The pKa value and accessibility of cysteine residues are key determinants for protein substrate discrimination by glutaredoxin

Biochemistry

Volumn 53, Issue 15, 2014, Pages 2533-2540

  Jensen, Kristine Steen ^a,b   Pedersen, Jeppe T ^a   Winther, Jakob R ^a   Teilum, Kaare ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CATALYSIS; ENZYMES; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEINS; RATE CONSTANTS;

BACKBONE DYNAMICS; BINDING PROTEINS; CYSTEINE RESIDUES; KEY DETERMINANTS; LOCAL STABILITY; ORDERS OF MAGNITUDE; PROTEIN INTERACTION; PROTEIN SUBSTRATE;

SUBSTRATES;

ACYL COENZYME A; CYSTEINE; GLUTAREDOXIN; GLUTATHIONE;

ARTICLE; ENZYME MECHANISM; ENZYME SUBSTRATE COMPLEX; IN VITRO STUDY; MOLECULAR DYNAMICS; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE; PKA; PRIORITY JOURNAL; BIOCATALYSIS; CHEMICAL STRUCTURE; KINETICS; METABOLISM;

BIOCATALYSIS; CYSTEINE; GLUTAREDOXINS; KINETICS; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR;

EID: 84899445690     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi4016633     Document Type: Article

References (45)

