Structural basis for substrate placement by an archaeal box C/D ribonucleoprotein particle

Molecular Cell

Volumn 39, Issue 6, 2010, Pages 939-949

  Xue, Song ^a   Wang, Ruiying ^a   Yang, Fangping ^a   Terns, Rebecca M ^b   Terns, Michael P ^b   Zhang, Xinxin ^c   Maxwell, E Stuart ^c   Li, Hong ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

^b University of Georgia ^*  (United States)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRILLARIN; L7AE PROTEIN; NOP56 58 PROTEIN; RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BASE PAIRING; CATALYSIS; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; METHYLATION; MOLECULAR MODEL; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PYROCOCCUS FURIOSUS;

ARCHAEAL PROTEINS; BINDING SITES; BIOCATALYSIS; CHROMOSOMAL PROTEINS, NON-HISTONE; CRYSTALLOGRAPHY, X-RAY; HOLOENZYMES; METHYLTRANSFERASES; MODELS, MOLECULAR; MUTAGENESIS, INSERTIONAL; NUCLEAR PROTEINS; NUCLEIC ACID CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; PYROCOCCUS FURIOSUS; RECOMBINANT PROTEINS; RIBONUCLEOPROTEINS, SMALL NUCLEOLAR; RNA, ARCHAEAL; RNA, SMALL NUCLEOLAR; SEQUENCE DELETION;

ARCHAEA;

EID: 77956912854     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2010.08.022     Document Type: Article

References (63)

