Domain stabilities in protein kinase R (PKR): Evidence for weak interdomain interactions

Biochemistry

Volumn 47, Issue 17, 2008, Pages 4887-4897

  Anderson, Eric ^a   Cole, James L ^a,b  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b Department of Molecular and Cell Biology ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; CHEMICAL STABILITY; CONFORMATIONS; DENATURATION; IMMUNOLOGY; INTERFERONS; MATHEMATICAL MODELS; MOLECULAR INTERACTIONS; PROTEOLYSIS; RNA;

AUTOINHIBITION; BLOCKS PROTEOLYSIS; CHEMICAL DENATURATION; CONFORMATION CHANGES; HOLENZYMES;

ENZYME INHIBITION;

DOUBLE STRANDED RNA; HOLOENZYME; INITIATION FACTOR 2ALPHA; INTERFERON; PROTEIN KINASE R; DNA; FLUORESCENT DYE; PROTEIN KINASE; TRYPTOPHAN; UREA;

ARTICLE; AUTOPHOSPHORYLATION; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; DIMERIZATION; ENZYME ACTIVATION; ENZYME CONFORMATION; ENZYME DENATURATION; ENZYME INDUCTION; ENZYME INHIBITION; INNATE IMMUNITY; MOLECULAR MODEL; MOLECULAR PROBE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN RNA BINDING; PROTEIN STABILITY; PROTEIN SYNTHESIS INHIBITION; CHEMICAL STRUCTURE; CHEMISTRY; CIRCULAR DICHROISM; DRUG EFFECT; ENZYME STABILITY; KINETICS; METABOLISM; PROTEIN DENATURATION; PROTEIN RENATURATION; PROTEIN TERTIARY STRUCTURE;

CIRCULAR DICHROISM; DNA; ENZYME STABILITY; FLUORESCENT DYES; KINETICS; MODELS, MOLECULAR; PROTEIN DENATURATION; PROTEIN KINASES; PROTEIN RENATURATION; PROTEIN STRUCTURE, TERTIARY; TRYPTOPHAN; UREA;

EID: 42449134458     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi702211j     Document Type: Article

References (52)

