Glutathione redox potential in the mitochondrial intermembrane space is linked to the cytosol and impacts the Mia40 redox state

EMBO Journal

Volumn 31, Issue 14, 2012, Pages 3169-3182

  Kojer, Kerstin ^a   Bien, Melanie ^a   Gangel, Heike ^a   Morgan, Bruce ^b   Dick, Tobias P ^b   Riemer, Jan ^a  

^a Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

^b GERMAN CANCER RESEARCH CENTER   (Germany)

Author keywords

glutathione; Mia40; mitochondrial intermembrane space; porin; roGFP

Indexed keywords

GLUTATHIONE; GLUTATHIONE REDUCTASE; OXIDOREDUCTASE; OXIDOREDUCTASE MIA40; PORIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVITY; ENZYME LOCALIZATION; MITOCHONDRIAL MEMBRANE; NONHUMAN; OXIDATION REDUCTION POTENTIAL; PRIORITY JOURNAL; STEADY STATE;

CYTOSOL; GLUTATHIONE; GLUTATHIONE REDUCTASE; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; OXIDATION-REDUCTION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84864119697     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.165     Document Type: Article

References (59)

1. Antos N, Budzinska M, Kmita H (2001) An interplay between the TOM complex and porin isoforms in the yeast Saccharomyces cerevisiae mitochondria. FEBS Lett 500: 12-16 (Pubitemid 32575310)
2. Appenzeller-Herzog C (2011) Glutathione-and non-glutathionebased oxidant control in the endoplasmic reticulum. J Cell Sci 124: 847-855
3. Ballatori N, Krance SM, Marchan R, Hammond CL (2009) Plasma membrane glutathione transporters and their roles in cell physiology and pathophysiology. Mol Aspects Med 30: 13-28
4. 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: 12213-12216
5. Bien M, Longen S, Wagener N, Chwalla I, Herrmann JM, Riemer J (2010) Mitochondrial disulfide bond formation is driven by intersubunit electron transfer in Erv1 and proofread by glutathione. Mol Cell 37: 516-528
6. 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: 389-395 (Pubitemid 350074784)
7. Braun NA, Morgan B, Dick TP, Schwappach B (2010) The yeast CLC protein counteracts vesicular acidification during iron starvation. J Cell Sci 123: 2342-2350
8. Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N (2009) Importing mitochondrial proteins: machineries and mechanisms. Cell 138: 628-644
9. Chacinska A, Pfannschmidt S, Wiedemann N, Kozjak V, Sanjuan Szklarz LK, Schulze-Specking A, Truscott KN, Guiard B, Meisinger C, Pfanner N (2004) Essential role of Mia40 in import and assembly of mitochondrial intermembrane space proteins. EMBO J 23: 3735-3746 (Pubitemid 39389705)
10. Chen Z, Lash LH (1998) Evidence for mitochondrial uptake of glutathione by dicarboxylate and 2-oxoglutarate carriers. J Pharmacol Exp Ther 285: 608-618 (Pubitemid 28237440)
11. Chen Z, Putt DA, Lash LH (2000) Enrichment and functional reconstitution of glutathione transport activity from rabbit kidney mitochondria: further evidence for the role of the dicarboxylate and 2-oxoglutarate carriers in mitochondrial glutathione transport. Arch Biochem Biophys 373: 193-202 (Pubitemid 30046504)
12. Colombini M (1989) Voltage gating in the mitochondrial channel, VDAC. J Membr Biol 111: 103-111 (Pubitemid 19272950)
13. Colombini M (2007) Measurement of VDAC permeability in intact mitochondria and in reconstituted systems. Methods Cell Biol 80: 241-260
14. Cortese JD, Voglino AL, Hackenbrock CR (1991) Ionic strength of the intermembrane space of intact mitochondria as estimated with fluorescein-BSA delivered by low pH fusion. J Cell Biol 113: 1331-1340 (Pubitemid 21909761)
15. Cummings BS, Angeles R, McCauley RB, Lash LH (2000) Role of voltage-dependent anion channels in glutathione transport into yeast mitochondria. Biochem Biophys Res Commun 276: 940-944
16. Deponte M, Hell K (2009) Disulphide bond formation in the intermembrane space of mitochondria. J Biochem 146: 599-608
17. 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: 22284-22293 (Pubitemid 38679425)
