The flexibility and dynamics of protein disulfide isomerase

Proteins: Structure, Function and Bioinformatics

Volumn 84, Issue 12, 2016, Pages 1776-1785

  Römer, Rudolf A ^a   Wells, Stephen A ^b   Emilio Jimenez Roldan, J ^a   Bhattacharyya, Moitrayee ^c,e   Vishweshwara, Saraswathi ^c   Freedman, Robert B ^d  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b University of Bath   (United Kingdom)

^c INDIAN INSTITUTE OF SCIENCE   (India)

^d UNIVERSITY OF WARWICK   (United Kingdom)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

and computer simulation; dynamics of biomolecules; large domain motion; modeling; PDI; protein dynamics; protein flexibility; theory

Indexed keywords

PROTEIN DISULFIDE ISOMERASE; PDI1 PROTEIN, S CEREVISIAE; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME STABILITY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; BINDING SITE; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION; PLIABILITY; PROTEIN SECONDARY STRUCTURE; SACCHAROMYCES CEREVISIAE; STRUCTURE ACTIVITY RELATION; THERMODYNAMICS;

BINDING SITES; GENE EXPRESSION; MOLECULAR DYNAMICS SIMULATION; PLIABILITY; PROTEIN BINDING; PROTEIN DISULFIDE-ISOMERASES; PROTEIN FOLDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, SECONDARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS;

EID: 84990029002     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.25159     Document Type: Article

References (53)

