An additional function of the rough endoplasmic reticulum protein complex prolyl 3-hydroxylase 1·cartilage-associated protein·Cyclophilin B: The CXXXC motif reveals disulfide isomerase activity in vitro

Journal of Biological Chemistry

Volumn 288, Issue 44, 2013, Pages 31437-31446

  Ishikawa, Yoshihiro ^a   Bächinger, Hans Peter ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO-TERMINAL DOMAIN; CARBOXYL-TERMINAL DOMAIN; ISOMERASE ACTIVITY; MOLECULAR CHAPERONES; MULTIFUNCTIONAL COMPLEX; PROLYL-4-HYDROXYLASE; PROTEIN DISULFIDE ISOMERASES; ROUGH ENDOPLASMIC RETICULUMS;

BIOCHEMISTRY; CARTILAGE; CELL MEMBRANES; COVALENT BONDS; PEPTIDES;

ENZYME ACTIVITY;

CARTILAGE ASSOCIATED PROTEIN; CHAPERONE; CYCLOPHILIN B; OXIDOREDUCTASE; PEPTIDYLPROLYL ISOMERASE; PROLYL 3 HYDROXYLASE 1; PROTEIN DISULFIDE ISOMERASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; ROUGH ENDOPLASMIC RETICULUM;

COLLAGEN; COLLAGEN BIOSYNTHESIS; DISULFIDE; ENDOPLASMIC RETICULUM (ER); OXIDATION-REDUCTION; PROLYL 3-HYDROXYLASE; PROTEIN ISOMERASE;

AMINO ACID MOTIFS; ANIMALS; CHICKENS; CYCLOPHILINS; ENDOPLASMIC RETICULUM, ROUGH; EXTRACELLULAR MATRIX PROTEINS; HUMANS; MEMBRANE GLYCOPROTEINS; MICE; MULTIPROTEIN COMPLEXES; PEPTIDES; PROTEIN DISULFIDE-ISOMERASES; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; PROTEINS; PROTEOGLYCANS;

EID: 84886260142     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.498063     Document Type: Article

References (80)

