Conservation and diversity of the cellular disulfide bond formation pathways

Antioxidants and Redox Signaling

Volumn 8, Issue 5-6, 2006, Pages 797-811

  Sevier, Carolyn S ^a   Kaiser, Chris A ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DISULFIDE; ENZYME; ERO1 PROTEIN; ERV2 PROTEIN; FLAVOPROTEIN; PROTEIN; PROTEIN DISULFIDE ISOMERASE; SECRETORY PROTEIN; UNCLASSIFIED DRUG;

BIODIVERSITY; BIOSYNTHESIS; CYTOPLASM; DISULFIDE BOND; DNA SEQUENCE; ENDOPLASMIC RETICULUM; ENZYME SUBUNIT; EUKARYOTE; GENETIC CONSERVATION; GENOMICS; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROKARYOTE; PROTEIN METABOLISM; PROTEIN MODIFICATION; REGNUM; REVIEW; SEQUENCE HOMOLOGY; STRUCTURAL PROTEOMICS; STRUCTURE ACTIVITY RELATION;

BACTERIAL PROTEINS; CYSTEINE; DISULFIDES; ENDOPLASMIC RETICULUM; FLAVOPROTEINS; FUNGAL PROTEINS; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; OXIDOREDUCTASES; PROTEIN DISULFIDE-ISOMERASE; PROTEIN DISULFIDE-ISOMERASES; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE PROTEINS; SULFHYDRYL COMPOUNDS; THIOREDOXIN; THIOREDOXINS;

EUKARYOTA; PROKARYOTA;

EID: 33745861722     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2006.8.797     Document Type: Review

References (119)

1. Alanen HI, Williamson RA, Howard MJ, Lappi AK, Jantti HP, Rautio SM, Kellokumpu S, and Ruddock LW. Functional characterization of ERp18, a new endoplasmic reticulum-located thioredoxin superfamily member. J Biol Chem 278: 28912-28920, 2003.
2. Anelli T, Alessio M, Bachi A, Bergamelli L, Bertoli G, Camerini S, Mezghrani A, Ruffato E, Simmen T, and Sitia R. Thiol-mediated protein retention in the endoplasmic reticulum: the role of ERp44. EMBO J 22: 5015-5022, 2003.
3. Anelli T, Alessio M, Mezghrani A, Simmen T, Talamo F, Bachi A, and Sitia R. ERp44, a novel endoplasmic reticulum folding assistant of the thioredoxin family. EMBO J 21: 835-844, 2002.
4. Antoniou AN and Powis SJ. Characterization of the ERp57-Tapasin complex by rapid cellular acidification and thiol modification. Antioxid Redox Signal 5: 375-379, 2003.
5. Bader M, Muse W, Ballou DP, Gassner C, and Bardwell JC. Oxidative protein folding is driven by the electron transport system. Cell 98: 217-227, 1999.
6. Bader MW, Hiniker A, Regeimbal J, Goldstone D, Haebel PW, Riemer J, Metcalf P, and Bardwell JC. Turning a disulfide isomerase into an oxidase: DsbC mutants that imitate DsbA. EMBO J 20: 1555-1562, 2001.
7. Bader MW, Xie T, Yu CA, and Bardwell JC. Disulfide bonds are generated by quinone reduction. J Biol Chem 275: 26082-26088, 2000.
8. Banhegyi G, Lusini L, Puskas F, Rossi R, Fulceri R, Braun L, Mile V, di Simplicio P, Mandl J, and Benedetti A. Preferential transport of glutathione versus glutathione disulfide in rat liver microsomal vesicles. J Biol Chem 274: 12213-12216, 1999.
9. Bass R, Ruddock LW, Klappa P, and Freedman RB. A major fraction of endoplasmic reticulum-located glutathione is present as mixed disulfides with protein. J Biol Chem 279: 5257-5262, 2004.
