The conformational bases for the two functionalities of 2-cysteine peroxiredoxins as peroxidase and chaperone

König J, Galliardt H, Jütte P, Schäper S, Dittmann L, Dietz K-J (2013)
Journal of experimental botany 64(11): 3483-3497.

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Abstract / Bemerkung
2-Cysteine peroxiredoxins (2-CysPrxs) are ubiquitous and highly abundant proteins that serve multiple functions as peroxidases, chaperones, and thiol oxidases and in redox-dependent cell signalling. The chloroplast protein plays a role in seedling development and protection of the photosynthetic apparatus. This study aimed to unequivocally link conformation and function. To this end, a set of non-tagged site-directed mutagenized At2-CysPrx variants was engineered, which mimicked the conformational states and their specific functions: hyperoxidized form (C54D), reduced form (C54S, C176S), oxidized form (C54DC176K), phosphorylated form (T92D), reduced ability for oligomerization by interfering with the dimer-dimer interface (F84R) and a C-terminally truncated form [ΔC (-20 aa)]. These variants were fully or partly fixed in their quaternary structure and function, respectively, and were analysed for their conformational state and peroxidase and chaperone activity, as well as for their sensitivity to hyperoxidation. The presence of a His6-tag strongly influenced the properties of the protein. The ΔC variant became insensitive to hyperoxidation, while T92D and F84R became more sensitive. The C54D variant revealed the highest chaperone activity. The highest peroxidase activity was observed for the F84R and ΔC variants. Efficient interaction with NADP-dependent thioredoxin reductase C depended on the presence of Cys residues and the C-terminal tail. The results suggest that the structural flexibility is important for the switch between peroxidase and chaperone function and that evolution has conserved the functional switch instead of maximizing a single function. These variants are ideal tools for future conformation-specific studies in vivo and in vitro.
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Journal of experimental botany
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64
Zeitschriftennummer
11
Seite
3483-3497
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eISSN
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König J, Galliardt H, Jütte P, Schäper S, Dittmann L, Dietz K-J. The conformational bases for the two functionalities of 2-cysteine peroxiredoxins as peroxidase and chaperone. Journal of experimental botany. 2013;64(11):3483-3497.
König, J., Galliardt, H., Jütte, P., Schäper, S., Dittmann, L., & Dietz, K. - J. (2013). The conformational bases for the two functionalities of 2-cysteine peroxiredoxins as peroxidase and chaperone. Journal of experimental botany, 64(11), 3483-3497. doi:10.1093/jxb/ert184
König, J., Galliardt, H., Jütte, P., Schäper, S., Dittmann, L., and Dietz, K. - J. (2013). The conformational bases for the two functionalities of 2-cysteine peroxiredoxins as peroxidase and chaperone. Journal of experimental botany 64, 3483-3497.
König, J., et al., 2013. The conformational bases for the two functionalities of 2-cysteine peroxiredoxins as peroxidase and chaperone. Journal of experimental botany, 64(11), p 3483-3497.
J. König, et al., “The conformational bases for the two functionalities of 2-cysteine peroxiredoxins as peroxidase and chaperone”, Journal of experimental botany, vol. 64, 2013, pp. 3483-3497.
König, J., Galliardt, H., Jütte, P., Schäper, S., Dittmann, L., Dietz, K.-J.: The conformational bases for the two functionalities of 2-cysteine peroxiredoxins as peroxidase and chaperone. Journal of experimental botany. 64, 3483-3497 (2013).
König, Janine, Galliardt, Helena, Jütte, Patrick, Schäper, Simon, Dittmann, Lea, and Dietz, Karl-Josef. “The conformational bases for the two functionalities of 2-cysteine peroxiredoxins as peroxidase and chaperone”. Journal of experimental botany 64.11 (2013): 3483-3497.

42 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Experimentally Dissecting the Origins of Peroxiredoxin Catalysis.
