1mek Citations

Structure determination of the N-terminal thioredoxin-like domain of protein disulfide isomerase using multidimensional heteronuclear 13C/15N NMR spectroscopy.

Biochemistry 35 7684-91 (1996)
Cited: 103 times
EuropePMC logo PMID: 8672469


As a first step in dissecting the structure of human protein disulfide isomerase (PDI), the structure of a fragment corresponding to the first 120 residues of its sequence has been determined using heteronuclear multidimensional NMR techniques. As expected from its primary structure homology, the fragment has the thioredoxin fold. Similarities and differences in their structures help to explain why thioredoxins are reductants, whereas PDI is an oxidant of protein thiol groups. The results confirm that PDI has a modular, multidomain structure, which will facilitate its structural and functional characterization.

Reviews - 1mek mentioned but not cited (1)

  1. Reactivity of thioredoxin as a protein thiol-disulfide oxidoreductase. Cheng Z, Zhang J, Ballou DP, Williams CH. Chem. Rev. 111 5768-5783 (2011)

Articles - 1mek mentioned but not cited (7)

  1. Prediction of catalytic residues using Support Vector Machine with selected protein sequence and structural properties. Petrova NV, Wu CH. BMC Bioinformatics 7 312 (2006)
  2. Correspondences between low-energy modes in enzymes: dynamics-based alignment of enzymatic functional families. Zen A, Carnevale V, Lesk AM, Micheletti C. Protein Sci. 17 918-929 (2008)
  3. Prediction of functional sites based on the fuzzy oil drop model. Bryliński M, Prymula K, Jurkowski W, Kochańczyk M, Stawowczyk E, Konieczny L, Roterman I. PLoS Comput. Biol. 3 e94 (2007)
  4. Automatic prediction of catalytic residues by modeling residue structural neighborhood. Cilia E, Passerini A. BMC Bioinformatics 11 115 (2010)
  5. Structural Elucidation of a Small Molecule Inhibitor of Protein Disulfide Isomerase. Kaplan A, Stockwell BR. ACS Med Chem Lett 6 966-971 (2015)
  6. In Silico Identification of Protein Disulfide Isomerase Gene Families in the De Novo Assembled Transcriptomes of Four Different Species of the Genus Conus. Figueroa-Montiel A, Ramos MA, Mares RE, Dueñas S, Pimienta G, Ortiz E, Possani LD, Licea-Navarro AF. PLoS ONE 11 e0148390 (2016)
  7. Glutaredoxin catalysis requires two distinct glutathione interaction sites. Begas P, Liedgens L, Moseler A, Meyer AJ, Deponte M. Nat Commun 8 14835 (2017)

Reviews citing this publication (27)

