Thioredoxins: Emerging Players in the Regulation of Protein S-Nitrosation in Plants
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, přehledy
Grantová podpora
IGA_PrF_2020_013
Univerzita Palackého v Olomouci
PubMed
33114295
PubMed Central
PMC7690881
DOI
10.3390/plants9111426
PII: plants9111426
Knihovny.cz E-zdroje
- Klíčová slova
- S-nitrosation, denitrosation, nitric oxide, plant redox signaling, reactive nitrogen species, thioredoxin, thioredoxin reductase,
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
S-nitrosation has been recognized as an important mechanism of ubiquitous posttranslational modification of proteins on the basis of the attachment of the nitroso group to cysteine thiols. Reversible S-nitrosation, similarly to other redox-based modifications of protein thiols, has a profound effect on protein structure and activity and is considered as a convergence of signaling pathways of reactive nitrogen and oxygen species. This review summarizes the current knowledge on the emerging role of the thioredoxin-thioredoxin reductase (TRXR-TRX) system in protein denitrosation. Important advances have been recently achieved on plant thioredoxins (TRXs) and their properties, regulation, and functions in the control of protein S-nitrosation in plant root development, translation of photosynthetic light harvesting proteins, and immune responses. Future studies of plants with down- and upregulated TRXs together with the application of genomics and proteomics approaches will contribute to obtain new insights into plant S-nitrosothiol metabolism and its regulation.
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Walsh C.T., Garneau-Tsodikova S., Gatto G.J., Jr. Protein Posttranslational Modifications: The Chemistry of Proteome Diversifications. Angew. Chem. Int. Ed. 2005;44:7342–7372. doi: 10.1002/anie.200501023. PubMed DOI
Duan G., Walther D. The Roles of Post-translational Modifications in the Context of Protein Interaction Networks. PLoS Comput. Biol. 2015;11:e1004049. doi: 10.1371/journal.pcbi.1004049. PubMed DOI PMC
Friso G., Van Wijk K.J. Update: Post-translational protein modifications in plant metabolism. Plant Physiol. 2015;169:1469–1487. doi: 10.1104/pp.15.01378. PubMed DOI PMC
Wu C., Liu T., Chen W., Oka S.-I., Fu C., Jain M.R., Parrott A.M., Baykal A.T., Sadoshima J., Li H. Redox Regulatory Mechanism of Transnitrosylation by Thioredoxin. Mol. Cell. Proteom. 2010;9:2262–2275. doi: 10.1074/mcp.M110.000034. PubMed DOI PMC
Hashiguchi A., Komatsu S. Posttranslational Modifications and Plant–Environment Interaction. Methods Enzymol. 2017;586:97–113. PubMed
Spoel S.H. Orchestrating the proteome with post-translational modifications. J. Exp. Bot. 2018;69:4499–4503. doi: 10.1093/jxb/ery295. PubMed DOI PMC
Klomsiri C., Karplus P.A., Poole L.B. Cysteine-Based Redox Switches in Enzymes. Antioxid. Redox Signal. 2011;14:1065–1077. doi: 10.1089/ars.2010.3376. PubMed DOI PMC
Poole L.B. The basics of thiols and cysteines in redox biology and chemistry. Free Radic. Biol. Med. 2015;80:148–157. doi: 10.1016/j.freeradbiomed.2014.11.013. PubMed DOI PMC
Waszczak C., Akter S., Jacques S., Huang J., Messens J., Van Breusegem F. Oxidative post-translational modifications of cysteine residues in plant signal transduction. J. Exp. Bot. 2015;66:2923–2934. doi: 10.1093/jxb/erv084. PubMed DOI