1. Bächinger, H. P., Mizuno, K., Vranka, J., and Boudko, S. (2010) in Comprehensive Natural Products II: Chemistry and Biology (Mander, L., and Liu, H.-W. eds) pp. 469-530, Elsevier, New York
2. Bateman, J. F., Boot-Handford, R. P., and Lamandé, S. R. (2009) Genetic diseases of connective tissues: cellular and extracellular effects of ECM mutations. Nat. Rev. Genet. 10, 173-183
3. Ishikawa, Y., and Bächinger, H. P. (2013) A molecular ensemble in the rER for procollagen maturation. Biochim. Biophys. Acta 1833, 2479-2491
4. Eyre, D., and Weis, M. (2013) Calcified Tissue Int. 10.1007/s00223-013- 9723-9
5. Berg, R. A., and Prockop, D. J. (1973) The thermal transition of a non-hydroxylated form of collagen: evidence for a role for hydroxyproline in stabilizing the triple-helix of collagen. Biochem. Biophys. Res. Commun. 52, 115-120
6. Jimenez, S., Harsch, M., and Rosenbloom, J. (1973) Hydroxyproline stabilizes the triple helix of chick tendon collagen. Biochem. Biophys. Res. Commun. 52, 106-114
7. Rosenbloom, J., Harsch, M., and Jimenez, S. (1973) Hydroxyproline content determines the denaturation temperature of chick tendon collagen. Arch. Biochem. Biophys. 158, 478-484
8. Kresina, T. F., and Miller, E. J. (1979) Isolation and characterization of basement membrane collagen from human placental tissue: evidence for the presence of two genetically distinct collagen chains. Biochemistry 18, 3089-3097 (Pubitemid 9245460)
9. Kefalides, N. A. (1975) Basement membranes: structural and biosynthetic considerations. J. Invest. Dermatol. 65, 85-92
10. Gryder, R. M., Lamon, M., and Adams, E. (1975) Sequence position of 3-hydroxyproline in basement membrane collagen: isolation of glycyl-3-hydroxyprolyl 4-hydroxyproline from swine kidney. J. Biol. Chem. 250, 2470-2474
11. Kivirikko, K. I., and Myllylä, R. (1982) Posttranslational enzymes in the biosynthesis of collagen: intracellular enzymes. Methods Enzymol. 82, 245-304
12. Myllyharju, J., and Kivirikko, K. I. (2004) Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet. 20, 33-43 (Pubitemid 38032818)
13. Wilkinson, B., and Gilbert, H. F. (2004) Protein disulfide isomerase. Biochim. Biophys. Acta 1699, 35-44 (Pubitemid 38680792)
14. Hatahet, F., and Ruddock, L. W. (2009) Protein disulfide isomerase: a critical evaluation of its function in disulfide bond formation. Antioxid. Redox Signal. 11, 2807-2850
15. Ellgaard, L., and Ruddock, L. W. (2005) The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep. 6, 28-32 (Pubitemid 41710070)
16. Wilson, R., and Lees., J. F., and Bulleid, N. J. (1998) Protein disulfide isomerase acts as a molecular chaperone during the assembly of procollagen. J. Biol. Chem. 273, 9637-9643 (Pubitemid 28183052)
17. Bottomley, M. J., and Batten., M. R., Lumb, R. A., and Bulleid, N. J. (2001) Quality control in the endoplasmic reticulum: PDI mediates the ER retention of unassembled procollagen C-propeptides. Curr. Biol. 11, 1114-1118 (Pubitemid 32675763)
18. Koide, T., and Nagata, K. (2005) Collagen Biosynthesis (Brinckmann, J., Notbohm, H., and Müller, P. K., eds), pp. 85-114, Springer, Berlin
19. John, D. C., and Grant., M. E., and Bulleid, N. J. (1993) Cell-free synthesis and assembly of prolyl 4-hydroxylase: the role of the β-subunit (PDI) in preventing misfolding and aggregation of the α-subunit. EMBO J. 12, 1587-1595 (Pubitemid 23112813)
20. Myllyharju, J. (2003) Prolyl 4-hydroxylases, the key enzymes of collagen biosynthesis. Matrix Biol. 22, 15-24 (Pubitemid 36444503)
21. Gorres, K. L., and Raines, R. T. (2010) Prolyl 4-hydroxylase. Crit. Rev. Biochem. Mol. Biol. 45, 106-124