1. Clemens, M. J., and Elia, A. (1997) The double-stranded RNA-dependent protein kinase PKR: Structure and function. J. Interferon Cytokine Res. 17, 503-524.
2. Kaufman, R. J. (2000) The double stranded RNA-activated protein kinase PKR, in Translational Control of Gene Expression (Sonenberg, N., Hershey, J. W. B., and Mathews, M. B., Eds.) pp 503-528, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
3. Toth, A. M., Zhang, P., Das, S., George, C. X., and Samuel, C. E. (2006) Interferon action and the double-stranded RNA-dependent enzymes ADAR1 adenosine deaminase and PKR protein kinase. Prog. Nucleic Acid Res. Mol. Biol. 81, 369-434.
4. Garcia, M. A., Meurs, E. F., and Esteban, M. (2007) The dsRNA protein kinase PKR: Virus and cell control. Biochimie 89, 799-811.
5. Williams, B. R. (2001) Signal integration via PKR, Sci. STKE 2001, RE2.
6. Weber, F., Wagner, V., Rasmussen, S. B., Hartmann, R., and Paludan, S. R. (2006) Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J. Virol. 80, 5059-5064.
7. Dever, T. E. (2002) Gene-specific regulation by general translation factors. Cell 108, 545-556.
8. Tian, B., Bevilacqua, P. C., Diegelman-Parente, A., and Mathews, M. B. (2004) The double-stranded RNA binding motif: Interference and much more. Nat. Rev. Mol. Cell Biol. 5, 1013-1023.
9. Nanduri, S., Carpick, B. W., Yang, Y., Williams, B. R., and Qin, J. (1998) Structure of the double-stranded RNA binding domain of the protein kinase PKR reveals the molecular basis of its dsRNA-mediated activation. EMBO J. 17, 5458-5465.
10. Nanduri, S., Rahman, F., Williams, B. R. G., and Qin, J. (2000) A dynamically tuned double-stranded RNA binding mechanism for the activation of antiviral kinase PKR. EMBO J. 19, 5567-5574.
11. Dar, A. C., Dever, T. E., and Sicheri, F. (2005) Higher-order substrate recognition of eIF2α by the RNA-dependent protein kinase PKR. Cell 122, 887-900.
12. Huse, M., and Kuriyan, J. (2002) The conformational plasticity of protein kinases. Cell 109, 275-282.
13. McKenna, S. A., Lindhout, D. A., Kim, I., Liu, C. W., Gelev, V. M., Wagner, G., and Puglisi, J. D. (2007) Molecular framework for the activation of RNA-dependent protein kinase. J. Biol. Chem. 282, 11474-11486.
14. Cole, J. L. (2007) Activation of PKR: An open and shut case? Trends Biochem. Sci. 32, 57-62.
15. Gelev, V., Aktas, H., Marintchev, A., Ito, T., Frueh, D., Hemond, M., Rovnyak, D., Debus, M., Hyberts, S., Usheva, A., Halperin, J., and Wagner, G. (2006) Mapping of the auto-inhibitory interactions of protein kinase R by nuclear magnetic resonance. J. Mol. Biol. 364, 352-363.
16. Lemaire, P. A., Lary, J., and Cole, J. L. (2005) Mechanism of PKR activation: Dimerization and kinase activation in the absence of double-stranded RNA. J. Mol. Biol. 345, 81-90.
17. Lemaire, P. A., Tessmer, I., Craig, R., Erie, D. A., and Cole, J. L. (2006) Unactivated PKR exists in an open conformation capable of binding nucleotides. Biochemistry 45, 9074-9084.
18. Carpick, B. W., Graziano, V., Schneider, D., Maitra, R. K., Lee, X., and Williams, B. R. G. (1997) Characterization of the solution complex between the interferon-induced double-stranded RNA-activated protein kinase and HIV-I trans-activating region RNA. J. Biol. Chem. 272, 9510-9516.
19. Gabel, F., Wang, D., Madern, D., Sadler, A., Dayie, K., Daryoush, M. Z., Schwahn, D., Zaccai, G., Lee, X., and Williams, B. R. (2006) Dynamic flexibility of double-stranded RNA activated PKR in solution. J. Mol. Biol. 359, 610-623.
20. Langland, J. O., and Jacobs, B. L. (1992) Cytosolic double-stranded RNA-dependent protein kinase is likely a dimer of partially phosphory lated Mr = 66,000 subunits. J. Biol. Chem. 267, 10729-10736.
21. Patel, R. C., Stanton, P., McMillan, N. M., Williams, B. R., and Sen, G. C. (1995) The interferon-inducible double-stranded RNA-activated protein kinase self-associates in vitro and in vivo. Proc. Natl. Acad. Sci. U.S.A. 92, 8283-8287.
22. Robertson, H. D., and Mathews, M. B. (1996) The regulation of the protein kinase PKR by RNA. Biochimie 78, 909-914.
23. Ung, T. L., Cao, C., Lu, J., Ozato, K., and Dever, T. E. (2001) Heterologous dimerization domains functionally substitute for the double-stranded RNA binding domains of the kinase PKR. EMBO J. 20, 3728-3737.
24. Vattem, K. M., Staschke, K. A., and Wek, R. C. (2001) Mechanism of activation of the double-stranded-RNA-dependent protein kinase, PKR: Role of dimerization and cellular localization in the stimulation of PKR phosphorylation of eukaryotic initiation factor-2 (eIF2). Eur. J. Biochem. 268, 3674-3684.
25. Hunter, T., Hunt, T., Jackson, R. J., and Robertson, H. D. (1975) The characteristics of inhibition of protein synthesis by double-stranded ribonucleic acid in reticulocyte lysates. J. Biol. Chem. 250, 409-417.
26. Kostura, M., and Mathews, M. B. (1989) Purification and activation of the double-stranded RNA-dependent eIF-2 kinase DAI. Mol. Cell. Biol. 9, 1576-1586.
27. Garel, J.-R. (1992) Folding of large proteins: Multidomain and multisubunit proteins, in Protein Folding (Creighton, T. E., Ed.) pp 405-454, W.H. Freeman and Company, New York.
