Balancing oxidative protein folding: The influences of reducing pathways on disulfide bond formation

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1844, Issue 8, 2014, Pages 1383-1390

  Kojer, Kerstin ^a   Riemer, Jan ^a  

^a Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

Author keywords

Glutathione; Mitochondrial intermembrane space; Oxidative folding; Reducing pathways

Indexed keywords

ENZYME; GLUTATHIONE; GLUTATHIONE REDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; THIOREDOXIN; THIOREDOXIN REDUCTASE;

DISULFIDE BOND; ENDOPLASMIC RETICULUM; HUMAN; ISOMERIZATION; NONHUMAN; OXIDATION; OXIDATION REDUCTION POTENTIAL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; REVIEW; STROMA;

BACTERIA (MICROORGANISMS);

GLUTATHIONE; MITOCHONDRIAL INTERMEMBRANE SPACE; OXIDATIVE FOLDING; REDUCING PATHWAYS;

ANIMALS; DISULFIDES; ENDOPLASMIC RETICULUM; HUMANS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEIN FOLDING; SIGNAL TRANSDUCTION;

EID: 84902253458     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2014.02.004     Document Type: Review

References (97)

1. P. Kosuri, J. Alegre-Cebollada, J. Feng, A. Kaplan, A. Ingles-Prieto, C.L. Badilla, B.R. Stockwell, J.M. Sanchez-Ruiz, A. Holmgren, and J.M. Fernandez Protein folding drives disulfide formation Cell 151 2012 794 806
2. F.X. Schmid Prolyl isomerase: enzymatic catalysis of slow protein-folding reactions Annu. Rev. Biophys. Biomol. Struct. 22 1993 123 142
3. W.K. Feng, L. Wang, Y. Lu, and X.Y. Wang A protein oxidase catalysing disulfide bond formation is localized to the chloroplast thylakoids FEBS J. 278 2011 3419 3430
4. M. Karamoko, S. Cline, K. Redding, N. Ruiz, and P.P. Hamel Lumen thiol oxidoreductase 1, a disulfide bond-forming catalyst, is required for the assembly of photosystem II in Arabidopsis Plant Cell 23 2011 4462 4475
5. M. Hakim, and D. Fass Cytosolic disulfide bond formation in cells infected with large nucleocytoplasmic DNA viruses Antioxid. Redox Signal. 13 2010 1261 1271
6. J.C. Bardwell, K. McGovern, and J. Beckwith Identification of a protein required for disulfide bond formation in vivo Cell 67 1991 581 589 (Pubitemid 121001472)
7. J.L. Martin, J.C. Bardwell, and J. Kuriyan Crystal structure of the DsbA protein required for disulphide bond formation in vivo Nature 365 1993 464 468 (Pubitemid 23311046)
8. J.C. Bardwell, J.O. Lee, G. Jander, N. Martin, D. Belin, and J. Beckwith A pathway for disulfide bond formation in vivo Proc. Natl. Acad. Sci. U. S. A. 90 1993 1038 1042 (Pubitemid 23053946)
9. M. Bader, W. Muse, D.P. Ballou, C. Gassner, and J.C. Bardwell Oxidative protein folding is driven by the electron transport system Cell 98 1999 217 227 (Pubitemid 29344909)
10. M.W. Bader, T. Xie, C.A. Yu, and J.C. Bardwell Disulfide bonds are generated by quinone reduction J. Biol. Chem. 275 2000 26082 26088
11. J. Regeimbal, S. Gleiter, B.L. Trumpower, C.A. Yu, M. Diwakar, D.P. Ballou, and J.C. Bardwell Disulfide bond formation involves a quinhydrone-type charge-transfer complex Proc. Natl. Acad. Sci. U. S. A. 100 2003 13779 13784 (Pubitemid 37499143)
12. K. Inaba, S. Murakami, M. Suzuki, A. Nakagawa, E. Yamashita, K. Okada, and K. Ito Crystal structure of the DsbB-DsbA complex reveals a mechanism of disulfide bond generation Cell 127 2006 789 801 (Pubitemid 44716258)
13. C.S. Sevier, H. Kadokura, V.C. Tam, J. Beckwith, D. Fass, and C.A. Kaiser The prokaryotic enzyme DsbB may share key structural features with eukaryotic disulfide bond forming oxidoreductases Protein Sci. 14 2005 1630 1642 (Pubitemid 41007924)
