Glycosidic Bond Conformation Preference Plays a Pivotal Role in Catalysis of RNA Pseudouridylation: A Combined Simulation and Structural Study

Journal of Molecular Biology

Volumn 401, Issue 5, 2010, Pages 690-695

  Zhou, Jing ^a   Lv, Chao ^a   Liang, Bo ^a   Chen, Mengen ^a   Yang, Wei ^a   Li, Hong ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Catalytic mechanism; Free energy simulation; H ACA ribonucleoprotein; Pseudouridine synthase; Ring conformation

Indexed keywords

BROXURIDINE; FLUOROURIDINE; GLYCOSIDE; PSEUDOURIDINE; RIBONUCLEOPROTEIN; RNA; URIDINE;

ARTICLE; CATALYSIS; CHEMICAL MODIFICATION; CONFORMATION; CRYSTAL STRUCTURE; ENERGY; ENZYME ACTIVITY; ISOMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PSEUDOURIDYLATION; SIMULATION;

EID: 77955559262     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.06.061     Document Type: Article

References (39)

1. Charette M., Gray M.W. Pseudouridine in RNA: what, where, how, and why. IUBMB Life 2000, 49:341-351.
2. Grosjean H., Benne R. Modification and Editing of RNA 1998, ASM Press, Washington, DC.
3. Arnez J.G., Steitz T.A. Crystal structure of unmodified tRNA(Gln) complexed with glutaminyl-tRNA synthetase and ATP suggests a possible role for pseudo-uridines in stabilization of RNA structure. Biochemistry 1994, 33:7560-7567.
4. Newby M.I., Greenbaum N.L. Investigation of Overhauser effects between pseudouridine and water protons in RNA helices. Proc. Natl Acad. Sci. USA 2002, 99:12697-12702. Electronic publication, September 19, 2002.
5. Davis D.R. Stabilization of RNA stacking by pseudouridine. Nucleic Acids Res. 1995, 23:5020-5026.
6. Yu Y.T., Shu M.D., Steitz J.A. Modifications of U2 snRNA are required for snRNP assembly and pre-mRNA splicing. EMBO J. 1998, 17:5783-5795.
7. King T.H., Liu B., McCully R.R., Fournier M.J. Ribosome structure and activity are altered in cells lacking snoRNPs that form pseudouridines in the peptidyl transferase center. Mol. Cell 2003, 11:425-435.
8. Spedaliere C.J., Ginter J.M., Johnston M.V., Mueller E.G. The pseudouridine synthases: revisiting a mechanism that seemed settled. J. Am. Chem. Soc. 2004, 126:12758-12759.
9. Huang L., Pookanjanatavip M., Gu X., Santi D.V. A conserved aspartate of tRNA pseudouridine synthase is essential for activity and a probable nucleophilic catalyst. Biochemistry 1998, 37:344-351.
10. Zhao X., Horne D.A. The role of cysteine residues in the rearrangement of uridine to pseudouridine catalyzed by pseudouridine synthase I. J. Biol. Chem. 1997, 272:1950-1955.
11. Sivaraman J., Iannuzzi P., Cygler M., Matte A. Crystal structure of the RluD pseudouridine synthase catalytic module, an enzyme that modifies 23S rRNA and is essential for normal cell growth of Escherichia coli. J. Mol. Biol. 2004, 335:87-101.
12. Kaya Y., Del Campo M., Ofengand J., Malhotra A. Crystal structure of TruD, a novel pseudouridine synthase with a new protein fold. J. Biol. Chem. 2004, 279:18107-18110.
13. Hoang C., Ferre-D'Amare A.R. Crystal structure of the highly divergent pseudouridine synthase TruD reveals a circular permutation of a conserved fold. RNA 2004, 10:1026-1033.
14. Sivaraman J., Sauve V., Larocque R., Stura E.A., Schrag J.D., Cygler M., Matte A. Structure of the 16S rRNA pseudouridine synthase RsuA bound to uracil and UMP. Nat. Struct. Biol. 2002, 9:353-358.
15. Dong X., Bessho Y., Shibata R., Nishimoto M., Shirouzu M., Kuramitsu S., Yokoyama S. Crystal structure of tRNA pseudouridine synthase TruA from Thermus thermophilus HB8. RNA Biol. 2006, 3:115-122.
16. Del Campo M., Ofengand J., Malhotra A. Crystal structure of the catalytic domain of RluD, the only rRNA pseudouridine synthase required for normal growth of Escherichia coli. RNA 2004, 10:231-239.