Ruiz-May E., Segura-Cabrera A., Elizalde-Contreras J.M., Shannon L.M., Loyola-Vargas V.M. A recent advance in the intracellular and extracellular redox post-translational modification of proteins in plants. J. Mol. Recognit. 2018;32:e2754. doi: 10.1002/jmr.2754. PubMed DOI
Šírová J., Sedlářová M., Piterková J., Luhová L., Petrivalsky M. The role of nitric oxide in the germination of plant seeds and pollen. Plant Sci. 2011;181:560–572. doi: 10.1016/j.plantsci.2011.03.014. PubMed DOI
Astier J., Gross I., Durner J. Nitric oxide production in plants: An update. J. Exp. Bot. 2017;69:3401–3411. doi: 10.1093/jxb/erx420. PubMed DOI
Corpas F.J., Del Río L.A., Palma J.M. Impact of Nitric Oxide (NO) on the ROS Metabolism of Peroxisomes. Plants. 2019;8:37. doi: 10.3390/plants8020037. PubMed DOI PMC
Hancock J.T., Neill S.J. Nitric Oxide: Its Generation and Interactions with Other Reactive Signaling Compounds. Plants. 2019;8:41. doi: 10.3390/plants8020041. PubMed DOI PMC
Petřivalský M., Luhová L. Nitrated Nucleotides: New Players in Signaling Pathways of Reactive Nitrogen and Oxygen Species in Plants. Front. Plant Sci. 2020;11:598. doi: 10.3389/fpls.2020.00598. PubMed DOI PMC
Astier J., Lindermayr C. Nitric Oxide-Dependent Posttranslational Modification in Plants: An Update. Int. J. Mol. Sci. 2012;13:15193–15208. doi: 10.3390/ijms131115193. PubMed DOI PMC
Kovacs I., Lindermayr C. Nitric oxide-based protein modification: Formation and site-specificity of protein S-nitrosylation. Front. Plant Sci. 2013;4:137. doi: 10.3389/fpls.2013.00137. PubMed DOI PMC
Begara-Morales J.C., Chaki M., Valderrama R., Mata-Pérez C., Padilla M.N., Barroso J.B. S-nitrosothiols function during abiotic stress in plants. J. Exp. Bot. 2019;70:4429–4439. doi: 10.1093/jxb/erz197. PubMed DOI
Umbreen S., Lubega J., Loake G.J. Sulphur: The heart of nitric oxide-dependent redox signalling. J. Exp. Bot. 2019;70:4279–4286. doi: 10.1093/jxb/erz135. PubMed DOI
Kolbert Z., Barroso J., Brouquisse R., Corpas F., Gupta K., Lindermayr C., Loake G., Palma J., Petřivalský M., Wendehenne D., et al. A forty year journey: The generation and roles of NO in plants. Nitric Oxide. 2019;93:53–70. doi: 10.1016/j.niox.2019.09.006. PubMed DOI
Gupta K.J., Kolbert Z., Durner J., Lindermayr C., Corpas F.J., Brouquisse R., Barroso J.B., Umbreen S., Palma J.M., Hancock J.T., et al. Regulating the regulator: Nitric oxide control of post-translational modifications. New Phytol. 2020;227:1319–1325. doi: 10.1111/nph.16622. PubMed DOI
Hess D.T., Stamler J.S. Regulation byS-Nitrosylation of Protein Post-translational Modification. J. Biol. Chem. 2011;287:4411–4418. doi: 10.1074/jbc.R111.285742. PubMed DOI PMC
Seth D., Stamler J.S. The SNO-proteome: Causation and classifications. Curr. Opin. Chem. Biol. 2011;15:129–136. doi: 10.1016/j.cbpa.2010.10.012. PubMed DOI PMC
Begara-Morales J.C., Chaki M., Valderrama R., Sánchez-Calvo B., Mata-Pérez C., Padilla M.N., Corpas F.J., Barroso J.B. Nitric oxide buffering and conditional nitric oxide release in stress response. J. Exp. Bot. 2018;69:3425–3438. doi: 10.1093/jxb/ery072. PubMed DOI