1. Henzler-Wildman K, Kern D. Dynamic personalities of proteins. Nature 2007;450:964–972.
2. Tzeng SR, Kalodimos CG. Protein activity regulation by conformational entropy. Nature 2012;488:236–240.
3. Finnis CJA, Payne T, Hay J, Dodsworth N, Wilkinson D, Morton P, Saxton MJ, Tooth DJ, Evans RW, Goldenberg H, Scheiber-Mojdehkar B, Ternes N, Sleep D. High-level production of animal-free recombinant transferrin from S. cerevisiae. Microb Cell Fact 2010;9:87.
4. Hatahet F, Ruddock LW. Protein disulfide isomerase: a critical evaluation of its function in disulfide bond formation. Antioxid Redox Signal 2009;11:2807–2850.
5. Kozlov G, Maattanen P, Thomas DY, Gehring K. A structural overview of the PDI family of proteins. FEBS J 2010;277:3924–3936.
6. Bulleid NJ, Ellgaard L. Multiple ways to make disulfides. Trends Biochem Sci 2011;36:485–492.
7. Braakman I, Bulleid NJ. Protein folding and modification in the mammalian endoplasmic reticulum. Annu Rev Biochem 2011;80:71–99.
8. Feige MJ, Hendershot LM. Disulfide bonds in ER protein folding and homeostasis. Curr Opin Cell Biol 2011;23:167–175.
9. Tian G, Xiang S, Noiva R, Lennarz WJ, Schindelin H. The crystal structure of yeast protein disulfide isomerase suggests cooperativity between its active sites. Cell 2006;124:61–73.
10. Nguyen VD, Wallis K, Howard MJ, Haapalainen AM, Salo KE, Saaranen MJ, Sidhu A, Wierenga RK, Freedman RB, Ruddock LW, Williamson RA. Alternative conformations of the x region of human protein disulphide-isomerase modulate exposure of the substrate binding b' domain. J Mol Biol 2008;383:1144–1155.
11. Byrne LJ, Sidhu A, Wallis AK, Ruddock LW, Freedman RB, Howard MJ, Williamson RA. Mapping of the ligand-binding site on the b' domain of human PDI: interaction with peptide ligands and the x-linker region. Biochem J 2009;423:209–217.
12. Wang C, Li W, Ren J, Fang J, Ke H, Gong W, Feng W, Wang CC. Structural insights into the redox-regulated dynamic conformations of human protein disulfide isomerase. Antioxid Redox Signal 2012; 120709084834006.
13. Freedman RB, Gane PJ, Hawkins HC, Hlodan R, McLaughlin SH, Parry JWL. Experimental and theoretical analyses of the domain architecture of mammalian protein disulphide-isomerase. Biol Chem 1998;379:321–328.
14. Wang C, Chen S, Wang X, Wang L, Wallis AK, Freedman RB, Wang CC. Plasticity of human protein disulfide isomerase: evidence for mobility around the x-linker region and its functional significance. J Biol Chem 2010;285:26788–26797.
15. Nakasako M, Maeno A, Kurimoto E, Harada T, Yamaguchi Y, Oka T, Takayama Y, Iwata A, Kato K. Redox-dependent domain rearrangement of protein disulfide isomerase from a thermophilic fungus. Biochemistry 2010;49:6953–6962.
16. 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. Redox-dependent domain rearrangement of protein disulfide isomerase coupled with exposure of its substrate-binding hydrophobic surface. J Mol Biol 2010;396:361–374.
17. Peng L, Rasmussen MI, Chailyan A, Houen G, Højrup P. Probing the structure of human protein disulfide isomerase by chemical cross-linking combined with mass spectrometry. J Proteomics 2014;108:1–16.
18. Tian G, Kober FX, Lewandrowski U, Sickmann A, Lennarz WJ, Schindelin H. The catalytic activity of protein-disulfide isomerase requires a conformationally flexible molecule. J Biol Chem 2008;283:33630–33640.
19. Jimenez-Roldan JE, Freedman RB, Römer RA, Wells SA. Rapid simulation of protein motion: merging flexibility, rigidity and normal mode analyses. Phys Biol 2012;9:016008.
20. Thorpe MF, Lei M, Rader AJ, Jacobs DJ, Kuhn LA. Protein flexibility and dynamics using constraint theory. J Mol Graph Model 2001;19:60–69.
21. Krebs WG, Alexandrov V, Wilson CA, Echols N, Yu H, Gerstein M. Normal mode analysis of macromolecular motions in a database framework: developing mode concentration as a useful classifying statistic. Proteins 2002;48:682–695.
22. Tama F, Sanejouand Y. Conformational change of proteins arising from normal mode calculations. Prot Eng 2001;14:1–6.
23. Suhre K, Sanejouand YH. ElNemo: a normal mode web server for protein movement analysis and the generation of templates for molecular replacement. Nucleic Acids Res 2004;32:610–614.
24. Suhre K, Sanejouand Y. On the potential of normal mode analysis for solving difficult molecular replacement problems. Acta Cryst D 2004;60:796–799.
25. Dykeman EC, Sankey OF. Normal mode analysis and applications in biological physics. J Phys Condens Matter 2010;22:423202.
26. Wells SA, Menor S, Hespenheide BM, Thorpe MF. Constrained geometric simulation of diffusive motion in proteins. Phys Biol 2005;2:S127–S136.
27. Jolley CC, Wells SA, Hespenheide BM, Thorpe MF, Fromme P. Docking of photosystem I subunit C using a constrained geometric simulation. J Am Chem Soc 2006;128:8803–8812.