1. Dalle-Donne, I., Rossi, R., Colombo, G., Giustarini, D., and Milzani, A. (2009) Protein S-glutathionylation: a regulatory device from bacteria to humans Trends Biochem. Sci. 34, 85-96
2. Gallogly, M. M., Starke, D. W., and Mieyal, J. J. (2009) Mechanistic and kinetic details of catalysis of thiol-disulfide exchange by glutaredoxins and potential mechanisms of regulation Antioxid. Redox. Signal. 11, 1059-1081
3. Lillig, C. H., Berndt, C., and Holmgren, A. (2008) Glutaredoxin systems Biochim. Biophys. Acta 1780, 1304-1317
4. Gravina, S. A. and Mieyal, J. J. (1993) Thioltransferase is a specific glutathionyl mixed disulfide oxidoreductase Biochemistry 32, 3368-3376
5. Jensen, K. S., Winther, J. R., and Teilum, K. (2011) Millisecond Dynamics in Glutaredoxin during Catalytic Turnover Is Dependent on Substrate Binding and Absent in the Resting States J. Am. Chem. Soc. 133, 3034-3042
6. Yang, Y., Jao, S. C., Nanduri, S., Starke, D. W., Mieyal, J. J., and Qin, J. (1998) Reactivity of the human thioltransferase (glutaredoxin) C7S, C25S, C78S, C82S mutant and NMR solution structure of its glutathionyl mixed disulfide intermediate reflect catalytic specificity Biochemistry 37, 17145-17156
7. Holmgren, A. (1985) Thioredoxin Annu. Rev. Biochem. 54, 237-271
8. Srinivasan, U., Mieyal, P. A., and Mieyal, J. J. (1997) pH profiles indicative of rate-limiting nucleophilic displacement in thioltransferase catalysis Biochemistry 36, 3199-3206
9. Elgán, T. H. and Berndt, K. D. (2008) Quantifying Escherichia coli glutaredoxin-3 substrate specificity using ligand-induced stability J. Biol. Chem. 283, 32839-32847
10. Ren, G., Stephan, D., Xu, Z., Zheng, Y., Tang, D., Harrison, R. S., Kurz, M., Jarrott, R., Shouldice, S. R., Hiniker, A., Martin, J. L., Heras, B., and Bardwell, J. C. A. (2009) Properties of the thioredoxin fold superfamily are modulated by a single amino acid residue J. Biol. Chem. 284, 10150-10159
11. Davis, D. A., Newcomb, F. M., Starke, D. W., Ott, D. E., Mieyal, J. J., and Yarchoan, R. (1997) Thioltransferase (glutaredoxin) is detected within HIV-1 and can regulate the activity of glutathionylated HIV-1 protease in vitro J. Biol. Chem. 272, 25935-25940
12. Wang, J., Boja, E. S., Tan, W., Tekle, E., Fales, H. M., English, S., Mieyal, J. J., and Chock, P. B. (2001) Reversible glutathionylation regulates actin polymerization in A431 cells J. Biol. Chem. 276, 47763-47766
13. Lind, C., Gerdes, R., Schuppe-Koistinen, I., and Cotgreave, I. A. (1998) Studies on the mechanism of oxidative modification of human glyceraldehyde-3- phosphate dehydrogenase by glutathione: catalysis by glutaredoxin Biochem. Biophys. Res. Commun. 247, 481-486
14. Bedhomme, M., Zaffagnini, M., Marchand, C. H., Gao, X.-H., Moslonka-Lefebvre, M., Michelet, L., Decottignies, P., and Lemaire, S. D. (2009) Regulation by glutathionylation of isocitrate lyase from Chlamydomonas reinhardtii J. Biol. Chem. 284, 36282-36291
15. Davis, D. A., Dorsey, K., Wingfield, P. T., Stahl, S. J., Kaufman, J., Fales, H. M., and Levine, R. L. (1996) Regulation of HIV-1 protease activity through cysteine modification Biochemistry 35, 2482-2488
16. Gallogly, M. M. and Mieyal, J. J. (2007) Mechanisms of reversible protein glutathionylation in redox signaling and oxidative stress Curr. Opin. Pharmacol. 7, 381-391
17. Holmgren, A., Johansson, C., Berndt, C., Lönn, M. E., Hudemann, C., and Lillig, C. H. (2005) Thiol redox control via thioredoxin and glutaredoxin systems Biochem. Soc. Trans. 33, 1375-1377
18. Hansen, R. E., Roth, D., and Winther, J. R. (2009) Quantifying the global cellular thiol-disulfide status Proc. Natl. Acad. Sci. U.S.A. 106, 422-427
19. Shelton, M. D., Chock, P. B., and Mieyal, J. J. (2005) Glutaredoxin: role in reversible protein s-glutathionylation and regulation of redox signal transduction and protein translocation Antioxid. Redox. Signal. 7, 348-366
20. Kragelund, B. B., Heinemann, B., Knudsen, J., and Poulsen, F. M. (1998) Mapping the lifetimes of local opening events in a native state protein Protein Sci. 7, 2237-2248
21. Kragelund, B. B., Knudsen, J., and Poulsen, F. M. (1995) Local perturbations by ligand binding of hydrogen deuterium exchange kinetics in a four-helix bundle protein, acyl coenzyme A binding protein (ACBP) J. Mol. Biol. 250, 695-706
22. Rischel, C., Madsen, J. C., Andersen, K. V., and Poulsen, F. M. (1994) Comparison of backbone dynamics of apo- and holo-acyl-coenzyme A binding protein using 15N relaxation measurements Biochemistry 33, 13997-14002