Nelson KJ, Perkins A, Van Swearingen AED, Hartman S, Brereton AE, Parsonage D, Salsbury FR, Karplus PA, Poole LB., Antioxid Redox Signal 28(7), 2018
PMID: 28375740
Peroxiredoxins and Redox Signaling in Plants.
Liebthal M, Maynard D, Dietz KJ., Antioxid Redox Signal 28(7), 2018
PMID: 28594234
Hyperoxidation of Peroxiredoxins: Gain or Loss of Function?
Veal EA, Underwood ZE, Tomalin LE, Morgan BA, Pillay CS., Antioxid Redox Signal 28(7), 2018
PMID: 28762774
Suppression of External NADPH Dehydrogenase-NDB1 in Arabidopsis thaliana Confers Improved Tolerance to Ammonium Toxicity via Efficient Glutathione/Redox Metabolism.
Podgórska A, Ostaszewska-Bugajska M, Borysiuk K, Tarnowska A, Jakubiak M, Burian M, Rasmusson AG, Szal B., Int J Mol Sci 19(5), 2018
PMID: 29747392
Protein Promiscuity in H2O2 Signaling.
Young D, Pedre B, Ezeriņa D, De Smet B, Lewandowska A, Tossounian MA, Bodra N, Huang J, Astolfi Rosado L, Van Breusegem F, Messens J., Antioxid Redox Signal (), 2018
PMID: 29635930
Functional switching of ascorbate peroxidase 2 of rice (OsAPX2) between peroxidase and molecular chaperone.
Hong SH, Tripathi BN, Chung MS, Cho C, Lee S, Kim JH, Bai HW, Bae HJ, Cho JY, Chung BY, Lee SS., Sci Rep 8(1), 2018
PMID: 29907832
Crystal structure of Arabidopsis thaliana peroxiredoxin A C119S mutant.
Yang Y, Cai W, Wang J, Pan W, Liu L, Wang M, Zhang M., Acta Crystallogr F Struct Biol Commun 74(pt 10), 2018
PMID: 30279313
The chloroplast 2-cysteine peroxiredoxin functions as thioredoxin oxidase in redox regulation of chloroplast metabolism.
Vaseghi MJ, Chibani K, Telman W, Liebthal MF, Gerken M, Schnitzer H, Mueller SM, Dietz KJ., Elife 7(), 2018
PMID: 30311601
Site-specific mutagenesis of yeast 2-Cys peroxiredoxin improves heat or oxidative stress tolerance by enhancing its chaperone or peroxidase function.
Hong SH, Lee SS, Chung JM, Jung HS, Singh S, Mondal S, Jang HH, Cho JY, Bae HJ, Chung BY., Protoplasma 254(1), 2017
PMID: 26843371
Surveying the Oligomeric State of Arabidopsis thaliana Chloroplasts.
Lundquist PK, Mantegazza O, Stefanski A, Stühler K, Weber APM., Mol Plant 10(1), 2017
PMID: 27794502
Evolution and function of the Mycoplasma hyopneumoniae peroxiredoxin, a 2-Cys-like enzyme with a single Cys residue.
Gonchoroski T, Virginio VG, Thompson CE, Paes JA, Machado CX, Ferreira HB., Mol Genet Genomics 292(2), 2017
PMID: 27858147
Multiple Functions and Regulation of Mammalian Peroxiredoxins.
Rhee SG, Kil IS., Annu Rev Biochem 86(), 2017
PMID: 28226215
Peroxiredoxin 6 from the Antarctic emerald rockcod: molecular characterization of its response to warming.
Tolomeo AM, Carraro A, Bakiu R, Toppo S, Place SP, Ferro D, Santovito G., J Comp Physiol B 186(1), 2016
PMID: 26433650
Functional analysis of recombinant 2-Cys peroxiredoxin from the hard tick Haemaphysalis longicornis.
