Abstract
Formation of intra-molecular disulfides and concomitant oxidative protein folding is essential for stability and catalytic function of many soluble and membrane-bound proteins in the endomembrane system, the mitochondrial inter-membrane space and the thylakoid lumen. Disulfide generation from free cysteines in nascent polypeptide chains is generally a catalysed process for which distinct pathways exist in all compartments. A high degree of similarities between highly diverse eukaryotic and bacterial systems for generation of protein disulfides indicates functional conservation of key processes throughout evolution. However, while many aspects about molecular function of enzymatic systems promoting disulfide formation have been demonstrated for bacterial and non-plant eukaryotic organisms, it is now clear that the plant machinery for oxidative protein folding displays distinct details, suggesting that the different pathways have been adapted to plant-specific requirements in terms of compartmentation, molecular function and regulation. Here, we aim to evaluate biological diversity by comparing the plant systems for oxidative protein folding to the respective systems from non-plant eukaryotes.
Similar content being viewed by others
Abbreviations
- CCS1:
-
Chaperone for copper/zinc superoxide dismutase 1
- CSD1:
-
Copper/zinc superoxide dismutase 1
- E GSH :
-
Glutathione redox potential
- ERO:
-
Endoplasmic reticulum thiol oxidase
- ERV:
-
Essential for respiration and viability
- FAD:
-
Flavin adenine dinucleotide
- GPX:
-
Glutathione peroxidase
- GR:
-
Glutathione reductase
- GSH:
-
Reduced glutathione
- GSSG:
-
Glutathione disulfide
- IMS:
-
Inter-membrane space
- LRR:
-
Leucine-rich repeat
- MIA40:
-
Mitochondrial IMS import and assembly pathway 40 kDa
- PDI:
-
Protein disulfide isomerase
- PRX:
-
Peroxiredoxin
- QSOX:
-
Quiescin sulfhydryl oxidase
- RALF:
-
Rapid alkalinisation factor
- TMD:
-
Transmembrane domain
- UPR:
-
Unfolded protein response
- VKOR:
-
Vitamin K epoxide reductase
References
Alejandro S, Rodriguez PL, Belles JM, Yenush L, Garcia-Sanchez MJ, Fernandez JA, Serrano R (2007) An Arabidopsis quiescin-sulfhydryl oxidase regulates cation homeostasis at the root symplast–xylem interface. EMBO J 26(13):3203–3215
Alergand T, Peled-Zehavi H, Katz Y, Danon A (2006) The chloroplast protein disulfide isomerase RB60 reacts with a regulatory disulfide of the RNA-binding protein RB47. Plant Cell Physiol 47(4):540–548
Andeme-Ondzighi C, Christopher DA, Cho EJ, Chang S-C, Staehelin LA (2008) Arabidopsis protein disulfide isomerase-5 inhibits cysteine proteases during trafficking to vacuoles before programmed cell death of the endothelium in developing seeds. Plant Cell 20(8):2205–2220
Anelli T, Alessio M, Bachi A, Bergamelli L, Bertoli G, Camerini S, Mezghrani A, Ruffato E, Simmen T, Sitia R (2003) Thiol-mediated protein retention in the endoplasmic reticulum: the role of ERp44. EMBO J 22(19):5015–5022
Appenzeller-Herzog C (2011) Glutathione- and non-glutathione-based oxidant control in the endoplasmic reticulum. J Cell Sci 124(6):847–855
Appenzeller-Herzog C, Ellgaard L (2008) In vivo reduction-oxidation state of protein disulfide isomerase: the two active sites independently occur in the reduced and oxidized forms. Antioxid Redox Signal 10(1):55–64
Appenzeller-Herzog C, Riemer J, Christensen B, Sorensen ES, Ellgaard L (2008) A novel disulphide switch mechanism in Ero1α balances ER oxidation in human cells. EMBO J 27(22):2977–2987
Appenzeller-Herzog C, Riemer J, Zito E, Chin KT, Ron D, Spiess M, Ellgaard L (2010) Disulphide production by Ero1α-PDI relay is rapid and effectively regulated. EMBO J 29(19):3318–3329
Araki K, Inaba K (2012) Structure, mechanism, and evolution of Ero1 family enzymes. Antioxid Redox Signal 16(8):790–799