22. Vranka, J. A., Pokidysheva, E., Hayashi, L., Zientek, K., Mizuno, K., Ishikawa, Y., Maddox, K., Tufa, S., Keene, D. R., Klein, R., and Bächinger, H. P. (2010) Prolyl 3-hydroxylase 1-null mice display abnormalities in fibrillar collagen-rich tissues such as tendons, skin, and bones. J. Biol. Chem. 285, 17253-17262
23. Cabral, W. A., Chang, W., Barnes, A. M., Weis, M., and Scott., M. A., Leikin, S., Makareeva, E., Kuznetsova, N. V., Rosenbaum, K. N, Tifft, C. J., and Bulas., D. I., Kozma, C, and Smith., P. A., Eyre, D. R., and Marini, J. C. (2007) Prolyl 3-hydroxylase 1 deficiency causes a recessive metabolic bone disorder resembling lethal/severe osteogenesis imperfecta. Nat. Genet. 39, 359-365 (Pubitemid 46328489)
24. Baldridge, D., Schwarze, U., Morello, R., Lennington, J., and Bertin., T. K., Pace, J. M., Pepin, M. G., Weis, M., and Eyre., D. R., Walsh, J., Lambert, D., Green, A., Robinson, H., Michelson, M., Houge, G., Lindman, C, Martin, J., Ward, J., Lemyre, E., and Mitchell., J. J., Krakow, D., Rimoin, D. L., and Cohn., D. H., Byers, P. H., and Lee, B. (2008) CRTAP and LEPRE1 mutations in recessive osteogenesis imperfecta. Hum. Mutat. 29, 1435-1442 (Pubitemid 352774897)
25. Willaert, A., Malfait, F., Symoens, S., Gevaert, K., Kayserili, H., Megarbane, A., Mortier, G., and Leroy., J. G., Coucke, P. J., and De Paepe, A. (2009) Recessive osteogenesis imperfecta caused by LEPRE1 mutations: clinical documentation and identification of the splice form responsible for prolyl 3-hydroxylation. J. Med. Genet. 46, 233-241
26. Takagi, M., Ishii, T., Barnes, A. M., Weis, M., Amano, N, Tanaka, M., Fukuzawa, R., Nishimura, G., and Eyre., D. R., Marini, J. C, and Hasegawa, T. (2012) A novel mutation in LEPRE1 that eliminates only the KDEL ER-retrieval sequence causes non-lethal osteogenesis imperfecta. PLoS One 7, e36809
27. Ishikawa, Y., Wirz, J., Vranka, J. A., Nagata, K., and Bächinger, H. P. (2009) Biochemical characterization of the prolyl 3-hydroxylase 1·cartilage-associated protein·cyclophilin B complex. J. Biol. Chem. 284, 17641-17647
28. Vranka, J. A., and Sakai., L. Y., and Bächinger, H. P. (2004) Prolyl 3-hydroxylase 1, enzyme characterization and identification of a novel family of enzymes. J. Biol. Chem. 279, 23615-23621 (Pubitemid 38685676)
29. Marini, J. C, Cabral, W. A., and Barnes., A. M., and Chang, W. (2007) Components of the collagen prolyl 3-hydroxylation complex are crucial for normal bone development. Cell Cycle 6, 1675-1681 (Pubitemid 47327916)
30. Morello, R., Bertin, T.K., Chen, Y., Hicks, J., Tonachini, L., Monticone, M., Castagnola, P., Rauch, F., and Glorieux., F. H., Vranka, J., Bächinger, H. P., Pace, J. M., Schwarze, U., and Byers., P. H., Weis, M., Fernandes, R. J., and Eyre., D. R., Yao, Z., Boyce, B. F., and Lee, B. (2006) CRTAP is required for prolyl 3-hydroxylation and mutations cause recessive osteogenesis imperfecta. Cell 127, 291-304 (Pubitemid 44604299)
31. Ochs, R. L., and Stein., T. W. Jr., Chan, E. K., Ruutu, M., and Tan, E. M. (1996) cDNA cloning and characterization of a novel nucleolar protein. Mol. Biol. Cell 7, 1015-1024 (Pubitemid 26244200)
32. Siedler, F., Rudolph-Böhner, S., Doi, M., Musiol, H. J., and Moroder, L. (1993) Redox potentials of active-site bis(cysteinyl) fragments of thiolprotein oxidoreductases. Biochemistry 32, 7488-7495 (Pubitemid 23232323)
33. Cabrele, C, Fiori, S., Pegoraro, S., and Moroder, L. (2002) Redox-active cyclic bis(cysteinyl)peptides as catalysts for in vitro oxidative protein folding. Chem. Biol. 9, 731-740 (Pubitemid 34653068)
34. Woycechowsky, K. J., and Wittrup., K. D., and Raines, R. T. (1999) A smallmolecule catalyst of protein folding in vitro and in vivo. Chem. Biol. 6, 871-879
35. Woycechowsky, K. J., and Raines, R. T. (2003) The CXC motif: a functional mimic of protein disulfide isomerase. Biochemistry 42, 5387-5394 (Pubitemid 36560435)