14. T. Xie, L. Yu, M.W. Bader, J.C. Bardwell, and C.A. Yu Identification of the ubiquinone-binding domain in the disulfide catalyst disulfide bond protein B J. Biol. Chem. 277 2002 1649 1652 (Pubitemid 34968734)
15. Y.H. Takahashi, K. Inaba, and K. Ito Characterization of the menaquinone-dependent disulfide bond formation pathway of Escherichia coli J. Biol. Chem. 279 2004 47057 47065 (Pubitemid 39518361)
16. M. Bien, S. Longen, N. Wagener, I. Chwalla, J.M. Herrmann, and J. Riemer Mitochondrial disulfide bond formation is driven by intersubunit electron transfer in Erv1 and proofread by glutathione Mol. Cell 37 2010 516 528
17. N. Mesecke, N. Terziyska, C. Kozany, F. Baumann, W. Neupert, K. Hell, and J.M. Herrmann A disulfide relay system in the intermembrane space of mitochondria that mediates protein import Cell 121 2005 1059 1069 (Pubitemid 40884396)
18. A. Chacinska, S. Pfannschmidt, N. Wiedemann, V. Kozjak, L.K. Sanjuan Szklarz, A. Schulze-Specking, K.N. Truscott, B. Guiard, C. Meisinger, and N. Pfanner Essential role of Mia40 in import and assembly of mitochondrial intermembrane space proteins EMBO J. 23 2004 3735 3746 (Pubitemid 39389705)
19. M. Rissler, N. Wiedemann, S. Pfannschmidt, K. Gabriel, B. Guiard, N. Pfanner, and A. Chacinska The essential mitochondrial protein Erv1 cooperates with Mia40 in biogenesis of intermembrane space proteins J. Mol. Biol. 353 2005 485 492 (Pubitemid 41414727)
20. K. Bihlmaier, N. Mesecke, C. Kloeppel, and J.M. Herrmann The disulfide relay of the intermembrane space of mitochondria: an oxygen-sensing system? Ann. N. Y. Acad. Sci. 1147 2008 293 302
21. S. Allen, V. Balabanidou, D.P. Sideris, T. Lisowsky, and K. Tokatlidis Erv1 mediates the Mia40-dependent protein import pathway and provides a functional link to the respiratory chain by shuttling electrons to cytochrome c J. Mol. Biol. 353 2005 937 944 (Pubitemid 41503262)
22. V.N. Daithankar, W. Wang, J.R. Trujillo, and C. Thorpe Flavin-linked Erv-family sulfhydryl oxidases release superoxide anion during catalytic turnover Biochemistry 51 2012 265 272
23. S.R. Farrell, and C. Thorpe Augmenter of liver regeneration: a flavin-dependent sulfhydryl oxidase with cytochrome c reductase activity Biochemistry 44 2005 1532 1541 (Pubitemid 40204396)
24. V.N. Daithankar, S.A. Schaefer, M. Dong, B.J. Bahnson, and C. Thorpe Structure of the human sulfhydryl oxidase augmenter of liver regeneration and characterization of a human mutation causing an autosomal recessive myopathy Biochemistry 49 2010 6737 6745
25. C.K. Wu, T.A. Dailey, H.A. Dailey, B.C. Wang, and J.P. Rose The crystal structure of augmenter of liver regeneration: a mammalian FAD-dependent sulfhydryl oxidase Protein Sci. 12 2003 1109 1118 (Pubitemid 36505444)
26. P.C. Guo, J.D. Ma, Y.L. Jiang, S.J. Wang, Z.Z. Bao, X.J. Yu, Y. Chen, and C.Z. Zhou Structure of yeast sulfhydryl oxidase erv1 reveals electron transfer of the disulfide relay system in the mitochondrial intermembrane space J. Biol. Chem. 287 2012 34961 34969
27. S. Kawano, K. Yamano, M. Naoe, T. Momose, K. Terao, S. Nishikawa, N. Watanabe, and T. Endo Structural basis of yeast Tim40/Mia40 as an oxidative translocator in the mitochondrial intermembrane space Proc. Natl. Acad. Sci. U. S. A. 106 2009 14403 14407
28. L. Banci, I. Bertini, C. Cefaro, S. Ciofi-Baffoni, A. Gallo, M. Martinelli, D.P. Sideris, N. Katrakili, and K. Tokatlidis MIA40 is an oxidoreductase that catalyzes oxidative protein folding in mitochondria Nat. Struct. Mol. Biol. 16 2009 198 206