Baker KM, Chakravarthi S, Langton KP, Sheppard AM, Lu H, Bulleid NJ (2008) Low reduction potential of Ero1α regulatory disulphides ensures tight control of substrate oxidation. EMBO J 27(22):2988–2997
Banhegyi G, Lusini L, Puskas F, Rossi R, Fulceri R, Braun L, Mile V, di Simplicio P, Mandl J, Benedetti A (1999) Preferential transport of glutathione versus glutathione disulfide in rat liver microsomal vesicles. J Biol Chem 274(18):12213–12216
Benham AM, Cabibbo A, Fassio A, Bulleid N, Sitia R, Braakman I (2000) The CXXCXXC motif determines the folding, structure and stability of human Ero1-Lα. EMBO J 19(17):4493–4502
Bertoli G, Simmen T, Anelli T, Molteni SN, Fesce R, Sitia R (2004) Two conserved cysteine triads in human Ero1α cooperate for efficient disulfide bond formation in the endoplasmic reticulum. J Biol Chem 279(29):30047–30052
Bienert GP, Moller AL, Kristiansen KA, Schulz A, Moller IM, Schjoerring JK, Jahn TP (2007) Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 282(2):1183–1192
Bihlmaier K, Mesecke N, Terziyska N, Bien M, Hell K, Herrmann JM (2007) The disulfide relay system of mitochondria is connected to the respiratory chain. J Cell Biol 179(3):389–395
Bonello J-F, Sevilla-Lecoq S, Berne A, Risueno M-C, Dumas C, Rogowsky PM (2002) Esr proteins are secreted by the cells of the embryo surrounding region. J Exp Bot 53(374):1559–1568
Brach T, Soyk S, Müller C, Hinz G, Hell R, Brandizzi F, Meyer AJ (2009) Non-invasive topology analysis of membrane proteins in the secretory pathway. Plant J 57(3):534–541
Buchanan BB, Balmer Y (2005) Redox regulation: a broadening horizon. Annu Rev Plant Biol 56:187–220
Bulleid NJ, Ellgaard L (2011) Multiple ways to make disulfides. Trends Biochem Sci 36(9):485–492
Cabibbo A, Pagani M, Fabbri M, Rocchi M, Farmery MR, Bulleid NJ, Sitia R (2000) ERO1-L, a human protein that favors disulfide bond formation in the endoplasmic reticulum. J Biol Chem 275(7):4827–4833
Carrie C, Giraud E, Duncan O, Xu L, Wang Y, Huang S, Clifton R, Murcha M, Filipovska A, Rackham O, Vrielink A, Whelan J (2010) Conserved and novel functions for Arabidopsis thaliana MIA40 in assembly of proteins in mitochondria and peroxisomes. J Biol Chem 285(46):36138–36148
Chakravarthi S, Jessop CE, Bulleid NJ (2006) The role of glutathione in disulphide bond formation and endoplasmic-reticulum-generated oxidative stress. EMBO Rep 7(3):271–275
Chakravarthi S, Jessop C, Willer M, Stirling C, Bulleid N (2007) Intracellular catalysis of disulfide bond formation by the human sulfhydryl oxidase, QSOX1. Biochem J 404(3):403–411
Chew O, Whelan J, Millar AH (2003) Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278(47):46869–46877
Cho EJ, Yuen CY, Kang BH, Ondzighi CA, Staehelin LA, Christopher DA (2011) Protein disulfide isomerase-2 of Arabidopsis mediates protein folding and localizes to both the secretory pathway and nucleus, where it interacts with maternal effect embryo arrest factor. Mol Cells 32(5):459–475
Coppock DL, Thorpe C (2006) Multidomain flavin-dependent sulfhydryl oxidases. Antioxid Redox Signal 8(3–4):300–311
Cuozzo JW, Kaiser CA (1999) Competition between glutathione and protein thiols for disulphide-bond formation. Nat Cell Biol 1(3):130–135
d’Aloisio E, Paolacci AR, Dhanapal AP, Tanzarella OA, Porceddu E, Ciaffi M (2010) The protein disulfide isomerase gene family in bread wheat (T. aestivum L.). BMC Plant Biol 10:101
Dabir DV, Leverich EP, Kim SK, Tsai FD, Hirasawa M, Knaff DB, Koehler CM (2007) A role for cytochrome c and cytochrome c peroxidase in electron shuttling from Erv1. EMBO J 26(23):4801–4811
Dias-Gunasekara S, Benham AM (2005) Defining the protein–protein interactions of the mammalian endoplasmic reticulum oxidoreductases (EROs). Biochem Soc Trans 33(Pt 6):1382–1384
