Comparative Study of Two Box H/ACA Ribonucleoprotein Pseudouridine-Synthases: Relation between Conformational Dynamics of the Guide RNA, Enzyme Assembly and Activity

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Fourmann, Jean Baptiste ^a,b   Tillault, Anne Sophie ^a   Blaud, Magali ^a,c   Leclerc, Fabrice ^a,c   Branlant, Christiane ^a   Charpentier, Bruno ^a  

^a UNIVERSITÉ DE LORRAINE   (France)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

H ACA RIBONUCLEOPROTEIN; PROTEIN ACBF5; PROTEIN AGAR1; PROTEIN ANOP10; PROTEIN L7AE; PROTEIN PAB21; PROTEIN PAB91; RIBONUCLEOPROTEIN; SMALL NUCLEOLAR RIBONUCLEOPROTEIN; SMALL NUCLEOLAR RNA; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CATALYSIS; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME RECONSTITUTION; MOLECULAR DYNAMICS; PROTEIN ASSEMBLY; PROTEIN CLEAVAGE; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA CONFORMATION;

AMINO ACID SUBSTITUTION; INTRAMOLECULAR TRANSFERASES; MODELS, MOLECULAR; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN CONFORMATION; PYROCOCCUS ABYSSI; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RNA, SMALL NUCLEOLAR;

EID: 84880775822     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070313     Document Type: Article

References (58)