  1. Protein disulfide-isomerase, a folding catalyst and a redox-regulated chaperone. Wang L, Wang X, Wang CC. Free Radic. Biol. Med. 83 305-313 (2015)
  2. Novel roles for protein disulphide isomerase in disease states: a double edged sword? Parakh S, Atkin JD. Front Cell Dev Biol 3 30 (2015)
  3. S-nitrosylation of the thioredoxin-like domains of protein disulfide isomerase and its role in neurodegenerative conditions. Conway ME, Harris M. Front Chem 3 27 (2015)
  4. Protein disulfide isomerase: a promising target for cancer therapy. Xu S, Sankar S, Neamati N. Drug Discov. Today 19 222-240 (2014)
  5. The thioredoxin superfamily in oxidative protein folding. Lu J, Holmgren A. Antioxid. Redox Signal. 21 457-470 (2014)
  6. How proteins form disulfide bonds. Depuydt M, Messens J, Collet JF. Antioxid. Redox Signal. 15 49-66 (2011)
  7. Multiple catalytically active thioredoxin folds: a winning strategy for many functions. Pedone E, Limauro D, D'Ambrosio K, De Simone G, Bartolucci S. Cell. Mol. Life Sci. 67 3797-3814 (2010)
  8. Protein disulfide isomerase: a critical evaluation of its function in disulfide bond formation. Hatahet F, Ruddock LW. Antioxid. Redox Signal. 11 2807-2850 (2009)
  9. Reconsideration of an early dogma, saying "there is no evidence for disulfide bonds in proteins from archaea". Ladenstein R, Ren B. Extremophiles 12 29-38 (2008)
  10. Thioredoxins and glutaredoxins as facilitators of protein folding. Berndt C, Lillig CH, Holmgren A. Biochim. Biophys. Acta 1783 641-650 (2008)
  11. The human PDI family: versatility packed into a single fold. Appenzeller-Herzog C, Ellgaard L. Biochim. Biophys. Acta 1783 535-548 (2008)
  12. Molecular mechanisms and potential clinical significance of S-glutathionylation. Dalle-Donne I, Milzani A, Gagliano N, Colombo R, Giustarini D, Rossi R. Antioxid. Redox Signal. 10 445-473 (2008)
  13. The machinery for oxidative protein folding in thermophiles. Pedone E, Limauro D, Bartolucci S. Antioxid. Redox Signal. 10 157-169 (2008)
  14. Substrate recognition by the protein disulfide isomerases. Hatahet F, Ruddock LW. FEBS J. 274 5223-5234 (2007)
  15. Similarities and differences in the thioredoxin superfamily. Carvalho AP, Fernandes PA, Ramos MJ. Prog. Biophys. Mol. Biol. 91 229-248 (2006)
  16. Protein disulfides and protein disulfide oxidoreductases in hyperthermophiles. Ladenstein R, Ren B. FEBS J. 273 4170-4185 (2006)
  17. Protein disulfide isomerase: the structure of oxidative folding. Gruber CW, Cemazar M, Heras B, Martin JL, Craik DJ. Trends Biochem. Sci. 31 455-464 (2006)
  18. Conservation and diversity of the cellular disulfide bond formation pathways. Sevier CS, Kaiser CA. Antioxid. Redox Signal. 8 797-811 (2006)
  19. The human protein disulphide isomerase family: substrate interactions and functional properties. Ellgaard L, Ruddock LW. EMBO Rep. 6 28-32 (2005)
  20. Glutaredoxins: glutathione-dependent redox enzymes with functions far beyond a simple thioredoxin backup system. Fernandes AP, Holmgren A. Antioxid. Redox Signal. 6 63-74 (2004)
  21. Catalysis of protein folding by protein disulfide isomerase and small-molecule mimics. Kersteen EA, Raines RT. Antioxid. Redox Signal. 5 413-424 (2003)
  22. Protein disulfide isomerases exploit synergy between catalytic and specific binding domains. Freedman RB, Klappa P, Ruddock LW. EMBO Rep. 3 136-140 (2002)
  23. Ca2+ signaling and calcium binding chaperones of the endoplasmic reticulum. Michalak M, Robert Parker JM, Opas M. Cell Calcium 32 269-278 (2002)
  24. Protein folding in a specialized compartment: the endoplasmic reticulum. Zapun A, Jakob CA, Thomas DY, Bergeron JJ. Structure 7 R173-82 (1999)
  25. Protein disulfide isomerase: the multifunctional redox chaperone of the endoplasmic reticulum. Noiva R. Semin. Cell Dev. Biol. 10 481-493 (1999)
  26. Prolyl 4-hydroxylases and their protein disulfide isomerase subunit. Kivirikko KI, Myllyharju J. Matrix Biol. 16 357-368 (1998)
  27. Making and breaking disulfide bonds. Raina S, Missiakas D. Annu. Rev. Microbiol. 51 179-202 (1997)

Articles citing this publication (68)

