The crystal structure of the Methanocaldococcus jannaschii multifunctional L7Ae RNA-binding protein reveals an induced-fit interaction with the box C/D RNAs

Biochemistry

Volumn 44, Issue 28, 2005, Pages 9657-9672

  Suryadi, Jimmy ^a,b   Tran, Elizabeth J ^c,d   Maxwell, E Stuart ^c   Brown II, Bernard A ^a,b  

^a WAKE FOREST UNIVERSITY   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BIOTECHNOLOGY; CRYSTAL STRUCTURE; NUCLEIC ACID SEQUENCES; RNA;

EVOLUTIONARY CONSERVATIONS; K-TURN MOTIF; RIBOSOMAL PROTEIN; RNA-BINDING PROTEINS;

PROTEINS;

BOX C D RNA; PROTEIN L7AE; RNA; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID COMPOSITION; ARCHAEBACTERIUM; ARTICLE; CIRCULAR DICHROISM; CRYSTAL STRUCTURE; METHANOCALDOCOCCUS JANNASCHII; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RNA BINDING; STRUCTURAL HOMOLOGY; STRUCTURE ANALYSIS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ARCHAEAL PROTEINS; BASE SEQUENCE; CRYSTALLOGRAPHY, X-RAY; METHANOCOCCUS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; RIBONUCLEOPROTEINS, SMALL NUCLEAR; RIBOSOMAL PROTEINS; RNA, ARCHAEAL; RNA-BINDING PROTEINS; STRUCTURAL HOMOLOGY, PROTEIN; THERMODYNAMICS;

ARCHAEA; METHANOCALDOCOCCUS JANNASCHII;

EID: 22244460838     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050568q     Document Type: Article

References (87)

