Redox pathways of the mitochondrion

Antioxidants and Redox Signaling

Volumn 8, Issue 5-6, 2006, Pages 813-822

  Koehler, Carla M ^a,b   Beverly, Kristen N ^a   Leverich, Edward P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUFFER; CARRIER PROTEIN; COPPER; CYTOCHROME C OXIDASE; CYTOCHROME C OXIDASE 17P; CYTOCHROME C OXIDASE 19P; DISULFIDE; GLUTAREDOXIN; GLUTATHIONE; MEMBRANE PROTEIN; METAL; PROTEIN SUBUNIT; REDUCING AGENT; SUPEROXIDE DISMUTASE; THIOREDOXIN; TRANSLOCASE OF INNER MITOCHONDRIAL MEMBRANE; TRANSLOCASE OF OUTER MITOCHONDRIAL MEMBRANE 20; UBIQUINOL CYTOCHROME C REDUCTASE; UNCLASSIFIED DRUG;

BIOSYNTHESIS; CELL MEMBRANE; CELL ORGANELLE; CELL PROTECTION; COPPER METABOLISM; CYTOSOL; DISULFIDE BOND; ENZYME ACTIVITY; ENZYME SUBUNIT; METAL BINDING; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROKARYOTE; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN TRANSPORT; REVIEW; SEQUENCE ANALYSIS;

AMINO ACID MOTIFS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; DISULFIDES; GLUTAREDOXINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; OXIDATION-REDUCTION; OXIDOREDUCTASES; THIOREDOXIN; THIOREDOXINS;

BACTERIA (MICROORGANISMS); PROKARYOTA;

EID: 33745856614     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2006.8.813     Document Type: Review

References (89)