  1. Very fast empirical prediction and rationalization of protein pKa values. Li H, Robertson AD, Jensen JH. Proteins 61 704-721 (2005)
  2. The crystal structure of yeast protein disulfide isomerase suggests cooperativity between its active sites. Tian G, Xiang S, Noiva R, Lennarz WJ, Schindelin H. Cell 124 61-73 (2006)
  3. Identification of proteins containing cysteine residues that are sensitive to oxidation by hydrogen peroxide at neutral pH. Kim JR, Yoon HW, Kwon KS, Lee SR, Rhee SG. Anal. Biochem. 283 214-221 (2000)
  4. A single dipeptide sequence modulates the redox properties of a whole enzyme family. Huber-Wunderlich M, Glockshuber R. Fold Des 3 161-171 (1998)
  5. The folding catalyst protein disulfide isomerase is constructed of active and inactive thioredoxin modules. Kemmink J, Darby NJ, Dijkstra K, Nilges M, Creighton TE. Curr. Biol. 7 239-245 (1997)
  6. Crystal structures of reduced and oxidized DsbA: investigation of domain motion and thiolate stabilization. Guddat LW, Bardwell JC, Martin JL. Structure 6 757-767 (1998)
  7. The multi-domain structure of protein disulfide isomerase is essential for high catalytic efficiency. Darby NJ, Penka E, Vincentelli R. J. Mol. Biol. 276 239-247 (1998)
  8. A conserved arginine plays a role in the catalytic cycle of the protein disulphide isomerases. Lappi AK, Lensink MF, Alanen HI, Salo KE, Lobell M, Juffer AH, Ruddock LW. J. Mol. Biol. 335 283-295 (2004)
  9. Solution structure of the bb' domains of human protein disulfide isomerase. Denisov AY, Määttänen P, Dabrowski C, Kozlov G, Thomas DY, Gehring K. FEBS J. 276 1440-1449 (2009)
  10. A protein disulfide oxidoreductase from the archaeon Pyrococcus furiosus contains two thioredoxin fold units. Ren B, Tibbelin G, de Pascale D, Rossi M, Bartolucci S, Ladenstein R. Nat. Struct. Biol. 5 602-611 (1998)
  11. Discovery of an orally active small-molecule irreversible inhibitor of protein disulfide isomerase for ovarian cancer treatment. Xu S, Butkevich AN, Yamada R, Zhou Y, Debnath B, Duncan R, Zandi E, Petasis NA, Neamati N. Proc. Natl. Acad. Sci. U.S.A. 109 16348-16353 (2012)
  12. Structural analysis of three His32 mutants of DsbA: support for an electrostatic role of His32 in DsbA stability. Guddat LW, Bardwell JC, Glockshuber R, Huber-Wunderlich M, Zander T, Martin JL. Protein Sci. 6 1893-1900 (1997)
  13. Complementation of DsbA deficiency with secreted thioredoxin variants reveals the crucial role of an efficient dithiol oxidant for catalyzed protein folding in the bacterial periplasm. Jonda S, Huber-Wunderlich M, Glockshuber R, Mössner E. EMBO J. 18 3271-3281 (1999)
  14. Active site mutations in yeast protein disulfide isomerase cause dithiothreitol sensitivity and a reduced rate of protein folding in the endoplasmic reticulum. Holst B, Tachibana C, Winther JR. J. Cell Biol. 138 1229-1238 (1997)
  15. The CXC motif: a functional mimic of protein disulfide isomerase. Woycechowsky KJ, Raines RT. Biochemistry 42 5387-5394 (2003)
  16. Structural insights into the redox-regulated dynamic conformations of human protein disulfide isomerase. Wang C, Li W, Ren J, Fang J, Ke H, Gong W, Feng W, Wang CC. Antioxid. Redox Signal. 19 36-45 (2013)
  17. Mapping of the ligand-binding site on the b' domain of human PDI: interaction with peptide ligands and the x-linker region. Byrne LJ, Sidhu A, Wallis AK, Ruddock LW, Freedman RB, Howard MJ, Williamson RA. Biochem. J. 423 209-217 (2009)
  18. Catalysing new reactions during evolution: economy of residues and mechanism. Bartlett GJ, Borkakoti N, Thornton JM. J. Mol. Biol. 331 829-860 (2003)