1. Adams P.D., Grosse-Kunstleve R.W., Hung L.W., Ioerger T.R., McCoy A.J., Moriarty N.W., Read R.J., Sacchettini J.C., Sauter N.K., Terwilliger T.C. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 2002, 58:1948-1954.
2. Aittaleb M., Rashid R., Chen Q., Palmer J.R., Daniels C.J., Li H. Structure and function of archaeal box C/D sRNP core proteins. Nat. Struct. Biol. 2003, 10:256-263.
3. Aittaleb M., Visone T., Fenley M.O., Li H. Structural and thermodynamic evidence for a stabilizing role of Nop5p in S-adenosyl-L-methionine binding to fibrillarin. J. Biol. Chem. 2004, 279:41822-41829.
4. Appel C.D., Maxwell E.S. Structural features of the guide:target RNA duplex required for archaeal box C/D sRNA-guided nucleotide 2'-O-methylation. RNA 2007, 13:899-911.
5. Bachellerie J.-P., Cavaille J. Small nucleolar RNAs guide the ribose methylations of eukaryotic rRNAs. Modification and Editing of RNA 1998, ASM Press, Washington, DC. H. Grosjean, R. Benne (Eds.).
6. Bleichert F., Gagnon K.T., Brown B.A., Maxwell E.S., Leschziner A.E., Unger V.M., Baserga S.J. A dimeric structure for archaeal box C/D small ribonucleoproteins. Science 2009, 325:1384-1387.
7. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 1998, 54:905-921.
8. Caffarelli E., Losito M., Giorgi C., Fatica A., Bozzoni I. In vivo identification of nuclear factors interacting with the conserved elements of box C/D small nucleolar RNAs. Mol. Cell. Biol. 1998, 18:1023-1028.
9. Cahill N.M., Friend K., Speckmann W., Li Z.H., Terns R.M., Terns M.P., Steitz J.A. Site-specific cross-linking analyses reveal an asymmetric protein distribution for a box C/D snoRNP. EMBO J. 2002, 21:3816-3828.
10. Cavaille J., Nicoloso M., Bachellerie J.P. Targeted ribose methylation of RNA in vivo directed by tailored antisense RNA guides. Nature 1996, 383:732-735.
11. Charron C., Manival X., Clery A., Senty-Segault V., Charpentier B., Marmier-Gourrier N., Branlant C., Aubry A. 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. 2004, 342:757-773.
12. Creighton T.E. Disulphide bonds between cysteine residues. Protein Structure-A Practical Approach 1989, 155-157. IRL Press at Oxford University Press, New York. First Edition. T. Creighton (Ed.).
13. Decatur W.A., Fournier M.J. RNA-guided nucleotide modification of ribosomal and other RNAs. J. Biol. Chem. 2003, 278:695-698.
14. DeLano, W.L. The PyMOL Molecular Graphics System (San Carlos, CA: DeLano Scientific LLC). http://www.pymol.org.
15. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2126-2132.
16. Fatica A., Tollervey D. Making ribosomes. Curr. Opin. Cell Biol. 2002, 14:313-318.
17. Gagnon K.T., Zhang X., Agris P.F., Maxwell E.S. Assembly of the archaeal box C/D sRNP can occur via alternative pathways and requires temperature-facilitated sRNA remodeling. J. Mol. Biol. 2006, 362:1025-1042.
18. Gagnon K.T., Zhang X., Qu G., Biswas S., Suryadi J., Brown B.A., Maxwell E.S. Signature amino acids enable the archaeal L7Ae box C/D RNP core protein to recognize and bind the K-loop RNA motif. RNA 2010, 16:79-90.
19. Gautier T., Berges T., Tollervey D., Hurt E. Nucleolar KKE/D repeat proteins Nop56p and Nop58p interact with Nop1p and are required for ribosome biogenesis. Mol. Cell. Biol. 1997, 17:7088-7098.
20. Hamma T., Ferre-D'Amare A.R. Structure of protein L7Ae bound to a K-turn derived from an archaeal box H/ACA sRNA at 1.8 A resolution. Structure 2004, 12:893-903.
21. Hannon G.J., Rivas F.V., Murchison E.P., Steitz J.A. The expanding universe of noncoding RNAs. Cold Spring Harb. Symp. Quant. Biol. 2006, 71:551-564.
22. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 1991, 47:110-119.
23. Kass S., Tyc K., Steitz J.A., Sollner-Webb B. The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing. Cell 1990, 60:897-908.
24. Kiss T. Small nucleolar RNAs: an abundant group of noncoding RNAs with diverse cellular functions. Cell 2002, 109:145-148.
25. Kiss-Laszlo Z., Henry Y., Bachellerie J.P., Caizergues-Ferrer M., Kiss T. Site-specific ribose methylation of preribosomal RNA: a novel function for small nucleolar RNAs. Cell 1996, 85:1077-1088.
26. Kiss-Laszlo Z., Henry Y., Kiss T. Sequence and structural elements of methylation guide snoRNAs essential for site-specific ribose methylation of pre-rRNA. EMBO J. 1998, 17:797-807.
27. Kuhn J.F., Tran E.J., Maxwell E.S. Archaeal ribosomal protein L7 is a functional homolog of the eukaryotic 15.5kD/Snu13p snoRNP core protein. Nucleic Acids Res. 2002, 30:931-941.
28. Lafontaine D.L., Tollervey D. Nop58p is a common component of the box C+D snoRNPs that is required for snoRNA stability. RNA 1999, 5:455-467.
29. Lafontaine D.L., Tollervey D. Synthesis and assembly of the box C+D small nucleolar RNPs. Mol. Cell. Biol. 2000, 20:2650-2659.
30. Liang W.Q., Fournier M.J. U14 base-pairs with 18S rRNA: a novel snoRNA interaction required for rRNA processing. Genes Dev. 1995, 9:2433-2443.
31. Liu S., Li P., Dybkov O., Nottrott S., Hartmuth K., Luhrmann R., Carlomagno T., Wahl M.C. Binding of the human Prp31 Nop domain to a composite RNA-protein platform in U4 snRNP. Science 2007, 316:115-120.
32. Lyman S.K., Gerace L., Baserga S.J. Human Nop5/Nop58 is a component common to the box C/D small nucleolar ribonucleoproteins. RNA 1999, 5:1597-1604.
33. Matera A.G., Terns R.M., Terns M.P. Non-coding RNAs: lessons from the small nuclear and small nucleolar RNAs. Nat. Rev. Mol. Cell Biol. 2007, 8:209-220.