36. Lambert, N, and Freedman, R. B. (1983) Structural properties of homogeneous protein disulphide-isomerase from bovine liver purified by a rapid high-yielding procedure. Biochem. J. 213, 225-234
37. Lambert, N, and Freedman, R. B. (1983) Kinetics and specificity of homogeneous protein disulphide-isomerase in protein disulphide isomerization and in thiol-protein-disulphide oxidoreduction. Biochem. J. 213, 235-243
38. Lyles, M. M., and Gilbert, H. F. (1991) Catalysis of the oxidative folding of ribonuclease A by protein disulfide isomerase: dependence of the rate on the composition of the redox buffer. Biochemistry 30, 613-619
39. Kikuchi, M., Doi, E., Tsujimoto, I., Horibe, T., and Tsujimoto, Y. (2002) Functional analysis of human P5, a protein disulfide isomerase homologue. J. Biochem. 132, 451-455
40. Ushioda, R., Hoseki, J., Araki, K., Jansen, G., and Thomas., D. Y., and Nagata, K. (2008) ERdj5 is required as a disulfide reductase for degradation of misfolded proteins in the ER. Science 321, 569-572
41. Kim, J. H, Johannes, L., Goud, B., Antony, C, and Lingwood., C. A., Daneman, R., and Grinstein, S. (1998) Noninvasive measurement of the pH of the endoplasmic reticulum at rest and during calcium release. Proc. Natl. Acad. Sci. U.S.A. 95, 2997-3002 (Pubitemid 28135843)
42. Hwang, C, and Sinskey., A. J., and Lodish, H. F. (1992) Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257, 1496-1502
43. Barnes, A. M., and Carter., E. M., Cabral, W. A., Weis, M., Chang, W., Makareeva, E., Leikin, S., Rotimi, C.N., Eyre, D.R., and Raggio., C. L., and Marini, J. C. (2010) Lack of cyclophilin B in osteogenesis imperfecta with normal collagen folding. N. Engl. J. Med. 362, 521-528
44. Choi, J. W., and Sutor., S. L., Lindquist, L., Evans, G. L., and Madden., B. J., Bergen, H. R., 3rd, Hefferan, T. E., Yaszemski, M. J., and Bram, R. J. (2009) Severe osteogenesis imperfecta in cyclophilin B-deficient mice. PLoS Genet. 5, e1000750
45. Pyott, S. M., Schwarze, U., Christiansen, H. E., and Pepin., M. G., Leistritz, D. F., Dineen, R., Harris, C., and Burton., B. K., Angle, B., Kim, K., Sussman, M. D., Weis, M., and Eyre., D. R., Russell, D. W., McCarthy, K. J., and Steiner., R. D., and Byers, P. H. (2011) Mutations in PPIB (cyclophilin B) delay type I procollagen chain association and result in perinatal lethal to moderate osteogenesis imperfecta phenotypes. Hum. Mol. Genet. 20, 1595-1609
46. Valli, M., and Barnes., A. M., Gallanti, A., Cabral, W. A., Viglio, S., and Weis., M. A., Makareeva, E., Eyre, D., Leikin, S., Antoniazzi, F., Marini, J.C., and Mottes, M. (2012) Deficiency of CRTAP in non-lethal recessive osteogenesis imperfecta reduces collagen deposition into matrix. Clin. Genet. 82, 453-459
47. Van Dijk, F. S., Nesbitt, I. M., and Nikkels., P. G., Dalton, A., Bongers, E. M., van de Kamp, J. M., Hilhorst-Hofstee, Y., Den Hollander, N. S., Lachmeijer, A. M., Marcelis, C. L., Tan-Sindhunata, G. M., van Rijn, R. R., Meijers-Heijboer, H., Cobben, J. M., and Pals, G. (2009) CRTAP mutations inlethal and severe osteogenesis imperfecta: the importance of combining biochemical and molecular genetic analysis. Eur. J. Hum. Genet. 17, 1560-1569
48. van Dijk, F. S., Nesbitt, I. M., and Zwikstra., E. H., Nikkels, P. G., Piersma, S. R., and Fratantoni., S. A., Jimenez, C. R., Huizer, M., Morsman, A. C., and Cobben., J. M., van Roij, M. H., Elting, M. W., Verbeke, J. I., Wijnaendts, L. C., Shaw, N. J., Högler, W., McKeown, C., Sistermans, E. A., Dalton, A., Meijers-Heijboer, H., and Pals, G. (2009) PPIB mutations cause severe osteogenesis imperfecta. Am. J. Hum. Genet. 85, 521-527
