Mass Spectrometry-Based Quantitative Cysteine Redox Proteome Profiling of Isolated Mitochondria Using Differential iodoTMT Labeling.
Cysteine
Iodoacetyl Tandem Mass Tag
Isobaric labeling
LC-MS/MS
MaxQuant
Mitochondria
Redox
Thiols
Journal
Methods in molecular biology (Clifton, N.J.)
ISSN: 1940-6029
Titre abrégé: Methods Mol Biol
Pays: United States
ID NLM: 9214969
Informations de publication
Date de publication:
2022
2022
Historique:
entrez:
21
9
2021
pubmed:
22
9
2021
medline:
11
1
2022
Statut:
ppublish
Résumé
Mitochondria are central hubs of redox biochemistry in the cell. An important role of mitochondrial carbon metabolism is to oxidize respiratory substrates and to pass the electrons down the mitochondrial electron transport chain to reduce oxygen and to drive oxidative phosphorylation. During respiration, reactive oxygen species are produced as a side reaction, some of which in turn oxidize cysteine thiols in proteins. Hence, the redox status of cysteine-containing mitochondrial proteins has to be controlled by the mitochondrial glutathione and thioredoxin systems, which draw electrons from metabolically derived NADPH. The redox status of mitochondrial cysteines can undergo fast transitions depending on the metabolic status of the cell, as for instance at early seed germination. Here, we describe a state-of-the-art method to quantify redox state of protein cysteines in isolated Arabidopsis seedling mitochondria of controlled metabolic and respiratory state by MS
Identifiants
pubmed: 34545496
doi: 10.1007/978-1-0716-1653-6_16
doi:
Substances chimiques
Proteome
0
Cysteine
K848JZ4886
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
215-234Informations de copyright
© 2022. Springer Science+Business Media, LLC, part of Springer Nature.
Références
Day DA, Millar AH, Whelan J (2004) Plant mitochondria: from genome to function. Springer Netherlands, Dordrecht
doi: 10.1007/978-1-4020-2400-9
Muller M, Mentel M, van Hellemond JJ et al (2012) Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76:444–495. https://doi.org/10.1128/MMBR.05024-11
doi: 10.1128/MMBR.05024-11
pubmed: 22688819
pmcid: 3372258
Sweetlove LJ, Beard KFM, Nunes-Nesi A et al (2010) Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci 15:462–470. https://doi.org/10.1016/j.tplants.2010.05.006
doi: 10.1016/j.tplants.2010.05.006
pubmed: 20554469
Friso G, van Wijk KJ (2015) Posttranslational protein modifications in plant metabolism. Plant Physiol 169:1469–1487. https://doi.org/10.1104/pp.15.01378
doi: 10.1104/pp.15.01378
pubmed: 26338952
pmcid: 4634103
Møller IM, Igamberdiev AU, Bykova NV et al (2020) Matrix redox physiology governs the regulation of plant mitochondrial metabolism through posttranslational protein modifications. Plant Cell 32:573–594. https://doi.org/10.1105/tpc.19.00535
doi: 10.1105/tpc.19.00535
pubmed: 31911454
pmcid: 7054041
Millar AH, Sweetlove LJ, Giegé P, Leaver CJ (2001) Analysis of the Arabidopsis mitochondrial proteome. Plant Physiol 127:1711–1727. https://doi.org/10.1104/pp.010387
doi: 10.1104/pp.010387
pubmed: 11743115
pmcid: 133575
Sweetlove LJ, Heazlewood JL, Herald V et al (2002) The impact of oxidative stress on Arabidopsis mitochondria. Plant J 32:891–904. https://doi.org/10.1046/j.1365-313X.2002.01474.x
doi: 10.1046/j.1365-313X.2002.01474.x
pubmed: 12492832
Heazlewood JL, Howell KA, Whelan J, Millar AH (2003) Towards an analysis of the rice mitochondrial proteome. Plant Physiol 132:230–242. https://doi.org/10.1104/pp.102.018986