29. J. Riemer, N. Bulleid, and J.M. Herrmann Disulfide formation in the ER and mitochondria: two solutions to a common process Science 324 2009 1284 1287
30. L. Ellgaard, and L.W. Ruddock The human protein disulphide isomerase family: substrate interactions and functional properties EMBO Rep. 6 2005 28 32 (Pubitemid 41710070)
31. N.J. Bulleid, and L. Ellgaard Multiple ways to make disulfides Trends Biochem. Sci. 36 2011 485 492
32. E. Gross, D.B. Kastner, C.A. Kaiser, and D. Fass Structure of Ero1p, source of disulfide bonds for oxidative protein folding in the cell Cell 117 2004 601 610 (Pubitemid 38692526)
33. C.S. Sevier, J.W. Cuozzo, A. Vala, F. Aslund, and C.A. Kaiser A flavoprotein oxidase defines a new endoplasmic reticulum pathway for biosynthetic disulphide bond formation Nat. Cell Biol. 3 2001 874 882 (Pubitemid 32952251)
34. E. Zito, E.P. Melo, Y. Yang, A. Wahlander, T.A. Neubert, and D. Ron Oxidative protein folding by an endoplasmic reticulum-localized peroxiredoxin Mol. Cell 40 2010 787 797
35. V.D. Nguyen, M.J. Saaranen, A.R. Karala, A.K. Lappi, L. Wang, I.B. Raykhel, H.I. Alanen, K.E. Salo, C.C. Wang, and L.W. Ruddock Two endoplasmic reticulum PDI peroxidases increase the efficiency of the use of peroxide during disulfide bond formation J. Mol. Biol. 406 2011 503 515
36. L. Wang, L. Zhang, Y. Niu, R. Sitia, and C.C. Wang Glutathione peroxidase 7 utilizes hydrogen peroxide generated by Ero1alpha to promote oxidative protein folding Antioxid. Redox Signal. 20 4 2014 545 556
37. E. Zito, H.G. Hansen, G.S. Yeo, J. Fujii, and D. Ron Endoplasmic reticulum thiol oxidase deficiency leads to ascorbic acid depletion and noncanonical scurvy in mice Mol. Cell 48 2012 39 51
38. L.W. Ruddock Low-molecular-weight oxidants involved in disulfide bond formation Antioxid. Redox Signal. 16 2012 1129 1138
39. C. Appenzeller-Herzog, J. Riemer, E. Zito, K.T. Chin, D. Ron, M. Spiess, and L. Ellgaard Disulphide production by Ero1alpha-PDI relay is rapid and effectively regulated EMBO J. 29 2010 3318 3329
40. A.K. Lappi, and L.W. Ruddock Reexamination of the role of interplay between glutathione and protein disulfide isomerase J. Mol. Biol. 409 2011 238 249
41. S. Raje, and C. Thorpe Inter-domain redox communication in flavoenzymes of the quiescin/sulfhydryl oxidase family: role of a thioredoxin domain in disulfide bond formation Biochemistry 42 2003 4560 4568 (Pubitemid 36457625)
42. J.A. Codding, B.A. Israel, and C. Thorpe Protein substrate discrimination in the quiescin sulfhydryl oxidase (QSOX) family Biochemistry 51 2012 4226 4235
43. A. Alon, I. Grossman, Y. Gat, V.K. Kodali, F. DiMaio, T. Mehlman, G. Haran, D. Baker, C. Thorpe, and D. Fass The dynamic disulphide relay of quiescin sulphydryl oxidase Nature 488 2012 414 418
44. A. Rietsch, D. Belin, N. Martin, and J. Beckwith An in vivo pathway for disulfide bond isomerization in Escherichia coli Proc. Natl. Acad. Sci. U. S. A. 93 1996 13048 13053 (Pubitemid 26382767)
45. D. Missiakas, F. Schwager, and S. Raina Identification and characterization of a new disulfide isomerase-like protein (DsbD) in Escherichia coli EMBO J. 14 1995 3415 3424
46. M. Sone, Y. Akiyama, and K. Ito Differential in vivo roles played by DsbA and DsbC in the formation of protein disulfide bonds J. Biol. Chem. 272 1997 10349 10352 (Pubitemid 27181032)