49. Horibe, T., Yosho, C., Okada, S., Tsukamoto, M., Nagai, H., Hagiwara, Y., Tujimoto, Y., and Kikuchi, M. (2002) The chaperone activity of protein disulfide isomerase is affected by cyclophilin B and cyclosporin A in vitro. J. Biochem. 132, 401-407
50. Ishikawa, Y., and Vranka., J. A., Boudko, S. P., Pokidysheva, E., Mizuno, K., Zientek, K., Keene, D. R., Rashmir-Raven, A. M., Nagata, K., Winand, N. J., and Bächinger, H. P. (2012) Mutation in cyclophilin B that causes hyperelastosis cutis in American Quarter Horse does not affect peptidylprolyl cis-trans isomerase activity but shows altered cyclophilin B-protein interactions and affects collagen folding. J. Biol. Chem. 287, 22253-22265
51. Kozlov, G., Bastos-Aristizabal, S., Määttänen, P., Rosenauer, A., Zheng, F., Killikelly, A., Trempe, J. F., Thomas, D. Y., and Gehring, K. (2010) Structural basis of cyclophilin B binding by the calnexin/calreticulin P-domain. J. Biol. Chem. 285, 35551-35557
52. Smith, T., and Ferreira., L. R., Hebert, C., Norris, K., and Sauk, J. J. (1995) Hsp47 and cyclophilin B traverse the endoplasmic reticulum with procollagen into pre-Golgi intermediate vesicles: a role for Hsp47 and cyclophilin B in the export of procollagen from the endoplasmic reticulum. J. Biol. Chem. 270, 18323-18328
53. Bächinger, H. P., Bruckner, P., Timpl, R., and Engel, J. (1978) The role of cis-trans isomerization of peptide bonds in the coil leads to and comes from triple helix conversion of collagen. Eur. J. Biochem. 90, 605-613
54. Bächinger, H.P., Bruckner, P., Timpl, R., Prockop, D.J., and Engel, J. (1980) Folding mechanism of the triple helix in type-III collagen and type-III pN-collagen: role of disulfide bridges and peptide bond isomerization. Eur. J. Biochem. 106, 619-632 (Pubitemid 10025788)
55. Bächinger, H. P., Morris, N. P., and Davis, J. M. (1993) Thermal stability and folding of the collagen triple helix and the effects of mutations in osteogenesis imperfecta on the triple helix of type I collagen. Am. J. Med. Genet. 45, 152-162 (Pubitemid 23030687)
56. Steinmann, B., Bruckner, P., and Superti-Furga, A. (1991) Cyclosporin A slows collagen triple-helix formation in vivo: indirect evidence for a physiologic role of peptidyl-prolyl cis-trans-isomerase. J. Biol. Chem. 266, 1299-1303 (Pubitemid 21907258)
57. Hagiwara, M., Maegawa, K., Suzuki, M., Ushioda, R., Araki, K., Matsumoto, Y., Hoseki, J., Nagata, K., and Inaba, K. (2011) Structural basis of an ERAD pathway mediated by the ER-resident protein disulfide reductase ERdj5. Mol. Cell 41, 432-444
58. Horibe, T., Gomi, M., Iguchi, D., Ito, H., Kitamura, Y., Masuoka, T., Tsujimoto, I., Kimura, T., and Kikuchi, M. (2004) Different contributions of the three CXXC motifs of human protein-disulfide isomerase-related protein to isomerase activity and oxidative refolding. J. Biol. Chem. 279, 4604-4611 (Pubitemid 38199052)
59. Satoh, M., Shimada, A., Kashiwai, A., Saga, S., and Hosokawa, M. (2005) Differential cooperative enzymatic activities of protein disulfide isomerase family in protein folding. Cell Stress Chaperones 10, 211-220 (Pubitemid 41813368)
60. Mesecke, N, Terziyska, N, Kozany, C, Baumann, F., Neupert, W., Hell, K., and Herrmann, J. M. (2005) A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell 121, 1059-1069 (Pubitemid 40884396)
61. Koehler, C. M., Beverly, K. N, and Leverich, E. P. (2006) Redox pathways of the mitochondrion. Antioxid. Redox Signal. 8, 813-822 (Pubitemid 44036499)
62. Mokranjac, D., and Neupert, W. (2009) Thirty years of protein translocation into mitochondria: unexpectedly complex and still puzzling. Biochim. Biophys. Acta 1793, 33-41