10. Benayoun B, Esnard-Feve A, Castella S, Courty Y, and Esnard F. Rat seminal vesicle FAD-dependent sulfhydryl oxidase. Biochemical characterization and molecular cloning of a member of the new sulfhydryl oxidase/quiescin Q6 gene family. J Biol Chem 276: 13830-13837, 2001.
11. Benham AM, Cabibbo A, Fassio A, Bulleid N, Sitia R, and Braakman I. The CXXCXXC motif determines the folding, structure and stability of human Ero1-Lalpha. EMBO J 19: 4493-4502, 2000.
12. Bertoli G, Simmen T, Anelli T, Molteni SN, Fesce R, and Sitia R. Two conserved cysteine triads in human Ero1 alpha cooperate for efficient disulfide bond formation in the endoplasmic reticulum. J Biol Chem 279: 30047-30052, 2004.
13. Cabibbo A, Pagani M, Fabbri M, Rocchi M, Farmery MR, Bulleid NJ, and Sitia R. ERO1-L, a human protein that favors disulfide bond formation in the endoplasmic reticulum. J Biol Chem 275: 4827-4833, 2000.
14. Chakravarthi S and Bulleid NJ. Glutathione is required to regulate the formation of native disulfide bonds within proteins entering the secretory pathway. J Biol Chem 279: 39872-39879, 2004.
15. Clissold PM and Bicknell R. The thioredoxin-like fold: hidden domains in protein disulfide isomerases and other chaperone proteins. Bioessays 25: 603-611, 2003.
16. Coppock D, Kopman C, Gudas J, and Cina-Poppe DA. Regulation of the quiescence-induced genes: quiescin Q6, decorin, and ribosomal protein S29. Biochem Biophys Res Commun 269: 604-610, 2000.
17. Cunnea PM, Miranda-Vizuete A, Bertoli G, Simmen T, Damdimopoulos AE, Hermann S, Leinonen S, Huikko MP, Gustafsson JA, Sitia R, and Spyrou G. ERdj5, an endoplasmic reticulum (ER)-resident protein containing DnaJ and thioredoxin domains, is expressed in secretory cells or following ER stress. J Biol Chem 278: 1059-1066, 2003.
18. Cuozzo JW and Kaiser CA. Competition between glutathione and protein thiols for disulphide-bond formation. Nat Cell Biol 1: 130-135, 1999.
19. Darby NJ and Creighton TE. Functional properties of the individual thioredoxin-like domains of protein disulfide isomerase. Biochemistry 34: 11725-11735, 1995.
20. Darby NJ, Penka E, and Vincentelli R. The multi-domain structure of protein disulfide isomerase is essential for high catalytic efficiency. J Mol Biol 276: 239-247, 1998.
21. Desilva MG, Lu J, Donadel G, Modi WS, Xie H, Notkins AL, and Lan MS. Characterization and chromosomal localization of a new protein disulfide isomerase, PDIp, highly expressed in human pancreas. DNA Cell Biol 15: 9-16, 1996.
22. Desilva MG, Notkins AL, and Lan MS. Molecular characterization of a pancreas-specific protein disulfide isomerase, PDIp. DNA Cell Biol 16: 269-274, 1997.
23. Dixon DP, Van Lith M, Edwards R, and Benham A. Cloning and initial characterization of the Arabidopsis thaliana endoplasmic reticulum oxidoreductins. Antioxid Redox Signal 5: 389-396, 2003.
24. Ellgaard L and Frickel EM. Calnexin, calreticulin, and ERp57: teammates in glycoprotein folding. Cell Biochem Biophys 39: 223-247, 2003.
25. Ellgaard L and Ruddock LW. The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep 6: 28-32, 2005.
26. Farrell SR and Thorpe C. Augmenter of liver regeneration: a flavin-dependent sulfhydryl oxidase with cytochrome c reductase activity. Biochemistry 44: 1532-1541, 2005.
27. Ferrari DM, Nguyen Van P, Kratzin HD, and Soling HD. ERp28, a human endoplasmic-reticulum-lumenal protein, is a member of the protein disulfide isomerase family but lacks a CXXC thioredoxin-box motif. Eur J Biochem 255: 570-579, 1998.