1. Maxwell, E. S., and Fournier, M. J. (1995) The small nucleolar RNAs, Annu. Rev. Biochem. 64, 897-934.
2. Kiss, T. (2001) Small nucleolar RNA-guided post-transcriptional modification of cellular RNAs, EMBO J. 20, 3617-3622.
3. Kiss, T. (2002) Small nucleolar RNAs: An abundant group of noncoding RNAs with diverse cellular functions, Cell 109, 145-148.
4. Bachellerie, J. P., Cavaille, J., and Huttenhofer, A. (2002) The expanding snoRNA world, Biochimie 84, 775-790.
5. Terns, M. P., and Terns, R. M. (2002) Small nucleolar RNAs: Versatile trans-acting molecules of ancient evolutionary origin, Gene Expression 10, 17-39.
6. Decatur, W. A., and Fournier, M. J. (2002) rRNA modifications and ribosome function, Trends Biochem. Sci. 27, 344-351.
7. King, T. H., Liu, B., McCully, R. R., and Fournier, M. J. (2003) Ribosome structure and activity are altered in cells lacking snoRNPs that form pseudouridines in the peptidyl transferase center, Mol. Cell 11, 425-435.
8. Henras, A. K., Dez, C., and Henry, Y. (2004) RNA structure and function in C/D and H/ACA s(no)RNPs, Curr. Opin. Struct. Biol. 14, 335-343.
9. Tran, E., Brown, J., and Maxwell, E. S. (2004) Evolutionary origins of the RNA-guided nucleotide-modification complexes: From the primitive translation apparatus? Trends Biochem. Sci. 29, 343-350.
10. Maden, B. E. (1990) The numerous modified nucleotides in eukaryotic ribosomal RNA, Prog. Nucleic Acids Res. 39, 241-303.
11. Gaspin, C., Cavaille, J., Erauso, G., and Bachellerie, J. P. (2000) Archaeal homologs of eukaryotic methylation guide small nucleolar RNAs: Lessons from the Pyrococcus genomes, J. Mol. Biol. 297, 895-906.
12. Omer, A. D., Lowe, T. M., Russell, A. G., Ebhardt, H., Eddy, S. R., and Dennis, P. P. (2000) Homologs of small nucleolar RNAs in Archaea, Science 288, 517-522.
13. Dennis, P. P., Omer, A., and Lowe, T. (2001) A guided tour: Small RNA function in Archaea, Mol. Microbiol. 40, 509-519.
14. Kuhn, J. F., Tran, E. J., and Maxwell, E. S. (2002) Archaeal ribosomal protein L7 is a functional homolog of the eukaryotic 15.5kD/Snu13p snoRNP core protein, Nucleic Acids Res. 30, 931-941.
15. Tollervey, D. (1996) Trans-acting factors in ribosome synthesis, Exp. Cell Res. 229, 226-232.
16. Kiss-Laszlo, Z., Henry, Y., and Kiss, T. (1998) Sequence and structural elements of methylation guide snoRNAs essential for site-specific ribose methylation of pre-rRNA, EMBO J. 17, 797-807.
17. Tycowski, K. T., You, Z. H., Graham, P. J., and Steitz, J. A. (1998) Modification of U6 spliceosomal RNA is guided by other small RNAs, Mol. Cell 2, 629-638.
18. Jady, B., and Kiss, T. (2001) A small nucleolar guide RNA functions both in 2′-O-ribose methylation and pseudouridylation of the U5 spliceosomal RNA, EMBO J. 20, 541-551.
19. Tyc, K., and Steitz, J. A. (1989) U3, U8 and U13 comprise a new class of mammalian snRNPs localized in the cell nucleolus, EMBO J. 8, 3113-3119.
20. Caffarelli, E., Fatica, A., Prislei, S., De Gregorio, E., Fragapane, P., and Bozzoni, I. (1996) Processing of the intron-encoded U16 and U18 snoRNAs: The conserved C and D boxes control both the processing reaction and the stability of the mature snoRNA, EMBO J. 15, 1121-1131.
21. Cavaille, J., Nicoloso, M., and Bachellerie, J. P. (1996) Targeted ribose methylation of RNA in vivo directed by tailored antisense RNA guides, Nature 383, 732-735.
22. Watkins, N. J., Leverette, R. D., Xia, L., Andrews, M. T., and Maxwell, E. S. (1996) Elements essential for processing intronic U14 snoRNA are located at the termini of the mature snoRNA sequence and include conserved nucleotide boxes C and D, RNA 2, 118-133.