  19. Structure of TcpG, the DsbA protein folding catalyst from Vibrio cholerae. Hu SH, Peek JA, Rattigan E, Taylor RK, Martin JL. J. Mol. Biol. 268 137-146 (1997)
  20. Thioredoxin fold as homodimerization module in the putative chaperone ERp29: NMR structures of the domains and experimental model of the 51 kDa dimer. Liepinsh E, Baryshev M, Sharipo A, Ingelman-Sundberg M, Otting G, Mkrtchian S. Structure 9 457-471 (2001)
  21. Defining the domain boundaries of the human protein disulfide isomerases. Alanen HI, Salo KE, Pekkala M, Siekkinen HM, Pirneskoski A, Ruddock LW. Antioxid. Redox Signal. 5 367-374 (2003)
  22. Zinc-dependent dimerization of the folding catalyst, protein disulfide isomerase. Solovyov A, Gilbert HF. Protein Sci. 13 1902-1907 (2004)
  23. The acidic C-terminal domain of protein disulfide isomerase is not critical for the enzyme subunit function or for the chaperone or disulfide isomerase activities of the polypeptide. Koivunen P, Pirneskoski A, Karvonen P, Ljung J, Helaakoski T, Notbohm H, Kivirikko KI. EMBO J. 18 65-74 (1999)
  24. Functional properties of the protein disulfide oxidoreductase from the archaeon Pyrococcus furiosus: a member of a novel protein family related to protein disulfide-isomerase. Pedone E, Ren B, Ladenstein R, Rossi M, Bartolucci S. Eur. J. Biochem. 271 3437-3448 (2004)
  25. Solution structure of the glycosylated second type 2 module of fibronectin. Sticht H, Pickford AR, Potts JR, Campbell ID. J. Mol. Biol. 276 177-187 (1998)
  26. Redox-dependent domain rearrangement of protein disulfide isomerase coupled with exposure of its substrate-binding hydrophobic surface. Serve O, Kamiya Y, Maeno A, Nakano M, Murakami C, Sasakawa H, Yamaguchi Y, Harada T, Kurimoto E, Yagi-Utsumi M, Iguchi T, Inaba K, Kikuchi J, Asami O, Kajino T, Oka T, Nakasako M, Kato K. J. Mol. Biol. 396 361-374 (2010)
  27. Oligomerization properties of ERp29, an endoplasmic reticulum stress protein. Mkrtchian S, Baryshev M, Matvijenko O, Sharipo A, Sandalova T, Schneider G, Ingelman-Sundberg M. FEBS Lett. 431 322-326 (1998)
  28. The thioredoxin-like fold: hidden domains in protein disulfide isomerases and other chaperone proteins. Clissold PM, Bicknell R. Bioessays 25 603-611 (2003)
  29. Functional properties of the two redox-active sites in yeast protein disulphide isomerase in vitro and in vivo. Westphal V, Darby NJ, Winther JR. J. Mol. Biol. 286 1229-1239 (1999)
  30. Insights on a new PDI-like family: structural and functional analysis of a protein disulfide oxidoreductase from the bacterium Aquifex aeolicus. Pedone E, D'Ambrosio K, De Simone G, Rossi M, Pedone C, Bartolucci S. J. Mol. Biol. 356 155-164 (2006)
  31. Identifying and characterizing a second structural domain of protein disulfide isomerase. Darby NJ, van Straaten M, Penka E, Vincentelli R, Kemmink J. FEBS Lett. 448 167-172 (1999)
  32. The pancreas-specific protein disulphide-isomerase PDIp interacts with a hydroxyaryl group in ligands. Klappa P, Freedman RB, Langenbuch M, Lan MS, Robinson GK, Ruddock LW. Biochem. J. 354 553-559 (2001)
  33. Molecular characterization of gene sequences coding for protein disulfide isomerase (PDI) in durum wheat (Triticum turgidum ssp. durum). Ciaffi M, Paolacci AR, Dominici L, Tanzarella OA, Porceddu E. Gene 265 147-156 (2001)
  34. Photomodulation of conformational states. III. Water-soluble bis-cysteinyl-peptides with (4-aminomethyl) phenylazobenzoic acid as backbone constituent. Renner C, Behrendt R, Heim N, Moroder L. Biopolymers 63 382-393 (2002)