doi: 10.1104/pp.102.018986
pubmed: 12746528
pmcid: 166968
Braun H-P, Millar AH (2004) Proteome analyses for characterization of plant mitochondria. In: Day DA, Millar AH, Whelan J (eds) Plant mitochondria: from genome to function. Springer Netherlands, Dordrecht, pp 143–162
doi: 10.1007/978-1-4020-2400-9_8
Salvato F, Havelund JF, Chen M et al (2014) The potato tuber mitochondrial proteome. Plant Physiol 164:637–653. https://doi.org/10.1104/pp.113.229054
doi: 10.1104/pp.113.229054
pubmed: 24351685
Senkler J, Senkler M, Eubel H et al (2017) The mitochondrial complexome of Arabidopsis thaliana. Plant J 89:1079–1092. https://doi.org/10.1111/tpj.13448
doi: 10.1111/tpj.13448
pubmed: 27943495
Fuchs P, Rugen N, Carrie C et al (2020) Single organelle function and organization as estimated from Arabidopsis mitochondrial proteomics. Plant J 101:420–441. https://doi.org/10.1111/tpj.14534
doi: 10.1111/tpj.14534
pubmed: 31520498
Huang S, Li L, Petereit J, Millar AH (2020) Protein turnover rates in plant mitochondria. Mitochondrion 53:57–65. https://doi.org/10.1016/j.mito.2020.04.011
doi: 10.1016/j.mito.2020.04.011
pubmed: 32387507
Rubin PM, Randall DD (1977) Regulation of plant pyruvate dehydrogenase complex by phosphorylation. Plant Physiol 60:34–39. https://doi.org/10.1104/pp.60.1.34
doi: 10.1104/pp.60.1.34
pubmed: 16660037
pmcid: 542541
König A-C, Hartl M, Boersema PJ et al (2014) The mitochondrial lysine acetylome of Arabidopsis. Mitochondrion 19:252–260. https://doi.org/10.1016/j.mito.2014.03.004
doi: 10.1016/j.mito.2014.03.004
pubmed: 24727099
König A-C, Hartl M, Pham PA et al (2014) The Arabidopsis class II sirtuin is a lysine deacetylase and interacts with mitochondrial energy metabolism. Plant Physiol 164:1401–1414. https://doi.org/10.1104/pp.113.232496
doi: 10.1104/pp.113.232496
pubmed: 24424322
pmcid: 3938629
Smakowska E, Blaszczyk RS, Czarna M et al (2016) Lack of FTSH4 protease affects protein carbonylation, mitochondrial morphology and phospholipid content in mitochondria of Arabidopsis: new insights into a complex interplay. Plant Physiol 171(4):2516–2535. https://doi.org/10.1104/pp.16.00370
Havelund JF, Thelen JJ, Møller IM (2013) Biochemistry, proteomics, and phosphoproteomics of plant mitochondria from non-photosynthetic cells. Front Plant Sci 4:51. https://doi.org/10.3389/fpls.2013.00051
doi: 10.3389/fpls.2013.00051
pubmed: 23494127
pmcid: 3595712
Daloso DM, Müller K, Obata T et al (2015) Thioredoxin, a master regulator of the tricarboxylic acid cycle in plant mitochondria. Proc Natl Acad Sci U S A 112:E1392–E1400. https://doi.org/10.1073/pnas.1424840112
doi: 10.1073/pnas.1424840112
pubmed: 25646482
pmcid: 4371975
Miseta A, Csutora P (2000) Relationship between the occurrence of cysteine in proteins and the complexity of organisms. Mol Biol Evol 17:1232–1239. https://doi.org/10.1093/oxfordjournals.molbev.a026406
doi: 10.1093/oxfordjournals.molbev.a026406
pubmed: 10908643
Marino SM, Gladyshev VN (2010) Cysteine function governs its conservation and degeneration and restricts its utilization on protein surfaces. J Mol Biol 404:902–916. https://doi.org/10.1016/j.jmb.2010.09.027
doi: 10.1016/j.jmb.2010.09.027
pubmed: 20950627
pmcid: 3061813
Paulsen CE, Carroll KS (2013) Cysteine-mediated redox signaling: chemistry, biology, and tools for discovery. Chem Rev 113:4633–4679. https://doi.org/10.1021/cr300163e
doi: 10.1021/cr300163e
pubmed: 23514336
pmcid: 4303468