18. Grabowska D, Chelstowska A (2003) The ALD6 gene product is indispensable for providing NADPH in yeast cells lacking glucose-6-phosphate dehydrogenase activity. J Biol Chem 278: 13984-13988 (Pubitemid 36799941)
19. Grant CM, MacIver FH, Dawes IW (1996) Glutathione is an essential metabolite required for resistance to oxidative stress in the yeast Saccharomyces cerevisiae. Curr Genet 29: 511-515 (Pubitemid 26166751)
20. Griffith OW, Meister A (1985) Origin and turnover of mitochondrial glutathione. Proc Natl Acad Sci USA 82: 4668-4672 (Pubitemid 16239624)
21. Gruschke S, Grone K, Heublein M, Holz S, Israel L, Imhof A, Herrmann JM, Ott M (2010) Proteins at the polypeptide tunnel exit of the yeast mitochondrial ribosome. J Biol Chem 285: 19022-19028
22. Gutscher M, Pauleau AL, Marty L, Brach T, Wabnitz GH, Samstag Y, Meyer AJ, Dick TP (2008) Real-time imaging of the intracellular glutathione redox potential. Nat Methods 5: 553-559 (Pubitemid 351761764)
23. Hanson GT, Aggeler R, Oglesbee D, Cannon M, Capaldi RA, Tsien RY, Remington SJ (2004) Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. J Biol Chem 279: 13044-13053 (Pubitemid 38445882)
24. Herrero E, Ros J, Tamarit J, Belli G (2006) Glutaredoxins in fungi. Photosynth Res 89: 127-140 (Pubitemid 44440489)
25. Herrmann JM, Riemer J (2010) The intermembrane space of mitochondria. Antioxid Redox Signal 13: 1341-1358
26. Holmgren A, Johansson C, Berndt C, Lonn ME, Hudemann C, Lillig CH (2005) Thiol redox control via thioredoxin and glutaredoxin systems. Biochem Soc Trans 33: 1375-1377 (Pubitemid 41779691)
27. 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: 29126-29134
28. Hwang C, Sinskey AJ, Lodish HF (1992) Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257: 1496-1502
29. Jessop CE, Bulleid NJ (2004) Glutathione directly reduces an oxidoreductase in the endoplasmic reticulum of mammalian cells. J Biol Chem 279: 55341-55347 (Pubitemid 40066532)
30. Jo SH, Son MK, Koh HJ, Lee SM, Song IH, Kim YO, Lee YS, Jeong KS, Kim WB, Park JW, Song BJ, Huh TL (2001) Control of mitochondrial redox balance and cellular defense against oxidative damage by mitochondrial NADP+-dependent isocitrate dehydrogenase. J Biol Chem 276: 16168-16176
31. Kloppel C, Suzuki Y, Kojer K, Petrungaro C, Longen S, Fiedler S, Keller S, Riemer J (2011) Mia40-dependent oxidation of cysteines in domain I of Ccs1 controls its distribution between mitochondria and the cytosol. Mol Biol Cell 22: 3749-3757
32. Kmita H, Antos N,Wojtkowska M, Hryniewiecka L (2004) Processes underlying the upregulation of Tom proteins in S. cerevisiae mitochondria depleted of the VDAC channel. J Bioenerg Biomembr 36: 187-193 (Pubitemid 39023636)
33. Kumar C, Igbaria A, D'Autreaux B, Planson AG, Junot C, Godat E, Bachhawat AK, Delaunay-Moisan A, Toledano MB (2011) Glutathione revisited: a vital function in iron metabolism and ancillary role in thiol-redox control. EMBO J 30: 2044-2056
34. Lee AC, Xu X, Blachly-Dyson E, Forte M, Colombini M (1998) The role of yeast VDAC genes on the permeability of the mitochondrial outer membrane. J Membr Biol 161: 173-181 (Pubitemid 28067862)
35. Lee JC, Straffon MJ, Jang TY, Higgins VJ, Grant CM, Dawes IW (2001) The essential and ancillary role of glutathione in Saccharomyces cerevisiae analysed using a grande gsh1 disruptant strain. FEMS Yeast Res 1: 57-65 (Pubitemid 34442294)
36. Lopez-Mirabal HR, Thorsen M, Kielland-Brandt MC, Toledano MB, Winther JR (2007) Cytoplasmic glutathione redox status determines survival upon exposure to the thiol-oxidant 4,4'-dipyridyl disulfide. FEMS Yeast Res 7: 391-403 (Pubitemid 46555516)
37. Mannella CA (1997) Minireview: on the structure and gating mechanism of the mitochondrial channel, VDAC. J Bioenerg Biomembr 29: 525-531 (Pubitemid 28164857)