1. Allen S, Lu H, Thornton D, and Tokatlidis K. Juxtaposition of the two distal "CX3C" motifs via intrachain disulfide bonding is essential for the folding of Tim10. J Biol Chem 278: 38505-38513, 2003.
2. Arnesano F, Balatri E, Banci L, Bertini I, and Winge DR. Folding studies of Cox17 reveal an important interplay of cysteine oxidation and copper binding. Structure 13: 713-722, 2005.
3. Balatri E, Banci L, Bertini I, Cantini F, and Ciofi-Baffoni S. Solution structure of Sco1: a thioredoxin-like protein involved in cytochrome c oxidase assembly. Structure 11: 1431-1443, 2003.
4. Barros MH, Johnson A, and Tzagoloff A. COX23, a homologue of COX17, is required for cytochrome oxidase assembly. J Biol Chem 279: 31943-31947, 2004.
5. Bauer MF, Rothbauer U, Muhlenbein N, Smith RJ, Gerbitz K, Neupert W, Brunner M, and Hofmann S. The mitochondrial TIM22 preprotein translocase is highly conserved throughout the eukaryotic kingdom. FEBS Lett 464: 41-47, 1999.
6. Benz R. Permeation of hydrophilic solutes through mitochondrial outer membranes: review on mitochondrial porins. Biochim Biophys Acta 1197: 167-196, 1994.
7. Bordo D, Djinovic K, and Bolognesi M. Conserved patterns in the Cu,Zn superoxide dismutase family. J Mol Biol 238: 366-386, 1994.
8. Carmel-Harel O and Storz G. Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu Rev Microbiol 54: 439-461, 2000.
9. Carr HS and Winge DR. Assembly of cytochrome c oxidase within the mitochondrion. Ace Chem Res 36: 309-316, 2003.
10. Chacinska A, Pfannschmidt S, Wiedemann N, Kozjak V, Sanjuan Szklarz LK, Schulze-Specking A, Truscott KN, Guiard B, Meisinger C, and Pfanner N. Essential role of Mia40 in import and assembly of mitochondrial intermembrane space proteins. EMBO J 23: 3735-3746, 2004.
11. Chen Z and Lash LH. Evidence for mitochondrial uptake of glutathione by dicarboxylate and 2-oxoglutarate carriers. J Pharmacol Exp Ther 285: 608-618, 1998.
12. Chinenov YV. Cytochrome c oxidase assembly factors with a thioredoxin fold are conserved among prokaryotes and eukaryotes. J Mol Med 78: 239-242, 2000.
13. Colbert CL, Couture MM, Eltis LD, and Bolin JT. A cluster exposed: structure of the Rieske ferredoxin from biphenyl dioxygenase and the redox properties of Rieske Fe-S proteins. Structure Fold Des 8: 1267-1278, 2000.
14. Collinson LP and Dawes IW. Isolation, characterization and overexpression of the yeast gene, GLR1, encoding glutathione reductase. Gene 156: 123-127, 1995.
15. Culotta VC, Lin SJ, Schmidt P, Klomp LW, Casareno RL, and Gitlin J. Intracellular pathways of copper trafficking in yeast and humans. Adv Exp Med Bio 448: 247-254, 1999.
16. Curran SP, Leuenberger D, Leverich EP, Hwang DK, Beverly KN, and Koehler CM. The role of Hot13p and redox chemistry in the mitochondrial TIM22 import pathway. J Biol Chem 279: 43744-43751, 2004.
17. Curran SP, Leuenberger D, Oppliger W, and Koehler CM. The Tim9p-Tim10p complex binds to the transmembrane domains of the ADP-ATP carrier. EMBO J 21: 942-953, 2002.
18. Curran SP, Leuenberger D, Schmidt E, and Koehler CM. The role of the Tim8p-Tim13p complex in a conserved import pathway for mitochondrial polytopic inner membrane proteins. J Cell Biol 158: 1017-1027, 2002.
19. Endres M, Neupert W, and Brunner M. Transport of the ADP/ATP carrier of mitochondria from the TOM complex to the TIM22.54 complex. EMBO J 18: 3214-3221, 1999.
20. Eraso JM and Kaplan S. From redox flow to gene regulation: role of the PrrC protein of Rhodobacter sphaeroides 2.4.1. Biochemistry 39: 2052-2062, 2000.
21. Field LS, Furukawa Y, O'Halloran TV, and Culotta VC. Factors controlling the uptake of yeast copper/zinc superoxide dismutase into mitochondria. J Biol Chem 278: 28052-28059, 2003.