  35. Crystal structures of E. coli CcmG and its mutants reveal key roles of the N-terminal beta-sheet and the fingerprint region. Ouyang N, Gao YG, Hu HY, Xia ZX. Proteins 65 1021-1031 (2006)
  36. The zinc center influences the redox and thermodynamic properties of Escherichia coli thioredoxin 2. El Hajjaji H, Dumoulin M, Matagne A, Colau D, Roos G, Messens J, Collet JF. J. Mol. Biol. 386 60-71 (2009)
  37. Generating an unfoldase from thioredoxin-like domains. Forster ML, Mahn JJ, Tsai B. J. Biol. Chem. 284 13045-13056 (2009)
  38. Molecular docking studies of dithionitrobenzoic acid and its related compounds to protein disulfide isomerase: computational screening of inhibitors to HIV-1 entry. Gowthaman U, Jayakanthan M, Sundar D. BMC Bioinformatics 9 Suppl 12 S14 (2008)
  39. Solution structure of cytochrome c6 from the thermophilic cyanobacterium Synechococcus elongatus. Beissinger M, Sticht H, Sutter M, Ejchart A, Haehnel W, Rösch P. EMBO J. 17 27-36 (1998)
  40. Protein disulfide isomerase, a multifunctional protein chaperone, shows copper-binding activity. Narindrasorasak S, Yao P, Sarkar B. Biochem. Biophys. Res. Commun. 311 405-414 (2003)
  41. Yeast Mpd1p reveals the structural diversity of the protein disulfide isomerase family. Vitu E, Gross E, Greenblatt HM, Sevier CS, Kaiser CA, Fass D. J. Mol. Biol. 384 631-640 (2008)
  42. Solution structure of human immunodeficiency virus type 1 Vpr(13-33) peptide in micelles. Engler A, Stangler T, Willbold D. Eur. J. Biochem. 268 389-395 (2001)
  43. Identification of redox sensitive thiols of protein disulfide isomerase using isotope coded affinity technology and mass spectrometry. Kozarova A, Sliskovic I, Mutus B, Simon ES, Andrews PC, Vacratsis PO. J. Am. Soc. Mass Spectrom. 18 260-269 (2007)
  44. The ligand-binding b' domain of human protein disulphide-isomerase mediates homodimerization. Wallis AK, Sidhu A, Byrne LJ, Howard MJ, Ruddock LW, Williamson RA, Freedman RB. Protein Sci. 18 2569-2577 (2009)
  45. Analysis of site-specific N-glycan remodeling in the endoplasmic reticulum and the Golgi. Hang I, Lin CW, Grant OC, Fleurkens S, Villiger TK, Soos M, Morbidelli M, Woods RJ, Gauss R, Aebi M. Glycobiology 25 1335-1349 (2015)
  46. Contributions of protein disulfide isomerase domains to its chaperone activity. Sun XX, Dai Y, Liu HP, Chen SM, Wang CC. Biochim. Biophys. Acta 1481 45-54 (2000)
  47. Compact conformations of human protein disulfide isomerase. Yang S, Wang X, Cui L, Ding X, Niu L, Yang F, Wang C, Wang CC, Lou J. PLoS ONE 9 e103472 (2014)
  48. Gene regulation of alpha4beta2 nicotinic receptors: microarray analysis of nicotine-induced receptor up-regulation and anti-inflammatory effects. Hosur V, Leppanen S, Abutaha A, Loring RH. J. Neurochem. 111 848-858 (2009)
  49. Structural comparison of oxidized and reduced FKBP13 from Arabidopsis thaliana. Gopalan G, He Z, Battaile KP, Luan S, Swaminathan K. Proteins 65 789-795 (2006)
  50. Electrostatic stabilization and general base catalysis in the active site of the human protein disulfide isomerase a domain monitored by hydrogen exchange. Hernández G, Anderson JS, LeMaster DM. Chembiochem 9 768-778 (2008)
  51. Thioredoxin motif of Caenorhabditis elegans PDI-3 provides Cys and His catalytic residues for transglutaminase activity. Blaskó B, Mádi A, Fésüs L. Biochem. Biophys. Res. Commun. 303 1142-1147 (2003)
  52. Fluorometric polyethyleneglycol-peptide hybrid substrates for quantitative assay of protein disulfide isomerase. Christiansen C, St Hilaire PM, Winther JR. Anal. Biochem. 333 148-155 (2004)