Corpas F.J., Palma J.M., Del Rio L.A., Barroso J.B. Evidence supporting the existence of l-arginine-dependent nitric oxide synthase activity in plants. New Phytol. 2009;184:9–14. doi: 10.1111/j.1469-8137.2009.02989.x. PubMed DOI
Corpas F.J., Palma J.M. Assessing Nitric Oxide (NO) in Higher Plants: An Outline. Nitrogen. 2018;1:12–20. doi: 10.3390/nitrogen1010003. DOI
Jeandroz S., Wipf D., Stuehr D.J., LaMattina L., Melkonian M., Tian Z., Zhu Y., Carpenter E.J., Wong G.K.-S., Wendehenne D. Occurrence, structure, and evolution of nitric oxide synthase–like proteins in the plant kingdom. Sci. Signal. 2016;9:re2. doi: 10.1126/scisignal.aad4403. PubMed DOI
Santolini J., André F., Jeandroz S., Wendehenne D. Nitric oxide synthase in plants: Where do we stand? Nitric Oxide. 2017;63:30–38. doi: 10.1016/j.niox.2016.09.005. PubMed DOI
Hill B.G., Dranka B.P., Bailey S.M., Lancaster J.R., Jr., Darley-Usmar V.M. What Part of NO Don’t You Understand? Some Answers to the Cardinal Questions in Nitric Oxide Biology. J. Biol. Chem. 2010;285:19699–19704. doi: 10.1074/jbc.R110.101618. PubMed DOI PMC
Heinrich T.A., Da Silva R.S., Miranda K.M., Switzer C.H., Wink D.A., Fukuto J.M. Biological nitric oxide signalling: Chemistry and terminology. Br. J. Pharmacol. 2013;169:1417–1429. doi: 10.1111/bph.12217. PubMed DOI PMC
Elamotte O., Bertoldo J.B., Besson-Bard A., Erosnoblet C., Aimé S., Ehichami S., Terenzi H., Wendehenne D. Protein S-nitrosylation: Specificity and identification strategies in plants. Front. Chem. 2015;2:114. PubMed PMC
Gaston B. Nitric oxide and thiol groups. Biochim. Biophys. Acta. 1999;1411:323–333. doi: 10.1016/S0005-2728(99)00023-7. PubMed DOI
Handy D.E., Loscalzo J. Nitric Oxide and Posttranslational Modification of the Vascular Proteome. Arter. Thromb. Vasc. Biol. 2006;26:1207–1214. doi: 10.1161/01.ATV.0000217632.98717.a0. PubMed DOI
Kuruthukulangarakoola G.T., Lindermayr C. Regulation and Function of Protein S-Nitrosylation in Plant Stress. In: Sarwat M., Ahmad A., Abdin M., editors. Stress Signaling in Plants: Genomics and Proteomics Perspective. Volume 1 Springer; New York, NY, USA: 2013.
Mata-Pérez C., Spoel S.H. Thioredoxin-mediated redox signalling in plant immunity. Plant Sci. 2019;279:27–33. doi: 10.1016/j.plantsci.2018.05.001. PubMed DOI
Yun B.-W., Skelly M.J., Yin M., Yu M., Mun B., Lee S., Hussain A., Spoel S.H., Loake G.J. Nitric oxide and S -nitrosoglutathione function additively during plant immunity. New Phytol. 2016;211:516–526. doi: 10.1111/nph.13903. PubMed DOI
Martínez-Ruiz A. S-nitrosylation: A potential new paradigm in signal transduction. Cardiovasc. Res. 2004;62:43–52. doi: 10.1016/j.cardiores.2004.01.013. PubMed DOI
Corpas F.J., Alché J.D.D., Barroso-Albarracín J.B. Current overview of S-nitrosoglutathione (GSNO) in higher plants. Front. Plant Sci. 2013;4:126. doi: 10.3389/fpls.2013.00126. PubMed DOI PMC
Malik S.I., Hussain A., Yun B.-W., Spoel S.H., Loake G.J. GSNOR-mediated de-nitrosylation in the plant defence response. Plant Sci. 2011;181:540–544. doi: 10.1016/j.plantsci.2011.04.004. PubMed DOI
Broniowska K.A., Hogg N. The chemical biology of S-nitrosothiols. Antioxid Redox Signal. 2012;17:969–980. doi: 10.1089/ars.2012.4590. PubMed DOI PMC
Lancaster J.R., Jr. Protein cysteine thiol nitrosation: Maker or marker of reactive nitrogen species-induced nonerythroid cellular signaling? Nitric Oxide. 2008;19:68–72. doi: 10.1016/j.niox.2008.04.028. PubMed DOI
