2018).
B. De Smet et al., In vivo detection of protein cysteine sulfenylation in plastids. Plant J. 97, 765–778 (2019).
C. Waszczak et al., Sulfenome mining in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 111, 11545–11550 (2014).
S. Akter et al., DYn-2 based identification of Arabidopsis sulfenomes. Mol. Cell. Proteomics 14, 1183–1200 (2015).
V. Gupta, J. Yang, D. C. Liebler, K. S. Carroll, Diverse redoxome reactivity profiles of carbon nucleophiles. J. Am. Chem. Soc. 139, 5588–5595 (2017).
L. Fu, K. Liu, R. B. Ferreira, K. S. Carroll, J. Yang, Proteome-wide analysis of cysteine S-sulfenylation using a benzothiazine-based probe. Curr. Protoc. Protein Sci. 95, e76 (2019).
S. Akter et al., Chemical proteomics reveals new targets of cysteine sulfinic acid reductase. Nat. Chem. Biol. 14, 995–1004 (2018).
J. Yang, V. Gupta, K. S. Carroll, D. C. Liebler, Site-specific mapping and quantification of protein S-sulphenylation in cells. Nat. Commun. 5, 4776 (2014).
X. Deng et al., Proteome-wide quantification and characterization of oxidation-sensitive cysteines in pathogenic bacteria. Cell Host Microbe 13, 358–370 (2013).
J. Guo et al., Proteome-wide light/dark modulation of thiol oxidation in cyanobac-teria revealed by quantitative site-specific redox proteomics. Mol. Cell. Proteomics 13, 3270–3285 (2014).
B. Ezraty, A. Gennaris, F. Barras, J. F. Collet, Oxidative stress, protein damage and repair in bacteria. Nat. Rev. Microbiol. 15, 385–396 (2017).
L. I. Leichert et al., Quantifying changes in the thiol redox proteome upon oxidative stress in vivo. Proc. Natl. Acad. Sci. U.S.A. 105, 8197–8202 (2008).
C. M. Hooper et al., Multiple marker abundance profiling: Combining selected reaction monitoring and data-dependent acquisition for rapid estimation of organelle abundance in subcellular samples. Plant J. 92, 1202–1217 (2017).
C. M. Hooper, I. R. Castleden, S. K. Tanz, N. Aryamanesh, A. H. Millar, SUBA4: The interactive data analysis centre for Arabidopsis subcellular protein locations. Nucleic Acids Res. 45, D1064–D1074 (2017).
D. A. Belostotsky, Unexpected complexity of poly(A)-binding protein gene families in flowering plants: Three conserved lineages that are at least 200 million years old and possible auto- and cross-regulation. Genetics 163, 311–319 (2003).
S.-H. Kim, D. Arnold, A. Lloyd, S. J. Roux, Antisense expression of an Arabidopsis Ran binding protein renders transgenic roots hypersensitive to auxin and alters auxin-induced root growth and development by arresting mitotic progress. Plant Cell 13, 2619–2630 (2001).
J. Li, A. Mahajan, M.-D. Tsai, Ankyrin repeat: A unique motif mediating protein–protein interactions. Biochemistry 45, 15168–15178 (2006).
C. Xu, J. Min, Structure and function of WD40 domain proteins. Protein Cell 2, 202–214 (2011).
UniProt Consortium, UniProt: A worldwide hub of protein knowledge. Nucleic Acids Res. 47, D506–D515 (2019).
A. Ikegami et al., The CHLI1 subunit of Arabidopsis thaliana magnesium chelatase is a target protein of the chloroplast thioredoxin. J. Biol. Chem. 282, 19282–19291 (2007).
X. Liu et al., Structural insights into the N-terminal GIY-YIG endonuclease activity of Arabidopsis glutaredoxin AtGRXS16 in chloroplasts. Proc. Natl. Acad. Sci. U.S.A. 110, 9565–9570 (2013).
K. Motohashi, F. Koyama, Y. Nakanishi, H. Ueoka-Nakanishi, T. Hisabori, Chloroplast cyclophilin is a target protein of thioredoxin. Thiol modulation of the peptidyl-prolyl cis-trans isomerase activity. J. Biol. Chem. 278, 31848–31852 (2003).
P. G. Blommel et al., Crystal structure of gene locus At3g16990 from Arabidopsis thaliana. Proteins 57, 221–222 (2004).
L. Men, Y. Wang, The oxidation of yeast alcohol dehydrogenase-1 by hydrogen peroxide in vitro. J. Proteome Res. 6, 216–225 (2007).
S. Dumont et al., Arabidopsis thaliana alcohol dehydrogenase is differently affected by several redox modifications. PLoS One 13, e0204530 (2018).
N. Colaert, K. Helsens, L. Martens, J. Vandekerckhove, K. Gevaert, Improved visualization of protein consensus sequences by iceLogo. Nat. Methods 6, 786–787 (2009).
V. Gupta, K. S. Carroll, Sulfenic acid chemistry, detection and cellular lifetime. Biochim. Biophys. Acta 1840, 847–875 (2014).
G. Roos, N. Foloppe, J. Messens, Understanding the pKa of redox cysteines: The key role of hydrogen bonding. Antioxid. Redox Signal. 18, 94–127 (2013).