Kusakisako K, Masatani T, Miyata T, Galay RL, Maeda H, Talactac MR, Tsuji N, Mochizuki M, Fujisaki K, Tanaka T., Insect Mol Biol 25(1), 2016
PMID: 26471013
Physiological relevance of plant 2-Cys peroxiredoxin overoxidation level and oligomerization status.
Cerveau D, Ouahrani D, Marok MA, Blanchard L, Rey P., Plant Cell Environ 39(1), 2016
PMID: 26138759
Kinetic analysis of structural influences on the susceptibility of peroxiredoxins 2 and 3 to hyperoxidation.
Poynton RA, Peskin AV, Haynes AC, Lowther WT, Hampton MB, Winterbourn CC., Biochem J 473(4), 2016
PMID: 26614766
Plant protein 2-Cys peroxiredoxin TaBAS1 alleviates oxidative and nitrosative stresses incurred during cryopreservation of mammalian cells.
Chow-Shi-Yée M, Grondin M, Averill-Bates DA, Ouellet F., Biotechnol Bioeng 113(7), 2016
PMID: 26724792
Roles of peroxiredoxins in cancer, neurodegenerative diseases and inflammatory diseases.
Park MH, Jo M, Kim YR, Lee CK, Hong JT., Pharmacol Ther 163(), 2016
PMID: 27130805
Structures of Human Peroxiredoxin 3 Suggest Self-Chaperoning Assembly that Maintains Catalytic State.
Yewdall NA, Venugopal H, Desfosses A, Abrishami V, Yosaatmadja Y, Hampton MB, Gerrard JA, Goldstone DC, Mitra AK, Radjainia M., Structure 24(7), 2016
PMID: 27238969
Redox-dependent Regulation of Gluconeogenesis by a Novel Mechanism Mediated by a Peroxidatic Cysteine of Peroxiredoxin.
Irokawa H, Tachibana T, Watanabe T, Matsuyama Y, Motohashi H, Ogasawara A, Iwai K, Naganuma A, Kuge S., Sci Rep 6(), 2016
PMID: 27634403
GUN1, a Jack-Of-All-Trades in Chloroplast Protein Homeostasis and Signaling.
Colombo M, Tadini L, Peracchio C, Ferrari R, Pesaresi P., Front Plant Sci 7(), 2016
PMID: 27713755
A primer on peroxiredoxin biochemistry.
Karplus PA., Free Radic Biol Med 80(), 2015
PMID: 25452140
Mitochondrial peroxiredoxin functions as crucial chaperone reservoir in Leishmania infantum.
Teixeira F, Castro H, Cruz T, Tse E, Koldewey P, Southworth DR, Tomás AM, Jakob U., Proc Natl Acad Sci U S A 112(7), 2015
PMID: 25646478
Site-directed mutagenesis substituting cysteine for serine in 2-Cys peroxiredoxin (2-Cys Prx A) of Arabidopsis thaliana effectively improves its peroxidase and chaperone functions.
Lee EM, Lee SS, Tripathi BN, Jung HS, Cao GP, Lee Y, Singh S, Hong SH, Lee KW, Lee SY, Cho JY, Chung BY., Ann Bot 116(4), 2015
PMID: 26141131
The sulfiredoxin-peroxiredoxin (Srx-Prx) axis in cell signal transduction and cancer development.
Mishra M, Jiang H, Wu L, Chawsheen HA, Wei Q., Cancer Lett 366(2), 2015
PMID: 26170166
An additional cysteine in a typical 2-Cys peroxiredoxin of Pseudomonas promotes functional switching between peroxidase and molecular chaperone.
An BC, Lee SS, Jung HS, Kim JY, Lee Y, Lee KW, Lee SY, Tripathi BN, Chung BY., FEBS Lett 589(19 pt b), 2015
PMID: 26278368
In vivo parameters influencing 2-Cys Prx oligomerization: The role of enzyme sulfinylation.
