Proteomic and 3D structure analyses highlight the C/D box snoRNP assembly mechanism and its control

Journal of Cell Biology

Volumn 207, Issue 4, 2014, Pages 463-480

  Bizarro, Jonathan ^a   Charron, Christophe ^b   Boulon, Séverine ^c   Westman, Belinda ^d   Pradet Balade, Bérengère ^a   Vandermoere, Franck ^e,g   Chagot, Marie Eve ^b   Hallais, Marie ^a   Ahmad, Yasmeen ^d   Leonhardt, Heinrich ^f   Lamond, Angus ^d   Manival, Xavier ^b   Branlant, Christiane ^b   Charpentier, Bruno ^b   Verheggen, Céline ^a   Bertrand, Edouard ^a  

^a CNRS   (France)

^b UNIVERSITÉ DE LORRAINE   (France)

^c Centre National de la Recherche Scientifique   (France)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

^e INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^f UNIVERSITY OF MUNICH   (Germany)

^g UNIV MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; AMINO ACID; CORE PROTEIN; DEOXYCHOLIC ACID; FIBRILLARIN; NOP56 PROTEIN; NOP58 PROTEIN; PROTEIN; RIBONUCLEASE; SMALL NUCLEOLAR RIBONUCLEOPROTEIN; SMALL NUCLEOLAR RNA; STABLE ISOTOPE; TRITON X 114; UNCLASSIFIED DRUG; CARRIER PROTEIN; DNA BINDING PROTEIN; DNA HELICASE; HEAT SHOCK PROTEIN 90; KLF6 PROTEIN, HUMAN; KRUPPEL LIKE FACTOR; NHP2L1 PROTEIN, HUMAN; NUCLEAR PROTEIN; NUFIP1 PROTEIN, HUMAN; NUFIP2 PROTEIN, HUMAN; ONCOPROTEIN; PROTEIN BINDING; RNA BINDING PROTEIN; RUVBL1 PROTEIN, HUMAN; RUVBL2 PROTEIN, HUMAN; SMALL NUCLEAR RIBONUCLEOPROTEIN; TRIP3 PROTEIN, HUMAN; TUMOR PROTEIN; ZNF331 PROTEIN, HUMAN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CELL CULTURE; CELL FRACTIONATION; CRYSTAL STRUCTURE; FLUORESCENCE MICROSCOPY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; HYDROGEN BOND; IMMUNOPRECIPITATION; MASS SPECTROMETRY; POINT MUTATION; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEOMICS; QUANTITATIVE ANALYSIS; RIBONUCLEASE PROTECTION ASSAY; SCHIZOSACCHAROMYCES POMBE; THREE DIMENSIONAL STRUCTURE; WESTERN BLOTTING; WILD TYPE; AMINO ACID SEQUENCE; BINDING SITE; CHEMICAL PHENOMENA; CHEMISTRY; GENETICS; HEK293 CELL LINE; HELA CELL LINE; METABOLISM; PROCEDURES; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; TUMOR CELL LINE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BINDING SITES; CARRIER PROTEINS; CELL LINE, TUMOR; CRYSTALLOGRAPHY, X-RAY; DNA HELICASES; DNA-BINDING PROTEINS; HEK293 CELLS; HELA CELLS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; NEOPLASM PROTEINS; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEOMICS; PROTO-ONCOGENE PROTEINS; RIBONUCLEASES; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RIBONUCLEOPROTEINS, SMALL NUCLEOLAR; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT;

EID: 84918533144     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201404160     Document Type: Article

References (72)