D. A. Meekins, C. W. Vander Kooi, M. S. Gentry, Structural mechanisms of plant glucan phosphatases in starch metabolism. FEBS J. 283, 2427–2447 (2016).
H. M. Lander et al., A molecular redox switch on p21ras. Structural basis for the nitric oxide-p21ras interaction. J. Biol. Chem. 272, 4323–4326 (1997).
J. Heo, S. L. Campbell, Mechanism of p21Ras S-nitrosylation and kinetics of nitric oxide-mediated guanine nucleotide exchange. Biochemistry 43, 2314–2322 (2004).
S. E. Leonard, K. G. Reddie, K. S. Carroll, Mining the thiol proteome for sulfenic acid modifications reveals new targets for oxidation in cells. ACS Chem. Biol. 4, 783–799 (2009).
M. Chatterjee, B. M. Paschal, Disruption of the Ran system by cysteine oxidation of the nucleotide exchange factor RCC1. Mol. Cell. Biol. 35, 566–581 (2015).
J. M. Denu, K. G. Tanner, Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: Evidence for a sulfenic acid intermediate and implications for redox regulation. Biochemistry 37, 5633–5642 (1998).
J.-S. Kim, T. Y. Huang, G. M. Bokoch, Reactive oxygen species regulate a slingshot-cofilin activation pathway. Mol. Biol. Cell 20, 2650–2660 (2009).
Z. Jandova, Z. Trosanova, V. Weisova, C. Oostenbrink, J. Hritz, Free energy calculations on the stability of the 14-3-3ζ protein. Biochim. Biophys. Acta. 1866, 442–450 (2018).
Y. Liu, C. He, A review of redox signaling and the control of MAP kinase pathway in plants. Redox Biol. 11, 192–204 (2017).
R. Desikan, J. T. Hancock, K. Ichimura, K. Shinozaki, S. J. Neill, Harpin induces activation of the Arabidopsis mitogen-activated protein kinases AtMPK4 and AtMPK6. Plant Physiol. 126, 1579–1587 (2001).
D. Ortiz-Masia, M. A. Perez-Amador, J. Carbonell, M. J. Marcote, Diverse stress signals activate the C1 subgroup MAP kinases of Arabidopsis. FEBS Lett. 581, 1834–1840 (2007).
R. Dóczi et al., The Arabidopsis mitogen-activated protein kinase kinase MKK3 is upstream of group C mitogen-activated protein kinases and participates in pathogen signaling. Plant Cell 19, 3266–3279 (2007).
H. Nakagami, H. Soukupová, A. Schikora, V. Žárský, H. Hirt, A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J. Biol. Chem. 281, 38697–38704 (2006).
D. Dorin et al., An atypical mitogen-activated protein kinase (MAPK) homologue expressed in gametocytes of the human malaria parasite Plasmodium falciparum. Identification of a MAPK signature. J. Biol. Chem. 274, 29912–29920 (1999).
B. Wang et al., Analysis of crystal structure of Arabidopsis MPK6 and generation of its mutants with higher activity. Sci. Rep. 6, 25646 (2016).
Á. Garai et al., Specificity of linear motifs that bind to a common mitogen-activated protein kinase docking groove. Sci. Signal. 5, ra74 (2012).
J. A. Smith et al., Creation of a stress-activated p90 ribosomal S6 kinase. The carboxyl-terminal tail of the MAPK-activated protein kinases dictates the signal transduction pathway in which they function. J. Biol. Chem. 275, 31588–31593 (2000).
A. Reményi, M. C. Good, W. A. Lim, Docking interactions in protein kinase and phosphatase networks. Curr. Opin. Struct. Biol. 16, 676–685 (2006).
T. Tanoue, M. Adachi, T. Moriguchi, E. Nishida, A conserved docking motif in MAP kinases common to substrates, activators and regulators. Nat. Cell Biol. 2, 110–116 (2000).
J. D. Keyes et al., Endogenous, regulatory cysteine sulfenylation of ERK kinases in response to proliferative signals. Free Radic. Biol. Med. 112, 534–543 (2017).
J. Wu et al., Autophosphorylation in vitro of recombinant 42-kilodalton mitogen-activated protein kinase on tyrosine. Proc. Natl. Acad. Sci. U.S.A. 88, 9508–9512 (1991).
J. Van Leene et al., A tandem affinity purification-based technology platform to study the cell cycle interactome in Arabidopsis thaliana. Mol. Cell. Proteomics 6, 1226–1238 (2007).
J. Yang, K. A. Tallman, N. A. Porter, D. C. Liebler, Quantitative chemoproteomics for site-specific analysis of protein alkylation by 4-hydroxy-2-nonenal in cells. Anal. Chem. 87, 2535–2541 (2015).
Y. Perez-Riverol et al., The PRIDE database and related tools and resources in 2019: Improving support for quantification data. Nucleic Acids Res. 47, D442–D450 (2019).
J. Huang et al., Self-protection of cytosolic malate dehydrogenase against oxidative stress in Arabidopsis. J. Exp. Bot. 69, 3491–3505 (2018).