Noichri Y, Palais G, Ruby V, D'Autreaux B, Delaunay-Moisan A, Nyström T, Molin M, Toledano MB., Redox Biol 6(), 2015
PMID: 26335398
Metal-induced self-assembly of peroxiredoxin as a tool for sorting ultrasmall gold nanoparticles into one-dimensional clusters.
Ardini M, Giansanti F, Di Leandro L, Pitari G, Cimini A, Ottaviano L, Donarelli M, Santucci S, Angelucci F, Ippoliti R., Nanoscale 6(14), 2014
PMID: 24910403
Kinetic and structural characterization of a typical two-cysteine peroxiredoxin from Leptospira interrogans exhibiting redox sensitivity.
Arias DG, Reinoso A, Sasoni N, Hartman MD, Iglesias AA, Guerrero SA., Free Radic Biol Med 77(), 2014
PMID: 25236736
Molecular recognition in the interaction of chloroplast 2-Cys peroxiredoxin with NADPH-thioredoxin reductase C (NTRC) and thioredoxin x.
Bernal-Bayard P, Ojeda V, Hervás M, Cejudo FJ, Navarro JA, Velázquez-Campoy A, Pérez-Ruiz JM., FEBS Lett 588(23), 2014
PMID: 25448674

43 References

Daten bereitgestellt von Europe PubMed Central.

Engineering of 2-Cys peroxiredoxin for enhanced stress-tolerance.
An BC, Lee SS, Lee JT, Hong SH, Wi SG, Chung BY., Mol. Cells 32(3), 2011
PMID: 21773675
Thermodynamics of the dimer-decamer transition of reduced human and plant 2-cys peroxiredoxin.
Barranco-Medina S, Kakorin S, Lazaro JJ, Dietz KJ., Biochemistry 47(27), 2008
PMID: 18553980
The oligomeric conformation of peroxiredoxins links redox state to function.
Barranco-Medina S, Lazaro JJ, Dietz KJ., FEBS Lett. 583(12), 2009
PMID: 19464293
Cloning and characterization of a 2-Cys peroxiredoxin from Pisum sativum.
Bernier-Villamor L, Navarro E, Sevilla F, Lazaro JJ., J. Exp. Bot. 55(406), 2004
PMID: 15333640
Non-reductive modulation of chloroplast fructose-1,6-bisphosphatase by 2-Cys peroxiredoxin.
Caporaletti D, D'Alessio AC, Rodriguez-Suarez RJ, Senn AM, Duek PD, Wolosiuk RA., Biochem. Biophys. Res. Commun. 355(3), 2007
PMID: 17307139
The function of the NADPH thioredoxin reductase C-2-Cys peroxiredoxin system in plastid redox regulation and signalling.
Cejudo FJ, Ferrandez J, Cano B, Puerto-Galan L, Guinea M., FEBS Lett. 586(18), 2012
PMID: 22796111
Role of peroxiredoxin I in rectal cancer and related to p53 status.
Chen MF, Lee KD, Yeh CH, Chen WC, Huang WS, Chin CC, Lin PY, Wang JY., Int. J. Radiat. Oncol. Biol. Phys. 78(3), 2010
PMID: 20732753
Phosphoproteins regulated by heat stress in rice leaves.
Chen X, Zhang W, Zhang B, Zhou J, Wang Y, Yang Q, Ke Y, He H., Proteome Sci 9(), 2011
PMID: 21718517
Redox signal integration: from stimulus to networks and genes.
Dietz KJ., Physiol Plant 133(3), 2008
PMID: 18429942
Peroxiredoxins in plants and cyanobacteria.
Dietz KJ., Antioxid. Redox Signal. 15(4), 2011
PMID: 21194355
Peroxiredoxins are conserved markers of circadian rhythms.