28. Heal JW, Wells SA, Blindauer CA, Freedman RB, Römer RA. Characterization of folding cores in the cyclophilin A-cyclosporin A complex. Biophys J 2015;108:1739–1746.
29. Heal JW, Jimenez-Roldan JE, Wells SA, Freedman RB, Römer RA. Inhibition of HIV-1 protease: the rigidity perspective. Bioinformatics 2012;28:350–357.
30. Li H, Wells SA, Jimenez-Roldan JE, Römer RA, Zhao Y, Sadler PJ, O'Connor PB. Protein flexibility is key to cisplatin crosslinking in calmodulin. Prot Sci 2012;21:1269–1279.
31. Wells SA, Crennell SJ, Danson MJ. Structures of mesophilic and extremophilic citrate synthases reveal rigidity and flexibility for function. Proteins 2014;82:2657–2670.
32. Soulby AJ, Heal JW, Barrow MP, Römer RA, O'Connor PB. Does deamidation cause protein unfolding? A top-down tandem mass spectrometry study. Prot Sci 2015;24:850–860.
33. Wells SA, van der Kamp MW, McGeagh JD, Mulholland AJ. Structure and function in homodimeric enzymes: simulations of cooperative and independent functional motions. PLoS One 2015;10:e0133372.
34. Farrell D, Speranskiy K, Thorpe M. Generating stereochemically-acceptable protein pathways. Proteins 2010;78:2908–2921.
35. Ahmed A, Gohlke H. Multiscale modeling of macromolecular conformational changes combining concepts from rigidity and elastic network theory. Proteins 2006;63:1038–1051.
36. Krüger DM, Ahmed A, Gohlke H. NMSim Web Server: integrated approach for normal mode-based geometric simulations of biologically relevant conformational transitions in proteins. Nucleic Acids Res 2012;40:W310–W316.
37. Ahmed A, Rippmann F, Barnickel G, Gohlke H. A normal mode-based geometric simulation approach for exploring biologically relevant conformational transitions in proteins. J Chem Inform Model 2011;51:1604–1622.
38. Case DT, Darden IT, Cheatham C, Simmerling J, Wang R, Duke R, Luo K, Merz D, Pearlman M, Crowley R, Walker W, Zhang B, Wang S, Hayik A, Roitberg G, Seabra K, Wong F, Paesani X, Wu S, Brozell V, Tsui H, Gohlke L, Yang C, Tan J, Mongan V, Hornak G, Cui P, Beroza D, Mathews C, Schafmeister W, Ross PK. Amber9. Technical report, University of California, San Francisco. 2006.
39. Duan Y, Wu C, Chowdhury S, Lee MC, Xiong G, Zhang W, Yang R, Cieplak P, Luo R, Lee T, Caldwell J, Wang J, Kollman P. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J Comput Chem 2003;24:1999–2012.
40. Levitt M. A simplified representation of protein conformations for rapid simulation of protein folding. J Mol Biol 1976;104:59–107.
41. Warshel A, Levitt W. Folding and stability of helical proteins: carp myogen. J Mol Biol 1976;106:421–437.
42. DeWitte RS, Shakhnovich EI. Pseudodihedrals: simplified protein backbone representation with knowledge-based energy. Prot Sci 1994;3:1570–1581.
43. Edman JC, Ellis L, Blacher RW, Roth RA, Rutter WJ. Sequence of protein disulphide isomerase and implications of its relationship to thioredoxin. Nature 1985;317:267–270.
44. Freedman R, Klappa P, Ruddock L. Protein disulfide isomerases exploit synergy between catalytic and specific binding domains. EMBO J 2002;15:136–140.
45. Amin NT, Wallis AK, Wells SA, Rowe ML, Williamson RA, Howard MJ, Freedman RB. Dynamics and inter-domain flexibility of human ERp27 indicated by high-resolution NMR studies. Biochem J 2013;450:321–332.
46. Caves LS, Evanseck JD, Karplus M. Locally accessible conformations of proteins: multiple molecular dynamics simulations of crambin. Prot Sci 1998;7:649–666.
47. Loccisano AE, Acevedo O, DeChancie J, Schulze BG, Evanseck JD. Enhanced sampling by multiple molecular dynamics trajectories: carbonmonoxy myoglobin 10 micros A0 → A(1-3) transition from ten 400 picosecond simulations. J Mol Graph Model 2004;22:369–376.
48. Yang S, Wang X, Cui L, Ding X, Niu L, Yang F, Wang C, Wang CC, Lou J. Compact conformations of human protein disulfide isomerase. PLoS One 2014;9:e103472.
49. Irvine AG, Wallis AK, Sanghera N, Rowe ML, Ruddock LW, Howard MJ, Williamson RA, Blindauer CA, Freedman RB. Protein disulfide-isomerase interacts with a substrate protein at all stages along its folding pathway. PLoS One 2014;9:e82511.
50. Masui S, Vavassori S, Fagioli C, Sitia R, Inaba K. Molecular bases of cyclic and specific disulfide interchange between human ERO1 protein and protein-disulfide isomerase (PDI). J Biol Chem 2011;286:16261–16271.
51. Liwo A, Czaplewski C, Oldziej S, Scheraga HA. Computational techniques for efficient conformational sampling of proteins. Curr Opin Struct Biol 2008;18:134–139.
52. Hawkins H, de Nardi M, Freedman R. Redox properties and cross-linking of the dithiol/disulphide active sites of mammalian protein disulphide-isomerase. Biochem J 1991;275:341–348.
53. Guex N, Peitsch M 1997. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723.