Dietz KJ (2003) Plant peroxiredoxins. Annu Rev Plant Biol 54:93–107
Dietz K-J, Jacob S, Oelze M-L, Laxa M, Tognetti V, de Miranda SMN, Baier M, Finkemeier I (2006) The function of peroxiredoxins in plant organelle redox metabolism. J Exp Bot 57(8):1697–1709
Dixon DP, Van Lith M, Edwards R, Benham A (2003) Cloning and initial characterization of the Arabidopsis thaliana endoplasmic reticulum oxidoreductins. Antioxid Redox Signal 5(4):389–396
Dooley CT, Dore TM, Hanson GT, Jackson WC, Remington SJ, Tsien RY (2004) Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators. J Biol Chem 279(21):22284–22293
Ellgaard L, Ruddock LW (2005) The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep 6(1):28–32
Enyedi B, Varnai P, Geiszt M (2010) Redox state of the endoplasmic reticulum is controlled by Ero1L-alpha and intraluminal calcium. Antioxid Redox Signal 13(6):721–729
Eubel H, Meyer EH, Taylor NL, Bussell JD, O'Toole N, Heazlewood JL, Castleden I, Small ID, Smith SM, Millar AH (2008) Novel proteins, putative membrane transporters, and an integrated metabolic network are revealed by quantitative proteomic analysis of Arabidopsis cell culture peroxisomes. Plant Physiol 148(4):1809–1829
Fass D (2008) The Erv family of sulfhydryl oxidases. Biochim Biophys Acta 1783(4):557–566
Feng WK, Wang L, Lu Y, Wang XY (2011) A protein oxidase catalysing disulfide bond formation is localized to the chloroplast thylakoids. FEBS J 278(18):3419–3430
Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11(4):861–905
Frand AR, Kaiser CA (1998) The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol Cell 1(2):161–170
Frand AR, Kaiser CA (1999) Ero1p oxidizes protein disulfide isomerase in a pathway for disulfide bond formation in the endoplasmic reticulum. Mol Cell 4(4):469–477
Frand AR, Kaiser CA (2000) Two pairs of conserved cysteines are required for the pxidative activity of Ero1p in protein disulfide bond formation in the endoplasmic reticulum. Mol Biol Cell 11(9):2833–2843
Fridovich I (1975) Superoxide dismutases. Annu Rev Biochem 44:147–159
Furt F, Oostende C, Widhalm JR, Dale MA, Wertz J, Basset GJ (2010) A bimodular oxidoreductase mediates the specific reduction of phylloquinone (vitamin K1) in chloroplasts. Plant J 64(1):38–46
Gess B, Hofbauer KH, Wenger RH, Lohaus C, Meyer HE, Kurtz A (2003) The cellular oxygen tension regulates expression of the endoplasmic oxidoreductase ERO1-Lα. Eur J Biochem 270(10):2228–2235
Goodstadt L, Ponting CP (2004) Vitamin K epoxide reductase: homology, active site and catalytic mechanism. Trends Biochem Sci 29(6):289–292
Gopalan G, He Z, Balmer Y, Romano P, Gupta R, Heroux A, Buchanan BB, Swaminathan K, Luan S (2004) Structural analysis uncovers a role for redox in regulating FKBP13, an immunophilin of the chloroplast thylakoid lumen. PNAS 101(38):13945–13950
Gross E, Kastner DB, Kaiser CA, Fass D (2004) Structure of Ero1p, source of disulfide bonds for oxidative protein folding in the cell. Cell 117(5):601–610
Gross E, Sevier CS, Heldman N, Vitu E, Bentzur M, Kaiser CA, Thorpe C, Fass D (2006) Generating disulfides enzymatically: reaction products and electron acceptors of the endoplasmic reticulum thiol oxidase Ero1p. PNAS 103(2):299–304
Gross DP, Burgard CA, Reddehase S, Leitch JM, Culotta VC, Hell K (2011) Mitochondrial Ccs1 contains a structural disulfide bond crucial for the import of this unconventional substrate by the disulfide relay system. Mol Biol Cell 22(20):3758–3767
Gutscher M, Sobotta MC, Wabnitz GH, Ballikaya S, Meyer AJ, Samstag Y, Dick TP (2009) Proximity-based protein thiol oxidation by H2O2-scavenging peroxidases. J Biol Chem 284(46):31532–31540
Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M, Sadri N, Yun C, Popko B, Paules R, Stojdl DF, Bell JC, Hettmann T, Leiden JM, Ron D (2003) An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11(3):619–633
Haruta M, Monshausen G, Gilroy S, Sussman MR (2008) A cytoplasmic Ca2+ functional assay for identifying and purifying endogenous cell signaling peptides in Arabidopsis seedlings: identification of AtRALF1 peptide. Biochemistry 47(24):6311–6321
Heckler EJ, Alon A, Fass D, Thorpe C (2008) Human quiescin-sulfhydryl oxidase, QSOX1: probing internal redox steps by mutagenesis. Biochemistry 47(17):4955–4963
Heldman N, Vonshak O, Sevier CS, Vitu E, Mehlman T, Fass D (2010) Steps in reductive activation of the disulfide-generating enzyme Ero1p. Protein Sci 19(10):1863–1876
Henzler T, Steudle E (2000) Transport and metabolic degradation of hydrogen peroxide in Chara corallina: model calculations and measurements with the pressure probe suggest transport of H2O2 across water channels. J Exp Bot 51(353):2053–2066
Herrmann JM, Riemer J (2012) Mitochondrial disulfide relay: redox-regulated protein import into the intermembrane space. J Biol Chem 287(7):4426–4433
Hong Z, Jin H, Tzfira T, Li J (2008) Multiple mechanism-mediated retention of a defective brassinosteroid receptor in the endoplasmic reticulum of Arabidopsis. Plant Cell 20(12):3418–3429
Hooijmaijers C, Rhee JY, Kwak KJ, Chung GC, Horie T, Katsuhara M, Kang H (2012) Hydrogen peroxide permeability of plasma membrane aquaporins of Arabidopsis thaliana. J Plant Res 125(1):147–153
Houston NL, Fan C, Xiang Q-Y, Schulze J-M, Jung R, Boston RS (2005) Phylogenetic analyses identify 10 classes of the protein disulfide isomerase family in plants, including single-domain protein disulfide isomerase-related proteins. Plant Physiol 137(2):762–778
Hu J, Dong L, Outten CE (2008) The redox environment in the mitochondrial intermembrane space is maintained separately from the cytosol and matrix. J Biol Chem 283(43):29126–29134
Huizinga EG, Tsuji S, Romijn RAP, Schiphorst ME, de Groot PG, Sixma JJ, Gros P (2002) Structures of glycoprotein Ibα and its complex with von Willebrand factor A1 domain. Science 297(5584):1176–1179
Hwang CC, Sinskey AJ, Lodish HF (1992) Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257(5076):1496–1502
Inaba K, Masui S, Iida H, Vavassori S, Sitia R, Suzuki M (2010) Crystal structures of human Ero1α reveal the mechanisms of regulated and targeted oxidation of PDI. EMBO J 29(19):3330–3343
Iqbal A, Yabuta Y, Takeda T, Nakano Y, Shigeoka S (2006) Hydroperoxide reduction by thioredoxin-specific glutathione peroxidase isoenzymes of Arabidopsis thaliana. FEBS J 273(24):5589–5597
Ito K, Inaba K (2008) The disulfide bond formation (Dsb) system. Curr Opin Struct Biol 18(4):450–458
Iuchi Y, Okada F, Tsunoda S, Kibe N, Shirasawa N, Ikawa M, Okabe M, Ikeda Y, Fujii J (2009) Peroxiredoxin 4 knockout results in elevated spermatogenic cell death via oxidative stress. Biochem J 419(1):149–158
Jessop CE, Bulleid NJ (2004) Glutathione directly reduces an oxidoreductase in the endoplasmic reticulum of mammalian cells. J Biol Chem 279(53):55341–55347
Jin DY, Tie JK, Stafford DW (2007) The conversion of vitamin K epoxide to vitamin K quinone and vitamin K quinone to vitamin K hydroquinone uses the same active site cysteines. Biochemistry 46(24):7279–7283
Karamoko M, Cline S, Redding K, Ruiz N, Hamel PP (2011) Lumen thiol oxidoreductase1, a disulfide bond-forming catalyst, is required for the assembly of photosystem II inArabidopsis. Plant Cell 23(12):4462–4475
Kawagoe Y, Suzuki K, Tasaki M, Yasuda H, Akagi K, Katoh E, Nishizawa NK, Ogawa M, Takaiwa F (2005) The critical role of disulfide bond formation in protein sorting in the endosperm of rice. Plant Cell 17(4):1141–1153
