Biophysical and structural characterization of the thioredoxin-binding domain of protein kinase ASK1 and its interaction with reduced thioredoxin

Journal of Biological Chemistry

Volumn 289, Issue 35, 2014, Pages 24463-24474

  Kosek, Dalibor ^a,b   Kylarova, Salome ^a,b   Psenakova, Katarina ^a,b   Rezabkova, Lenka ^a   Herman, Petr ^a   Vecer, Jaroslav ^a   Obsilova, Veronika ^b   Obsil, Tomas ^a,b  

^a CHARLES UNIVERSITY   (Czech Republic)

^b INSTITUTE OF PHYSIOLOGY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CELL DEATH; CHARACTERIZATION; COVALENT BONDS;

BINDING INTERACTION; BINDING INTERFACE; CONFORMATIONAL CHANGE; INTERMOLECULAR DISULFIDE BOND; MITOGEN-ACTIVATED PROTEIN KINASE KINASE KINASE; SMALL ANGLE X-RAY SCATTERING; STRUCTURAL CHARACTERIZATION; TIME-RESOLVED FLUORESCENCE;

ENZYMES;

APOPTOSIS SIGNAL REGULATING KINASE 1; THIOREDOXIN 1; TRYPTOPHAN; PROTEIN BINDING; THIOREDOXIN;

ARTICLE; BINDING SITE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISULFIDE BOND; ENZYME ANALYSIS; ENZYME STRUCTURE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; STOICHIOMETRY; THIOREDOXIN BINDING DOMAIN; BIOPHYSICS; CIRCULAR DICHROISM; METABOLISM; OXIDATION REDUCTION REACTION; PROTEIN CONFORMATION; SPECTROFLUOROMETRY; ULTRACENTRIFUGATION;

BIOPHYSICS; CIRCULAR DICHROISM; MAP KINASE KINASE KINASE 5; OXIDATION-REDUCTION; PROTEIN BINDING; PROTEIN CONFORMATION; SPECTROMETRY, FLUORESCENCE; THIOREDOXINS; ULTRACENTRIFUGATION;

EID: 84906875259     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.583807     Document Type: Article

References (45)