28. Francavilla A, Hagiya M, Porter KA, Polimeno L, Ihara I, and Starzl TE. Augmenter of liver regeneration: its place in the universe of hepatic growth factors. Hepatology 20: 747-757, 1994.
29. Frand AR and Kaiser CA. The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol Cell 1: 161-170, 1998.
30. Frand AR and Kaiser CA. Ero1p oxidizes protein disulfide isomerase in a pathway for disulfide bond formation in the endoplasmic reticulum. Mol Cell 4: 469-477, 1999.
31. Frand AR and Kaiser CA. Two pairs of conserved cysteines are required for the oxidative activity of Ero1p in protein disulfide bond formation in the endoplasmic reticulum. Mol Biol Cell 11: 2833-2843, 2000.
32. Freedman RB, Klappa P, and Ruddock LW. Protein disulfide isomerases exploit synergy between catalytic and specific binding domains. EMBO Rep 3: 136-140, 2002.
33. Gerber J, Muhlenhoff U, Hofhaus G, Lill R, and Lisowsky T. Yeast ERV2p is the first microsomal FAD-linked sulfhydryl oxidase of the Erv1p/Alrp protein family. J Biol Chem 276: 23486-23491, 2001.
34. Gess B, Hofbauer KH, Wenger RH, Lohaus C, Meyer HE, and Kurtz A. The cellular oxygen tension regulates expression of the endoplasmic oxidoreductase ERO1-Lalpha. Eur J Biochem 270: 2228-2235, 2003.
35. Grauschopf U, Fritz A, and Glockshuber R. Mechanism of the electron transfer catalyst DsbB from Escherichia coli. EMBO J 22: 3503-3513, 2003.
36. Gross E, Kastner DB, Kaiser CA, and Fass D. Structure of Ero1p, source of disulfide bonds for oxidative protein folding in the cell. Cell 117: 601-610, 2004.
37. Gross E, Sevier CS, Vala A, Kaiser CA, and Fass D. A new FAD-binding fold and intersubunit disulfide shuttle in the thiol oxidase Erv2p. Nat Struct Biol 9: 61-67, 2002.
38. Guilhot C, Jander G, Martin NL, and Beckwith J. Evidence that the pathway of disulfide bond formation in Escherichia coli involves interactions between the cysteines of DsbB and DsbA. Proc Natl Acad Sci USA 92: 9895-9899, 1995.
39. Gunther R, Srinivasan M, Haugejorden S, Green M, Ehbrecht IM, and Kuntzel H. Functional replacement of the Saccharomyces cerevisiae Trg1/Pdi1 protein by members of the mammalian protein disulfide isomerase family. J Biol Chem 268: 7728-7732, 1993.
40. 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, and Ron D. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11: 619-633, 2003.
41. Haugstetter J, Blicher T, and Ellgaard L. Identification and characterization of a novel thioredoxin-related transmembrane protein of the endoplasmic reticulum. J Biol Chem 280: 8371-8380, 2005.
42. Hayano T and Kikuchi M. Molecular cloning of the cDNA encoding a novel protein disulfide isomerase-related protein (PDIR). FEBS Lett 372: 210-214, 1995.
43. Higo T, Hattori M, Nakamura T, Natsume T, Michikawa T, and Mikoshiba K. Subtype-specific and ER lumenal environment-dependent regulation of inositol 1,4,5-trisphosphate receptor type 1 by ERp44. Cell 120: 85-98, 2005.
44. Hiniker A and Bardwell JC. Disulfide bond isomerization in prokaryotes. Biochemistry 42: 1179-1185, 2003.
45. Hiniker A and Bardwell JC. Disulfide relays between and within proteins: the Ero1p structure. Trends Biochem Sci 29: 516-519, 2004.
46. 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.
47. Hoober KL, Glynn NM, Burnside J, Coppock DL, and Thorpe C. Homology between egg white sulfhydryl oxidase and quiescin Q6 defines a new class of flavin-linked sulfhydryl oxidases. J Biol Chem 274: 31759-31762, 1999.