Edgar RS, Green EW, Zhao Y, van Ooijen G, Olmedo M, Qin X, Xu Y, Pan M, Valekunja UK, Feeney KA, Maywood ES, Hastings MH, Baliga NS, Merrow M, Millar AJ, Johnson CH, Kyriacou CP, O'Neill JS, Reddy AB., Nature 485(7399), 2012
PMID: 22622569
Proximity-based protein thiol oxidation by H2O2-scavenging peroxidases.
Gutscher M, Sobotta MC, Wabnitz GH, Ballikaya S, Meyer AJ, Samstag Y, Dick TP., J. Biol. Chem. 284(46), 2009
PMID: 19755417
Characterization of plant sulfiredoxin and role of sulphinic form of 2-Cys peroxiredoxin.
Iglesias-Baena I, Barranco-Medina S, Lazaro-Payo A, Lopez-Jaramillo FJ, Sevilla F, Lazaro JJ., J. Exp. Bot. 61(5), 2010
PMID: 20176891
Phosphorylation and concomitant structural changes in human 2-Cys peroxiredoxin isotype I differentially regulate its peroxidase and molecular chaperone functions.
Jang HH, Kim SY, Park SK, Jeon HS, Lee YM, Jung JH, Lee SY, Chae HB, Jung YJ, Lee KO, Lim CO, Chung WS, Bahk JD, Yun DJ, Cho MJ, Lee SY., FEBS Lett. 580(1), 2005
PMID: 16376335
Two enzymes in one; two yeast peroxiredoxins display oxidative stress-dependent switching from a peroxidase to a molecular chaperone function.
Jang HH, Lee KO, Chi YH, Jung BG, Park SK, Park JH, Lee JR, Lee SS, Moon JC, Yun JW, Choi YO, Kim WY, Kang JS, Cheong GW, Yun DJ, Rhee SG, Cho MJ, Lee SY., Cell 117(5), 2004
PMID: 15163410
Up-regulation of peroxiredoxin 1 in lung cancer and its implication as a prognostic and therapeutic target.
Kim JH, Bogner PN, Baek SH, Ramnath N, Liang P, Kim HR, Andrews C, Park YM., Clin. Cancer Res. 14(8), 2008
PMID: 18413821
Overexpression of 2-cysteine peroxiredoxin enhances tolerance to methyl viologen-mediated oxidative stress and high temperature in potato plants.
Kim MD, Kim YH, Kwon SY, Jang BY, Lee SY, Yun DJ, Cho JH, Kwak SS, Lee HS., Plant Physiol. Biochem. 49(8), 2011
PMID: 21620719
Oligomerization and chaperone activity of a plant 2-Cys peroxiredoxin in response to oxidative stress
Kim SY, Jang HH, Lee JR., 2009
The plant-specific function of 2-Cys peroxiredoxin-mediated detoxification of peroxides in the redox-hierarchy of photosynthetic electron flux
König J, Baier M, Horling F, Kahmann U, Harris G, Schurmann P, Dietz KJ., 2002
Reaction mechanism of plant 2-Cys peroxiredoxin. Role of the C terminus and the quaternary structure.
Konig J, Lotte K, Plessow R, Brockhinke A, Baier M, Dietz KJ., J. Biol. Chem. 278(27), 2003
PMID: 12702727
Mechanisms and dynamics in the thiol/disulfide redox regulatory network: transmitters, sensors and targets.
Konig J, Muthuramalingam M, Dietz KJ., Curr. Opin. Plant Biol. 15(3), 2012
PMID: 22226570
Regulation of thioredoxin peroxidase activity by C-terminal truncation.
Koo KH, Lee S, Jeong SY, Kim ET, Kim HJ, Kim K, Song K, Chae HZ., Arch. Biochem. Biophys. 397(2), 2002
PMID: 11795888
Multiple redox and non-redox interactions define 2-Cys peroxiredoxin as a regulatory hub in the chloroplast.
Muthuramalingam M, Seidel T, Laxa M, Nunes de Miranda SM, Gartner F, Stroher E, Kandlbinder A, Dietz KJ., Mol Plant 2(6), 2009
PMID: 19995730
Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression.
