Specificity of the double-stranded RNA-binding domain from the RNA-activated protein kinase PKR for double-stranded RNA: Insights from thermodynamics and small-angle X-ray scattering

Biochemistry

Volumn 51, Issue 46, 2012, Pages 9312-9322

  Patel, Sunita ^a   Blose, Joshua M ^b   Sokoloski, Joshua E ^a,c   Pollack, Lois ^b   Bevilacqua, Philip C ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b Cornell University   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; DISTRIBUTION FUNCTIONS; ELECTROPHORETIC MOBILITY; ENZYMES; RNA; THERMODYNAMICS; X RAY SCATTERING;

ACTIVATED PROTEINS; CONFORMATIONAL CHANGE; DISTANCE DISTRIBUTION FUNCTIONS; DOUBLE-STRANDED RNA; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ISOTHERMAL TITRATION CALORIMETRY; SECONDARY AND TERTIARY STRUCTURES; VIRAL PATHOGENESIS;

NUCLEIC ACIDS;

DOUBLE STRANDED RNA; DOUBLE STRANDED RNA BINDING DOMAIN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; GEL MOBILITY SHIFT ASSAY; ISOTHERMAL TITRATION CALORIMETRY; PRIORITY JOURNAL; PROTEIN BINDING; THERMODYNAMICS; X RAY CRYSTALLOGRAPHY;

EID: 84869414509     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300935p     Document Type: Article

References (50)