22. Furukawa Y, Torres AS, and O'Halloran TV. Oxygen-induced maturation of SOD1: a key role for disulfide formation by the copper chaperone CCS. EMBO J 23: 2872-2881, 2004.
23. Geller BL and Winge DR. Subcellular distribution of superoxide dismutases in rat liver. Methods Enzymol 105: 105-114, 1984.
24. Giorda R, Hagiya M, Seki T, Shimonishi M, Sakai H, Michaelson J, Francavilla A, Starzl TE, and Trucco M. Analysis of the structure and expression of the augmenter of liver regeneration (ALR) gene. Mol Med 2: 97-108, 1996.
25. Gladyshev VN, Liu A, Novoselov SV, Krysan K, Sun QA, Kryukov VM, Kryukov GV, and Lou MF. Identification and characterization of a new mammalian glutaredoxin (thioltransferase), Grx2. J Biol Chem 276: 30374-30380, 2001.
26. Glerum DM, Shtanko A, and Tzagoloff A. Characterization of COX17, a yeast gene involved in copper metabolism and assembly of cytochrome oxidase. J Biol Chem 271: 14504-14509, 1996.
27. Glerum DM, Shtanko A, and Tzagoloff A. SCO1 and SCO2 act as high copy suppressors of a mitochondrial copper recruitment defect in Saccharomyces cerevisiae. J Biol Chem 271: 20531-20535, 1996.
28. Grant CM. Role of the glutathione/glutaredoxin and thioredoxin systems in yeast growth and response to stress conditions. Mol Microbiol 39: 533-541, 2001.
29. Griffith OW and Meister A. Origin and turnover of mitochondrial glutathione. Proc Natl Acad Sci USA 82: 4668-4672, 1985.
30. Herrero E and Ros J. Glutaredoxins and oxidative stress defense in yeast. Methods Enzymol 348: 136-146, 2002.
31. Hofhaus G, Lee JE, Tews I, Rosenberg B, and Lisowsky T. The N-terminal cysteine pair of yeast sulfhydryl oxidase Erv1p is essential for in vivo activity and interacts with the primary redox centre. Eur J Biochem 270: 1528-1535, 2003.
32. Holmgren A. Thioredoxin and glutaredoxin systems. J Biol Chem 264: 13963-13966, 1989.
33. Holmgren A and Aslund F. Glutaredoxin. Methods Enzymol 252: 283-292, 1995.
34. Hwang C, Sinskey AJ, and Lodish HF. Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257: 1496-1502, 1992.
35. 1 complex. Science 281: 64-71, 1998.
36. 1 complex determined by MAD phasing at 1.5 Å resolution. Structure 4: 567-579, 1996.
37. Kaplowitz N, Fernandez-Checa JC, Kannan R, Garcia-Ruiz C, Ookhtens M, and Yi JR. GSH transporters: molecular characterization and role in GSH homeostasis. Biol Chem Hoppe Seyler 377: 267-273, 1996.
38. Karniely S and Pines O. Single translation-dual destination: mechanisms of dual protein targeting in eukaryotes. EMBO Rep 6: 420-425, 2005.
39. 1-c complex. Isolation, purification, and properties. J Biol Chem 258: 13543-13551, 1983.
40. Koehler CM. New developments in mitochondrial assembly. Annu Rev Cell Dev Biol 20: 309-335, 2004.
41. Koehler CM. The small Tim proteins and the twin Cx3C motif. Trends Biochem Sci 29: 1-4, 2004.
42. Koehler CM, Leuenberger D, Merchant S, Renold A, Junne T, and Schatz G. Human deafness dystonia syndrome is a mitochondrial disease. Proc Natl Acad Sci USA 96: 2141-2146, 1999.
43. Koehler CM, Merchant S, and Schatz G. How membrane proteins travel across the mitochondrial intermembrane space. Trends Biochem Sci 24: 428-432, 1999.
44. Lamb AL, Torres AS, O'Halloran TV, and Rosenzweig AC. Heterodimeric structure of superoxide dismutase in complex with its metallochaperone. Nat Sruct Biol 8: 751-755, 2001.
45. Lange H, Lisowsky T, Gerber J, Muhlenhoff U, Kispal G, and Lill R. An essential function of the mitochondrial sulfhydryl oxidase Erv1p/ALR in the maturation of cytosolic Fe/S proteins. EMBO Rep 2: 715-720, 2001.
46. Lee J, Hofhaus G, and Lisowsky T. Erv1p from Saccharomyces cerevisiae is a FAD-linked sulfhydryl oxidase. FEBS Lett 477: 62-66, 2000.
47. Levitan A, Danon A, and Lisowsky T. Unique features of plant mitochondrial sulfhydryl oxidase. J Biol Chem 279: 20002-20008, 2004.
