The structure of the box C/D enzyme reveals regulation of RNA methylation

Nature

Volumn 502, Issue 7472, 2013, Pages 519-523

  Lapinaite, Audrone ^a   Simon, Bernd ^a   Skjaerven, Lars ^a   Rakwalska Bange, Magdalena ^a   Gabel, Frank ^b,c,d,e   Carlomagno, Teresa ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b UNIV GRENOBLE ALPES   (France)

^c INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^d CNRS   (France)

^e INSTITUT LAUE LANGEVIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BOX C/D RIBONUCLEOPROTEIN; RIBONUCLEOPROTEIN; RIBOSE; RIBOSOME RNA; UNCLASSIFIED DRUG;

ENZYME; LIFE CYCLE; METHYLATION; NEUTRON SCATTERING; NUCLEAR MAGNETIC RESONANCE; RNA;

ARCHAEON; ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; ENZYME STRUCTURE; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; PYROCOCCUS FURIOSUS; REGULATORY MECHANISM; RNA FOLDING; RNA METHYLATION; RNA PROCESSING; RNA SEQUENCE; SMALL ANGLE SCATTERING;

APOPROTEINS; ARCHAEAL PROTEINS; BIOCATALYSIS; CHROMOSOMAL PROTEINS, NON-HISTONE; METHYLATION; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; NUCLEIC ACID CONFORMATION; PYROCOCCUS FURIOSUS; RIBONUCLEOPROTEINS, SMALL NUCLEOLAR; RNA FOLDING; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, ARCHAEAL; RNA, GUIDE; RNA, RIBOSOMAL;

ARCHAEA;

EID: 84886953122     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature12581     Document Type: Article

References (49)

