Steroid receptor RNA activator (SRA) modification by the human pseudouridine synthase 1 (hPus1p): RNA binding, activity, and atomic model

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Huet, Tiphaine ^a   Miannay, François Alexandre ^a   Patton, Jeffrey R ^b   Thore, Stéphane ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS RECEPTOR; HOMODIMER; NUCLEOSIDE; PSEUDOURIDINE; RNA; STEROID RECEPTOR; HYDROLYASE; LONG UNTRANSLATED RNA; PSEUDOURIDYLATE SYNTHETASE; STEROID RECEPTOR RNA ACTIVATOR;

ANISOTROPY; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CRYSTAL STRUCTURE; HUMAN; PROTEIN DOMAIN; RNA BINDING; RNA SYNTHESIS; SITE DIRECTED MUTAGENESIS; STOICHIOMETRY; CHEMICAL STRUCTURE; GENETICS; METABOLISM;

HUMANS; HYDRO-LYASES; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; RNA, LONG NONCODING;

EID: 84899512894     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094610     Document Type: Article

References (43)

1. Bjork GR, Ericson JU, Gustafsson CE, Hagervall TG, Jonsson YH, et al. (1987) Transfer RNA modification. Annu Rev Biochem 56: 263-287.
2. Ofengand J (2002) Ribosomal RNA pseudouridines and pseudouridine synthases. FEBS Lett 514: 17-25.
3. Samuelsson T, Olsson M (1990) Transfer RNA pseudouridine synthases in Saccharomyces cerevisiae. J Biol Chem 265: 8782-8787.
4. Hamma T, Ferre-D'Amare AR (2006) Pseudouridine synthases. Chem Biol 13: 1125-1135. (Pubitemid 44750730)
5. McCleverty CJ, Hornsby M, Spraggon G, Kreusch A (2007) Crystal structure of human Pus10, a novel pseudouridine synthase. J Mol Biol 373: 1243-1254. (Pubitemid 47539484)
6. Foster PG, Huang L, Santi DV, Stroud RM (2000) The structural basis for tRNA recognition and pseudouridine formation by pseudouridine synthase I. Nat Struct Biol7: 23-27. (Pubitemid 30043243)
7. Sivaraman J, Sauve V, Larocque R, Stura EA, Schrag JD, et al. (2002) Structure of the 16S rRNA pseudouridine synthase RsuA bound to uracil and UMP. Nat Struct Biol 9: 353-358. (Pubitemid 34462553)
8. Ericsson UB, Nordlund P, Hallberg BM (2004) X-ray structure of tRNA pseudouridine synthase TruD reveals an inserted domain with a novel fold. FEBS Lett 565: 59-64. (Pubitemid 38595321)
9. Mizutani K, Machida Y, Unzai S, Park SY, Tame JR (2004) Crystal structures of the catalytic domains of pseudouridine synthases RluC and RluD from Escherichia coli. Biochemistry 43: 4454-4463. (Pubitemid 38500574)
10. Hoang C, Ferre-D'Amare AR (2001) Cocrystal structure of a tRNA Psi55 pseudouridine synthase: nucleotide flipping by an RNA-modifying enzyme. Cell 107: 929-939. (Pubitemid 34084983)
11. Koonin EV (1996) Pseudouridine synthases: four families of enzymes containing a putative uridine-binding motif also conserved in dUTPases and dCTP deaminases. Nucleic Acids Res 24: 2411-2415.
12. Zhao X, Patton JR, Davis SL, Florence B, Ames SJ, et al. (2004) Regulation of nuclear receptor activity by a pseudouridine synthase through posttranscriptional modification of steroid receptor RNA activator. Mol Cell 15: 549-558. (Pubitemid 39141782)
13. Behm-Ansmant I, Massenet S, Immel F, Patton JR, Motorin Y, et al. (2006) A previously unidentified activity of yeast and mouse RNA:pseudouridine synthases 1 (Pus1p) on tRNAs. RNA 12: 1583-1593. (Pubitemid 44141537)
14. Simos G, Tekotte H, Grosjean H, Segref A, Sharma K, et al. (1996) Nuclear pore proteins are involved in the biogenesis of functional tRNA. EMBO J 15: 2270-2284. (Pubitemid 26141143)
15. Zhao X, Patton JR, Ghosh SK, Fischel-Ghodsian N, Shen L, et al. (2007) Pus3p- and Pus1p-dependent pseudouridylation of steroid receptor RNA activator controls a functional switch that regulates nuclear receptor signaling. Mol Endocrinol 21: 686-699.
16. Ghosh SK, Patton JR, Spanjaard RA (2012) A small RNA derived from RNA coactivator SRA blocks steroid receptor signaling via inhibition of Pus1p-mediated pseudouridylation of SRA: evidence of a novel RNA binding domain in the N-terminus of steroid receptors. Biochemistry 51: 8163-8172.
17. Pan H, Agarwalla S, Moustakas DT, Finer-Moore J, Stroud RM (2003) Structure of tRNA pseudouridine synthase TruB and its RNA complex: RNA recognition through a combination of rigid docking and induced fit. Proc Natl Acad Sci U S A 100: 12648-12653. (Pubitemid 37339953)
18. Hoang C, Ferre-D'Amare AR (2004) Crystal structure of the highly divergent pseudouridine synthase TruD reveals a circular permutation of a conserved fold. RNA 10: 1026-1033. (Pubitemid 38822139)