1. Aittaleb, M., R. Rashid, Q. Chen, J.R. Palmer, C.J. Daniels, and H. Li. 2003. Structure and function of archaeal box C/D sRNP core proteins. Nat. Struct. Biol. 10:256-263. http://dx.doi.org/10.1038/nsb905
2. Back, R., C. Dominguez, B. Rothé, C. Bobo, C. Beaufils, S. Moréra, P. Meyer, B. Charpentier, C. Branlant, F.H. Allain, and X. Manival. 2013. High-resolution structural analysis shows how Tah1 tethers Hsp90 to the R2TP complex. Structure. 21:1834-1847. http://dx.doi.org/10.1016/j.str.2013.07.024
3. Bardoni, B., A. Schenck, and J.L. Mandel. 1999. A novel RNA-binding nuclear protein that interacts with the fragile X mental retardation (FMR1) protein. Hum. Mol. Genet. 8:2557-2566. http://dx.doi.org/10.1093/hmg/8.13.2557
4. Battle, D.J., C.K. Lau, L. Wan, H. Deng, F. Lotti, and G. Dreyfuss. 2006. The Gemin5 protein of the SMN complex identifies snRNAs. Mol. Cell. 23:273-279. http://dx.doi.org/10.1016/j.molcel.2006.05.036
5. Boulon, S., C. Verheggen, B.E. Jady, C. Girard, C. Pescia, C. Paul, J.K. Ospina, T. Kiss, A.G. Matera, R. Bordonné, and E. Bertrand. 2004. PHAX and CRM1 are required sequentially to transport U3 snoRNA to nucleoli. Mol. Cell. 16:777-787. http://dx.doi.org/10.1016/j.molcel.2004.11.013
6. Boulon, S., N. Marmier-Gourrier, B. Pradet-Balade, L. Wurth, C. Verheggen, B.E. Jády, B. Rothé, C. Pescia, M.C. Robert, T. Kiss, et al. 2008. The Hsp90 chaperone controls the biogenesis of L7Ae RNPs through conserved machinery. J. Cell Biol. 180:579-595. http://dx.doi.org/10.1083/jcb.200708110
7. Boulon, S., Y. Ahmad, L. Trinkle-Mulcahy, C. Verheggen, A. Cobley, P. Gregor, E. Bertrand, M. Whitehorn, and A.I. Lamond. 2010a. Establishment of a protein frequency library and its application in the reliable identification of specific protein interaction partners. Mol. Cell. Proteomics. 9:861-879.http://dx.doi.org/10.1074/mcp.M900517-MCP200
8. Boulon, S., B. Pradet-Balade, C. Verheggen, D. Molle, S. Boireau, M. Georgieva, K. Azzag, M.C. Robert, Y. Ahmad, H. Neel, et al. 2010b. HSP90 and its R2TP/Prefoldin-like cochaperone are involved in the cytoplasmic assembly of RNA polymerase II. Mol. Cell. 39:912-924. http://dx.doi.org/10.1016/j.molcel.2010.08.023
9. Cavaillé, J., M. Nicoloso, and J.P. Bachellerie. 1996. Targeted ribose methylation of RNA in vivo directed by tailored antisense RNA guides. Nature. 383:732-735. http://dx.doi.org/10.1038/383732a0
10. Chari, A., M.M. Golas, M. Klingenhäger, N. Neuenkirchen, B. Sander, C. Englbrecht, A. Sickmann, H. Stark, and U. Fischer. 2008. An assembly chaperone collaborates with the SMN complex to generate spliceosomal SnRNPs. Cell. 135:497-509. http://dx.doi.org/10.1016/j.cell.2008.09.020
11. Charron, C., X. Manival, B. Charpentier, C. Branlant, and A. Aubry. 2004a. Purification, crystallization and preliminary X-ray diffraction data of L7Ae sRNP core protein from Pyrococcus abyssii. Acta Crystallogr. D Biol. Crystallogr. 60:122-124. http://dx.doi.org/10.1107/S090744490302239X
12. Charron, C., X. Manival, A. Cléry, V. Senty-Ségault, B. Charpentier, N. Marmier- Gourrier, C. Branlant, and A. Aubry. 2004b. 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. http://dx.doi.org/10.1016/j.jmb.2004.07.046
13. Cheung, K.L., J. Huen, Y. Kakihara, W.A. Houry, and J. Ortega. 2010. Alternative oligomeric states of the yeast Rvb1/Rvb2 complex induced by histidine tags. J. Mol. Biol. 404:478-492. http://dx.doi.org/10.1016/j.jmb.2010.10.003