48. rd, and Thorpe C. A sulfhydryl oxidase from chicken egg white. J Biol Chem 271: 30510-30516, 1996.
49. Hosoda A, Kimata Y, Tsuru A, and Kohno K. JPDI, a novel endoplasmic reticulum-resident protein containing both a BiP-interacting J-domain and thioredoxin-like motifs. J Biol Chem 278: 2669-2676, 2003.
50. Hwang C, Sinskey AJ, and Lodish HF. Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257: 1496-1502, 1992.
51. Inaba K, Takahashi YH, Fujieda N, Kano K, Miyoshi H, and Ito K. DsbB elicits a red-shift of bound ubiquinone during the catalysis of DsbA oxidation. J Biol Chem 279: 6761-6768, 2004.
52. Inaba K, Takahashi YH, and Ito K. Reactivities of quinone-free DsbB from Escherichia coli. J Biol Chem 280: 33035-33044, 2005.
53. Jessop CE and Bulleid NJ. Glutathione directly reduces an oxidoreductase in the endoplasmic reticulum of mammalian cells. J Biol Chem 279: 55341-55347, 2004.
54. Kadokura H, Katzen F, and Beckwith J. Protein disulfide bond formation in prokaryotes. Annu Rev Biochem 72: 111-135, 2003.
55. Katti SK, LeMaster DM, and Eklund H. Crystal structure of thioredoxin from Escherichia coli at 1.68 A resolution. J Mol Biol 212: 167-184, 1990.
56. Kemmink J, Darby NJ, Dijkstra K, Nilges M, and Creighton TE. Structure determination of the N-terminal thioredoxin-like domain of protein disulfide isomerase using multidimensional heteronuclear 13C/15N NMR spectroscopy. Biochemistry 35: 7684-7691, 1996.
57. Kemmink J, Dijkstra K, Mariani M, Scheek RM, Penka E, Nilges M, and Darby NJ. The structure in solution of the b domain of protein disulfide isomerase. J Biomol NMR 13: 357-368, 1999.
58. Kettner K, Blomberg A, and Rodel G. Schizosaccharomyces pombe ER oxidoreductin-like proteins SpEro1a p and SpEro1b p. Yeast 21: 1035-1044, 2004.
59. Kimura T, Hosoda Y, Kitamura Y, Nakamura H, Horibe T, and Kikuchi M. Functional differences between human and yeast protein disulfide isomerase family proteins. Biochem Biophys Res Commun 320: 359-365, 2004.
60. Kishigami S, Akiyama Y, and Ito K. Redox states of DsbA in the periplasm of Escherichia coli. FEBS Lett 364: 55-58, 1995.
61. Kishigami S, Kanaya E, Kikuchi M, and Ito K. DsbA-DsbB interaction through their active site cysteines. Evidence from an odd cysteine mutant of DsbA. J Biol Chem 270: 17072-17074, 1995.
62. Knoblach B, Keller BO, Groenendyk J, Aldred S, Zheng J, Lemire BD, Li L, and Michalak M. ERp19 and ERp46, new members of the thioredoxin family of endoplasmic reticulum proteins. Mol Cell Proteomics 2: 1104-1119, 2003.
63. Kobayashi T and Ito K. Respiratory chain strongly oxidizes the CXXC motif of DsbB in the Escherichia coli disulfide bond formation pathway. EMBO J 18: 1192-1198, 1999.
64. Kobayashi T, Kishigami S, Sone M, Inokuchi H, Mogi T, and Ito K. Respiratory chain is required to maintain oxidized states of the DsbA-DsbB disulfide bond formation system in aerobically growing Escherichia coli cells. Proc Natl Acad Sci USA 94: 11857-11862, 1997.
65. Kramer B, Ferrari DM, Klappa P, Pohlmann N, and Soling HD. Functional roles and efficiencies of the thioredoxin boxes of calcium-binding proteins 1 and 2 in protein folding. Biochem J 357: 83-95, 2001.