38. McKernan TB, Woods EB, Lash LH (1991) Uptake of glutathione by renal cortical mitochondria. Arch Biochem Biophys 288: 653-663
39. Merksamer PI, Trusina A, Papa FR (2008) Real-time redox measurements during endoplasmic reticulum stress reveal interlinked protein folding functions. Cell 135: 933-947
40. 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: 1059-1069 (Pubitemid 40884396)
41. Meyer AJ, Brach T, Marty L, Kreye S, Rouhier N, Jacquot JP, 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: 973-986 (Pubitemid 350157751)
42. Meyer AJ, Dick TP (2010) Fluorescent protein-based redox probes. Antioxid Redox Signal 13: 621-650
43. Miyagi H, Kawai S, Murata K (2009) Two sources of mitochondrial NADPH in the yeast Saccharomyces cerevisiae. J Biol Chem 284: 7553-7560
44. Morgan B, Sobotta MC, Dick TP (2011) Measuring E(GSH) and H(2)O(2) with roGFP2-based redox probes. Free Radic Biol Med 51: 1943-1951
45. Naoe M, Ohwa Y, Ishikawa D, Ohshima C, Nishikawa S, Yamamoto H, Endo T (2004) Identification of Tim40 that mediates protein sorting to the mitochondrial intermembrane space. J Biol Chem 279: 47815-47821 (Pubitemid 39540931)
46. Ostergaard H, Henriksen A, Hansen FG, Winther JR (2001) Shedding light on disulfide bond formation: engineering a redox switch in green fluorescent protein. EMBO J 20: 5853-5862 (Pubitemid 33049261)
47. Ostergaard H, Tachibana C, Winther JR (2004) Monitoring disulfide bond formation in the eukaryotic cytosol. J Cell Biol 166: 337-345 (Pubitemid 39031237)
48. Outten CE, Culotta VC (2003) A novel NADH kinase is the mitochondrial source of NADPH in Saccharomyces cerevisiae. EMBO J 22: 2015-2024 (Pubitemid 36565527)
49. Outten CE, Culotta VC (2004) Alternative start sites in the Saccharomyces cerevisiae GLR1 gene are responsible for mitochondrial and cytosolic isoforms of glutathione reductase. J Biol Chem 279: 7785-7791 (Pubitemid 38294662)
50. Pai HV, Starke DW, Lesnefsky EJ, Hoppel CL, Mieyal JJ (2007) What is the functional significance of the unique location of glutaredoxin 1 (GRx1) in the intermembrane space of mitochondria? Antioxid Redox Signal 9: 2027-2033 (Pubitemid 47622345)
51. Pedrajas JR, Kosmidou E, Miranda-Vizuete A, Gustafsson JA, Wright AP, Spyrou G (1999) Identification and functional characterization of a novel mitochondrial thioredoxin system in Saccharomyces cerevisiae. J Biol Chem 274: 6366-6373 (Pubitemid 29111050)
52. Riemer J, Bulleid N, Herrmann JM (2009) Disulfide formation in the ER and mitochondria: two solutions to a common process. Science 324: 1284-1287
53. Shoshan-Barmatz V, De Pinto V, Zweckstetter M, Raviv Z, Keinan N, Arbel N (2010) VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol Aspects Med 31: 227-285
54. Summers WA, Court DA (2010) Origami in outer membrane mimetics: correlating the first detailed images of refolded VDAC with over 20 years of biochemical data. Biochem Cell Biol 88: 425-438
55. Tienson HL, Dabir DV, Neal SE, Loo R, Hasson SA, Boontheung P, Kim SK, Loo JA, Koehler CM (2009) Reconstitution of the mia40-erv1 oxidative folding pathway for the small tim proteins. Mol Biol Cell 20: 3481-3490
56. Trotter EW, Grant CM (2005) Overlapping roles of the cytoplasmic and mitochondrial redox regulatory systems in the yeast Saccharomyces cerevisiae. Eukaryot Cell 4: 392-400 (Pubitemid 40257138)
57. Waypa GB, Marks JD, Guzy R, Mungai PT, Schriewer J, Dokic D, Schumacker PT (2010) Hypoxia triggers subcellular compartmental redox signaling in vascular smooth muscle cells. Circ Res 106: 526-535
58. Zechmann B, Liou LC, Koffler BE, Horvat L, Tomasic A, Fulgosi H, Zhang Z (2011) Subcellular distribution of glutathione and its dynamic changes under oxidative stress in the yeast Saccharomyces cerevisiae. FEMS Yeast Res 11: 631-642
59. Zeth K (2010) Structure and evolution of mitochondrial outer membrane proteins of beta-barrel topology. Biochim Biophys Acta 1797: 1292-1299