47. A. Hiniker, J.F. Collet, and J.C. Bardwell Copper stress causes an in vivo requirement for the Escherichia coli disulfide isomerase DsbC J. Biol. Chem. 280 2005 33785 33791 (Pubitemid 41443097)
48. A.A. McCarthy, P.W. Haebel, A. Torronen, V. Rybin, E.N. Baker, and P. Metcalf Crystal structure of the protein disulfide bond isomerase, DsbC, from Escherichia coli Nat. Struct. Biol. 7 2000 196 199 (Pubitemid 30140763)
49. P.W. Haebel, D. Goldstone, F. Katzen, J. Beckwith, and P. Metcalf The disulfide bond isomerase DsbC is activated by an immunoglobulin-fold thiol oxidoreductase: crystal structure of the DsbC-DsbDalpha complex EMBO J. 21 2002 4774 4784
50. E.J. Stewart, F. Katzen, and J. Beckwith Six conserved cysteines of the membrane protein DsbD are required for the transfer of electrons from the cytoplasm to the periplasm of Escherichia coli EMBO J. 18 1999 5963 5971 (Pubitemid 29515673)
51. A. Rietsch, P. Bessette, G. Georgiou, and J. Beckwith Reduction of the periplasmic disulfide bond isomerase, DsbC, occurs by passage of electrons from cytoplasmic thioredoxin J. Bacteriol. 179 1997 6602 6608 (Pubitemid 27465291)
52. A. Rozhkova, and R. Glockshuber Thermodynamic aspects of DsbD-mediated electron transport J. Mol. Biol. 380 2008 783 788
53. A. Rozhkova, C.U. Stirnimann, P. Frei, U. Grauschopf, R. Brunisholz, M.G. Grutter, G. Capitani, and R. Glockshuber Structural basis and kinetics of inter- and intramolecular disulfide exchange in the redox catalyst DsbD EMBO J. 23 2004 1709 1719 (Pubitemid 38649634)
54. J.F. Collet, J. Riemer, M.W. Bader, and J.C. Bardwell Reconstitution of a disulfide isomerization system J. Biol. Chem. 277 2002 26886 26892 (Pubitemid 34951697)
55. F. Shao, M.W. Bader, U. Jakob, and J.C. Bardwell DsbG, a protein disulfide isomerase with chaperone activity J. Biol. Chem. 275 2000 13349 13352 (Pubitemid 30257393)
56. P.H. Bessette, J.J. Cotto, H.F. Gilbert, and G. Georgiou In vivo and in vitro function of the Escherichia coli periplasmic cysteine oxidoreductase DsbG J. Biol. Chem. 274 1999 7784 7792
57. C.U. Stirnimann, A. Rozhkova, U. Grauschopf, M.G. Grutter, R. Glockshuber, and G. Capitani Structural basis and kinetics of DsbD-dependent cytochrome c maturation Structure 13 2005 985 993 (Pubitemid 40943330)
58. M. Depuydt, S.E. Leonard, D. Vertommen, K. Denoncin, P. Morsomme, K. Wahni, J. Messens, K.S. Carroll, and J.F. Collet A periplasmic reducing system protects single cysteine residues from oxidation Science 326 2009 1109 1111
59. E. Reid, J. Cole, and D.J. Eaves The Escherichia coli CcmG protein fulfils a specific role in cytochrome c assembly Biochem. J. 355 2001 51 58 (Pubitemid 32304234)
60. S. Chakravarthi, and N.J. Bulleid Glutathione is required to regulate the formation of native disulfide bonds within proteins entering the secretory pathway J. Biol. Chem. 279 2004 39872 39879 (Pubitemid 39258259)
61. C.E. Jessop, and N.J. Bulleid Glutathione directly reduces an oxidoreductase in the endoplasmic reticulum of mammalian cells J. Biol. Chem. 279 2004 55341 55347 (Pubitemid 40066532)
62. S.N. Molteni, A. Fassio, M.R. Ciriolo, G. Filomeni, E. Pasqualetto, C. Fagioli, and R. Sitia Glutathione limits Ero1-dependent oxidation in the endoplasmic reticulum J. Biol. Chem. 279 2004 32667 32673 (Pubitemid 39014725)
63. G. Banhegyi, L. Lusini, F. Puskas, R. Rossi, R. Fulceri, L. Braun, V. Mile, P. di Simplicio, J. Mandl, and A. Benedetti Preferential transport of glutathione versus glutathione disulfide in rat liver microsomal vesicles J. Biol. Chem. 274 1999 12213 12216