17. Hoang C., Chen J., Vizthum C.A., Kandel J.M., Hamilton C.S., Mueller E.G., Ferre-D'Amare A.R. Crystal structure of pseudouridine synthase RluA: indirect sequence readout through protein-induced RNA structure. Mol. Cell 2006, 24:535-545.
18. McCleverty C.J., Hornsby M., Spraggon G., Kreusch A. Crystal structure of human Pus10, a novel pseudouridine synthase. J. Mol. Biol. 2007, 373:1243-1254.
19. Hoang C., Ferre-D'Amare A.R. Cocrystal structure of a tRNA Psi55 pseudouridine synthase: nucleotide flipping by an RNA-modifying enzyme. Cell 2001, 107:929-939.
20. Balakin A.G., Smith L., Fournier M.J. The RNA world of the nucleolus: two major families of small RNAs defined by different box elements with related functions. Cell 1996, 86:823-834.
21. Ganot P., Bortolin M.L., Kiss T. Site-specific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs. Cell 1997, 89:799-809.
22. Decatur W.A., Fournier M.J. RNA-guided nucleotide modification of ribosomal and other RNAs. J. Biol. Chem. 2003, 278:695-698.
23. Baker D.L., Youssef O.A., Chastkofsky M.I., Dy D.A., Terns R.M., Terns M.P. RNA-guided RNA modification: functional organization of the archaeal H/ACA RNP. Genes Dev. 2005, 19:1238-1248.
24. Meier U.T. The many facets of H/ACA ribonucleoproteins. Chromosoma 2005, 114:1-14.
25. Hamma T., Ferre-D'Amare A.R. Pseudouridine synthases. Chem. Biol. 2006, 13:1125-1135.
26. Koonin E.V. Pseudouridine synthases: four families of enzymes containing a putative uridine-binding motif also conserved in dUTPases and dCTP deaminases. Nucleic Acids Res. 1996, 24:2411-2415.
27. Ramamurthy V., Swann S.L., Paulson J.L., Spedaliere C.J., Mueller E.G. Critical aspartic acid residues in pseudouridine synthases. J. Biol. Chem. 1999, 274:22225-22230.
28. Charpentier B., Muller S., Branlant C. Reconstitution of archaeal H/ACA small ribonucleoprotein complexes active in pseudouridylation. Nucleic Acids Res. 2005, 33:3133-3144.
29. Gu X., Liu Y., Santi D.V. The mechanism of pseudouridine synthase I as deduced from its interaction with 5-fluorouracil-tRNA. Proc. Natl Acad. Sci. USA 1999, 96:14270-14275.
30. Hamilton C.S., Greco T.M., Vizthum C.A., Ginter J.M., Johnston M.V., Mueller E.G. Mechanistic investigations of the pseudouridine synthase RluA using RNA containing 5-fluorouridine. Biochemistry 2006, 45:12029-12038.
31. Duan J., Li L., Lu J., Wang W., Ye K. Structural mechanism of substrate RNA recruitment in H/ACA RNA-guided pseudouridine synthase. Mol. Cell 2009, 34:427-439.
32. Liang B., Zhou J., Kahen E., Terns R.M., Terns M.P., Li H. Structure of a functional ribonucleoprotein pseudouridine synthase bound to a substrate RNA. Nat. Struct. Mol. Biol. 2009, 16:740-746.
33. Hoang C., Hamilton C.S., Mueller E.G., Ferre-D'Amare A.R. Precursor complex structure of pseudouridine synthase TruB suggests coupling of active site perturbations to an RNA-sequestering peripheral protein domain. Protein Sci. 2005, 14:2201-2206.
34. Zheng L.Q., Chen M.G., Yang W. Simultaneous escaping of explicit and hidden free energy barriers: application of the orthogonal space random walk strategy in generalized ensemble based conformational sampling. J. Chem. Phys. 2009, 130:234105.
35. Zheng L.Q., Chen M.G., Yang W. Random walk in orthogonal space to achieve efficient free-energy simulation of complex systems. Proc. Natl Acad. Sci. USA 2008, 105:20227-20232.
36. Tembe B.L., Mccammon J.A. Ligand receptor interactions. Comput. Chem. 1984, 8:281-283.
37. Kollman P. Free-energy calculations-applications to chemical and biochemical phenomena. Chem. Rev. 1993, 93:2395-2417.
38. Moore M.J., Sharp P.A. Site-specific modification of pre-mRNA: the 2′-hydroxyl groups at the splice sites. Science 1992, 256:992-997.
39. Spedaliere C.J., Mueller E.G. Not all pseudouridine synthases are potently inhibited by RNA containing 5-fluorouridine. RNA 2004, 10:192-199.