Kim J, Mayfield SP (2002) The active site of the thioredoxin-like domain of chloroplast protein disulfide isomerase, RB60, catalyzes the redox-regulated binding of chloroplast poly(A)-binding protein, RB47, to the 5′ untranslated region of psbA mRNA. Plant Cell Physiol 43(10):1238–1243
Kojer K, Bien M, Gangel H, Morgan B, Dick TP, Riemer J (2012) Glutathione redox potential in the mitochondrial intermembrane space is linked to the cytosol and impacts the Mia40 redox state. EMBO J 31(14):3169–3182
Leshem Y, Melamed-Book N, Cagnac O, Ronen G, Nishri Y, Solomon M, Cohen G, Levine A (2006) Suppression of Arabidopsis vesicle-SNARE expression inhibited fusion of H2O2-containing vesicles with tonoplast and increased salt tolerance. PNAS 103(47):18008–18013
Levitan A, Danon A, Lisowsky T (2004) Unique features of plant mitochondrial sulfhydryl oxidase. J Biol Chem 279(19):20002–20008
Levitan A, Trebitsh T, Kiss V, Pereg Y, Dangoor I, Danon A (2005) Dual targeting of the protein disulfide isomerase RB60 to the chloroplast and the endoplasmic reticulum. PNAS 102(17):6225–6230
Li CP, Larkins BA (1996) Expression of protein disulfide isomerase is elevated in the endosperm of the maize floury-2 mutant. Plant Mol Biol 30(5):873–882
Li L, Shimada T, Takahashi H, Ueda H, Fukao Y, Kondo M, Nishimura M, Hara-Nishimura I (2006) MAIGO2 is involved in exit of seed storage proteins from the endoplasmic reticulum in Arabidopsis thaliana. Plant Cell 18(12):3535–3547
Li W, Schulman S, Dutton RJ, Boyd D, Beckwith J, Rapoport TA (2010) Structure of a bacterial homologue of vitamin K epoxide reductase. Nature 463(7280):507–512
Lima A, Lima S, Wong JH, Phillips RS, Buchanan BB, Luan S (2006) A redox-active FKBP-type immunophilin functions in accumulation of the photosystem II supercomplex in Arabidopsis thaliana. PNAS 103(33):12631–12636
Lu DP, Christopher DA (2006) Immunolocalization of a protein disulfide isomerase to Arabidopsis thaliana chloroplasts and its association with starch biogenesis. Int J Plant Sci 167(1):1–9
Lu DP, Christopher DA (2008) Light enhances the unfolded protein response as measured by BiP2 gene expression and the secretory GFP-2SC marker in Arabidopsis. Physiol Plant 134(2):360–368
Margittai E, Sitia R (2011) Oxidative protein folding in the secretory pathway and redox signaling across compartments and cells. Traffic 12(1):1–8
Marshall E, Costa LM, Gutierrez-Marcos J (2011) Cysteine-rich peptides (CRPs) mediate diverse aspects of cell–cell communication in plant reproduction and development. J Exp Bot 62(5):1677–1686
Marty L, Siala W, Schwarzlander M, Fricker MD, Wirtz M, Sweetlove LJ, Meyer Y, Meyer AJ, Reichheld J-P, Hell R (2009) The NADPH-dependent thioredoxin system constitutes a functional backup for cytosolic glutathione reductase in Arabidopsis. PNAS 106(22):9109–9114
Mattei B, Bernalda MS, Federici L, Roepstorff P, Cervone F, Boffi A (2001) Secondary structure and post-translational modifications of the leucine-rich repeat protein PGIP (polygalacturonase-inhibiting protein) from Phaseolus vulgaris. Biochemistry 40(2):569–576
Merksamer PI, Trusina A, Papa FR (2008) Real-time redox measurements during endoplasmic reticulum stress reveal interlinked protein folding functions. Cell 135(5):933–947
Mesecke N, Terziyska N, Kozany C, Baumann F, Neupert W, Hell K, Herrmann JM (2005) A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell 121(7):1059–1069
Meyer AJ (2008) The integration of glutathione homeostasis and redox signaling. J Plant Physiol 165(13):1390–1403
Meyer AJ, Dick TP (2010) Fluorescent protein-based redox probes. Antioxid Redox Signal 13(5):621–650
Meyer AJ, Brach T, Marty L, Kreye S, Rouhier N, Jacquot J-P, Hell R (2007) Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J 52(5):973–986