Li Q., Lancaster J.R. A Conspectus of Cellular Mechanisms of Nitrosothiol Formation from Nitric Oxide. Forum Immunopathol. Dis. Ther. 2012;3:183–191. doi: 10.1615/ForumImmunDisTher.2012006372. PubMed DOI PMC
Lancaster J.R. How are nitrosothiols formed de novo in vivo ? Arch. Biochem. Biophys. 2017;617:137–144. doi: 10.1016/j.abb.2016.10.015. PubMed DOI
Nakamura T., Lipton S.A. Emerging Role of Protein-Protein Transnitrosylation in Cell Signaling Pathways. Antioxid. Redox Signal. 2013;18:239–249. doi: 10.1089/ars.2012.4703. PubMed DOI PMC
Seth D., Hess D.T., Hausladen A., Wang L., Wang Y.-J., Stamler J.S. A Multiplex Enzymatic Machinery for Cellular Protein S-nitrosylation. Mol. Cell. 2018;69:451–464.e6. doi: 10.1016/j.molcel.2017.12.025. PubMed DOI PMC
Wolhuter K., Whitwell H.J., Switzer C.H., Burgoyne J.R., Timms J.F., Eaton P. Evidence against Stable Protein S-Nitrosylation as a Widespread Mechanism of Post-translational Regulation. Mol. Cell. 2018;69:438–450.e5. doi: 10.1016/j.molcel.2017.12.019. PubMed DOI PMC
Clementi E., Brown G.C., Feelisch M., Moncada S. Persistent inhibition of cell respiration by nitric oxide: Crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione. Proc. Natl. Acad. Sci. USA. 1998;95:7631–7636. doi: 10.1073/pnas.95.13.7631. PubMed DOI PMC
Benhar M., Forrester M.T., Stamler J.S. Protein denitrosylation: Enzymatic mechanisms and cellular functions. Nat. Rev. Mol. Cell Biol. 2009;10:721–732. doi: 10.1038/nrm2764. PubMed DOI
Paige J.S., Xu G., Stancevic B., Jaffrey S.R. Nitrosothiol Reactivity Profiling Identifies S-Nitrosylated Proteins with Unexpected Stability. Chem. Biol. 2008;15:1307–1316. doi: 10.1016/j.chembiol.2008.10.013. PubMed DOI PMC
Liu L., Hausladen A., Zeng M., Que L., Heitman J., Stamler J.S. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nat. Cell Biol. 2001;410:490–494. doi: 10.1038/35068596. PubMed DOI
Barnett S.D., Buxton I.L.O. The role of S-nitrosoglutathione reductase (GSNOR) in human disease and therapy. Crit. Rev. Biochem. Mol. Biol. 2017;52:340–354. doi: 10.1080/10409238.2017.1304353. PubMed DOI PMC
Jahnová J., Luhová L., Petrivalsky M. S-Nitrosoglutathione Reductase—The Master Regulator of Protein S-Nitrosation in Plant NO Signaling. Plants. 2019;8:48. doi: 10.3390/plants8020048. PubMed DOI PMC
Kubienová L., Kopečný D., Tylichová M., Briozzo P., Skopalová J., Šebela M., Navrátil M., Tâche R., Luhová L., Barroso J.B., et al. Structural and functional characterization of a plant S-nitrosoglutathione reductase from Solanum lycopersicum. Biochimie. 2013;95:889–902. doi: 10.1016/j.biochi.2012.12.009. PubMed DOI
Xu S., Guerra D., Lee U., Vierling E. S-nitrosoglutathione reductases are low-copy number, cysteine-rich proteins in plants that control multiple developmental and defense responses in Arabidopsis. Front. Plant Sci. 2013;4:430. doi: 10.3389/fpls.2013.00430. PubMed DOI PMC
Guerra D., Ballard K., Truebridge I., Vierling E. S-Nitrosation of Conserved Cysteines Modulates Activity and Stability ofS-Nitrosoglutathione Reductase (GSNOR) Biochemie. 2016;55:2452–2464. doi: 10.1021/acs.biochem.5b01373. PubMed DOI PMC