66. Laboissiere MC, Sturley SL, and Raines RT. The essential function of protein-disulfide isomerase is to unscramble non-native disulfide bonds. J Biol Chem 270: 28006-28009, 1995.
67. 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.
68. Lee J, Hofhaus G, and Lisowsky T. Erv1p from Saccharomyces cerevisiae is a FAD-linked sulfhydryl oxidase. FEBS Lett 477: 62-66, 2000.
69. Levitan A, Danon A, and Lisowsky T. Unique features of plant mitochondrial sulfhydryl oxidase. J Biol Chem 279: 20002-20008, 2004.
70. Li Y, Liu W, Xing G, Tian C, Zhu Y, and He F. Direct association of hepatopoietin with thioredoxin constitutes a redox signal transduction in activation of AP-1/NF-kappaB. Cell Signal 17: 985-996, 2005.
71. 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.
72. Liu F, Rong YP, Zeng LC, Zhang X, and Han ZG. Isolation and characterization of a novel human thioredoxin-like gene hTLP19 encoding a secretory protein. Gene 315: 71-78, 2003.
73. Martin JL. Thioredoxin-a fold for all reasons. Structure 3: 245-250, 1995.
74. Martin JL, Bardwell JC, and Kuriyan J. Crystal structure of the DsbA protein required for disulphide bond formation in vivo. Nature 365: 464-468, 1993.
75. Matsuo Y, Akiyama N, Nakamura H, Yodoi J, Noda M, and Kizaka-Kondoh S. Identification of a novel thioredoxin-related transmembrane protein. J Biol Chem 276: 10032-10038, 2001.
76. Matsuo Y, Nishinaka Y, Suzuki S, Kojima M, Kizaka-Kondoh S, Kondo N, Son A, Sakakura-Nishiyama J, Yamaguchi Y, Masutani H, Ishii Y, and Yodoi J. TMX, a human transmembrane oxidoreductase of the thioredoxin family: the possible role in disulfide-linked protein folding in the endoplasmic reticulum. Arch Biochem Biophys 423: 81-87, 2004.
77. May D, Itin A, Gal O, Kalinski H, Feinstein E, and Keshet E. Ero1-L alpha plays a key role in a HIF-1-mediated pathway to improve disulfide bond formation and VEGF secretion under hypoxia: implication for cancer. Oncogene 24: 1011-1020, 2005.
78. McCarthy AA, Haebel PW, Torronen A, Rybin V, Baker EN, and Metcalf P. Crystal structure of the protein disulfide bond isomerase, DsbC, from Escherichia coli. Nat Struct Biol 1: 196-199, 2000.
79. Meng X, Zhang C, Chen J, Peng S, Cao Y, Ying K, Xie Y, and Mao Y Cloning and identification of a novel cDNA coding thioredoxin-related transmembrane protein 2. Biochem Genet 41: 99-106, 2003.
80. 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.
81. Mezghrani A, Fassio A, Benham A, Simmen T, Braakman I, and Sitia R. Manipulation of oxidative protein folding and PDI redox state in mammalian cells. EMBO J 20: 6288-6296, 2001.
82. Molteni SN, Fassio A, Ciriolo MR, Filomeni G, Pasqualetto E, Fagioli C, and Sitia R. Glutathione limits Ero1-dependent oxidation in the endoplasmic reticulum. J Biol Chem 279: 32667-32673, 2004.
83. Nakamoto H and Bardwell JC. Catalysis of disulfide bond formation and isomerization in the Escherichia coli periplasm. Biochim Biophys Acta 1694: 111-119, 2004.
84. Norgaard P, Westphal V, Tachibana C, Alsoe L, Holst B, and Winther JR. Functional differences in yeast protein disulfide isomerases. J Cell Biol 152: 553-562, 2001.
85. Ostrowski MC and Kistler WS. Properties of a flavoprotein sulfhydryl oxidase from rat seminal vesicle secretion. Biochemistry 19: 2639-2645, 1980.