Mishima M, Takayama S, K-i S, J-g J, Kojima C, Isogai A, Shirakawa M (2003) Structure of the male determinant factor for Brassica self-incompatibility. J Biol Chem 278(38):36389–36395
Navrot N, Collin V, Gualberto J, Gelhaye E, Hirasawa M, Rey P, Knaff DB, Issakidis E, Jacquot J-P, Rouhier N (2006) Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiol 142(4):1364–1379
Nguyen VD, Saaranen MJ, Karala AR, Lappi AK, Wang L, Raykhel IB, Alanen HI, Salo KE, Wang CC, Ruddock LW (2011) Two endoplasmic reticulum PDI peroxidases increase the efficiency of the use of peroxide during disulfide bond formation. J Mol Biol 406(3):503–515
Okita TW, Rogers JC (1996) Compartmentation of proteins in the endomembrane system of plant cells. Annu Rev Plant Physiol Plant Mol Biol 47:327–350
Onda Y, Kumamaru T, Kawagoe Y (2009) ER membrane-localized oxidoreductase Ero1 is required for disulfide bond formation in the rice endosperm. PNAS 106(33):14156–14161
Onda Y, Nagamine A, Sakurai M, Kumamaru T, Ogawa M, Kawagoe Y (2011) Distinct roles of protein disulfide isomerase and P5 sulfhydryl oxidoreductases in multiple pathways for oxidation of structurally diverse storage proteins in rice. Plant Cell 23(1):210–223
Orsi A, Sparvoli F, Ceriotti A (2001) Role of individual disulfide bonds in the structural maturation of a low molecular weight glutenin subunit. J Biol Chem 276(34):32322–32329
Ostrowski MC, Kistler WS (1980) Properties of a flavoprotein sulfhydryl oxidase from rat seminal vesicle secretion. Biochemistry 19(12):2639–2645
Otsu M, Bertoli G, Fagioli C, Guerini-Rocco E, Nerini-Molteni S, Ruffato E, Sitia R (2006) Dynamic retention of Ero1α and Ero1β in the endoplasmic reticulum by interactions with PDI and ERp44. Antioxid Redox Signal 8(3–4):274–282
Pagani M, Fabbri M, Benedetti C, Fassio A, Pilati S, Bulleid NJ, Cabibbo A, Sitia R (2000) Endoplasmic reticulum oxidoreductin 1-Lβ (ERO1-Lβ), a human gene induced in the course of the unfolded protein response. J Biol Chem 275(31):23685–23692
Pagani M, Pilati S, Bertoli G, Valsasina B, Sitia R (2001) The C-terminal domain of yeast Ero1p mediates membrane localization and is essential for function. FEBS Lett 508(1):117–120
Pearce G, Moura DS, Stratmann J, Ryan CA Jr (2001) RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. PNAS 98(22):12843–12847
Peltier J-B, Friso G, Kalume DE, Roepstorff P, Nilsson F, Adamska I, van Wijk KJ (2000) Proteomics of the chloroplast: systematic identification and targeting analysis of lumenal and peripheral thylakoid proteins. Plant Cell 12(3):319–342
Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8(10):785–786
Pfeifer H, Conrad M, Roethlein D, Kyriakopoulos A, Brielmeier M, Bornkamm GW, Behne D (2001) Identification of a specific sperm nuclei selenoenzyme necessary for protamine thiol cross-linking during sperm maturation. FASEB J:00-0655fje
Pollard MG, Travers KJ, Weissman JS (1998) Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Mol Cell 1(2):171–182
Pompa A, Vitale A (2006) Retention of a bean phaseolin/maize γ-zein fusion in the endoplasmic reticulum depends on disulfide bond formation. Plant Cell 18(10):2608–2621
Rancy PC, Thorpe C (2008) Oxidative protein folding in vitro: a study of the cooperation between quiescin-sulfhydryl oxidase and protein disulfide isomerase. Biochemistry 47(46):12047–12056
Reumann S, Babujee L, Ma C, Wienkoop S, Siemsen T, Antonicelli GE, Rasche N, Luder F, Weckwerth W, Jahn O (2007) Proteome analysis of Arabidopsis leaf peroxisomes reveals novel targeting peptides, metabolic pathways, and defense mechanisms. Plant Cell 19(10):3170–3193
Riemer J, Bulleid N, Herrmann JM (2009) Disulfide formation in the ER and mitochondria: two solutions to a common process. Science 324(5932):1284–1287