Kovacs I., Holzmeister C., Wirtz M., Geerlof A., Fröhlich T., Römling G., Kuruthukulangarakoola G.T., Linster E., Hell R., Arnold G.J., et al. ROS-Mediated Inhibition of S-nitrosoglutathione Reductase Contributes to the Activation of Anti-oxidative Mechanisms. Front. Plant Sci. 2016;7:1669. doi: 10.3389/fpls.2016.01669. PubMed DOI PMC
Tichá T., Lochman J., Činčalová L., Luhová L., Petřivalský M. Redox regulation of plant S-nitrosoglutathione reductase activity through post-translational modifications of cysteine residues. Biochem. Biophys. Res. Commun. 2017;494:27–33. doi: 10.1016/j.bbrc.2017.10.090. PubMed DOI
Tichá T., Činčalová L., Kopečný D., Sedlářová M., Kopečná M., Luhová L., Petřivalský M. Characterization of S-nitrosoglutathione reductase from Brassica and Lactuca spp. and its modulation during plant development. Nitric Oxide. 2017;68:68–76. doi: 10.1016/j.niox.2016.12.002. PubMed DOI
Leterrier M., Chaki M., Airaki M., Valderrama R., Palma J.M., Barroso J.B., Corpas F.J. Function of S-nitrosoglutathione reductase (GSNOR) in plant development and under biotic/abiotic stress. Plant Signal. Behav. 2011;6:789–793. doi: 10.4161/psb.6.6.15161. PubMed DOI PMC
Kubienová L., Tichá T., Jahnová J., Luhová L., Mieslerová B., Petřivalský M. Effect of abiotic stress stimuli on S-nitrosoglutathione reductase in plants. Planta. 2013;239:139–146. doi: 10.1007/s00425-013-1970-5. PubMed DOI
Lu J., Holmgren A. The thioredoxin antioxidant system. Free. Radic. Biol. Med. 2014;66:75–87. doi: 10.1016/j.freeradbiomed.2013.07.036. PubMed DOI
Rouhier N., Cerveau D., Couturier J., Reichheld J.-P., Rey P. Involvement of thiol-based mechanisms in plant development. Biochim. Biophys. Acta. 2015;1850:1479–1496. doi: 10.1016/j.bbagen.2015.01.023. PubMed DOI
Hondal R.J., Ruggles E.L. Differing views of the role of selenium in thioredoxin reductase. Amino Acids. 2011;41:73–89. doi: 10.1007/s00726-010-0494-6. PubMed DOI PMC
Nikitovic D., Holmgren A. S-Nitrosoglutathione Is Cleaved by the Thioredoxin System with Liberation of Glutathione and Redox Regulating Nitric Oxide. J. Biol. Chem. 1996;271:19180–19185. doi: 10.1074/jbc.271.32.19180. PubMed DOI
Benhar M., Forrester M.T., Hess U.T., Stamler J.S. Regulated Protein Denitrosylation by Cytosolic and Mitochondrial Thioredoxins. Science. 2008;320:1050–1054. doi: 10.1126/science.1158265. PubMed DOI PMC
Ben-Lulu S., Ziv T., Admon A., Weisman-Shomer P., Benhar M. A Substrate Trapping Approach Identifies Proteins Regulated by Reversible S-nitrosylation. Mol. Cell. Proteom. 2014;13:2573–2583. doi: 10.1074/mcp.M114.038166. PubMed DOI PMC
Stoyanovsky D.A., Tyurina Y.Y., Tyurin V.A., Anand D., Mandavia D.N., Gius D., Ivanova J., Pitt B., Billiar T.R., Kagan V.E. Thioredoxin and Lipoic Acid Catalyze the Denitrosation of Low Molecular Weight and ProteinS-Nitrosothiols. J. Am. Chem. Soc. 2005;127:15815–15823. doi: 10.1021/ja0529135. PubMed DOI
Sengupta R., Ryter S.W., Zuckerbraun B.S., Tzeng E., Billiar T.R., Stoyanovsky D.A. Thioredoxin Catalyzes the Denitrosation of Low-Molecular Mass and ProteinS-Nitrosothiols. Biochemistry. 2007;46:8472–8483. doi: 10.1021/bi700449x. PubMed DOI
Barglow K.T., Knutson C.G.F., Wishnok J.S., Tannenbaum S.R., Marletta M.A. Site-specific and redox-controlled S-nitrosation of thioredoxin. Proc. Natl. Acad. Sci. USA. 2011;108:E600–E606. doi: 10.1073/pnas.1110736108. PubMed DOI PMC