86. Pagani M, Fabbri M, Benedetti C, Fassio A, Pilati S, Bulleid NJ, Cabibbo A, and Sitia R. Endoplasmic reticulum oxidoreductin 1-1beta (ERO1-Lbeta), a human gene induced in the course of the unfolded protein response. J Biol Chem 275: 23685-23692, 2000.
87. Pittman MS, Corker H, Wu G, Binet MB, Moir AJ, and Poole RK. Cysteine is exported from the Escherichia coli cytoplasm by CydDC, an ATP-binding cassette-type transporter required for cytochrome assembly. J Biol Chem 111: 49841-49849, 2002.
88. Pollard MG, Travers KJ, and Weissman JS. Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Mol Cell 1: 171-182, 1998.
89. Porat A, Cho SH, and Beckwith J. The unusual transmembrane electron transporter DsbD and its homologues: a bacterial family of disulfide reductases. Res Microbiol 155: 617-622, 2004.
90. Raczko AM, Bujnicki JM, Pawlowski M, Godlewska R, Lewandowska M, and Jagusztyn-Krynicka EK. Characterization of new DsbB-like thiol-oxidoreductases of Campylobacter jejuni and Helicobacter pylori and classification of the DsbB family based on phylogenomic, structural and functional criteria. Microbiology 151: 219-231, 2005.
91. Raje S and Thorpe C. Inter-domain redox communication in flavoenzymes of the quiescin/sulfhydryl oxidase family: role of a thioredoxin domain in disulfide bond formation. Biochemistry 42: 4560-4568, 2003.
92. Regeimbal J and Bardwell JC. DsbB catalyzes disulfide bond formation de novo. J Biol Chem 277: 32706-32713, 2002.
93. Rozhkova A, Stirnimann CU, Frei P, Grauschopf U, Brunisholz R, Grutter MG, Capitani G, and Glockshuber R. Structural basis and kinetics of inter- and intramolecular disulfide exchange in the redox catalyst DsbD. EMBO J 23: 1709-1719, 2004.
94. Scherens B, Dubois E, and Messenguy F. Determination of the sequence of the yeast YCL313 gene localized on chromosome III. Homology with the protein disulfide isomerase (PDI gene product) of other organisms. Yeast 7: 185-193, 1991.
95. Senkevich TG, White CL, Koonin EV, and Moss B. A viral member of the ERV1/ALR protein family participates in a cytoplasmic pathway of disulfide bond formation. Proc Natl Acad Sci USA 97: 12068-12073, 2000.
96. 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.
97. Sevier CS, Cuozzo JW, Vala A, Aslund F, and Kaiser CA. A flavoprotein oxidase defines a new endoplasmic reticulum pathway for biosynthetic disulphide bond formation. Nat Cell Biol 3: 874-882, 2001.
98. Sevier CS, Kadokura H, Tam VC, Beckwith J, Fass D, and Kaiser CA. The prokaryotic enzyme DsbB may share key structural features with eukaryotic disulfide bond forming oxidoreductases. Protein Sci 14: 1630-1642, 2005.
99. Sevier CS and Kaiser CA. Disulfide transfer between two conserved cysteine pairs imparts selectivity to protein oxidation by Ero1. Mol Biol Cell Epub ahead of print. Feb 2006.
100. Sinha S, Langford PR, and Kroll JS. Functional diversity of three different DsbA proteins from Neisseria meningitidis. Microbiology 150: 2993-3000, 2004.
101. Solovyov A, Xiao R, and Gilbert HF. Sulfhydryl oxidation, not disulfide isomerization, is the principal function of protein disulfide isomerase in yeast Saccharomyces cerevisiae. J Biol Chem 279: 34095-34100, 2004.
102. Stein G and Lisowsky T. Functional comparison of the yeast scERV1 and scERV2 genes. Yeast 14: 171-180, 1998.
103. Sullivan DC, Huminiecki L, Moore JW, Boyle JJ, Poulsom R, Creamer D, Barker J, and Bicknell R. EndoPDI, a novel protein-disulfide isomerase-like protein that is preferentially expressed in endothelial cells acts as a stress survival factor. J Biol Chem 278: 47079-47088, 2003.