1. Decatur, W. A. & Fournier, M. J. rRNA modifications and ribosome function. Trends Biochem. Sci. 27, 344-351 (2002).
2. Herschlag, D., Eckstein, F. & Cech, T. R. The importance of being ribose at the cleavage site in the Tetrahymena ribozyme reaction. Biochemistry 32, 8312-8321 (1993).
3. Williams, D. J., Boots, J. L. & Hall, K. B. Thermodynamics of 29-ribose substitutions in UUCG tetraloops. RNA 7, 44-53 (2001).
4. Helm, M. Post-transcriptional nucleotide modification and alternative folding of RNA. Nucleic Acids Res. 34, 721-733 (2006).
5. Kawai, G. et al. Conformational rigidity of specific pyrimidine residues in tRNA arises from posttranscriptional modifications that enhance steric interaction betweenthebaseandthe29-hydroxylgroup. Biochemistry 31, 1040-1046(1992).
6. Schimmang, T., Tollervey, D., Kern, H., Frank, R. & Hurt, E. A yeast nucleolar protein related to mammalian fibrillarin is associated with small nucleolar RNA and is essential for viability. EMBO J. 8, 4015-4024 (1989).
7. Tollervey, D., Lehtonen, H., Carmo-Fonseca, M. & Hurt, E. The small nucleolar RNP protein NOP1 (fibrillarin) is required for pre-rRNA processing inyeast. EMBO J. 10, 573-583 (1991).
8. Kiss-László, Z., Henry, Y. & Kiss, T. Sequence and structural elements of methylation guide snoRNAs essential for site-specific ribose methylation of pre-rRNA. EMBO J. 17, 797-807 (1998).
9. Nolivos, S., Carpousis, A. J. & Clouet-d'Orval, B. The K-loop, a general feature of the Pyrococcus C/D guide RNAs, is an RNA structural motif related to the K-turn. Nucleic Acids Res. 33, 6507-6514 (2005).
10. Reichow, S. L., Hamma, T., Ferre-D'Amare, A. R. & Varani, G. The structure and functionofsmall nucleolar ribonucleoproteins. Nucleic Acids Res. 35, 1452-1464 (2007).
11. 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. 30, 931-941 (2002).
12. Xue, S. et al. Structural basis for substrate placement by an archaeal box C/D ribonucleoprotein particle. Mol. Cell 39, 939-949 (2010).
13. Liu, S. et al. Binding ofthe human Prp31 nop domaintoa composite RNA-protein platform in U4 snRNP. Science 316, 115-120 (2007).
14. Aittaleb, M. et al. Structure and function of archaeal box C/D sRNP core proteins. Nature Struct. Mol. Biol. 10, 256-263 (2003).
15. Wang, H., Boisvert, D., Kim, K. K., Kim, R. & Kim, S. H. Crystal structure ofa fibrillarin homologue from Methanococcus jannaschii, a hyperthermophile, at 1. 6 A resolution. EMBO J. 19, 317-323 (2000).
16. Lin, J. et al. Structural basis for site-specific ribose methylation by box C/D RNA protein complexes. Nature 469, 559-563 (2011).
17. Bleichert, F. et al. A dimeric structure for archaeal box C/D small ribonucleoproteins. Science 325, 1384-1387 (2009).
18. Bower-Phipps, K. R., Taylor, D., Wang, H. & Baserga, S. The box C/D sRNP dimeric architecture is conserved across domain Archaea. RNA 18, 1527-1540 (2012).
19. Moore, T., Zhang, Y., Fenley, M. O. & Li, H. Molecular basis of box C/D RNA-protein interactions; cocrystal structureofarchaeal L7Ae andabox C/D RNA. Structure 12, 807-818 (2004).
20. Tugarinov, V. & Kay, L. E. Ile, Leu, and Val methyl assignments of the 723-residue malate synthase G using a new labeling strategy and novel NMR methods. J. Am. Chem. Soc. 125, 13868-13878 (2003).
21. Battiste, J. L. & Wagner, G. Utilization of site-directed spin labeling and high-resolution heteronuclear nuclear magnetic resonance for global fold determination of large proteins with limited nuclear Overhauser effect data. Biochemistry 39, 5355-5365 (2000).
22. Ghalei, H., Hsiao, H.-H., Urlaub, H., Wahl, M. C. & Watkins, N. J. A novel Nop5-sRNA interactionthatisrequiredfor efficientarchaealbox C/D sRNPformation. RNA16, 2341-2348 (2010).
23. Milligan, J. F., Groebe, D. R., Witherell, G. W. & Uhlenbeck, O. C. Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res. 15, 8783-8798 (1987).
24. Gosh, R. E., Egelhaaf, S. U. & Rennie, A. R. Computing Guide for Small Angle Scattering Experiments Technical Report ILL06GH05T (Institut Laue-Langevin, 2006).
25. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. J. & Svergun, D. I. PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Cryst. 36, 1277-1282 (2003).
26. Guinier, A. La diffraction des rayons X aux très petits angles: applications à l'étude de phénomènes ultramicroscopiques. Ann. Phys. 12, 161-237 (1939).
27. Svergun, D. I. et al. Protein hydrationinsolution: experimental observationbyX-ray and neutron scattering. Proc. Natl Acad. Sci. USA 95, 2267-2272 (1998).
28. Svergun, D. I. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25, 495-503 (1992).
29. Svergun, D. I. Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys. J. 76, 2879-2886 (1999)
30. Volkov, V. V. & Svergun, D. I. Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 36, 860-864 (2003).
31. Mylonas, E. & Svergun, D. I. Accuracyofmolecular mass determinationof proteins in solution by small-angle X-ray scattering. J. Appl. Crystallogr. 40, s245-s249 (2007).
32. Svergun, D., Barberato, C. & Koch, M. H. J. CRYSOL-A program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28, 768-773 (1995).
33. Grzesiek, S. & Bax, A. Improved 3Dtriple-resonance NMR techniques applied to a 31kDa protein. J. Magn. Reson. 96, 432-440 (1992).
34. Muhandiram, D. R. & Kay, L. E. Gradient-enhanced triple-resonance three-dimensional NMR experiments with improved sensitivity. J. Magn. Reson. B 103, 203-216 (1994).
35. Wittekind, M. G. & Mueller, L. HNCACB, a high-sensitivity 3D NMR experiment to correlate amide-proton and nitrogen resonances with the alpha-and beta-carbon resonances in proteins. J. Magn. Reson. B. 101, 201-205 (1993).
36. 13C magnetization. J. Magn. Reson. B. 101, 114-119 (1993).
37. Montelione, G. T., Lyons, B. A., Emerson, S. D. & Tashiro, M. An efficient triple resonance experiment using carbon-13 isotropic mixing for determining sequence-specific resonance assignmentsofisotopically-enriched proteins. J. Am. Chem. Soc. 114, 10974-10975 (1992).
38. Bax, A., Griffey, R. H. & Hawkins, B. L. Correlation of proton and nitrogen-15 chemical shifts by multiple quantum NMR. J. Magn. Reson. 55, 301-315 (1983).
39. Delaglio, F. et al. NMRPipe:a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293 (1995).
40. Johnson, B. A. & Blevins, R. A. NMR View:acomputer program for the visualization and analysis of NMR data. J. Biomol. NMR 4, 603-614 (1994).
41. Mulder, F. A., Schipper, D., Bott, R. & Boelens, R. Altered flexibility in the substrate-binding site of related native and engineered high-alkaline Bacillus subtilisins. J. Mol. Biol. 292, 111-123 (1999).
42. Simon, B., Madl, T., Mackereth, C. D., Nilges, M. & Sattler, M. Anefficient protocol for NMR-spectroscopy-based structure determination of protein complexes in solution. Angew. Chem. 49, 1967-1970 (2010).
43. Nilges, M. Calculation of protein structures with ambiguous distance restraints-Automated assignment of ambiguous NOE crosspeaks and disulfide connectivities. J. Mol. Biol. 245, 645-660 (1995).
44. Brünger, A. T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905-921 (1998).
45. 1H NMR. Proteins 17, 297-309 (1993).
46. Rambo, R. P. & Tainer, J. A. Accurate assessment of mass, models and resolution by small-angle scattering. Nature 496, 477-481 (2013)
47. AMBER. 12 (Univ. California, San Francisco, 2012).
48. Hornak, V. et al. Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65, 712-725 (2006)
49. Baker, N. A., Sept, D., Joseph, S., Holst, M. J. & McCammon, J. A. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl Acad. Sci. USA 98, 10037-10041 (2001).