14. Cloutier, P., R. Al-Khoury, M. Lavallée-Adam, D. Faubert, H. Jiang, C. Poitras, A. Bouchard, D. Forget, M. Blanchette, and B. Coulombe. 2009. Highresolution mapping of the protein interaction network for the human transcription machinery and affinity purification of RNA polymerase II-associated complexes. Methods. 48:381-386. http://dx.doi.org/10.1016/j.ymeth.2009.05.005
15. Cox, J., I. Matic, M. Hilger, N. Nagaraj, M. Selbach, J.V. Olsen, and M. Mann. 2009. A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat. Protoc. 4:698-705. http://dx.doi.org/10.1038/nprot.2009.36
16. Diebold, M.L., S. Fribourg, M. Koch, T. Metzger, and C. Romier. 2011. Deciphering correct strategies for multiprotein complex assembly by coexpression: application to complexes as large as the histone octamer. J. Struct. Biol. 175:178-188. http://dx.doi.org/10.1016/j.jsb.2011.02.001
17. Eckert, K., J.M. Saliou, L. Monlezun, A. Vigouroux, N. Atmane, C. Caillat, S. Quevillon-Chéruel, K. Madiona, M. Nicaise, S. Lazereg, et al. 2010. The Pih1-Tah1 cochaperone complex inhibits Hsp90 molecular chaperone ATPase activity. J. Biol. Chem. 285:31304-31312. http://dx.doi.org/10.1074/jbc.M110.138263
18. Emsley, P., B. Lohkamp, W.G. Scott, and K. Cowtan. 2010. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66:486-501. http://dx.doi.org/10.1107/S0907444910007493
19. Eswar, N., B. Webb, M.A. Marti-Renom, M.S. Madhusudhan, D. Eramian, M.Y. Shen, U. Pieper, and A. Sali. 2006. Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinformatics. Chapter 5:Unit 5.6.
20. Fischer, U., Q. Liu, and G. Dreyfuss. 1997. The SMN-SIP1 complex has an essential role in spliceosomal snRNP biogenesis. Cell. 90:1023-1029. http://dx.doi.org/10.1016/S0092-8674(00)80368-2
21. Fischer, U., C. Englbrecht, and A. Chari. 2011. Biogenesis of spliceosomal small nuclear ribonucleoproteins. Wiley Interdiscip. Rev. RNA. 2:718-731. http://dx.doi.org/10.1002/wrna.87
22. Gonzales, F.A., N.I. Zanchin, J.S. Luz, and C.C. Oliveira. 2005. Characterization of Saccharomyces cerevisiae Nop17p, a novel Nop58p-interacting protein that is involved in Pre-rRNA processing. J. Mol. Biol. 346:437-455. http://dx.doi.org/10.1016/j.jmb.2004.11.071
23. Gorynia, S., T.M. Bandeiras, F.G. Pinho, C.E. McVey, C. Vonrhein, A. Round, D.I. Svergun, P. Donner, P.M. Matias, and M.A. Carrondo. 2011. Structural and functional insights into a dodecameric molecular machine - the RuvBL1/RuvBL2 complex. J. Struct. Biol. 176:279-291. http://dx.doi.org/10.1016/j.jsb.2011.09.001
24. Grimm, C., A. Chari, J.P. Pelz, J. Kuper, C. Kisker, K. Diederichs, H. Stark, H. Schindelin, and U. Fischer. 2013. Structural basis of assembly chaperonemediated snRNP formation. Mol. Cell. 49:692-703. http://dx.doi.org/10.1016/j.molcel.2012.12.009
25. Grozdanov, P.N., S. Roy, N. Kittur, and U.T. Meier. 2009. SHQ1 is required prior to NAF1 for assembly of H/ACA small nucleolar and telomerase RNPs. RNA. 15:1188-1197. http://dx.doi.org/10.1261/rna.1532109
26. Ito, T., T. Chiba, R. Ozawa, M. Yoshida, M. Hattori, and Y. Sakaki. 2001. A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. USA. 98:4569-4574. http://dx.doi.org/10.1073/pnas.061034498
27. Jeronimo, C., D. Forget, A. Bouchard, Q. Li, G. Chua, C. Poitras, C. Thérien, D. Bergeron, S. Bourassa, J. Greenblatt, et al. 2007. Systematic analysis of the protein interaction network for the human transcription machinery reveals the identity of the 7SK capping enzyme. Mol. Cell. 27:262-274.http://dx.doi.org/10.1016/j.molcel.2007.06.027
28. Kabsch, W. 2010. XDS. Acta Crystallogr. D Biol. Crystallogr. 66:125-132.http://dx.doi.org/10.1107/S0907444909047337