28. Han, J. H., Batey, S., Nickson, A. A., Teichmann, S. A., and Clarke, J. (2007) The folding and evolution of multidomain proteins. Nat. Rev. Mol. Cell Biol. 8, 319-330.
29. Jaenicke, R., and Lilie, H. (2000) Folding and association of oligomeric and multimeric proteins. Adv. Protein Chem. 53, 329-401.
30. Scott, K. A., Steward, A., Fowler, S. B., and Clarke, J. (2002) Titin; a multidomain protein that behaves as the sum of its parts. J. Mol. Biol. 315, 819-829.
31. Steward, A., Adhya, S., and Clarke, J. (2002) Sequence conservation in Ig-like domains: The role of highly conserved proline residues in the fibronectin type III superfamily. J. Mol. Biol. 318, 935-940.
32. Zarnt, T., Tradler, T., Stoller, G., Scholz, C., Schmid, F. X., and Fischer, G. (1997) Modular structure of the trigger factor required for high activity in protein folding. J. Mol. Biol. 271, 827-837.
33. Ucci, J. W., and Cole, J. L. (2004) Global analysis of nonspecific protein-nucleic interactions by sedimentation equilibrium. Biophys. Chem. 108, 127-140.
34. Ucci, J. W., Kobayashi, Y., Choi, G., Alexandrescu, A. T., and Cole, J. L. (2007) Mechanism of interaction of the double-stranded RNA (dsRNA) binding domain of protein kinase R with short dsRNA sequences. Biochemistry 46, 55-65.
35. Bilsel, O., Zitzewitz, J. A., Bowers, K. E., and Matthews, C. R. (1999) Folding mechanism of the α-subunit of tryptophan synthase, an α/β barrel protein: Global analysis highlights the interconversion of multiple native, intermediate, and unfolded forms through parallel channels. Biochemistry 38, 1018-1029.
36. Gualfetti, P. J., Bilsel, O., and Matthews, C. R. (1999) The progressive development of structure and stability during the equilibrium folding of the α subunit of tryptophan synthase from Escherichia coli. Protein Sci. 8, 1623-1635.
37. Laue, T. M., Shah, B. D., Ridgeway, T. M., and Pelletier, S. L. (1992) Computer-aided interpretation of analytical sedimentation data for proteins, in Analytical Ultracentrifugation in Biochemistry and Polymer Science (Harding, S., Rowe, A., and Horton, J., Eds.) pp 90-125, Royal Society of Chemistry, Cambridge, U.K.
38. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 78, 1606-1619.
39. Philo, J. S. (2006) Improved methods for fitting sedimentation coefficient distributions derived by time-derivative techniques. Anal. Biochem. 354, 238-246.
40. Stafford, W. F., and Sherwood, P. J. (2004) Analysis of heterologous interacting systems by sedimentation velocity: Curve fitting algorithms for estimation of sedimentation coefficients, equilibrium and kinetic constants. Biophys. Chem. 108, 231-243.
41. Schuck, P. (2003) On the analysis of protein self-association by sedimentation velocity analytical ultracentrifugation. Anal. Biochem. 320, 104-124.
42. Myers, J. K., Pace, C. N., and Scholtz, J. M. (1995) Denaturant m values and heat capacity changes: Relation to changes in accessible surface areas of protein unfolding. Protein Sci. 4, 2138-2148.
43. Fraczkiewicz, R., and Braun, W. (1998) Exact and efficient analytical calculation of the accessible surface areas and their gradients for macromolecules. J. Comput. Chem. 19, 319-333.
44. Bishop, S. M., Ross, J. B., and Kohanski, R. A. (1999) Autophosphorylation dependent destabilization of the insulin receptor kinase domain: Tryptophan-1175 reports changes in the catalytic cleft. Biochemistry 38, 3079-3089.
45. Lee, S., Lin, X., McMurray, J., and Sun, G. (2002) Contribution of an active site cation-π interaction to the spectroscopic properties and catalytic function of protein tyrosine kinase Csk. Biochemistry 41, 12107-12114.
46. Zhou, H. X. (2004) Polymer models of protein stability, folding, and interactions. Biochemistry 43, 2141-2154.
47. Zhou, H. X. (2001) Loops in proteins can be modeled as wormlike chains. J. Phys. Chem. B 105, 6763-6766.
48. Saelens, X., Kalai, M., and Vandenabeele, P. (2001) Translation inhibition in apoptosis: Caspase-dependent PKR activation and eIF2-a phosphorylation. J. Biol. Chem. 276, 41620-41628.
49. Nolen, B., Taylor, S., and Ghosh, G. (2004) Regulation of protein kinases; controlling activity through activation segment conformation. Mol. Cell 15, 661-675.
50. Romano, P. R., Garcia-Barrio, M. T., Zhang, X., Wang, Q., Taylor, D. R., Zhang, F., Herring, C., Mathews, M. B., Qin, J., and Hinnebusch, A. G. (1998) Autophosphorylation in the activation loop is required for full kinase activity in vivo of human and yeast eukaryotic initiation factor 2α kinases PKR and GCN2. Mol. Cell. Biol. 18, 2282-2297.
51. Zhang, X., Herring, C. J., Romano, P. R., Szczepanowska, J., Brzeska, H., Hinnebusch, A. G., and Qin, J. (1998) Identification of phosphorylation sites in proteins separated by polyacrylamide gel electrophoresis. Anal. Chem. 70, 2050-2059.
52. Zhang, F., Romano, P. R., Nagamura-Inoue, T., Tian, B., Dever, T. E., Mathews, M. B., Ozato, K., and Hinnebusch, A. G. (2001) Binding of double-stranded RNA to protein kinase PKR is required for dimerization and promotes critical autophosphorylation events in the activation loop. J. Biol. Chem. 276, 24946-24958.