23. Watkins, N. J., Segault, V., Charpentier, B., Nottrott, S., Fabrizio, P., Bachi, A., Wilm, M., Rosbash, M., Branlant, C., and Lührmann, R. (2000) A common core RNP structure shared between the small nucleolar box C/D RNPs and the spliceosomal U4 snRNP, Cell 103, 457-466.
24. Kiss-Laszlo, Z., Henry, Y., Bachellerie, J. P., Caizergues-Ferrer, M., and Kiss, T. (1996) Site-specific ribose methylation of preribosomal RNA: A novel function for small nucleolar RNAs, Cell 85, 1077-1088.
25. Bachellerie, J. P., and Cavaille, J. (1997) Guiding ribose methylation of rRNA, Trends Biochem. Sci. 22, 257-261.
26. Klein, D. J., Schmeing, T. M., Moore, P. B., and Steitz, T. A. (2001) The kink-turn: A new RNA secondary structure motif, EMBO J. 20, 4214-4221.
27. Mao, H., White, S. A., and Williamson, J. R. (1999) A novel loop-loop recognition motif in the yeast ribosomal protein L30 autoregulatory RNA complex, Nat. Struct. Biol. 6, 1139-1147.
28. Ban, N., Nissen, P., Hansen, J., Moore, P. B., and Steitz, T. A. (2000) The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution, Science 289, 905-920.
29. Schluenzen, F., Tocilj, A., Zarivach, R., Harms, J., Gluehmann, M., Janell, D., Bashan, A., Bartels, H., Agmon, I., Franceschi, F., and Yonath, A. (2000) Structure of functionally activated small ribosomal subunit at 3.3 Å resolution, Cell 102, 615-623.
30. Vidovic, I., Nottrott, S., Hartmuth, K., Luhrmann, R., and Ficner, R. (2000) Crystal structure of the spliceosomal 15.5kD protein bound to a U4 snRNA fragment, Mol. Cell 6, 1331-1342.
31. Wimberly, B. T., Brodersen, D. E., Clemons, W. M., Jr., Morgan-Warren, R. J., Carter, A. P., Vonrhein, C., Hartsch, T., and Ramakrishnan, V. (2000) Structure of the 30S ribosomal subunit, Nature 407, 327-339.
32. Winkler, W. C., Grundy, F. J., Murphy, B. A., and Henkin, T. M. (2001) The G·A motif: An RNA element common to bacterial antitermination systems, rRNA, and eukaryotic RNAs, RNA 7, 1165-1172.
33. Allmang, C., Carbon, P., and Krol, A. (2002) The SBP2 and 15.5 kD/Snu13p proteins share the same RNA binding domain: Identification of SBP2 amino acids important to SECIS RNA binding, RNA 8, 1308-1318.
34. Rozhdestvensky, T. S., Tang, T. H., Tchirkova, I. V., Brosius, J., Bachellerie, J. P., and Huttenhofer, A. (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.
35. Hamma, T., and Ferré-D'Amaré, A. R. (2004) Structure of protein L7Ae bound to a K-turn derived from an archaeal box H/ACA sRNA at 1.8 Å resolution, Structure 12, 893-903.
36. Moore, T., Zhang, Y., Fenley, M. O., and Li, H. (2004) Molecular basis of box C/D RNA-protein interactions: Cocrystal structure of archaeal L7Ae and a box C/D RNA, Structure 12, 807-818.
37. Strobel, S. A., Adams, P. L., Stanley, M. R., and Wang, J. (2004) RNA kink turns to the left and to the right, RNA 10, 1852-1854.
38. Matsumura, S., Ikawa, Y., and Inoue, T. (2003) Biochemical characterization of the kink-turn RNA motif, Nucleic Acids Res. 31, 5544-5551.
39. Goody, T. A., Melcher, S. E., Norman, D. G., and Lilley, D. M. (2004) The kink-turn motif in RNA is dimorphic, and metal ion-dependent, RNA 10, 254-264.
40. Cahill, N. M., Friend, K., Speckmann, W., Li, Z. H., Terns, R. M., Terns, M. P., and Steitz, J. A. (2002) Site-specific cross-linking analyses reveal an asymmetric protein distribution for a box C/D snoRNP, EMBO J. 21, 3816-3828.
41. Szewczak, L. B., DeGregorio, S. J., Strobel, S. A., and Steitz, J. A. (2002) Exclusive interaction of the 15.5 kD protein with the terminal box C/D motif of a methylation guide snoRNP. Chem. Biol. 9, 1095-1107.
42. Tran, E. J., Zhang, X., and Maxwell, E. S. (2003) Efficient RNA 2′-O-methylation requires juxtaposed and symmetrically assembled archaeal box C/D and C′/D′ RNPs, EMBO J. 22, 3930-3940.