23. Teilum, K., Kragelund, B. B., and Poulsen, F. M. (2002) Transient structure formation in unfolded acyl-coenzyme A-binding protein observed by site-directed spin labelling J. Mol. Biol. 324, 349-357
24. Mandrup, S., Højrup, P., Kristiansen, K., and Knudsen, J. (1991) Gene synthesis, expression in Escherichia coli, purification and characterization of the recombinant bovine acyl-CoA-binding protein Biochem. J. 276 (Pt 3) 817-823
25. Johnson, K. A., Simpson, Z. B., and Blom, T. (2009) Global kinetic explorer: a new computer program for dynamic simulation and fitting of kinetic data Anal. Biochem. 387, 20-29
26. Iversen, R., Andersen, P. A., Jensen, K. S., Winther, J. R., and Sigurskjold, B. W. (2010) Thiol-disulfide exchange between glutaredoxin and glutathione Biochemistry 49, 810-820
27. Thomsen, J. K., Kragelund, B. B., Teilum, K., Knudsen, J., and Poulsen, F. M. (2002) Transient intermediary states with high and low folding probabilities in the apparent two-state folding equilibrium of ACBP at low pH J. Mol. Biol. 318, 805-814
28. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR 6, 277-293
29. Vranken, W. F., Boucher, W., Stevens, T. J., Fogh, R. H., Pajon, A., Llinas, M., Ulrich, E. L., Markley, J. L., Ionides, J., and Laue, E. D. (2005) The CCPN data model for NMR spectroscopy: development of a software pipeline Proteins 59, 687-696
30. Webb, H., Tynan-Connolly, B. M., Lee, G. M., Farrell, D., O'Meara, F., Søndergaard, C. R., Teilum, K., Hewage, C., McIntosh, L. P., and Nielsen, J. E. (2011) Remeasuring HEWL pK(a) values by NMR spectroscopy: methods, analysis, accuracy, and implications for theoretical pK(a) calculations Proteins 79, 685-702
31. Lee, B. and Richards, F. M. (1971) The interpretation of protein structures: estimation of static accessibility J. Mol. Biol. 55, 379-400
32. Cole, R. and Loria, J. P. (2003) FAST-Modelfree: a program for rapid automated analysis of solution NMR spin-relaxation data J. Biomol. NMR 26, 203-213
33. Xiao, R., Lundström-Ljung, J., Holmgren, A., and Gilbert, H. F. (2005) Catalysis of thiol/disulfide exchange. Glutaredoxin 1 and protein-disulfide isomerase use different mechanisms to enhance oxidase and reductase activities J. Biol. Chem. 280, 21099-21106
34. Jensen, K. S., Hansen, R. E., and Winther, J. R. (2009) Kinetic and thermodynamic aspects of cellular thiol-disulfide redox regulation Antioxid. Redox. Signal. 11, 1047-1058
35. Gilbert, H. F. (1990) Molecular and cellular aspects of thiol-disulfide exchange Adv. Enzymol. Relat. Areas Mol. Biol. 63, 69-172
36. Farrell, D., Miranda, E. S., Webb, H., Georgi, N., Crowley, P. B., McIntosh, L. P., and Nielsen, J. E. (2010) Titration-DB: storage and analysis of NMR-monitored protein pH titration curves Proteins 78, 843-857
37. García de la Torre, J., Huertas, M. L., and Carrasco, B. (2000) HYDRONMR: prediction of NMR relaxation of globular proteins from atomic-level structures and hydrodynamic calculations J. Magn. Reson. 147, 138-146
38. Hansen, R. E., Østergaard, H., and Winther, J. R. (2005) Increasing the reactivity of an artificial dithiol-disulfide pair through modification of the electrostatic milieu Biochemistry 44, 5899-5906
39. Sackewitz, M., Scheidt, H. A., Lodderstedt, G., Schierhorn, A., Schwarz, E., and Huster, D. (2008) Structural and dynamical characterization of fibrils from a disease-associated alanine expansion domain using proteolysis and solid-state NMR spectroscopy J. Am. Chem. Soc. 130, 7172-7173
40. Mittag, T., Kay, L. E., and Forman-Kay, J. D. (2010) Protein dynamics and conformational disorder in molecular recognition J. Mol. Recognit. 23, 105-116
41. Boehr, D. D., Nussinov, R., and Wright, P. E. (2009) The role of dynamic conformational ensembles in biomolecular recognition Nat. Chem. Biol. 5, 789-796
42. Qanungo, S., Starke, D. W., Pai, H. V., Mieyal, J. J., and Nieminen, A.-L. (2007) Glutathione supplementation potentiates hypoxic apoptosis by S-glutathionylation of p65-NFkappaB J. Biol. Chem. 282, 18427-18436
43. Johansson, C., Lillig, C. H., and Holmgren, A. (2004) Human mitochondrial glutaredoxin reduces S-glutathionylated proteins with high affinity accepting electrons from either glutathione or thioredoxin reductase J. Biol. Chem. 279, 7537-7543
44. Gallogly, M. M., Starke, D. W., Leonberg, A. K., Ospina, S. M. E., and Mieyal, J. J. (2008) Kinetic and mechanistic characterization and versatile catalytic properties of mammalian glutaredoxin 2: implications for intracellular roles Biochemistry 47, 11144-11157
45. Winther, J. R. and Thorpe, C. (2014) Quantification of thiols and disulfides Biochim. Biophys. Acta 1840, 838-846