29. Kemmler, S., L. Occhipinti, M. Veisu, and V.G. Panse. 2009. Yvh1 is required for a late maturation step in the 60S biogenesis pathway. J. Cell Biol. 186:863-880. http://dx.doi.org/10.1083/jcb.200904111
30. King, T.H., W.A. Decatur, E. Bertrand, E.S. Maxwell, and M.J. Fournier. 2001. A well-connected and conserved nucleoplasmic helicase is required for production of box C/D and H/ACA snoRNAs and localization of snoRNP proteins. Mol. Cell. Biol. 21:7731-7746. http://dx.doi.org/10.1128/MCB.21.22.7731-7746.2001
31. Kiss, T., E. Fayet, B.E. Jády, P. Richard, and M. Weber. 2006. Biogenesis and intranuclear trafficking of human box C/D and H/ACA RNPs. Cold Spring Harb. Symp. Quant. Biol. 71:407-417. http://dx.doi.org/10.1101/sqb.2006.71.025
32. Kiss, T., E. Fayet-Lebaron, and B.E. Jády. 2010. Box H/ACA small ribonucleoproteins. Mol. Cell. 37:597-606. http://dx.doi.org/10.1016/j.molcel.2010.01.032
33. Kiss-László, Z., Y. Henry, J.P. Bachellerie, M. Caizergues-Ferrer, and T. Kiss. 1996. Site-specific ribose methylation of preribosomal RNA: a novel function for small nucleolar RNAs. Cell. 85:1077-1088. http://dx.doi.org/10.1016/S0092-8674(00)81308-2
34. Lapinaite, A., B. Simon, L. Skjaerven, M. Rakwalska-Bange, F. Gabel, and T. Carlomagno. 2013. The structure of the box C/D enzyme reveals regulation of RNA methylation. Nature. 502:519-523. http://dx.doi.org/10.1038/nature12581
35. Laskowski, R.A., M.W. McArthur, D.S. Moss, and J.M. Thornton. 1993. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 26:283-291. http://dx.doi.org/10.1107/S0021889892009944
36. Li, S., J. Duan, D. Li, S. Ma, and K. Ye. 2011a. Structure of the Shq1-Cbf5-Nop10-Gar1 complex and implications for H/ACA RNP biogenesis and dyskeratosis congenita. EMBO J. 30:5010-5020. http://dx.doi.org/10.1038/emboj.2011.427
37. Li, S., J. Duan, D. Li, B. Yang, M. Dong, and K. Ye. 2011b. Reconstitution and structural analysis of the yeast box H/ACA RNA-guided pseudouridine synthase. Genes Dev. 25:2409-2421. http://dx.doi.org/10.1101/gad.175299.111
38. Liang, B., and H. Li. 2011. Structures of ribonucleoprotein particle modification enzymes. Q. Rev. Biophys. 44:95-122. http://dx.doi.org/10.1017/S0033583510000235
39. Lin, J., S. Lai, R. Jia, A. Xu, L. Zhang, J. Lu, and K. Ye. 2011. Structural basis for site-specific ribose methylation by box C/D RNA protein complexes.Nature. 469:559-563. http://dx.doi.org/10.1038/nature09688
40. Liu, S., P. Li, O. Dybkov, S. Nottrott, K. Hartmuth, R. Lührmann, T. Carlomagno, and M.C. Wahl. 2007. Binding of the human Prp31 Nop domain to a composite RNA-protein platform in U4 snRNP. Science. 316:115-120.http://dx.doi.org/10.1126/science.1137924
41. Lukowiak, A.A., S. Granneman, S.A. Mattox, W.A. Speckmann, K. Jones, H. Pluk, W.J. Venrooij, R.M. Terns, and M.P. Terns. 2000. Interaction of the U3-55k protein with U3 snoRNA is mediated by the box B/C motif of U3 and the WD repeats of U3-55k. Nucleic Acids Res. 28:3462-3471.http://dx.doi.org/10.1093/nar/28.18.3462
42. Machado-Pinilla, R., D. Liger, N. Leulliot, and U.T. Meier. 2012. Mechanism of the AAA+ ATPases pontin and reptin in the biogenesis of H/ACA RNPs. RNA. 18:1833-1845. http://dx.doi.org/10.1261/rna.034942.112
43. Matera, A.G., R.M. Terns, and M.P. Terns. 2007. Non-coding RNAs: lessons from the small nuclear and small nucleolar RNAs. Nat. Rev. Mol. Cell Biol. 8:209-220. http://dx.doi.org/10.1038/nrm2124