Sengupta R., Holmgren A. Thioredoxin and Thioredoxin Reductase in Relation to Reversible S-Nitrosylation. Antioxid. Redox Signal. 2013;18:259–269. doi: 10.1089/ars.2012.4716. PubMed DOI
Engelman R., Ziv T., Arnér E.S.J., Benhar M. Inhibitory nitrosylation of mammalian thioredoxin reductase 1: Molecular characterization and evidence for its functional role in cellular nitroso-redox imbalance. Free Radic. Biol. Med. 2016;97:375–385. doi: 10.1016/j.freeradbiomed.2016.06.032. PubMed DOI
Benhar M. Roles of mammalian glutathione peroxidase and thioredoxin reductase enzymes in the cellular response to nitrosative stress. Free Radic. Biol. Med. 2018;127:160–164. doi: 10.1016/j.freeradbiomed.2018.01.028. PubMed DOI
Espinosa B., Arnér E.S.J. Thioredoxin-related protein of 14 kDa as a modulator of redox signalling pathways. Br. J. Pharmacol. 2018;176:544–553. doi: 10.1111/bph.14479. PubMed DOI PMC
Meyer Y., Belin C., Delorme-Hinoux V., Reichheld J.-P., Riondet C. Thioredoxin and Glutaredoxin Systems in Plants: Molecular Mechanisms, Crosstalks, and Functional Significance. Antioxid. Redox Signal. 2012;17:1124–1160. doi: 10.1089/ars.2011.4327. PubMed DOI
Geigenberger P., Thormählen I., Daloso D.M., Fernie A.R. The Unprecedented Versatility of the Plant Thioredoxin System. Trends Plant Sci. 2017;22:249–262. doi: 10.1016/j.tplants.2016.12.008. PubMed DOI
Dos Santos C.V., Rey P. Plant thioredoxins are key actors in the oxidative stress response. Trends Plant Sci. 2006;11:329–334. doi: 10.1016/j.tplants.2006.05.005. PubMed DOI
Reichheld J.-P., Khafif M., Riondet C., Droux M., Bonnard G., Meyer Y. Inactivation of Thioredoxin Reductases Reveals a Complex Interplay between Thioredoxin and Glutathione Pathways in Arabidopsis Development. Plant Cell. 2007;19:1851–1865. doi: 10.1105/tpc.107.050849. PubMed DOI PMC
Cha J.-Y., Barman D.N., Kim M.G., Kim W.-Y. Stress defense mechanisms of NADPH-dependent thioredoxin reductases (NTRs) in plants. Plant Signal. Behav. 2015;10:e1017698. doi: 10.1080/15592324.2015.1017698. PubMed DOI PMC
Delorme-Hinoux V., Bangash S.A., Meyer A.J., Reichheld J.-P. Nuclear thiol redox systems in plants. Plant Sci. 2016;243:84–95. doi: 10.1016/j.plantsci.2015.12.002. PubMed DOI
Correa-Aragunde N., Foresi N., Delledonne M., LaMattina L. Auxin induces redox regulation of ascorbate peroxidase 1 activity by S-nitrosylation/denitrosylation balance resulting in changes of root growth pattern in Arabidopsis. J. Exp. Bot. 2013;64:3339–3349. doi: 10.1093/jxb/ert172. PubMed DOI
Berger H., De Mia M., Morisse S., Marchand C.H., Lemaire S.D., Wobbe L., Kruse O. A Light Switch Based on Protein S-Nitrosylation Fine-Tunes Photosynthetic Light Harvesting in Chlamydomonas1. Plant Physiol. 2016;171:821–832. PubMed PMC
Tada Y., Spoel S.H., Pajerowska-Mukhtar K., Mou Z., Song J., Wang C., Zuo J., Dong X. Plant Immunity Requires Conformational Charges of NPR1 via S-Nitrosylation and Thioredoxins. Science. 2008;321:952–956. doi: 10.1126/science.1156970. PubMed DOI PMC
Kneeshaw S., Gelineau S., Tada Y., Loake G.J., Spoel S.H. Selective Protein Denitrosylation Activity of Thioredoxin-h5 Modulates Plant Immunity. Mol. Cell. 2014;56:153–162. doi: 10.1016/j.molcel.2014.08.003. PubMed DOI