48. Link TA. The structures of Rieske and Rieske-type proteins. Adv Inorg Chem 47: 83-157, 1999.
49. Linke K and Jakob U. Not every disulfide lasts forever: disulfide bond formation as a redox switch. Antioxid Redox Signal 5: 425-434, 2003.
50. Lisowsky T, Weinstat-Saslow DL, Barton N, Reeders ST, and Schneider MC. A new human gene located in the PKD1 region of chromosome 16 is a functional homologue to ERV1 of yeast. Genomics 29: 690-697, 1995.
51. Lu H, Allen S, Wardleworth L, Savory P, and Tokatlidis K. Functional TIM10 chaperone assembly is redox-regulated in vivo. J Biol Chem 279: 18952-18958, 2004.
52. Luciano P, Vial S, Vergnolle MA, Dyall SD, Robinson DR, and Tokatlidis K. Functional reconstitution of the import of the yeast ADP/ATP carrier mediated by the TIM10 complex. EMBO J 20: 4099-4106, 2001.
53. Lundberg M, Johansson C, Chandra J, Enoksson M, Jacobsson G, Ljung J, Johansson M, and Holmgren A. Cloning and expression of a novel human glutaredoxin (Grx2) with mitochondrial and nuclear isoforms. J Biol Chem 276: 26269-26275, 2001.
54. Lutz T, Neupert W, and Herrmann JM. Import of small Tim proteins into the mitochondrial intermembrane space. EMBO J 22: 4400-4408, 2003.
55. 1 complex. Biochemistry 42: 13637-13645, 2003.
56. Mesecke N, Terziyska N, Kozany C, Baumann F, Neupert W, Hell K, and Herrmann JM. A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell 121: 1059-1069, 2005.
57. 1 subcomplex and the status of cysteine residues in the subunits. J Biochem 98: 1417-1425, 1985.
58. Muller EG. Thioredoxin deficiency in yeast prolongs S phase and shortens the G1 interval of the cell cycle. J Biol Chem 266: 9194-9202, 1991.
59. Nakamoto H and Bardwell JC. Catalysis of disulfide bond formation and isomerization in the Escherichia coli periplasm. Biochim Biophys Acta 1694: 111-119, 2004.
60. Naoe M, Ohwa Y, Ishikawa D, Ohshima C, Nishikawa SI, Yamamoto H, and Endo T. Identification of Tim40 that mediates protein sorting to the mitochondrial intermembrane space. J Biol Chem 279: 47815-47821, 2004.
61. Nittis T, George GN, and Winge DR. Yeast Sco1, a protein essential for cytochrome c oxidase function is a Cu(I)-binding protein. J Biol Chem 276: 42520-42526, 2001.
62. Nobrega MP, Bandeira SC, Beers J, and Tzagoloff A. Characterization of COX19, a widely distributed gene required for expression of mitochondrial cytochrome oxidase. J Biol Chem 277: 40206-40211, 2002.
63. Ohtake Y and Yabuuchi S. Molecular cloning of the gamma-glutamylcysteine synthetase gene of Saccharomyces cerevisiae. Yeast 7: 953-961, 1991.
64. Olafsdottir K and Reed DJ. Retention of oxidized glutathione by isolated rat liver mitochondria during hydroperoxide treatment. Biochim Biophys Acta 964: 377-382, 1988.
65. Østergaard H, Tachibana C, and Winther JR. Monitoring disulfide bond formation in the eukaryotic cytosol. J Cell Biol 166: 337-345, 2004.
66. Outten CE and Culotta VC. 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, 2004.
67. Paget MS and Buttner MJ. Thiol-based regulatory switches. Annu Rev Genet 37: 91-121, 2003.
68. Palumaa P, Kangur L, Voronova A, and Sillard R. Metal-binding mechanism of Cox17, a copper chaperone for cytochrome c oxidase. Biochem J 382: 307-314, 2004.
69. Pedrajas JR, Kostnidou E, Miranda-Vizuete A, Gustafsson JA, Wright AP, and Spyrou G. Identification and functional characterization of a novel mitochondrial thioredoxin system in Saccharomyces cerevisiae. J Biol Chem 274: 6366-6373, 1999.
70. Pedrajas JR, Porras P, Martínez-Galisteo E, Padilla CA, Miranda-Vizuete A, and Bárcena JA. Two isoforms of Saccharomyces cerevisiae glutaredoxin 2 are expressed in vivo and localize to different subcellular compartments. Biochem J 364: 617-623, 2002.