Rodriguez Milla MA, Maurer A, Rodriguez Huete A, Gustafson JP (2003) Glutathione peroxidase genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signaling pathway. Plant J 36(5):602–615
Roy A, Kucukural A, Zhang Y (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5(4):725–738
Rutkevich LA, Williams DB (2012) Vitamin K epoxide reductase contributes to protein disulfide formation and redox homeostasis within the endoplasmic reticulum. Mol Biol Cell 23(11):2017–2027
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425
Satoh-Cruz M, Crofts AJ, Takemoto-Kuno Y, Sugino A, Washida H, Crofts N, Okita TW, Ogawa M, Satoh H, Kumamaru T (2010) Protein disulfide isomerase like 1-1 participates in the maturation of proglutelin within the endoplasmic reticulum in rice endosperm. Plant Cell Physiol 51(9):1581–1593
Schopfer CR, Nasrallah ME, Nasrallah JB (1999) The male determinant of self-incompatibility in Brassica. Science 286(5445):1697–1700
Schulman S, Wang B, Li W, Rapoport TA (2010) Vitamin K epoxide reductase prefers ER membrane-anchored thioredoxin-like redox partners. PNAS 107(34):15027–15032
Schwacke R, Schneider A, van der Graaff E, Fischer K, Catoni E, Desimone M, Frommer WB, Flugge UI, Kunze R (2003) ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol 131(1):16–26
Schwarzländer M, Fricker MD, Müller C, Marty L, Brach T, Novak T, Sweetlove LJ, Hell R, Meyer AJ (2008) Confocal imaging of glutathione redox potential in living plant cells. J Microsc Oxf 231(2):299–316
Selles B, Jacquot JP, Rouhier N (2011) Comparative genomic study of protein disulfide isomerases from photosynthetic organisms. Genomics 97(1):37–50
Sevier C, Qu H, Heldman N, Gross E, Fass D, Kaiser C (2007) Modulation of cellular disulfide-bond formation and the ER redox environment by feedback regulation of Ero1. Cell 129(2):333–344
Shimoni Y, Zhu X, Levanony H, Segal G, Galili G (1995) Purification, characterization, and intracellular localization of glycosylated protein disulfide isomerase from wheat grains. Plant Physiol 108(1):327–335
Silverstein KAT, Graham MA, Paape TD, VandenBosch KA (2005) Genome organization of more than 300 defensin-like genes in Arabidopsis. Plant Physiol 138:600–610
Singh AK, Bhattacharyya-Pakrasi M, Pakrasi HB (2008) Identification of an atypical membrane protein involved in the formation of protein disulfide bonds in oxygenic photosynthetic organisms. J Biol Chem 283(23):15762–15770
Takayama S, Shiba H, Iwano M, Shimosato H, Che F-S, Kai N, Watanabe M, Suzuki G, Hinata K, Isogai A (2000) The pollen determinant of self-incompatibility in Brassica campestris. PNAS 97(4):1920–1925
Takayama S, Shimosato H, Shiba H, Funato M, Che FS, Watanabe M, Iwano M, Isogai A (2001) Direct ligand–receptor complex interaction controls Brassica self-incompatibility. Nature 413(6855):534–538
Takemoto Y, Coughlan SJ, Okita TW, Satoh H, Ogawa M, Kumamaru T (2002) The rice mutant esp2 greatly accumulates the glutelin precursor and deletes the protein disulfide isomerase. Plant Physiol 128(4):1212–1222
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739
Tavender TJ, Bulleid NJ (2010) Peroxiredoxin IV protects cells from oxidative stress by removing H2O2 produced during disulphide formation. J Cell Sci 123(15):2672–2679
Thorpe C, Coppock DL (2007) Generating disulfides in multicellular organisms: emerging roles for a new flavoprotein family. J Biol Chem 282(19):13929–13933
Tie J-K, Jin D-Y, Stafford DW (2012) Human vitamin K epoxide reductase and its bacterial homologue have different membrane topologies and reaction mechanisms. J Biol Chem. doi:10.1074/jbc.M1112.402941
Tien A-C, Rajan A, Schulze KL, Ryoo HD, Acar M, Steller H, Bellen HJ (2008) Ero1L, a thiol oxidase, is required for Notch signaling through cysteine bridge formation of the Lin12-Notch repeats in Drosophila melanogaster. J Cell Biol 182(6):1113–1125