Neumann CA, Krause DS, Carman CV, Das S, Dubey DP, Abraham JL, Bronson RT, Fujiwara Y, Orkin SH, Van Etten RA., Nature 424(6948), 2003
PMID: 12891360
A unique cascade of oxidoreductases catalyses trypanothione-mediated peroxide metabolism in Crithidia fasciculata.
Nogoceke E, Gommel DU, Kiess M, Kalisz HM, Flohe L., Biol. Chem. 378(8), 1997
PMID: 9377478
Circadian rhythms persist without transcription in a eukaryote.
O'Neill JS, van Ooijen G, Dixon LE, Troein C, Corellou F, Bouget FY, Reddy AB, Millar AJ., Nature 469(7331), 2011
PMID: 21270895
The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts.
Peltier JB, Cai Y, Sun Q, Zabrouskov V, Giacomelli L, Rudella A, Ytterberg AJ, Rutschow H, van Wijk KJ., Mol. Cell Proteomics 5(1), 2005
PMID: 16207701
Rice NTRC is a high-efficiency redox system for chloroplast protection against oxidative damage.
Perez-Ruiz JM, Spinola MC, Kirchsteiger K, Moreno J, Sahrawy M, Cejudo FJ., Plant Cell 18(9), 2006
PMID: 16891402
Functional analysis of the pathways for 2-Cys peroxiredoxin reduction in Arabidopsis thaliana chloroplasts.
Pulido P, Spinola MC, Kirchsteiger K, Guinea M, Pascual MB, Sahrawy M, Sandalio LM, Dietz KJ, Gonzalez M, Cejudo FJ., J. Exp. Bot. 61(14), 2010
PMID: 20616155
Peroxiredoxin functions as a peroxidase and a regulator and sensor of local peroxides.
Rhee SG, Woo HA, Kil IS, Bae SH., J. Biol. Chem. 287(7), 2011
PMID: 22147704
Novel protective mechanism against irreversible hyperoxidation of peroxiredoxin: Nalpha-terminal acetylation of human peroxiredoxin II.
Seo JH, Lim JC, Lee DY, Kim KS, Piszczek G, Nam HW, Kim YS, Ahn T, Yun CH, Kim K, Chock PB, Chae HZ., J. Biol. Chem. 284(20), 2009
PMID: 19286652
Peroxiredoxin family proteins are key initiators of post-ischemic inflammation in the brain.
Shichita T, Hasegawa E, Kimura A, Morita R, Sakaguchi R, Takada I, Sekiya T, Ooboshi H, Kitazono T, Yanagawa T, Ishii T, Takahashi H, Mori S, Nishibori M, Kuroda K, Akira S, Miyake K, Yoshimura A., Nat. Med. 18(6), 2012
PMID: 22610280
Detection and function of an intramolecular disulfide bond in the pH-responsive CadC of Escherichia coli.
Tetsch L, Koller C, Donhofer A, Jung K., BMC Microbiol. 11(), 2011
PMID: 21486484
The yeast Hsp70 Ssa1 is a sensor for activation of the heat shock response by thiol-reactive compounds.
Wang Y, Gibney PA, West JD, Morano KA., Mol. Biol. Cell 23(17), 2012
PMID: 22809627
Structure, mechanism and regulation of peroxiredoxins.
Wood ZA, Schroder E, Robin Harris J, Poole LB., Trends Biochem. Sci. 28(1), 2003
PMID: 12517450
Hydroxyoctadecadienoic acid and oxidatively modified peroxiredoxins in the blood of Alzheimer's disease patients and their potential as biomarkers.
Yoshida Y, Yoshikawa A, Kinumi T, Ogawa Y, Saito Y, Ohara K, Yamamoto H, Imai Y, Niki E., Neurobiol. Aging 30(2), 2007
PMID: 17688973

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