1. Garcia, M. A., Meurs, E. F., and Esteban, M. (2007) The dsRNA protein kinase PKR: Virus and cell control Biochimie 89, 799-811 (Pubitemid 47001637)
2. Manche, L., Green, S. R., Schmedt, C., and Mathews, M. B. (1992) Interactions between double-stranded RNA regulators and the protein kinase DAI Mol. Cell. Biol. 12, 5238-5248
3. Zheng, X. and Bevilacqua, P. C. (2004) Activation of the protein kinase PKR by short double-stranded RNAs with single-stranded tails RNA 10, 1934-1945 (Pubitemid 39557831)
4. St Johnston, D., Brown, N. H., Gall, J. G., and Jantsch, M. (1992) A conserved double-stranded RNA-binding domain Proc. Natl. Acad. Sci. U.S.A. 89, 10979-10983
5. 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 (Pubitemid 39611537)
6. Chang, K. Y. and Ramos, A. (2005) The double-stranded RNA-binding motif, a versatile macromolecular docking platform FEBS J. 272, 2109-2117 (Pubitemid 40646782)
7. Bevilacqua, P. C. and Cech, T. R. (1996) Minor-groove recognition of double-stranded RNA by the double-stranded RNA-binding domain from the RNA-activated protein kinase PKR Biochemistry 35, 9983-9994 (Pubitemid 26269913)
8. Ryter, J. M. and Schultz, S. C. (1998) Molecular basis of double-stranded RNA-protein interactions: Structure of a dsRNA-binding domain complexed with dsRNA EMBO J. 17, 7505-7513 (Pubitemid 29002717)
9. Nallagatla, S. R. and Bevilacqua, P. C. (2008) Nucleoside modifications modulate activation of the protein kinase PKR in an RNA structure-specific manner RNA 14, 1201-1213 (Pubitemid 351717499)
10. Goodman, R. A., Macbeth, M. R., and Beal, P. A. (2012) ADAR proteins: Structure and catalytic mechanism Curr. Top. Microbiol. Immunol. 353, 1-33
11. Hundley, H. A. and Bass, B. L. (2010) ADAR editing in double-stranded UTRs and other noncoding RNA sequences Trends Biochem. Sci. 35, 377-383
12. Kim, Y. K., Furic, L., Desgroseillers, L., and Maquat, L. E. (2005) Mammalian Staufen1 recruits Upf1 to specific mRNA 3′UTRs so as to elicit mRNA decay Cell 120, 195-208 (Pubitemid 40174763)
13. Martel, C., Dugre-Brisson, S., Boulay, K., Breton, B., Lapointe, G., Armando, S., Trepanier, V., Duchaine, T., Bouvier, M., and Desgroseillers, L. (2010) Multimerization of Staufen1 in live cells RNA 16, 585-597
14. Han, J., Lee, Y., Yeom, K. H., Nam, J. W., Heo, I., Rhee, J. K., Sohn, S. Y., Cho, Y., Zhang, B. T., and Kim, V. N. (2006) Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex Cell 125, 887-901 (Pubitemid 43810154)
15. Nallagatla, S. R., Toroney, R., and Bevilacqua, P. C. (2011) Regulation of innate immunity through RNA structure and the protein kinase PKR Curr. Opin. Struct. Biol. 21, 119-127
16. Cohen-Chalamish, S., Hasson, A., Weinberg, D., Namer, L. S., Banai, Y., Osman, F., and Kaempfer, R. (2009) Dynamic refolding of IFN-λ mRNA enables it to function as PKR activator and translation template Nat. Chem. Biol. 5, 896-903
17. Nallagatla, S. R., Hwang, J., Toroney, R., Zheng, X., Cameron, C. E., and Bevilacqua, P. C. (2007) 5′-Triphosphate-dependent activation of PKR by RNAs with short stem-loops Science 318, 1455-1458 (Pubitemid 350208957)
18. Heinicke, L. A., Wong, C. J., Lary, J., Nallagatla, S. R., Diegelman-Parente, A., Zheng, X., Cole, J. L., and Bevilacqua, P. C. (2009) RNA dimerization promotes PKR dimerization and activation J. Mol. Biol. 390, 319-338
19. Toroney, R., Nallagatla, S. R., Boyer, J. A., Cameron, C. E., and Bevilacqua, P. C. (2010) Regulation of PKR by HCV IRES RNA: Importance of domain II and NS5A J. Mol. Biol. 400, 393-412
20. Ben-Asouli, Y., Banai, Y., Pel-Or, Y., Shir, A., and Kaempfer, R. (2002) Human interferon-λ mRNA autoregulates its translation through a pseudoknot that activates the interferon-inducible protein kinase PKR Cell 108, 221-232 (Pubitemid 34161142)
21. McKenna, S. A., Lindhout, D. A., Shimoike, T., Aitken, C. E., and Puglisi, J. D. (2007) Viral dsRNA inhibitors prevent self-association and autophosphorylation of PKR J. Mol. Biol. 372, 103-113 (Pubitemid 47223221)
22. Wahid, A. M., Coventry, V. K., and Conn, G. L. (2009) The PKR-binding domain of adenovirus VA RNAI exists as a mixture of two functionally non-equivalent structures Nucleic Acids Res. 37, 5830-5837
23. Launer-Felty, K., Wong, C. J., Wahid, A. M., Conn, G. L., and Cole, J. L. (2010) Magnesium-dependent interaction of PKR with adenovirus VAI RNA J. Mol. Biol. 402, 638-644
24. Heinicke, L. A., Nallagatla, S. R., Hull, C. M., and Bevilacqua, P. C. (2011) RNA helical imperfections regulate activation of the protein kinase PKR: Effects of bulge position, size, and geometry RNA 17, 957-966