Bashandy T., Guilleminot J., Vernoux T., Caparros-Ruiz D., Ljung K., Meyer Y., Reichheld J.-P. Interplay between the NADP-Linked Thioredoxin and Glutathione Systems in Arabidopsis Auxin Signaling. Plant Cell. 2010;22:376–391. doi: 10.1105/tpc.109.071225. PubMed DOI PMC
Correa-Aragunde N., Cejudo F.J., LaMattina L. Nitric oxide is required for the auxin-induced activation of NADPH-dependent thioredoxin reductase and protein denitrosylation during root growth responses in arabidopsis. Ann. Bot. 2015;116:695–702. doi: 10.1093/aob/mcv116. PubMed DOI PMC
Ghanta S., Bhattacharyya D., Sinha R., Banerjee A., Chattopadhyay S. Nicotiana tabacum overexpressing γ-ECS exhibits biotic stress tolerance likely through NPR1-dependent salicylic acid-mediated pathway. Planta. 2011;233:895–910. doi: 10.1007/s00425-011-1349-4. PubMed DOI
Zaffagnini M., Morisse S., Bedhomme M., Marchand C.H., Festa M., Rouhier N., Lemaire S.D., Trost P. Mechanisms of Nitrosylation and Denitrosylation of Cytoplasmic Glyceraldehyde-3-phosphate Dehydrogenase fromArabidopsis thaliana. J. Biol. Chem. 2013;288:22777–22789. doi: 10.1074/jbc.M113.475467. PubMed DOI PMC
Zhao Y., He M., Ding J., Xi Q., Loake G.J., Zheng W. Regulation of Anticancer Styrylpyrone Biosynthesis in the Medicinal Mushroom Inonotus obliquus Requires Thioredoxin Mediated Transnitrosylation of S-nitrosoglutathione Reductase. Sci. Rep. 2016;6:37601. doi: 10.1038/srep37601. PubMed DOI PMC
Liebthal M., Maynard D., Dietz K.-J. Peroxiredoxins and Redox Signaling in Plants. Antioxid. Redox Signal. 2018;28:609–624. doi: 10.1089/ars.2017.7164. PubMed DOI PMC
Dietz K.-J. Peroxiredoxins in Plants and Cyanobacteria. Antioxid. Redox Signal. 2011;15:1129–1159. doi: 10.1089/ars.2010.3657. PubMed DOI PMC
Sakamoto A., Tsukamoto S., Yamamoto H., Ueda-Hashimoto M., Takahashi M., Suzuki H., Morikawa H. Functional complementation in yeast reveals a protective role of chloroplast 2-Cys peroxiredoxin against reactive nitrogen species. Plant J. 2003;33:841–851. doi: 10.1046/j.1365-313X.2003.01669.x. PubMed DOI
Lindermayr C., Saalbach G., Durner J. Proteomic Identification of S-Nitrosylated Proteins in Arabidopsis. Plant Physiol. 2005;137:921–930. doi: 10.1104/pp.104.058719. PubMed DOI PMC
Romero-Puertas M.C., Laxa M., Mattè A., Zaninotto F., Finkemeier I., Jones A.M., Perazzolli M., Vandelle E., Dietz K.-J., Delledonne M. S-Nitrosylation of Peroxiredoxin II E Promotes Peroxynitrite-Mediated Tyrosine Nitration. Plant Cell. 2007;19:4120–4130. doi: 10.1105/tpc.107.055061. PubMed DOI PMC
Engelman R., Weisman-Shomer P., Ziv T., Xu J., Arnér E.S.J., Benhar M. Multilevel Regulation of 2-Cys Peroxiredoxin Reaction Cycle byS-Nitrosylation. J. Biol. Chem. 2013;288:11312–11324. doi: 10.1074/jbc.M112.433755. PubMed DOI PMC
Biteau B., Labarre J., Toledano M.B. ATP-dependent reduction of cysteine–sulphinic acid by S. cerevisiae sulphiredoxin. Nat. Cell Biol. 2003;425:980–984. doi: 10.1038/nature02075. PubMed DOI
Sunico C.R., Sultan A., Nakamura T., Dolatabadi N., Parker J., Shan B., Han X., Yates J.R., Masliah E., Ambasudhan R., et al. Role of sulfiredoxin as a peroxiredoxin-2 denitrosylase in human iPSC-derived dopaminergic neurons. Proc. Natl. Acad. Sci. USA. 2016;113:E7564–E7571. doi: 10.1073/pnas.1608784113. PubMed DOI PMC