34. McKeegan K.S., Debieux C.M., Boulon S., Bertrand E., Watkins N.J. A dynamic scaffold of pre-snoRNP factors facilitates human box C/D snoRNP assembly. Mol. Cell. Biol. 2007, 27:6782-6793.
35. McKeegan K.S., Debieux C.M., Watkins N.J. Evidence that the AAA+ proteins TIP48 and TIP49 bridge interactions between 15.5K and the related NOP56 and NOP58 proteins during box C/D snoRNP biogenesis. Mol. Cell. Biol. 2009, 29:4971-4981.
36. Moore T., Zhang Y., Fenley M.O., Li H. Molecular basis of box C/D RNA-protein interactions; cocrystal structure of archaeal L7Ae and a box C/D RNA. Structure 2004, 12:807-818.
37. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. 1997, 53:240-255.
38. Nottrott S., Urlaub H., Luhrmann R. Hierarchical, clustered protein interactions with U4/U6 snRNA: a biochemical role for U4/U6 proteins. EMBO J. 2002, 21:5527-5538.
39. Omer A.D., Ziesche S., Ebhardt H., Dennis P.P. In vitro reconstitution and activity of a C/D box methylation guide ribonucleoprotein complex. Proc. Natl. Acad. Sci. USA 2002, 99:5289-5294.
40. Oruganti S., Zhang Y., Li H. Structural comparison of yeast snoRNP and spliceosomal protein Snu13p with its homologs. Biochem. Biophys. Res. Commun. 2005, 333:550-554.
41. Oruganti S., Zhang Y., Li H., Robinson H., Terns M.P., Terns R.M., Yang W., Li H. Alternative conformations of the archaeal Nop56/58-fibrillarin complex imply flexibility in box C/D RNPs. J. Mol. Biol. 2007, 371:1141-1150.
42. Otwinowski Z., Minor W. Processing of X-ray Diffraction Data Collected in Oscillation Mode 1997, Volume 276. Academic Press, San Diego.
43. Peculis B.A., Steitz J.A. Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte. Cell 1993, 73:1233-1245.
44. Rashid R., Aittaleb M., Chen Q., Spiegel K., Demeler B., Li H. Functional requirement for symmetric assembly of archaeal box C/D small ribonucleoprotein particles. J. Mol. Biol. 2003, 333:295-306.
45. Savino R., Gerbi S.A. In vivo disruption of Xenopus U3 snRNA affects ribosomal RNA processing. EMBO J. 1990, 9:2299-2308.
46. Schimmang T., Tollervey D., Kern H., Frank R., Hurt E.C. A yeast nucleolar protein related to mammalian fibrillarin is associated with small nucleolar RNA and is essential for viability. EMBO J. 1989, 8:4015-4024.
47. Szewczak L.B., DeGregorio S.J., Strobel S.A., Steitz J.A. Exclusive interaction of the 15.5 kD protein with the terminal box C/D motif of a methylation guide snoRNP. Chem. Biol. 2002, 9:1095-1107.
48. Terns M.P., Terns R.M. Small nucleolar RNAs: versatile trans-acting molecules of ancient evolutionary origin. Gene Expr. 2002, 10:17-39.
49. Tollervey D., Lehtonen H., Jansen R., Kern H., Hurt E.C. Temperature-sensitive mutations demonstrate roles for yeast fibrillarin in pre-rRNA processing, pre-rRNA methylation, and ribosome assembly. Cell 1993, 72:443-457.
50. Tran E.J., Zhang X., Maxwell E.S. Efficient RNA 2'-O-methylation requires juxtaposed and symmetrically assembled archaeal box C/D and C'/D' RNPs. EMBO J. 2003, 22:3930-3940.
51. Tran E., Zhang X., Lackey L., Maxwell E.S. Conserved spacing between the box C/D and C'/D' RNPs of the archaeal box C/D sRNP complex is required for efficient 2'-O-methylation of target RNAs. RNA 2005, 11:285-293.
52. Tyc K., Steitz J.A. U3, U8 and U13 comprise a new class of mammalian snRNPs localized in the cell nucleolus. EMBO J. 1989, 8:3113-3119.
53. Tycowski K.T., Smith C.M., Shu M.D., Steitz J.A. A small nucleolar RNA requirement for site-specific ribose methylation of rRNA in Xenopus. Proc. Natl. Acad. Sci. USA 1996, 93:14480-14485.
54. Vagin A., Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Cryst. 1997, 30:1022-1025.
55. Venema J., Tollervey D. Processing of pre-ribosomal RNA in Saccharomyces cerevisiae. Yeast 1995, 11:1629-1650.
56. Vidovic I., Nottrott S., Hartmuth K., Luhrmann R., Ficner R. Crystal structure of the spliceosomal 15.5kD protein bound to a U4 snRNA fragment. Mol. Cell 2000, 6:1331-1342.
57. Watkins N.J., Newman D.R., Kuhn J.F., Maxwell E.S. In vitro assembly of the mouse U14 snoRNP core complex and identification of a 65-kDa box C/D-binding protein. RNA 1998, 4:582-593.
58. Watkins N.J., Segault V., Charpentier B., Nottrott S., Fabrizio P., Bachi A., Wilm M., Rosbash M., Branlant C., Luhrmann R. A common core RNP structure shared between the small nucleoar box C/D RNPs and the spliceosomal U4 snRNP. Cell 2000, 103:457-466.
59. Watkins N.J., Dickmanns A., Luhrmann R. Conserved stem II of the box C/D motif is essential for nucleolar localization and is required, along with the 15.5K protein, for the hierarchical assembly of the box C/D snoRNP. Mol. Cell. Biol. 2002, 22:8342-8352.
60. Weinstein L.B., Steitz J.A. Guided tours: from precursor snoRNA to functional snoRNP. Curr. Opin. Cell Biol. 1999, 11:378-384.
61. Wu P., Brockenbrough J.S., Metcalfe A.C., Chen S., Aris J.P. Nop5p is a small nucleolar ribonucleoprotein component required for pre- 18 S rRNA processing in yeast. J. Biol. Chem. 1998, 273:16453-16463.
62. Ye K., Jia R., Lin J., Ju M., Peng J., Xu A., Zhang L. Structural organization of box C/D RNA-guided RNA methyltransferase. Proc. Natl. Acad. Sci. USA 2009, 106:13808-13813.
63. Zhang X., Champion E.A., Tran E.J., Brown B.A., Baserga S.J., Maxwell E.S. The coiled-coil domain of the Nop56/58 core protein is dispensable for sRNP assembly but is critical for archaeal box C/D sRNP-guided nucleotide methylation. RNA 2006, 12:1092-1103.