25. Zheng, X. and Bevilacqua, P. C. (2000) Straightening of bulged RNA by the double-stranded RNA-binding domain from the protein kinase PKR Proc. Natl. Acad. Sci. U.S.A. 97, 14162-14167 (Pubitemid 32016547)
26. Nielsen, S. S., Moller, M., and Gillilan, R. E. (2012) High-throughput biological small-angle X-ray scattering with a robotically loaded capillary cell J. Appl. Crystallogr. 45, 213-223
27. Tate, M. W., Eikenberry, E. F., Barna, S. L., Wall, M. E., Lowrance, J. L., and Gruner, S. M. (1995) A large-format high-resolution area X-ray detector based on a fiber-optically bonded charge-coupled device (CCD) J. Appl. Crystallogr. 28, 196-205
28. Svergun, D. I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria J. Appl. Crystallogr. 25, 495-503 (Pubitemid 23564996)
29. Franke, D. and Svergun, D. I. (2009) DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering J. Appl. Crystallogr. 42, 342-346
30. Svergun, D. I. (1999) Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing Biophys. J. 76, 2879-2886 (Pubitemid 29269438)
31. Volkov, V. V. and Svergun, D. I. (2003) Uniqueness of ab initio shape determination in small-angle scattering J. Appl. Crystallogr. 36, 860-864
32. Kozin, M. B. and Svergun, D. I. (2001) Automated matching of high-and low-resolution structural models J. Appl. Crystallogr. 34, 33-41 (Pubitemid 32151714)
33. DeLano, W. L. (2002) The PyMOL molecular graphics system, DeLano Scientific, San Carlos, CA.
34. Bhattacharyya, A., Murchie, A. I. H., and Lilley, D. M. J. (1990) RNA bulges and the helical periodicity of double-stranded RNA Nature 343, 484-487 (Pubitemid 20065240)
35. Zacharias, M. and Hagerman, P. J. (1995) Bulge-induced bends in RNA: Quantification by transient electric birefringence J. Mol. Biol. 247, 486-500
36. Williams, B. R. (1999) PKR; a sentinel kinase for cellular stress Oncogene 18, 6112-6120
37. McGhee, J. D. and von Hippel, P. H. (1974) Theoretical aspects of DNA-protein interactions: Co-operative and non-co-operative binding of large ligands to a one-dimensional homogeneous lattice J. Mol. Biol. 86, 469-489
38. Bass, B. L., Hurst, S. R., and Singer, J. D. (1994) Binding properties of newly identified Xenopus proteins containing dsRNA-binding motifs Curr. Biol. 4, 301-314
39. VanOudenhove, J., Anderson, E., Krueger, S., and Cole, J. L. (2009) Analysis of PKR structure by small-angle scattering J. Mol. Biol. 387, 910-920
40. 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 (Pubitemid 28427059)
41. Zimmerman, S. B. and Pheiffer, B. H. (1981) A RNAÅ·DNA hybrid that can adopt two conformations: An X-ray diffraction study of poly(rA)Å·poly(dT) in concentrated solution or in fibers Proc. Natl. Acad. Sci. U.S.A. 78, 78-82
42. Romainczyk, O., Endeward, B., Prisner, T. F., and Engels, J. W. (2011) The RNA-DNA hybrid structure determined by EPR, CD and RNase H1 Mol. Biosyst. 7, 1050-1052
43. Tang, R. S. and Draper, D. E. (1990) Bulge loops used to measure the helical twist of RNA in solution Biochemistry 29, 5232-5237 (Pubitemid 20193925)
44. Riordan, F. A., Bhattacharyya, A., McAteer, S., and Lilley, D. M. (1992) Kinking of RNA helices by bulged bases, and the structure of the human immunodeficiency virus transactivator response element J. Mol. Biol. 226, 305-310
45. Stroud, J. (2012) Make-na webserver (Nucleic Acid Builder).
46. Szyperski, T., Gotte, M., Billeter, M., Perola, E., Cellai, L., Heumann, H., and Wuthrich, K. (1999) NMR structure of the chimeric hybrid duplex r(gcaguggc)Å·r(gcca)d(CTGC) comprising the tRNA-DNA junction formed during initiation of HIV-1 reverse transcription J. Biomol. NMR 13, 343-355 (Pubitemid 29210327)
47. Nanduri, S., Rahman, F., Williams, B. R., and Qin, J. (2000) A dynamically tuned double-stranded RNA binding mechanism for the activation of antiviral kinase PKR EMBO J. 19, 5567-5574
48. Blaszczyk, J., Gan, J., Tropea, J. E., Court, D. L., Waugh, D. S., and Ji, X. (2004) Noncatalytic assembly of ribonuclease III with double-stranded RNA Structure 12, 457-466 (Pubitemid 38353066)
49. Parisien, M. and Major, F. (2008) The MC-Fold and MC-Sym pipeline infers RNA structure from sequence data Nature 452, 51-55 (Pubitemid 351355097)
50. Zhu, S., Romano, P. R., and Wek, R. C. (1997) Ribosome targeting of PKR is mediated by two double-stranded RNA-binding domains and facilitates in vivo phosphorylation of eukaryotic initiation factor-2 J. Biol. Chem. 272, 14434-14441 (Pubitemid 27232862)