104. Tachibana C and Stevens TH. The yeast EUG1 gene encodes an endoplasmic reticulum protein that is functionally related to protein disulfide isomerase. Mol Cell Biol 12: 4601-4611, 1992.
105. Tachikawa H, Funahashi W, Takeuchi Y, Nakanishi H, Nishihara R, Katoh S, Gao XD, Mizunaga T, and Fujimoto D. Overproduction of Mpd2p suppresses the lethality of protein disulfide isomerase depletion in a CXXC sequence dependent manner. Biochem Biophys Res Commun 239: 710-714, 1997.
106. Tachikawa H, Takeuchi Y, Funahashi W, Miura T, Gao XD, Fujimoto D, Mizunaga T, and Onodera K. Isolation and characterization of a yeast gene, MPD1, the overexpression of which suppresses inviability caused by protein disulfide isomerase depletion. FEBS Lett 369: 212-216, 1995.
107. Takahashi YH, Inaba K, and Ito K. Characterization of the menaquinone-dependent disulfide bond formation pathway of Escherichia coli. J Biol Chem 279: 47057-47065, 2004.
108. Tan JT and Bardwell JC. Key players involved in bacterial disulfide-bond formation. Chembiochem 5: 1479-1487, 2004.
109. Thorpe C, Hoober KL, Raje S, Glynn NM, Burnside J, Turi GK, and Coppock DL. Sulfhydryl oxidases: emerging catalysts of protein disulfide bond formation in eukaryotes. Arch Biochem Biophys 405: 1-12, 2002.
110. Tinsley CR, Voulhoux R, Beretti JL, Tommassen J, and Nassif X. Three homologues, including two membrane-bound proteins, of the disulfide oxidoreductase DsbA in Neisseria meningitidis: effects on bacterial growth and biogenesis of functional type IV pili. J Biol Chem 279: 27078-27087, 2004.
111. Tu BP, Ho-Schleyer SC, Travers KJ, and Weissman JS. Biochemical basis of oxidative protein folding in the endoplasmic reticulum. Science 290: 1571-1574, 2000.
112. Tu BP and Weissman JS. The FAD- and O(2)-dependent reaction cycle of Ero1-mediated oxidative protein folding in the endoplasmic reticulum. Mol Cell 10: 983-994, 2002.
113. Tu BP and Weissman JS. Oxidative protein folding in eukaryotes: mechanisms and consequences. J Cell Biol 164: 341-346, 2004.
114. Vala A, Sevier CS, and Kaiser CA. Structural determinants of substrate access to the disulfide oxidase Erv2p. J Mol Biol 354: 952-966, 2005.
115. van Lith M, Hartigan N, Hatch J, and Benham AM. PDILT, a divergent testis-specific protein disulfide isomerase with a non-classical SXXC motif that engages in disulfide-dependent interactions in the endoplasmic reticulum. J Biol Chem 280: 1376-1383, 2005.
116. Wang Q and Chang A. Eps1, a novel PDI-related protein involved in ER quality control in yeast. EMBO J 18: 5972-5982, 1999.
117. White CL, Senkevich TG, and Moss B. Vaccinia virus G4L glutaredoxin is an essential intermediate of a cytoplasmic disulfide bond pathway required for virion assembly. J Virol 76: 467-472, 2002.
118. Wilkinson B and Gilbert HF. Protein disulfide isomerase. Biochim Biophys Acta 1699: 35-44, 2004.
119. Wittke I, Wiedemeyer R, Pillmann A, Savelyeva L, Westermann F, and Schwab M. Neuroblastoma-derived sulfhydryl oxidase, a new member of the sulfhydryl oxidase/Quiescin6 family, regulates sensitization to interferon gamma-induced cell death in human neuroblastoma cells. Cancer Res 63: 7742-7752, 2003.