1. Badis G, Fromont-Racine M, Jacquier A, (2003) A snoRNA that guides the two most conserved pseudouridine modifications within rRNA confers a growth advantage in yeast. RNA 9: 771-779.
2. Decatur WA, Fournier MJ, (2002) rRNA modifications and ribosome function. Trends Biochem Sci 27: 344-351.
3. Ejby M, Sorensen MA, Pedersen S, (2007) Pseudouridylation of helix 69 of 23S rRNA is necessary for an effective translation termination. Proc Natl Acad Sci U S A 104: 19410-19415.
4. King TH, Liu B, McCully RR, Fournier MJ, (2003) Ribosome structure and activity are altered in cells lacking snoRNPs that form pseudouridines in the peptidyl transferase center. Mol Cell 11: 425-435.
5. Newby MI, Greenbaum NL, (2002) Sculpting of the spliceosomal branch site recognition motif by a conserved pseudouridine. Nat Struct Biol 9: 958-965.
6. Ofengand J, (2002) Ribosomal RNA pseudouridines and pseudouridine synthases. FEBS Lett 514: 17-25.
7. Yang C, McPheeters DS, Yu YT, (2005) Psi35 in the branch site recognition region of U2 small nuclear RNA is important for pre-mRNA splicing in Saccharomyces cerevisiae. J Biol Chem 280: 6655-6662.
8. Yu YT, Shu MD, Steitz JA, (1998) Modifications of U2 snRNA are required for snRNP assembly and pre-mRNA splicing. EMBO J 17: 5783-5795.
9. Koonin EV, Tatusov RL, Rudd KE, (1996) Protein sequence comparison at genome scale. Methods Enzymol 266: 295-322.
10. Kaya Y, Ofengand J, (2003) A novel unanticipated type of pseudouridine synthase with homologs in bacteria, archaea, and eukarya. RNA 9: 711-721.
11. Watanabe Y, Gray MW, (2000) Evolutionary appearance of genes encoding proteins associated with box H/ACA snoRNAs: Cbf5p in Euglena gracilis, an early diverging eukaryote, and candidate Gar1p and Nop10p homologs in archaebacteria. Nucleic Acids Res 28: 2342-2352.
12. Roovers M, Hale C, Tricot C, Terns MP, Terns RM, et al. (2006) Formation of the conserved pseudouridine at position 55 in archaeal tRNA. Nucleic Acids Res 34: 4293-4301.
13. Ferre-D'Amare AR, (2003) RNA-modifying enzymes. Curr Opin Struct Biol 13: 49-55.
14. Omer AD, Ziesche S, Decatur WA, Fournier MJ, Dennis PP, (2003) RNA-modifying machines in archaea. Mol Microbiol 48: 617-629.
15. Bachellerie JP, Cavaille J, Huttenhofer A, (2002) The expanding snoRNA world. Biochimie 84: 775-790.
16. Kiss T, (2002) Small nucleolar RNAs: an abundant group of noncoding RNAs with diverse cellular functions. Cell 109: 145-148.
17. Baker DL, Youssef OA, Chastkofsky MI, Dy DA, Terns RM, et al. (2005) RNA-guided RNA modification: functional organization of the archaeal H/ACA RNP. Genes Dev 19: 1238-1248.
18. Charpentier B, Muller S, Branlant C, (2005) Reconstitution of archaeal H/ACA small ribonucleoprotein complexes active in pseudouridylation. Nucleic Acids Res 33: 3133-3144.
19. Muller S, Leclerc F, Behm-Ansmant I, Fourmann JB, Charpentier B, et al. (2008) Combined in silico and experimental identification of the Pyrococcus abyssi H/ACA sRNAs and their target sites in ribosomal RNAs. Nucleic Acids Res 36: 2459-2475.
20. Rozhdestvensky TS, Tang TH, Tchirkova IV, Brosius J, Bachellerie JP, et al. (2003) Binding of L7Ae protein to the K-turn of archaeal snoRNAs: a shared RNA binding motif for C/D and H/ACA box snoRNAs in Archaea. Nucleic Acids Res 31: 869-877.
21. Tang TH, Bachellerie JP, Rozhdestvensky T, Bortolin ML, Huber H, et al. (2002) Identification of 86 candidates for small non-messenger RNAs from the archaeon Archaeoglobus fulgidus. Proc Natl Acad Sci U S A 99: 7536-7541.
22. Ni J, Tien AL, Fournier MJ, (1997) Small nucleolar RNAs direct site-specific synthesis of pseudouridine in ribosomal RNA. Cell 89: 565-573.
23. Ganot P, Bortolin ML, Kiss T, (1997) Site-specific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs. Cell 89: 799-809.
24. Bortolin ML, Ganot P, Kiss T, (1999) Elements essential for accumulation and function of small nucleolar RNAs directing site-specific pseudouridylation of ribosomal RNAs. Embo J 18: 457-469.
25. Manival X, Charron C, Fourmann JB, Godard F, Charpentier B, et al. (2006) Crystal structure determination and site-directed mutagenesis of the Pyrococcus abyssi aCBF5-aNOP10 complex reveal crucial roles of the C-terminal domains of both proteins in H/ACA sRNP activity. Nucleic Acids Res 34: 826-839.
26. Youssef OA, Terns RM, Terns MP, (2007) Dynamic interactions within sub-complexes of the H/ACA pseudouridylation guide RNP. Nucleic Acids Res 35: 6196-6206.
27. Charpentier B, Fourmann JB, Branlant C, (2007) Reconstitution of archaeal H/ACA sRNPs and test of their activity. Methods Enzymol 425: 389-405.
28. Rashid R, Liang B, Baker DL, Youssef OA, He Y, et al. (2006) Crystal structure of a Cbf5-Nop10-Gar1 complex and implications in RNA-guided pseudouridylation and dyskeratosis congenita. Mol Cell 21: 249-260.
29. Muller S, Fourmann JB, Loegler C, Charpentier B, Branlant C, (2007) Identification of determinants in the protein partners aCBF5 and aNOP10 necessary for the tRNA:Psi55-synthase and RNA-guided RNA:Psi-synthase activities. Nucleic Acids Res 35: 5610-5624.