Rey P., Bécuwe N., Barrault M.-B., Rumeau D., Havaux M., Biteau B., Toledano M.B. The Arabidopsis thaliana sulfiredoxin is a plastidic cysteine-sulfinic acid reductase involved in the photooxidative stress response. Plant J. 2007;49:505–514. doi: 10.1111/j.1365-313X.2006.02969.x. PubMed DOI
Sevilla F., Camejo D., Ortiz-Espín A., Calderón A., Lázaro J.J., Jiménez A. The thioredoxin/peroxiredoxin/sulfiredoxin system: Current overview on its redox function in plants and regulation by reactive oxygen and nitrogen species. J. Exp. Bot. 2015;66:2945–2955. doi: 10.1093/jxb/erv146. PubMed DOI
Root P., Sliskovic I., Mutus B. Platelet cell-surface protein disulphide-isomerase mediated S-nitrosoglutathione consumption. Biochem. J. 2004;382:575–580. doi: 10.1042/BJ20040759. PubMed DOI PMC
Sliskovic I., Raturi A., Mutus B. Characterization of the S-Denitrosation Activity of Protein Disulfide Isomerase. J. Biol. Chem. 2004;280:8733–8741. doi: 10.1074/jbc.M408080200. PubMed DOI
Houston N.L., Fan C., Xiang J.Q., Schulze J.-M., Jung R., Boston R.S. Phylogenetic Analyses Identify 10 Classes of the Protein Disulfide Isomerase Family in Plants, Including Single-Domain Protein Disulfide Isomerase-Related Proteins. Plant Physiol. 2005;137:762–778. doi: 10.1104/pp.104.056507. PubMed DOI PMC
Zhang Z., Liu X., Li R., Yuan L., Dai Y., Wang X. Identification and Functional Analysis of a Protein Disulfide Isomerase (AtPDI1) in Arabidopsis thaliana. Front. Plant Sci. 2018;9:913. doi: 10.3389/fpls.2018.00913. PubMed DOI PMC
Jourd’Heuila D., Larouxa F.S., Miles A.M., Wink D.A., Grisham M.B. Effect of Superoxide Dismutase on the Stability ofS-Nitrosothiols. Arch. Biochem. Biophys. 1999;361:323–330. doi: 10.1006/abbi.1998.1010. PubMed DOI
Johnson M.A., Macdonald T.L., Mannick J.B., Conaway M.R., Gaston B. AcceleratedS-Nitrosothiol Breakdown by Amyotrophic Lateral Sclerosis Mutant Copper,Zinc-Superoxide Dismutase. J. Biol. Chem. 2001;276:39872–39878. doi: 10.1074/jbc.M102781200. PubMed DOI
Schonhoff C.M., Matsuoka M., Tummala H., Johnson M.A., Estevéz A.G., Wu R., Kamaid A., Ricart K.C., Hashimoto Y., Gaston B., et al. S-nitrosothiol depletion in amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. USA. 2006;103:2404–2409. doi: 10.1073/pnas.0507243103. PubMed DOI PMC
Tsang C.K., Liu Y., Thomas J., Zhang Y., Zheng X.F.S. Superoxide dismutase 1 acts as a nuclear transcription factor to regulate oxidative stress resistance. Nat. Commun. 2014;5:3446. doi: 10.1038/ncomms4446. PubMed DOI PMC
Emengel A., Echaki M., Eshekariesfahlan A., Lindermayr C. Effect of nitric oxide on gene transcription—S-nitrosylation of nuclear proteins. Front. Plant Sci. 2013;4:293. PubMed PMC
Spyrou G., Enmark E., Miranda-Vizuete A., Gustafsson J. Cloning and Expression of a Novel Mammalian Thioredoxin. J. Biol. Chem. 1997;272:2936–2941. doi: 10.1074/jbc.272.5.2936. PubMed DOI
Kneeshaw S., Spoel S.H. Thioredoxin-Dependent Decomposition of Protein S-Nitrosothiols. In: Mengel A., Lindermayr C., editors. Nitric Oxide. Methods in Molecular Biology. Volume 1747 Humana Press; New York, NY, USA: 2018. PubMed
Borrelli V.M.G., Brambilla V., Rogowsky P., Marocco A., Lanubile A. The Enhancement of Plant Disease Resistance Using CRISPR/Cas9 Technology. Front. Plant Sci. 2018;9:1245. doi: 10.3389/fpls.2018.01245. PubMed DOI PMC