Toledano MB, Delaunay A, Monceau L, Tacnet F (2004) Microbial H2O2 sensors as archetypical redox signaling modules. Trends Biochem Sci 29(7):351–357
Toppo S, Vanin S, Bosello V, Tosatto SC (2008) Evolutionary and structural insights into the multifaceted glutathione peroxidase (Gpx) superfamily. Antioxid Redox Signal 10(9):1501–1514
Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, Walter P (2000) Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101(3):249–258
Tu BP, Weissman JS (2002) The FAD- and O2-dependent reaction cycle of Ero1-mediated oxidative protein folding in the endoplasmic reticulum. Mol Cell 10(5):983–994
Tu BP, Ho-Schleyer SC, Travers KJ, Weissman JS (2000) Biochemical basis of oxidative protein folding in the endoplasmic reticulum. Science 290(5496):1571–1574
van Lith M, Tiwari S, Pediani J, Milligan G, Bulleid NJ (2011) Real-time monitoring of redox changes in the mammalian endoplasmic reticulum. J Cell Sci 124(14):2349–2356
Vander Heyden AB, Naismith TV, Snapp EL, Hanson PI (2011) Static retention of the lumenal monotopic membrane protein torsinA in the endoplasmic reticulum. EMBO J 30(16):3217–3231
van der Hoorn RAL, Wulff BBH, Rivas S, Durrant MC, van der Ploeg A, de Wit PJGM, Jones JDG (2005) Structure-function analysis of Cf-9, a receptor-like protein with extracytoplasmic leucine-rich repeats. Plant Cell 17(3):1000–1015
Vitu E, Kim S, Sevier CS, Lutzky O, Heldman N, Bentzur M, Unger T, Yona M, Kaiser CA, Fass D (2010) Oxidative activity of yeast Ero1p on protein disulfide isomerase and related oxidoreductases of the endoplasmic reticulum. J Biol Chem 285(24):18155–18165
Wajih N, Sane DC, Hutson SM, Wallin R (2005) Engineering of a recombinant vitamin K-dependent γ-carboxylation system with enhanced γ-carboxyglutamic acid forming capacity: evidence for a functional CXXC redox center in the system. J Biol Chem 280(11):10540–10547
Wajih N, Hutson SM, Wallin R (2007) Disulfide-dependent protein folding is linked to operation of the vitamin K cycle in the endoplasmic reticulum: a protein disulfide isomerase-VKORC1 redox enzyme complex appears to be responsible for a vitamin K1 2,3-epoxide. J Biol Chem 282(4):2626–2635
Wang H, Boavida LC, Ron M, McCormick S (2008) Truncation of a proteindisulfide isomerase, PDIL2-1, delays embryo sac maturation and disrupts pollen tube guidance in Arabidopsis thaliana. Plant Cell 20(12):3300–3311
Wang L, Zhu L, Wang CC (2011) The endoplasmic reticulum sulfhydryl oxidase Ero1β drives efficient oxidative protein folding with loose regulation. Biochem J 434(1):113–121
Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An “electronic fluorescent pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS One 2(8):e718
Winterbourn CC, Metodiewa D (1999) Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide. Free Radic Biol Med 27(3–4):322–328
Zhang Y (2007) Template-based modeling and free modeling by I-TASSER in CASP7. Proteins 69(Suppl 8):108–117
Zito E, Chin K-T, Blais J, Harding HP, Ron D (2010) ERO1β, a pancreas-specific disulfide oxidase, promotes insulin biogenesis and glucose homeostasis. J Cell Biol 189(4):769
Zuckerkandl E, Pauling L (1965) Molecules as documents of evolutionary history. J Theor Biol 8(2):357–366
Zybailov B, Rutschow H, Friso G, Rudella A, Emanuelsson O, Sun Q, van Wijk KJ (2008) Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS One 3(4):e1994
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: David Robinson
Rights and permissions
About this article
Cite this article
Aller, I., Meyer, A.J. The oxidative protein folding machinery in plant cells. Protoplasma 250, 799–816 (2013). https://doi.org/10.1007/s00709-012-0463-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-012-0463-x