30. Yang X, Duan J, Li S, Wang P, Ma S, et al. (2012) Kinetic and thermodynamic characterization of the reaction pathway of box H/ACA RNA-guided pseudouridine formation. Nucleic Acids Res 40: 10925-10936.
31. Duan J, Li L, Lu J, Wang W, Ye K, (2009) Structural mechanism of substrate RNA recruitment in H/ACA RNA-guided pseudouridine synthase. Mol Cell 34: 427-439.
32. Hamma T, Ferre-D'Amare AR, (2004) Structure of protein L7Ae bound to a K-turn derived from an archaeal box H/ACA sRNA at 1.8 A resolution. Structure (Camb) 12: 893-903.
33. Charron C, Manival X, Clery A, Senty-Segault V, Charpentier B, et al. (2004) The archaeal sRNA binding protein L7Ae has a 3D structure very similar to that of its eukaryal counterpart while having a broader RNA-binding specificity. J Mol Biol 342: 757-773.
34. Suryadi J, Tran EJ, Maxwell ES, Brown BA, 2nd (2005) The crystal structure of the Methanocaldococcus jannaschii multifunctional L7Ae RNA-binding protein reveals an induced-fit interaction with the box C/D RNAs. Biochemistry 44: 9657-9672.
35. Reichow SL, Varani G, (2008) Nop10 is a conserved H/ACA snoRNP molecular adaptor. Biochemistry 47: 6148-6156.
36. Hamma T, Reichow SL, Varani G, Ferre-D'Amare AR, (2005) The Cbf5-Nop10 complex is a molecular bracket that organizes box H/ACA RNPs. Nat Struct Mol Biol 12: 1101-1107.
37. Li L, Ye K, (2006) Crystal structure of an H/ACA box ribonucleoprotein particle. Nature 443: 302-307.
38. Liang B, Zhou J, Kahen E, Terns RM, Terns MP, et al. (2009) Structure of a functional ribonucleoprotein pseudouridine synthase bound to a substrate RNA. Nat Struct Mol Biol 16: 740-746.
39. Hamma T, Ferre-D'Amare AR, (2010) The box H/ACA ribonucleoprotein complex: interplay of RNA and protein structures in post-transcriptional RNA modification. J Biol Chem 285: 805-809.
40. Liang B, Xue S, Terns RM, Terns MP, Li H, (2007) Substrate RNA positioning in the archaeal H/ACA ribonucleoprotein complex. Nat Struct Mol Biol 14: 1189-1195.
41. Liang B, Kahen EJ, Calvin K, Zhou J, Blanco M, et al. (2008) Long-distance placement of substrate RNA by H/ACA proteins. RNA 14: 2086-2094.
42. Major F, Turcotte M, Gautheret D, Lapalme G, Fillion E, et al. (1991) The combination of symbolic and numerical computation for three-dimensional modeling of RNA. Science 253: 1255-1260.
43. Miller BT, Singh RP, Klauda JB, Hodoscek M, Brooks BR, et al. (2008) CHARMMing: a new, flexible web portal for CHARMM. J Chem Inf Model 48: 1920-1929.
44. MacKerell AD Jr, Banavali N, Foloppe N, (2000) Development and current status of the CHARMM force field for nucleic acids. Biopolymers 56: 257-265.
45. Reddy SY, Leclerc F, Karplus M, (2003) DNA polymorphism: a comparison of force fields for nucleic acids. Biophys J 84: 1421-1449.
46. Lu XJ, Olson WK, (2008) 3DNA: a versatile, integrated software system for the analysis, rebuilding and visualization of three-dimensional nucleic-acid structures. Nat Protoc 3: 1213-1227.
47. Lavery R, Moakher M, Maddocks JH, Petkeviciute D, Zakrzewska K, (2009) Conformational analysis of nucleic acids revisited: Curves+. Nucleic Acids Res 37: 5917-5929.
48. Loomis C AM, Bégin ME, Floro E, Kenny S and O'Callaghan D (2012) StratusLab Cloud Distribution. European Research Activities in Cloud Computing.
49. Lindell M, Romby P, Wagner EG, (2002) Lead(II) as a probe for investigating RNA structure in vivo. RNA 8: 534-541.
50. Baker DL, Seyfried NT, Li H, Orlando R, Terns RM, et al. (2008) Determination of protein-RNA interaction sites in the Cbf5-H/ACA guide RNA complex by mass spectrometric protein footprinting. Biochemistry 47: 1500-1510.
51. Sosnick TR, Fang X, Shelton VM, (2000) Application of circular dichroism to study RNA folding transitions. Methods Enzymol 317: 393-409.
52. Woody RW, (1995) Circular dichroism. Methods Enzymol 246: 34-71.
53. Marmier-Gourrier N, Clery A, Senty-Segault V, Charpentier B, Schlotter F, et al. (2003) A structural, phylogenetic, and functional study of 15.5-kD/Snu13 protein binding on U3 small nucleolar RNA. RNA 9: 821-838.
54. Wang C, Meier UT, (2004) Architecture and assembly of mammalian H/ACA small nucleolar and telomerase ribonucleoproteins. EMBO J 23: 1857-1867.
55. Koo BK, Park CJ, Fernandez CF, Chim N, Ding Y, et al. (2011) Structure of H/ACA RNP protein Nhp2p reveals cis/trans isomerization of a conserved proline at the RNA and Nop10 binding interface. J Mol Biol 411: 927-942.
56. Li S, Duan J, Li D, Yang B, Dong M, et al. (2011) Reconstitution and structural analysis of the yeast box H/ACA RNA-guided pseudouridine synthase. Genes Dev 25: 2409-2421.
57. Darzacq X, Kittur N, Roy S, Shav-Tal Y, Singer RH, et al. (2006) Stepwise RNP assembly at the site of H/ACA RNA transcription in human cells. J Cell Biol 173: 207-218.
58. Zhou J, Liang B, Li H, (2010) Functional and structural impact of target uridine substitutions on the H/ACA ribonucleoprotein particle pseudouridine synthase. Biochemistry 49: 6276-6281.