63. Wagner, K., and Mick., D. U., and Rehling, P. (2009) Protein transport machineries for precursor translocation across the inner mitochondrial membrane. Biochim. Biophys. Acta 1793, 52-59
64. Koehler, C. M. (2004) The small Tim proteins and the twin CX3C motif. TrendsBiochem. Sci. 29, 1-4 (Pubitemid 38068471)
65. Ettema, T. J., and Huynen., M. A., de Vos, W. M., and van der Oost, J. (2003) TRASH: a novel metal-binding domain predicted to be involved in heavymetal sensing, trafficking and resistance. Trends Biochem. Sci. 28, 170-173 (Pubitemid 36507153)
66. Castagnola, P., Gennari, M., Morello, R., Tonachini, L., Marin, O., Gaggero, A., and Cancedda, R. (1997) Cartilage-associated protein (CASP) is a novel developmentally regulated chick embryo protein. J. Cell Sci. 110, 1351-1359 (Pubitemid 27299931)
67. Tian, G., Xiang, S., Noiva, R., Lennarz, W. J., and Schindelin, H. (2006) The crystal structure of yeast protein disulfide isomerase suggests cooperativity between its active sites. Cell 124, 61-73 (Pubitemid 43069310)
68. Klappa, P., Koivunen, P., Pirneskoski, A., Karvonen, P., and Ruddock., L. W., Kivirikko, K. I., and Freedman, R. B. (2000) Mutations that destabilize the a'-domain of human protein-disulfide isomerase indirectly affect peptide binding. J. Biol. Chem. 275, 13213-13218 (Pubitemid 30257375)
69. Pirneskoski, A., and Ruddock., L. W., Klappa, P., Freedman, R. B., and Kivirikko., K. I., and Koivunen, P. (2001) Domains b' and a' of protein disulfide isomerase fulfill the minimum requirement for function as a subunit of prolyl 4-hydroxylase: the N-terminal domains a and b enhance this function and can be substituted in part by those of ERp57. J. Biol. Chem. 276, 11287-11293 (Pubitemid 38089317)
70. Blatch, G. L., and Lässle, M. (1999) The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays 21, 932-939 (Pubitemid 29530602)
71. DAndrea, L. D., and Regan, L. (2003) TPR proteins: the versatile helix. Trends Biochem. Sci. 28, 655-662 (Pubitemid 37500900)
72. Wouters, M. A., and Fan., S. W., and Haworth, N. L. (2010) Disulfides as redox switches: from molecular mechanisms to functional significance. Antioxid. Redox Signal. 12, 53-91
73. Araki, K., and Nagata, K. (2011) Functional in vitro analysis of the ERO1 protein and protein-disulfide isomerase pathway. J. Biol. Chem. 286, 32705-32712
74. Sato, Y., and Inaba, K. (2012) Disulfide bond formation network in the three biological kingdoms, bacteria, fungi and mammals. FEBS J. 279, 2262-2271
75. Zito, E., and Hansen., H. G., Yeo, G. S., Fujii, J., and Ron, D. (2012) Endoplasmic reticulum thiol oxidase deficiency leads to ascorbic acid depletion and noncanonical scurvy in mice. Mol. Cell 48, 39-51
76. Holster, T., Pakkanen, O., Soininen, R., Sormunen, R., Nokelainen, M., Kivirikko, K. I., and Myllyharju, J. (2007) Loss of assembly of the main basement membrane collagen, type IV, but not fibril-forming collagens and embryonic death in collagen prolyl 4-hydroxylase I-null mice. J. Biol. Chem. 282, 2512-2519 (Pubitemid 47076763)
77. a values of Escherichia coli thioredoxin. Biochemistry 36, 14985-14991 (Pubitemid 27524424)
78. Moore, E. C., Reichard, P., and Thelander, L. (1964) Enzymatic synthesis of deoxyribonucleotides. V. Purification and properties of thioredoxin reductase from Escherichia coli B. J. Biol. Chem. 239, 3445-3452
79. Hawkins, H. C., and Freedman, R. B. (1991) The reactivities and ionization properties of the active-site dithiol groups of mammalian protein disulphide-isomerase. Biochem. J. 275, 335-339
80. Lundström, J., and Holmgren, A. (1993) Determination of the reduction-oxidation potential of the thioredoxin-like domains of protein disulfide-isomerase from the equilibrium with glutathione and thioredoxin. Biochemistry 32, 6649-6655 (Pubitemid 23217134)