64. M. Csala, R. Fulceri, J. Mandl, A. Benedetti, and G. Banhegyi Glutathione transport in the endo/sarcoplasmic reticulum Biofactors 17 2003 27 35 (Pubitemid 37267139)
65. G. Banhegyi, A. Benedetti, R. Fulceri, and S. Senesi Cooperativity between 11beta-hydroxysteroid dehydrogenase type 1 and hexose-6-phosphate dehydrogenase in the lumen of the endoplasmic reticulum J. Biol. Chem. 279 2004 27017 27021 (Pubitemid 38812537)
66. I. Czegle, S. Piccirella, S. Senesi, M. Csala, J. Mandl, G. Banhegyi, R. Fulceri, and A. Benedetti Cooperativity between 11beta-hydroxysteroid dehydrogenase type 1 and hexose-6-phosphate dehydrogenase is based on a common pyridine nucleotide pool in the lumen of the endoplasmic reticulum Mol. Cell. Endocrinol. 248 2006 24 25
67. I. Gerin, and E. Van Schaftingen Evidence for glucose-6-phosphate transport in rat liver microsomes FEBS Lett. 517 2002 257 260 (Pubitemid 34327670)
68. S. Grubb, L. Guo, E.A. Fisher, and J.L. Brodsky Protein disulfide isomerases contribute differentially to the endoplasmic reticulum-associated degradation of apolipoprotein B and other substrates Mol. Biol. Cell 23 2012 520 532
69. C. Fagioli, A. Mezghrani, and R. Sitia Reduction of interchain disulfide bonds precedes the dislocation of Ig-mu chains from the endoplasmic reticulum to the cytosol for proteasomal degradation J. Biol. Chem. 276 2001 40962 40967
70. R. Mancini, C. Fagioli, A.M. Fra, C. Maggioni, and R. Sitia Degradation of unassembled soluble Ig subunits by cytosolic proteasomes: evidence that retrotranslocation and degradation are coupled events FASEB J. 14 2000 769 778 (Pubitemid 30198575)
71. O.B. Oka, M.A. Pringle, I.M. Schopp, I. Braakman, and N.J. Bulleid ERdj5 is the ER reductase that catalyzes the removal of non-native disulfides and correct folding of the LDL receptor Mol. Cell 50 2013 793 804
72. R. Ushioda, J. Hoseki, K. Araki, G. Jansen, D.Y. Thomas, and K. Nagata ERdj5 is required as a disulfide reductase for degradation of misfolded proteins in the ER Science 321 2008 569 572
73. J.M. Williams, T. Inoue, L. Banks, and B. Tsai The ERdj5-Sel1L complex facilitates cholera toxin retrotranslocation Mol. Biol. Cell 24 2013 785 795
74. M.W. Bader, A. Hiniker, J. Regeimbal, D. Goldstone, P.W. Haebel, J. Riemer, P. Metcalf, and J.C. Bardwell Turning a disulfide isomerase into an oxidase: DsbC mutants that imitate DsbA EMBO J. 20 2001 1555 1562 (Pubitemid 32299393)
75. M. Eser, L. Masip, H. Kadokura, G. Georgiou, and J. Beckwith Disulfide bond formation by exported glutaredoxin indicates glutathione's presence in the E. coli periplasm Proc. Natl. Acad. Sci. U. S. A. 106 2009 1572 1577
76. M.S. Pittman, H.C. Robinson, and R.K. Poole A bacterial glutathione transporter (Escherichia coli CydDC) exports reductant to the periplasm J. Biol. Chem. 280 2005 32254 32261 (Pubitemid 41361833)
77. G. Smirnova, N. Muzyka, and O. Oktyabrsky Transmembrane glutathione cycling in growing Escherichia coli cells Microbiol. Res. 167 2012 166 172
78. C. Appenzeller-Herzog, and L. Ellgaard 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 2008 55 64 (Pubitemid 350115985)
79. C. Appenzeller-Herzog, J. Riemer, B. Christensen, E.S. Sorensen, and L. Ellgaard A novel disulphide switch mechanism in Ero1alpha balances ER oxidation in human cells EMBO J. 27 2008 2977 2987
80. K.M. Baker, S. Chakravarthi, K.P. Langton, A.M. Sheppard, H. Lu, and N.J. Bulleid Low reduction potential of Ero1alpha regulatory disulphides ensures tight control of substrate oxidation EMBO J. 27 2008 2988 2997