  53. Increased catalytic activity of protein disulfide isomerase using aromatic thiol based redox buffers. Gough JD, Lees WJ. Bioorg. Med. Chem. Lett. 15 777-781 (2005)
  54. Description of the topographical changes associated to the different stages of the DsbA catalytic cycle. Vinci F, Couprie J, Pucci P, Quéméneur E, Moutiez M. Protein Sci. 11 1600-1612 (2002)
  55. Structural basis of redox-dependent substrate binding of protein disulfide isomerase. Yagi-Utsumi M, Satoh T, Kato K. Sci Rep 5 13909 (2015)
  56. Besnoitia besnoiti protein disulfide isomerase (BbPDI): molecular characterization, expression and in silico modelling. Marcelino E, Martins TM, Morais JB, Nolasco S, Cortes H, Hemphill A, Leitão A, Novo C. Exp. Parasitol. 129 164-174 (2011)
  57. In silico identification of the protein disulfide isomerase family from a protozoan parasite. Ramos MA, Mares RE, Magaña PD, Ortega JE, Cornejo-Bravo JM. Comput Biol Chem 32 66-70 (2008)
  58. Probing the structure of human protein disulfide isomerase by chemical cross-linking combined with mass spectrometry. Peng L, Rasmussen MI, Chailyan A, Houen G, Højrup P. J Proteomics 108 1-16 (2014)
  59. Disulfide bond formation in refolding of thermophilic fungal protein disulfide isomerase. Harada T, Kurimoto E, Tokuhiro K, Asami O, Sakai T, Nohara D, Kato K. J. Biosci. Bioeng. 91 596-598 (2001)
  60. Solution structure of a zinc substituted eukaryotic rubredoxin from the cryptomonad alga Guillardia theta. Schweimer K, Hoffmann S, Wastl J, Maier UG, Rösch P, Sticht H. Protein Sci. 9 1474-1486 (2000)
  61. Acyl cystamine: small-molecular foldase mimics accelerating oxidative refolding of disulfide-containing proteins. Wang GZ, Dong XY, Sun Y. Biotechnol. Prog. 27 377-385 (2011)
  62. Two thioredoxin-superfamily members from sea bass (Dicentrarchus labrax, L.): characterization of PDI (PDIA1) and ERp57 (PDIA3). Pinto RD, Moreira AR, Pereira PJ, dos Santos NM. Fish Shellfish Immunol. 35 1163-1175 (2013)
  63. Correlation of the 15N(i + 1), 13Calpha(i), and 1Halpha(i) Backbone Resonances in 13C/15N-Labeled Proteins by the (CO)N(CO)CAH Experiment Dijkstra K, Kroon GJA, Ab E, Scheek RM, Kemmink J. J. Magn. Reson. 125 149-152 (1997)
  64. Redox-coupled structural changes of the catalytic a' domain of protein disulfide isomerase. Inagaki K, Satoh T, Yagi-Utsumi M, Le Gulluche AC, Anzai T, Uekusa Y, Kamiya Y, Kato K. FEBS Lett. 589 2690-2694 (2015)
  65. Research Support, Non-U.S. Gov't Oxidative protein folding: recent advances and some remaining challenges. Benham A. Antioxid. Redox Signal. 5 355-357 (2003)
  66. Expression, purification and X-ray crystallographic analysis of thioredoxin from Streptomyces coelicolor. Stefankova P, Maderova J, Barak I, Kollarova M, Otwinowski Z. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 61 164-168 (2005)
  67. Crystallization and preliminary X-ray diffraction analysis of Q4DV70 from Trypanosoma cruzi, a hypothetical protein with a putative thioredoxin domain. dos Santos CR, Fessel MR, Vieira Lde C, Krieger MA, Goldenberg S, Guimarães BG, Zanchin NI, Barbosa JA. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 65 641-644 (2009)
  68. Preferential regeneration of thioredoxin from parasitic flatworm Fasciola gigantica using glutathione system. Gupta A, Pandey T, Kumar B, Tripathi T. Int. J. Biol. Macromol. 81 983-990 (2015)

Related citations provided by authors (1)

  1. Nuclear Magnetic Resonance Characterization of the N-Terminal Thioredoxin-Like Domain of Protein Disulfide Isomerase. Kemmink J, Darby NJ, Dijkstra K, Scheek RM, Creighton TE Protein Sci. 4 2587- (1995)