43. Omer, A. D., Ziesche, S., Ebhardt, H., and Dennis, P. P. (2002) In vitro reconstitution and activity of a C/D box methylation guide ribonucleoprotein complex, Proc. Natl. Acad. Sci. U.S.A. 99, 5289-5294.
44. Koonin, E. V., Bork, P., and Sander, C. (1994) A novel RNA-binding motif in omnipotent suppressors of translation termination, ribosomal proteins and a ribosome modification enzyme? Nucleic Acids Res. 22, 2166-2167.
45. Chavatte, L., Brown, B. A., and Driscoll, D. M. (2005) Ribosomal protein L30 is a component of the UGA-selenocysteine recoding machinery in eukaryotes, Nat. Struct. Mol. Biol. 12, 408-416.
46. Klein, D. J., Moore, P. B., and Steitz, T. A. (2004) The roles of ribosomal proteins in the structure assembly, and evolution of the large ribosomal subunit, J. Mol. Biol. 340, 141-177.
47. Charron, C., Manival, X., Clery, A., Senty-Segault, V., Charpentier, B., Marmier-Gourrier, N., Branlant, C., and Aubry, A. (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.
48. Mao, H., and Williamson, J. R. (1999) Local folding coupled to RNA binding in the yeast ribosomal protein L30, J. Mol. Biol. 292, 345-359.
49. Chao, J. A., Prasad, G. S., White, S. A., Stout, C. D., and Williamson, J. R. (2003) Inherent protein structural flexibility at the RNA-binding interface of L30e, J. Mol. Biol. 326, 999-1004.
50. Chen, Y. W., Bycroft, M., and Wong, K. B. (2003) Crystal structure of ribosomal protein L30e from the extreme thermophile Thermococcus celer: Thermal stability and RNA binding. Biochemistry 42, 2857-2865.
51. Wong, K. B., Lee, C. F., Chan, S. H., Leung, T. Y., Chen, Y. W., and Bycroft, M. (2003) Solution structure and thermal stability of ribosomal protein L30e from hyperthermophilic archaeon Thermococcus celer, Protein Sci. 12, 1483-1495.
52. Chao, J. A., and Williamson, J. R. (2004) Joint X-ray and NMR refinement of the yeast L30e-mRNA complex. Structure 12, 1165-1176.
53. Scaringe, S. A. (2000) Advanced 5′-silyl-2′-ortho ester approach to RNA oligonucleotide synthesis, Methods Enzymol. 317, 3-18.
54. Otwinowski, Z., and Minor, W. (1997) Processing of X-ray data in collected in oscillation mode, Methods Enzymol. 276, 307-326.
55. Kissinger, C. R., Gehlhaar, D. K., and Fogel, D. B. (1999) Rapid automated molecular replacement by evolutionary search. Acta Crystallogr. D55, 484-491.
56. Brünger, 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., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr. D54, 905-921.
57. McRee, D. E. (1999) XtalView/Xfit: A versatile program for manipulating atomic coordinates and electron density, J. Struct. Biol. 125, 156-165.
58. Collaborative Computational Project, No. 4 (1994) The CCP4 suite: Programs for protein crystallography, Acta Crystallogr. D50, 760-763.
59. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method, Acta Crystallogr. D53, 240-255.
60. Vaguine, A. A., Richelle, J., and Wodak, S. J. (1999) SFCHECK: A unified set of procedures for evaluating the quality of macromolecular structure-factor data and their agreement with the atomic model, Acta Crystallogr. D55, 191-205.
61. Laskowsky, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK: A program to check stereochemical quality of protein structure coordinates, J. Appl. Crystallogr. 26, 283-291.
62. Lovell, S. C., Davis, I. W., Arendall, W. B., III, de Bakker, P. I., Word, J. M., Prisant, M. G., Richardson, J. S., and Richardson, D. C. (2003) Structure validation by Cα geometry: φ, ψ, and Cβ deviation, Proteins 50, 437-450.
63. Kabsch, W., and Sander, C. (1983) Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features, Biopolymers 22, 2577-2637.