44. McKeegan, K.S., C.M. Debieux, S. Boulon, E. Bertrand, and N.J. Watkins. 2007. A dynamic scaffold of pre-snoRNP factors facilitates human box C/D snoRNP assembly. Mol. Cell. Biol. 27:6782-6793. http://dx.doi.org/10.1128/MCB.01097-07
45. McKeegan, K.S., C.M. Debieux, and N.J. Watkins. 2009. 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. 29:4971-4981. http://dx.doi.org/10.1128/MCB.00752-09
46. Meister, G., D. Bühler, R. Pillai, F. Lottspeich, and U. Fischer. 2001. A multiprotein complex mediates the ATP-dependent assembly of spliceosomal U snRNPs. Nat. Cell Biol. 3:945-949. http://dx.doi.org/10.1038/ncb1101-945
47. Newman, D.R., J.F. Kuhn, G.M. Shanab, and E.S. Maxwell. 2000. Box C/D snoRNA-associated proteins: two pairs of evolutionarily ancient proteins and possible links to replication and transcription. RNA. 6:861-879. http://dx.doi.org/10.1017/S1355838200992446
48. Oruganti, S., Y. Zhang, and H. Li. 2005. Structural comparison of yeast snoRNP and spliceosomal protein Snu13p with its homologs. Biochem. Biophys. Res. Commun. 333:550-554. http://dx.doi.org/10.1016/j.bbrc.2005.05.141
49. Pal, M., M. Morgan, S.E. Phelps, S.M. Roe, S. Parry-Morris, J.A. Downs, S. Polier, L.H. Pearl, and C. Prodromou. 2014. Structural basis for phosphorylation-dependent recruitment of Tel2 to Hsp90 by Pih1. Structure. 22:805-818. http://dx.doi.org/10.1016/j.str.2014.04.001
50. Peng, W.T., M.D. Robinson, S. Mnaimneh, N.J. Krogan, G. Cagney, Q. Morris, A.P. Davierwala, J. Grigull, X. Yang, W. Zhang, et al. 2003. A panoramic view of yeast noncoding RNA processing. Cell. 113:919-933. http://dx.doi.org/10.1016/S0092-8674(03)00466-5
51. Rothé, B., R. Back, M. Quinternet, J. Bizarro, M.C. Robert, M. Blaud, C. Romier, X. Manival, B. Charpentier, E. Bertrand, and C. Branlant. 2014. Characterization of the interaction between protein Snu13p/15.5K and the Rsa1p/NUFIP factor and demonstration of its functional importance for snoRNP assembly. Nucleic Acids Res. 42:2015-2036. http://dx.doi.org/10.1093/nar/gkt1091
52. Schultz, A., S. Nottrott, N.J. Watkins, and R. Lührmann. 2006. Protein-protein and protein-RNA contacts both contribute to the 15.5K-mediated assembly of the U4/U6 snRNP and the box C/D snoRNPs. Mol. Cell. Biol.26:5146-5154. http://dx.doi.org/10.1128/MCB.02374-05
53. Terns, M., and R. Terns. 2006. Noncoding RNAs of the H/ACA family. Cold Spring Harb. Symp. Quant. Biol. 71:395-405. http://dx.doi.org/10.1101/sqb.2006.71.034
54. Terwilliger, T.C. 2000. Maximum-likelihood density modification. Acta Crystallogr. D Biol. Crystallogr. 56:965-972. http://dx.doi.org/10.1107/S0907444900005072
55. Terwilliger, T.C., and J. Berendzen. 1999. Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr. 55:849-861. http://dx.doi.org/10.1107/S0907444999000839
56. Tosi, A., C. Haas, F. Herzog, A. Gilmozzi, O. Berninghausen, C. Ungewickell, C.B. Gerhold, K. Lakomek, R. Aebersold, R. Beckmann, and K.P. Hopfner. 2013. Structure and subunit topology of the INO80 chromatin remodeler and its nucleosome complex. Cell. 154:1207-1219. http://dx.doi.org/10.1016/j.cell.2013.08.016
57. Vagin, A.A., R.A. Steiner, A.A. Lebedev, L. Potterton, S. McNicholas, F. Long, and G.N. Murshudov. 2004. REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use. Acta Crystallogr. D Biol. Crystallogr. 60:2184-2195. http://dx.doi.org/10.1107/S0907444904023510
58. Verheggen, C., D.L. Lafontaine, D. Samarsky, J. Mouaikel, J.M. Blanchard, R. Bordonné, and E. Bertrand. 2002. Mammalian and yeast U3 snoRNPs are matured in specific and related nuclear compartments. EMBO J. 21:2736-2745. http://dx.doi.org/10.1093/emboj/21.11.2736