Poole LB (2015) The basics of thiols and cysteines in redox biology and chemistry. Free Radic Biol Med 80:148–157. https://doi.org/10.1016/j.freeradbiomed.2014.11.013
doi: 10.1016/j.freeradbiomed.2014.11.013
pubmed: 25433365
Handy DE, Loscalzo J (2012) Redox regulation of mitochondrial function. Antioxid Redox Signal 16:1323–1367. https://doi.org/10.1089/ars.2011.4123
doi: 10.1089/ars.2011.4123
pubmed: 22146081
pmcid: 3324814
Li LZ (2012) Imaging mitochondrial redox potential and its possible link to tumor metastatic potential. J Bioenerg Biomembr 44:645–653. https://doi.org/10.1007/s10863-012-9469-5
doi: 10.1007/s10863-012-9469-5
pubmed: 22895837
pmcid: 3508148
Requejo R, Hurd TR, Costa NJ, Murphy MP (2010) Cysteine residues exposed on protein surfaces are the dominant intramitochondrial thiol and may protect against oxidative damage: protein thiols. FEBS J 277:1465–1480. https://doi.org/10.1111/j.1742-4658.2010.07576.x
doi: 10.1111/j.1742-4658.2010.07576.x
pubmed: 20148960
pmcid: 2847196
Mailloux RJ (2019) Cysteine switches and the regulation of mitochondrial bioenergetics and ROS production. In: Urbani A, Babu M (eds) Mitochondria in health and in sickness. Springer Singapore, Singapore, pp 197–216
doi: 10.1007/978-981-13-8367-0_11
Bak DW, Pizzagalli MD, Weerapana E (2017) Identifying functional cysteine residues in the mitochondria. ACS Chem Biol 12:947–957. https://doi.org/10.1021/acschembio.6b01074
doi: 10.1021/acschembio.6b01074
pubmed: 28157297
pmcid: 5400717
Nietzel T, Mostertz J, Hochgräfe F, Schwarzländer M (2017) Redox regulation of mitochondrial proteins and proteomes by cysteine thiol switches. Mitochondrion 33:72–83. https://doi.org/10.1016/j.mito.2016.07.010
doi: 10.1016/j.mito.2016.07.010
pubmed: 27456428
Schwarzländer M, Finkemeier I (2013) Mitochondrial energy and redox signaling in plants. Antioxid Redox Signal 18:2122–2144. https://doi.org/10.1089/ars.2012.5104
doi: 10.1089/ars.2012.5104
pubmed: 23234467
pmcid: 3698670
García-Santamarina S, Boronat S, Hidalgo E (2014) Reversible cysteine oxidation in hydrogen peroxide sensing and signal transduction. Biochemistry 53:2560–2580. https://doi.org/10.1021/bi401700f
doi: 10.1021/bi401700f
pubmed: 24738931
García-Santamarina S, Boronat S, Domènech A et al (2014) Monitoring in vivo reversible cysteine oxidation in proteins using ICAT and mass spectrometry. Nat Protoc 9:1131–1145. https://doi.org/10.1038/nprot.2014.065
doi: 10.1038/nprot.2014.065
pubmed: 24743420
Iglesias-Baena I, Barranco-Medina S, Sevilla F, Lázaro J-J (2011) The dual-targeted plant sulfiredoxin retroreduces the sulfinic form of atypical mitochondrial peroxiredoxin. Plant Physiol 155:944–955. https://doi.org/10.1104/pp.110.166504
doi: 10.1104/pp.110.166504
pubmed: 21139087
Iglesias-Baena I, Barranco-Medina S, Lázaro-Payo A et al (2010) Characterization of plant sulfiredoxin and role of sulphinic form of 2-Cys peroxiredoxin. J Exp Bot 61:1509–1521. https://doi.org/10.1093/jxb/erq016
doi: 10.1093/jxb/erq016
pubmed: 20176891
pmcid: 2837264
Lamotte O, Bertoldo JB, Besson-Bard A et al (2015) Protein S-nitrosylation: specificity and identification strategies in plants. Front Chem 2:114. https://doi.org/10.3389/fchem.2014.00114
doi: 10.3389/fchem.2014.00114
pubmed: 25750911
pmcid: 4285867
Menger KE, James AM, Cochemé HM et al (2015) Fasting, but not aging, dramatically alters the redox status of cysteine residues on proteins in Drosophila melanogaster. Cell Rep 11:1856–1865. https://doi.org/10.1016/j.celrep.2015.05.033
doi: 10.1016/j.celrep.2015.05.033