71. Rentzsch A, Krummeck-Weiss G, Hofer A, Bartuschka A, Ostermann K, and Rodel G. Mitochondrial copper metabolism in yeast: mutational analysis of Sco1p involved in the biogenesis of cytochrome c oxidase. Curr Genet 35: 103-108, 1999.
72. Rietsch A and Beckwith J. The genetics of disulfide bond metabolism. Annu Rev Genet 32: 163-184, 1998.
73. Rodriguez-Manzaneque MT, Tamarit J, Belli G, Ros J, and Herrero E. Grx5 is a mitochondrial glutaredoxin required for the activity of iron/sulfur enzymes. Mol Biol Cell 13: 1109-1121, 2002.
74. Roesch K, Curran SP, Tranebjaerg L, and Koehler CM. Human deafness dystonia syndrome is caused by a defect in assembly of the DDP1/TIMM8a-TIMM13 complex. Hum Mol Genet 11: 477-486, 2002.
75. Roesch K, Hynds PJ, Varga R, Tranebjaerg L, and Koehler CM. The calcium-binding aspartate/glutamate carriers, citrin and ara1ar1, are new substrates for the DDP1/TIMM8a-TIMM13 complex. Hum Mol Genet 13: 2101-2111, 2004.
76. Senkevich TG, White CL, Koonin EV, and Moss B. Complete pathway for protein disulfide bond formation encoded by poxviruses. Proc Natl Acad Sci USA 99: 6667-6672, 2002.
77. Sirrenberg C, Endres M, Folsch H, Stuart RA, Neupert W, and Brunner M. Carrier protein import into mitochondria mediated by the intermembrane proteins Tim10/Mrs11 and Tim12/Mrs5. Nature 391: 912-915, 1998.
78. Stein G and Lisowsky T. Functional comparison of the yeast scERV1 and scERV2 genes. Yeast 14: 171-180, 1998.
79. Sturtz LA, Diekert K, Jensen LT, Lill R, and Culotta VC. A fraction of yeast Cu,Zn-superoxide dismutase and Its metallochaperone, CCS, localize to the intermembrane space of mitochondria: a physiological role for SOD1 in guarding against mitochondrial oxidative damage. J Biol Chem 276: 38084-38089, 2001.
80. Tamura T, McMicken HW, Smith CV, and Hansen TN. Gene structure for mouse glutathione reductase, including a putative mitochondrial targeting signal. Biochem Biophys Res Commun 237: 419-422, 1997.
81. Terziyska N, Lutz T, Kozany C, Mokranjac D, Mesecke N, Neupert W, Herrmann JM, and Hell K. Mia40, a novel factor for protein import into the intermembrane space of mitochondria is able to bind metal ions. FEBS Lett 579: 179-184, 2005.
82. Tokatlidis K. A disulfide relay system in mitochondria. Cell 121: 965-967, 2005.
83. Trotter EW and Grant CM. Overlapping roles of the cytoplasmic and mitochondrial redox regulatory systems in the yeast Saccharomyces cerevisiae. Eukaryot Cell 4: 392-400, 2005.
84. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H, Shinzawa-Itoh K, Nakashima R, Yaono R, and Yoshikawa S. Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 Å. Science 269: 1069-1074, 1995.
85. Westerman BA, Poutsma A, Steegers EA, and Oudejans CB. C2360, a nuclear protein expressed in human proliferative cytotrophoblasts, is a representative member of a novel protein family with a conserved coiled coil-helix-coiled coil-helix domain. Genomics 83: 1094-1104, 2004.
86. Wheeler GL and Grant CM. Regulation of redox homeostasis in the yeast Saccharomyces cerevisiae. Physiol Plant 120: 12-20, 2004.
87. Williams JC, Sue C, Banting GS, Yang H, Glerum DM, Hendrickson WA, and Schon EA. Crystal structure of human SCO1: implications for redox signaling by a mitochondrial cytochrome c oxidase "assembly" protein. J Biol Chem 280: 15202-15211, 2005.
88. Zhang L, Yu L, and Yu CA. Generation of superoxide anion by succinate-cytochrome c reductase from bovine heart mitochondria. J Biol Chem 273: 33972-33976, 1998.
89. Zu Y, Fee JA, and Hirst J. Breaking and re-forming the disulfide bond at the high-potential, respiratory-type Rieske [2Fe-2S] center of Thermus thermophilus: characterization of the sulfhydryl state by protein-film voltammetry. Biochemistry 41: 14054-14065, 2002.