1. Saitoh, M., Nishitoh, H., Fujii, M., Takeda, K., Tobiume, K., Sawada, Y., Kawabata, M., Miyazono, K., and Ichijo, H. (1998) Mammalian thioredoxin is a direct inhibitor of apoptosis signal-regulating kinase (ASK) 1. EMBO J. 17, 2596-2606 (Pubitemid 28221195)
2. Nishitoh, H., Matsuzawa, A., Tobiume, K., Saegusa, K., Takeda, K., Inoue, K., Hori, S., Kakizuka, A., and Ichijo, H. (2002) ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev. 16, 1345-1355 (Pubitemid 34615088)
3. 2+-induced p38 MAP kinase activation. EMBO Rep. 5, 161-166
4. Kawarazaki, Y., Ichijo, H., and Naguro, I. (2014) Apoptosis signal-regulating kinase 1 as a therapeutic target. Expert Opin. Ther. Targets 18, 651-664
5. Tobiume, K., Saitoh, M., and Ichijo, H. (2002) Activation of apoptosis signal-regulating kinase 1 by the stress-induced activating phosphorylation of pre-formed oligomer. J. Cell Physiol. 191, 95-104 (Pubitemid 34195221)
6. Bunkoczi, G., Salah, E., Filippakopoulos, P., Fedorov, O., Müller, S., Sobott, F., Parker, S. A., Zhang, H., Min, W., Turk, B. E., and Knapp, S. (2007) Structural and functional characterization of the human protein kinase ASK1. Structure 15, 1215-1226 (Pubitemid 47539165)
7. Noguchi, T., Takeda, K., Matsuzawa, A., Saegusa, K., Nakano, H., Gohda, J., Inoue, J., and Ichijo, H. (2005) Recruitment of tumor necrosis factor receptor-associated factor family proteins to apoptosis signal-regulating kinase 1 signalosome is essential for oxidative stress-induced cell death. J. Biol. Chem. 280, 37033-37040 (Pubitemid 41587787)
8. Zhang, L., Chen, J., and Fu, H. (1999) Suppression of apoptosis signal-regulating kinase 1-induced cell death by 14-3-3 proteins. Proc. Natl. Acad. Sci. U.S.A. 96, 8511-8515 (Pubitemid 29354822)
9. Fujino, G., Noguchi, T., Matsuzawa, A., Yamauchi, S., Saitoh, M., Takeda, K., and Ichijo, H. (2007) Thioredoxin and TRAF family proteins regulate reactive oxygen species-dependent activation of ASK1 through reciprocal modulation of the N-terminal homophilic interaction of ASK1. Mol. Cell Biol. 27, 8152-8163 (Pubitemid 350234230)
10. Liu, H., Nishitoh, H., Ichijo, H., and Kyriakis, J. M. (2000) Activation of apoptosis signal-regulating kinase 1 (ASK1) by tumor necrosis factor receptor-associated factor 2 requires prior dissociation of the ASK1 inhibitor thioredoxin. Mol. Cell. Biol. 20, 2198-2208 (Pubitemid 30123835)
11. Powis, G., and Montfort, W. R. (2001) Properties and biological activities of thioredoxins. Annu. Rev. Biophys. Biomol. Struct. 30, 421-455 (Pubitemid 32566170)
12. Qin, J., Clore, G. M., Kennedy, W. M., Huth, J. R., and Gronenborn, A. M. (1995) Solution structure of human thioredoxin in a mixed disulfide intermediate complex with its target peptide from the transcription factor NFκB. Structure 3, 289-297
13. Huber, H. E., Russel, M., Model, P., and Richardson, C. C. (1986) Interaction of mutant thioredoxins of Escherichia coli with the gene 5 protein of phage T7: the redox capacity of thioredoxin is not required for stimulation of DNA polymerase activity. J. Biol. Chem. 261, 15006-15012 (Pubitemid 17218065)
14. Hwang, C. Y., Ryu, Y. S., Chung, M. S., Kim, K. D., Park, S. S., Chae, S. K., Chae, H. Z., and Kwon, K. S. (2004) Thioredoxin modulates activator protein 1 (AP-1) activity and p27 Kip1 degradation through direct interaction with Jab1. Oncogene 23, 8868-8875 (Pubitemid 39657777)
15. Holmgren, A., Söderberg, B. O., Eklund, H., and Brändén, C. I. (1975) Three-dimensional structure of Escherichia coli thioredoxin-S2 to 2.8-Å resolution. Proc. Natl. Acad. Sci. U.S.A. 72, 2305-2309
16. Zhang, R., Al-Lamki, R., Bai, L., Streb, J. W., Miano, J. M., Bradley, J., and Min, W. (2004) Thioredoxin-2 inhibits mitochondria-located ASK1-mediated apoptosis in a JNK-independent manner. Circ. Res. 94, 1483-1491 (Pubitemid 38780321)
17. 250 is essential for activation of JNK and induction of apoptosis. Mol. Biol. Cell 20, 3628-3637
18. Liu, Y., and Min, W. (2002) Thioredoxin promotes ASK1 ubiquitination and degradation to inhibit ASK1-mediated apoptosis in a redox activity-independent manner. Circ. Res. 90, 1259-1266 (Pubitemid 34787407)
19. 2-terminal kinase activation and apoptosis. Mol. Biol. Cell 18, 3903-3913