pubmed: 26095360
pmcid: 4508341
Leichert LI, Gehrke F, Gudiseva HV et al (2008) Quantifying changes in the thiol redox proteome upon oxidative stress in vivo. Proc Natl Acad Sci U S A 105:8197–8202. https://doi.org/10.1073/pnas.0707723105
doi: 10.1073/pnas.0707723105
pubmed: 18287020
pmcid: 2448814
Waszczak C, Akter S, Eeckhout D et al (2014) Sulfenome mining in Arabidopsis thaliana. Proc Natl Acad Sci U S A 111:11545–11550. https://doi.org/10.1073/pnas.1411607111
doi: 10.1073/pnas.1411607111
pubmed: 25049418
pmcid: 4128149
Huang J, Willems P, Wei B et al (2019) Mining for protein S-sulfenylation in Arabidopsis uncovers redox-sensitive sites. Proc Natl Acad Sci U S A 116:21256–21261. https://doi.org/10.1073/pnas.1906768116
doi: 10.1073/pnas.1906768116
pubmed: 31578252
pmcid: 6800386
Yang J, Carroll KS, Liebler DC (2016) The expanding landscape of the thiol redox proteome. Mol Cell Proteomics 15:1–11. https://doi.org/10.1074/mcp.O115.056051
doi: 10.1074/mcp.O115.056051
pubmed: 26518762
Xie K, Bunse C, Marcus K, Leichert LI (2019) Quantifying changes in the bacterial thiol redox proteome during host-pathogen interaction. Redox Biol 21:101087. https://doi.org/10.1016/j.redox.2018.101087
doi: 10.1016/j.redox.2018.101087
pubmed: 30682706
McConnell EW, Berg P, Westlake TJ et al (2019) Proteome-wide analysis of cysteine reactivity during effector-triggered immunity. Plant Physiol 179:1248–1264. https://doi.org/10.1104/pp.18.01194
doi: 10.1104/pp.18.01194
pubmed: 30510037
Hurd TR, Prime TA, Harbour ME et al (2007) Detection of reactive oxygen species-sensitive thiol proteins by redox difference gel electrophoresis: implications for mitochondrial redox signaling. J Biol Chem 282:22040–22051. https://doi.org/10.1074/jbc.M703591200
doi: 10.1074/jbc.M703591200
pubmed: 17525152
Murray CI, Uhrigshardt H, O’Meally RN et al (2012) Identification and quantification of S-nitrosylation by cysteine reactive tandem mass tag switch assay. Mol Cell Proteomics 11:M111.013441. https://doi.org/10.1074/mcp.M111.013441
doi: 10.1074/mcp.M111.013441
pubmed: 22126794
Qu Z, Meng F, Bomgarden RD et al (2014) Proteomic quantification and site-mapping of S-nitrosylated proteins using isobaric iodoTMT reagents. J Proteome Res 13:3200–3211. https://doi.org/10.1021/pr401179v
doi: 10.1021/pr401179v
pubmed: 24926564
pmcid: 4084841
Thompson A, Schäfer J, Kuhn K et al (2003) Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal Chem 75:1895–1904. https://doi.org/10.1021/ac0262560
doi: 10.1021/ac0262560
pubmed: 12713048
Nietzel T, Mostertz J, Ruberti C et al (2020) Redox-mediated kick-start of mitochondrial energy metabolism drives resource-efficient seed germination. Proc Natl Acad Sci U S A 117:741–751. https://doi.org/10.1073/pnas.1910501117
doi: 10.1073/pnas.1910501117
pubmed: 31871212
Schwacke R, Ponce-Soto GY, Krause K et al (2019) MapMan4: a refined protein classification and annotation framework applicable to multi-omics data analysis. Mol Plant 12:879–892. https://doi.org/10.1016/j.molp.2019.01.003
doi: 10.1016/j.molp.2019.01.003
pubmed: 30639314
Tyanova S, Temu T, Cox J (2016) The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nat Protoc 11:2301–2319. https://doi.org/10.1038/nprot.2016.136
doi: 10.1038/nprot.2016.136
pubmed: 27809316
Tyanova S, Temu T, Sinitcyn P et al (2016) The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat Methods 13:731–740. https://doi.org/10.1038/nmeth.3901
doi: 10.1038/nmeth.3901
pubmed: 27348712