81. C.S. Sevier, H. Qu, N. Heldman, E. Gross, D. Fass, and C.A. Kaiser Modulation of cellular disulfide-bond formation and the ER redox environment by feedback regulation of Ero1 Cell 129 2007 333 344 (Pubitemid 46574965)
82. S. Kim, D.P. Sideris, C.S. Sevier, and C.A. Kaiser Balanced Ero1 activation and inactivation establishes ER redox homeostasis J. Cell Biol. 196 2012 713 725
83. K. Araki, S. Iemura, Y. Kamiya, D. Ron, K. Kato, T. Natsume, and K. Nagata Ero1-alpha and PDIs constitute a hierarchical electron transfer network of endoplasmic reticulum oxidoreductases J. Cell Biol. 202 2013 861 874
84. H.G. Hansen, J.D. Schmidt, C.L. Soltoft, T. Ramming, H.M. Geertz-Hansen, B. Christensen, E.S. Sorensen, A.S. Juncker, C. Appenzeller-Herzog, and L. Ellgaard Hyperactivity of the Ero1alpha oxidase elicits endoplasmic reticulum stress but no broad antioxidant response J. Biol. Chem. 287 2012 39513 39523
85. S. Chakravarthi, C.E. Jessop, and N.J. Bulleid The role of glutathione in disulphide bond formation and endoplasmic-reticulum-generated oxidative stress EMBO Rep. 7 2006 271 275
86. J. Birk, M. Meyer, I. Aller, H.G. Hansen, A. Odermatt, T.P. Dick, A.J. Meyer, and C. Appenzeller-Herzog Endoplasmic reticulum: reduced and oxidized glutathione revisited J. Cell Sci. 126 2013 1604 1617
87. M. van Lith, S. Tiwari, J. Pediani, G. Milligan, and N.J. Bulleid Real-time monitoring of redox changes in the mammalian endoplasmic reticulum J. Cell Sci. 124 2011 2349 2356
88. C. Hwang, A.J. Sinskey, and H.F. Lodish Oxidized redox state of glutathione in the endoplasmic reticulum Science 257 1992 1496 1502
89. K. Kojer, M. Bien, H. Gangel, B. Morgan, T.P. Dick, and J. Riemer Glutathione redox potential in the mitochondrial intermembrane space is linked to the cytosol and impacts the Mia40 redox state EMBO J. 31 2012 3169 3182
90. M. Fischer, S. Horn, A. Belkacemi, K. Kojer, C. Petrungaro, M. Habich, M. Ali, V. Kuttner, M. Bien, F. Kauff, J. Dengjel, J.M. Herrmann, and J. Riemer Protein import and oxidative folding in the mitochondrial intermembrane space of intact mammalian cells Mol. Biol. Cell 24 2013 2160 2170
91. J. Hu, L. Dong, and C.E. Outten The redox environment in the mitochondrial intermembrane space is maintained separately from the cytosol and matrix J. Biol. Chem. 283 2008 29126 29134
92. F.N. Vogtle, J.M. Burkhart, S. Rao, C. Gerbeth, J. Hinrichs, J.C. Martinou, A. Chacinska, A. Sickmann, R.P. Zahedi, and C. Meisinger Intermembrane space proteome of yeast mitochondria Mol. Cell. Proteomics 11 2012 1840 1852
93. P.I. Merksamer, A. Trusina, and F.R. Papa Real-time redox measurements during endoplasmic reticulum stress reveal interlinked protein folding functions Cell 135 2008 933 947
94. B. Morgan, D. Ezerina, T.N. Amoako, J. Riemer, M. Seedorf, and T.P. Dick Multiple glutathione disulfide removal pathways mediate cytosolic redox homeostasis Nat. Chem. Biol. 9 2013 119 125
95. H. Ostergaard, C. Tachibana, and J.R. Winther Monitoring disulfide bond formation in the eukaryotic cytosol J. Cell Biol. 166 2004 337 345 (Pubitemid 39031237)
96. C.T. Dooley, T.M. Dore, G.T. Hanson, W.C. Jackson, S.J. Remington, and R.Y. Tsien Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators J. Biol. Chem. 279 2004 22284 22293 (Pubitemid 38679425)
97. J.R. Lohman, and S.J. Remington Development of a family of redox-sensitive green fluorescent protein indicators for use in relatively oxidizing subcellular environments Biochemistry 47 2008 8678 8688