59. Vidovic, I., S. Nottrott, K. Hartmuth, R. Lührmann, and R. Ficner. 2000. Crystal structure of the spliceosomal 15.5kD protein bound to a U4 snRNA fragment. Mol. Cell. 6:1331-1342. http://dx.doi.org/10.1016/S1097-2765(00)00131-3
60. Walbott, H., R. Machado-Pinilla, D. Liger, M. Blaud, S. Réty, P.N. Grozdanov, K. Godin, H. van Tilbeurgh, G. Varani, U.T. Meier, and N. Leulliot. 2011. The H/ACA RNP assembly factor SHQ1 functions as an RNA mimic. Genes Dev. 25:2398-2408. http://dx.doi.org/10.1101/gad.176834.111
61. Wang, C., and U.T. Meier. 2004. Architecture and assembly of mammalian H/ACA small nucleolar and telomerase ribonucleoproteins. EMBO J. 23:1857-1867. http://dx.doi.org/10.1038/sj.emboj.7600181
62. Watkins, N.J., and M.T. Bohnsack. 2012. The box C/D and H/ACA snoRNPs: key players in the modification, processing and the dynamic folding of ribosomal RNA. Wiley Interdiscip Rev RNA. 3:397-414. http://dx.doi.org/10.1002/wrna.117
63. Watkins, N.J., V. Ségault, B. Charpentier, S. Nottrott, P. Fabrizio, A. Bachi, M. Wilm, M. Rosbash, C. Branlant, and R. Lührmann. 2000. A common core RNP structure shared between the small nucleoar box C/D RNPs and the spliceosomal U4 snRNP. Cell. 103:457-466. http://dx.doi.org/10.1016/S0092-8674(00)00137-9
64. Watkins, N.J., A. Dickmanns, and R. Lührmann. 2002. 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. 22:8342-8352. http://dx.doi.org/10.1128/MCB.22.23.8342-8352.2002
65. Watkins, N.J., I. Lemm, D. Ingelfinger, C. Schneider, M. Hossbach, H. Urlaub, and R. Lührmann. 2004. Assembly and maturation of the U3 snoRNP in the nucleoplasm in a large dynamic multiprotein complex. Mol. Cell. 16:789-798. http://dx.doi.org/10.1016/j.molcel.2004.11.012
66. Winn, M.D., C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, P.R. Evans, R.M. Keegan, E.B. Krissinel, A.G. Leslie, A. McCoy, et al. 2011. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67:235-242. http://dx.doi.org/10.1107/S0907444910045749
67. Xue, S., R. Wang, F. Yang, R.M. Terns, M.P. Terns, X. Zhang, E.S. Maxwell, and H. Li. 2010. Structural basis for substrate placement by an archaeal box C/D ribonucleoprotein particle. Mol. Cell. 39:939-949. http://dx.doi.org/10.1016/j.molcel.2010.08.022
68. Ye, K., R. Jia, J. Lin, M. Ju, J. Peng, A. Xu, and L. Zhang. 2009. Structural organization of box C/D RNA-guided RNA methyltransferase. Proc. Natl. Acad. Sci. USA. 106:13808-13813. http://dx.doi.org/10.1073/pnas.0905128106
69. Yong, J., M. Kasim, J.L. Bachorik, L. Wan, and G. Dreyfuss. 2010. Gemin5 delivers snRNA precursors to the SMN complex for snRNP biogenesis. Mol. Cell. 38:551-562. http://dx.doi.org/10.1016/j.molcel.2010.03.014
70. Zhang, R., B.R. So, P. Li, J. Yong, T. Glisovic, L. Wan, and G. Dreyfuss. 2011. Structure of a key intermediate of the SMN complex reveals Gemin2's crucial function in snRNP assembly. Cell. 146:384-395. http://dx.doi.org/10.1016/j.cell.2011.06.043
71. Zhao, R., M. Davey, Y.C. Hsu, P. Kaplanek, A. Tong, A.B. Parsons, N. Krogan, G. Cagney, D. Mai, J. Greenblatt, et al. 2005. Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone. Cell. 120:715-727. http://dx.doi.org/10.1016/j.cell.2004.12.024
72. Zhao, R., Y. Kakihara, A. Gribun, J. Huen, G. Yang, M. Khanna, M. Costanzo, R.L.Brost, C. Boone, T.R. Hughes, et al. 2008. Molecular chaperone Hsp90 stabilizes Pih1/Nop17 to maintain R2TP complex activity that regulates snoRNA accumulation. J. Cell Biol. 180:563-578. http://dx.doi.org/10.1083/jcb.200709061