19. Pan H, Ho JD, Stroud RM, Finer-Moore J (2007) The crystal structure of E. coli rRNA pseudouridine synthase RluE. J Mol Biol 367: 1459-1470. (Pubitemid 46413280)
20. Alian A, DeGiovanni A, Griner SL, Finer-Moore JS, Stroud RM (2009) Crystal structure of an RluF-RNA complex: a base-pair rearrangement is the key to selectivity of RluF for U2604 of the ribosome. J Mol Biol 388: 785-800.
21. Sibert BS, Patton JR (2012) Pseudouridine synthase 1: a site-specific synthase without strict sequence recognition requirements. Nucleic Acids Res 40: 2107-2118.
22. Chen J, Patton JR (1999) Cloning and characterization of a mammalian pseudouridine synthase. RNA 5: 409-419. (Pubitemid 29125000)
23. Motorin Y, Keith G, Simon C, Foiret D, Simos G, et al. (1998) The yeast tRNA:pseudouridine synthase Pus1p displays a multisite substrate specificity. RNA 4: 856-869. (Pubitemid 28317833)
24. Massenet S, Motorin Y, Lafontaine DL, Hurt EC, Grosjean H, et al. (1999) Pseudouridine mapping in the Saccharomyces cerevisiae spliceosomal U small nuclear RNAs (snRNAs) reveals that pseudouridine synthase pus1p exhibits a dual substrate specificity for U2 snRNA and tRNA. Mol Cell Biol 19: 2142-2154. (Pubitemid 29098272)
25. Bykhovskaya Y, Casas K, Mengesha E, Inbal A, Fischel-Ghodsian N (2004) Missense mutation in pseudouridine synthase 1 (PUS1) causes mitochondrial myopathy and sideroblastic anemia (MLASA). Am J Hum Genet 74: 1303-1308. (Pubitemid 38669331)
26. Kabsch W (2010) Xds. Acta Crystallogr D Biol Crystallogr 66: 125-132.
27. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674. (Pubitemid 47080256)
28. Czudnochowski N, Wang AL, Finer-Moore J, Stroud RM (2013) In Human Pseudouridine Synthase 1 (hPus1), a C-Terminal Helical Insert Blocks tRNA from Binding in the Same Orientation as in the Pus1 Bacterial Homologue TruA, Consistent with Their Different Target Selectivities. J Mol Biol 425: 3875-3887.
29. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221.
30. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132. (Pubitemid 41742764)
31. Cortese R, Kammen HO, Spengler SJ, Ames BN (1974) Biosynthesis of pseudouridine in transfer ribonucleic acid. J Biol Chem 249: 1103-1108.
32. Patton JR (1991) Pseudouridine modification of U5 RNA in ribonucleoprotein particles assembled in vitro. Mol Cell Biol 11: 5998-6006.
33. Novikova IV, Hennelly SP, Sanbonmatsu KY (2012) Structural architecture of the human long non-coding RNA, steroid receptor RNA activator. Nucleic Acids Res 40: 5034-5051.
34. Hur S, Stroud RM (2007) How U38, 39, and 40 of many tRNAs become the targets for pseudouridylation by TruA. Mol Cell 26: 189-203. (Pubitemid 46617334)
35. Arluison V, Batelier G, Ries-Kautt M, Grosjean H (1999) RNA:pseudouridine synthetase Pus1 from Saccharomyces cerevisiae: oligomerization property and stoichiometry of the complex with yeast tRNA(Phe). Biochimie 81: 751-756.
36. Sunita S, Zhenxing H, Swaathi J, Cygler M, Matte A, et al. (2006) Domain organization and crystal structure of the catalytic domain of E.coli RluF, a pseudouridine synthase that acts on 23S rRNA. J Mol Biol 359: 998-1009. (Pubitemid 43842052)
37. Sibert BS, Fischel-Ghodsian N, Patton JR (2008) Partial activity is seen with many substitutions of highly conserved active site residues in human Pseudouridine synthase 1. RNA 14: 1895-1906.
38. Ramamurthy V, Swann SL, Paulson JL, Spedaliere CJ, Mueller EG (1999) Critical aspartic acid residues in pseudouridine synthases. J Biol Chem 274: 22225-22230.
39. Gu X, Liu Y, Santi DV (1999) The mechanism of pseudouridine synthase I as deduced from its interaction with 5-fluorouracil-tRNA. Proc Natl Acad Sci U S A 96: 14270-14275. (Pubitemid 30000640)
40. Golden BL, Gooding AR, Podell ER, Cech TR (1998) A preorganized active site in the crystal structure of the Tetrahymena ribozyme. Science 282: 259-264. (Pubitemid 28487190)
41. Dong X, Bessho Y, Shibata R, Nishimoto M, Shirouzu M, et al. (2006) Crystal structure of tRNA pseudouridine synthase TruA from Thermus thermophilus HB8. RNA Biol 3: 115-122.
42. Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N (2010) ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 38: W529-533.
43. Plewniak F, Bianchetti L, Brelivet Y, Carles A, Chalmel F, et al. (2003) PipeAlign: A new toolkit for protein family analysis. Nucleic Acids Res 31: 3829-3832. (Pubitemid 37442258)