20. Tan, S. (2001) A modular polycistronic expression system for overexpressing protein complexes in Escherichia coli. Protein Expr. Purif. 21, 224-234
21. Hashemy, S. I., and Holmgren, A. (2008) Regulation of the catalytic activity and structure of human thioredoxin 1 via oxidation and S-nitrosylation of cysteine residues. J. Biol. Chem. 283, 21890-21898
22. Rezabkova, L., Kacirova, M., Sulc, M., Herman, P., Vecer, J., Stepanek, M., Obsilova, V., and Obsil, T. (2012) Structural modulation of phosducin by phosphorylation and 14-3-3 protein binding. Biophys. J. 103, 1960-1969
23. Vecer, J., and Herman, P. (2011) Maximum entropy analysis of analytically simulated complex fluorescence decays. J. Fluoresc. 21, 873-881
24. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619
25. Dam, J., Velikovsky, C. A., Mariuzza, R. A., Urbanke, C., and Schuck, P. (2005) Sedimentation velocity analysis of heterogeneous protein-protein interactions: Lamm equation modeling and sedimentation coefficient distributions c(s). Biophys. J. 89, 619-634 (Pubitemid 41098314)
26. Roessle, M. W., Klaering, R., Ristau, U., Robrahn, B., Jahn, D., Gehrmann, T., Konarev, P., Round, A., Fiedler, S., Hermes, C., and Svergun, D. (2007) Upgrade of the small-angle x-ray scattering beamline X33 at the European Molecular Biology Laboratory, Hamburg. J. Appl. Crystallogr. 40, S190-S194 (Pubitemid 46732685)
27. Guinier, A. (1939) La diffraction des rayons X aux très faibles angles: applications à l'etude des phénomènes ultra-microscopies. Ann. Phys. Paris 12, 161-237
28. Svergun, D. I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25, 495-503
29. Svergun, D. I. (1999) Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys. J. 76, 2879-2886
30. Volkov, V. V., and Svergun, D. I. (2003) Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 36, 860-864
31. Whitmore, L., and Wallace, B. A. (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res. 32, W668-673 (Pubitemid 38997420)
32. Zhang, Y. (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9, 40
33. Kelley, L. A., and Sternberg, M. J. (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4, 363-371
34. Song, Y., DiMaio, F., Wang, R. Y., Kim, D., Miles, C., Brunette, T., Thompson, J., and Baker, D. (2013) High-resolution comparative modeling with RosettaCM. Structure 21, 1735-1742
35. Svergun, D., Barberato, C., and Koch, M. H. J. (1995) CRYSOL: a program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28, 768-773 (Pubitemid 3014671)
36. 15N resonance assignments and secondary structure of the human thioredoxin C62A, C69A, C73A mutant. J. Biomol. NMR 2, 431-445
37. Weichsel, A., Gasdaska, J. R., Powis, G., and Montfort, W. R. (1996) Crystal structures of reduced, oxidized, and mutated human thioredoxins: evidence for a regulatory homodimer. Structure 4, 735-751 (Pubitemid 126661296)
38. Qin, J., Clore, G. M., and Gronenborn, A. M. (1994) The high-resolution three-dimensional solution structures of the oxidized and reduced states of human thioredoxin. Structure 2, 503-522
39. Lakowicz, J. R. (1999) Principles of Fluorescence Spectroscopy, Second Ed., Kluwer Academic/Plenum Publishers, New York
40. Schauerte, J. A., and Gafni, A. (1989) Long-lived tryptophan fluorescence in phosphoglycerate mutase. Biochemistry 28, 3948-3954 (Pubitemid 19125447)
41. Andrade, M. A., Chacón, P., Merelo, J. J., and Morán, F. (1993) Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network. Protein Eng. 6, 383-390 (Pubitemid 23197398)
42. Jones, D. T. (1999) Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 292, 195-202
43. Kelly, S. M., and Price, N. C. (2000) The use of circular dichroism in the investigation of protein structure and function. Curr. Protein Peptide Sci. 1, 349-384
44. Oblong, J. E., Berggren, M., Gasdaska, P. Y., and Powis, G. (1994) Site-directed mutagenesis of active site cysteines in human thioredoxin produces competitive inhibitors of human thioredoxin reductase and elimination of mitogenic properties of thioredoxin. J. Biol. Chem. 269, 11714-11720 (Pubitemid 24196652)
45. Lupas, A., Van Dyke, M., and Stock, J. (1991) Predicting coiled coils from protein sequences. Science 252, 1162-1164 (Pubitemid 21917026)