64. McDonald, I. K., and Thornton, J. M. (1994) Satisfying hydrogen bonding potential in proteins, J. Mol. Biol. 238, 777-793.
65. Kleywegt, G. J. (1997) Validation of protein models from Cα coordinates alone, J. Mol. Biol. 273, 371-376.
66. Merritt, E. A. (1999) Expanding the model: Anisotropic displacement parameters in protein structure refinement, Acta Crystallogr. D55, 1109-1117.
67. Nicholls, A., and Honig, B. (1991) A rapid finite difference algorithm, utilizing successive over-relaxation to solve the Poisson-Boltzmann equation, J. Comput. Chem. 12, 435-445.
68. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice, Nucleic Acids Res. 22, 4673-4680.
69. Stothard, P. (2000) The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences, BioTechniques 28, 1102-1104.
70. Glaser, F., Pupko, T., Paz, I., Bell, R. E., Bechor-Shental, D., Martz, E., and Ben-Tal, N. (2003) ConSurf: Identification of functional regions in proteins by surface-mapping of phylogenetic information, Bioinformatics 19, 163-164.
71. Gibrat, J. F., Madej, T., and Bryant, S. H. (1996) Surprising similarities in structure comparison. Curr. Opin. Struct. Biol. 6, 377-385.
72. Holm, L., and Sander, C. (1996) Mapping the protein universe, Science 273, 595-603.
73. Kraulis, P. J. (1991) MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures, J. Appl. Crystallogr. 24, 946-950.
74. Merritt, E. A., and Bacon, D. J. (1997) Raster3D: Photorealistic Molecular Graphics, Methods Enzymol. 277, 505-524.
75. Marky, L. A., and Breslauer, K. J. (1987) Calculating thermodynamic data for transitions of any molecularity from equilibrium melting curves, Biopolymers 26, 1601-1620.
76. Puglisi, J. D., and Tinoco, I., Jr. (1989) Absorbance melting curves of RNA, Methods Enzymol. 180, 304-325.
77. Pace, C. N. (1986) Determination and analysis of urea and guanidine hydrochloride denaturation curves, Methods Enzymol. 131, 266-280.
78. Murshudov, G. N., Vagin, A. A., Lebedev, A., Wilson, K. S., and Dodson, E. J. (1999) Efficient anisotropic refinement of macromolecular structures using FFT, Acta Crystallogr. D55, 247-255.
79. Szilagyi, A., and Zavodszky, P. (2000) Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: Results of a comprehensive survey, Structure 8, 493-504.
80. Williamson, J. R. (2000) Induced fit in RNA-protein recognition, Nat. Struct. Biol. 7, 834-837.
81. Song, H., Mugnier, P., Das, A. K., Webb, H. M., Evans, D. R., Tuite, M. F., Hemmings, B. A., and Barford, D. (2000) The crystal structure of human eukaryotic release factor eRF1: Mechanism of stop codon recognition and peptidyl-tRNA hydrolysis, Cell 100, 311-321.
82. Nureki, O., Shirouzu, M., Hashimoto, K., Ishitani, R., Terada, T., Tamakoshi, M., Oshima, T., Chijimatsu, M., Takio, K., Vassylyev, D. G., Shibata, T., Inoue, Y., Kuramitsu, S., and Yokoyama, S. (2002) An enzyme with a deep trefoil knot for the active-site architecture, Acta Crystallogr. D58, 1129-1137.
83. Michel, G., Sauve, V., Larocque, R., Li, Y., Matte, A., and Cygler, M. (2002) The structure of the RlmB 23 S rRNA methyltransferase reveals a new methyltransferase fold with a unique knot, Structure 10, 1303-1315.
84. Kim, M.-S., and Oh, B.-H. (2003) RCSB Protein Data Bank 1OGD.
85. Zago, M. A., Dennis, P. P., and Omer, A. D. (2005) The expanding world of small RNAs in the hyperthermophilic archaeon Sulfolobus solfataricus, Mol. Microbiol. 55, 1812-1828.
86. Tang, T. H., Polacek, N., Zywicki, M., Huber, H., Brugger, K., Garrett, R., Bachellerie, J. P., and Huttenhofer, A. (2005) Identification of novel non-coding RNAs as potential antisense regulators in the archaeon Sulfolobus solfataricus, Mol. Microbiol. 55, 469-481.
87. Turner, B., Melcher, S. E., Wilson, T. J., Norman, D. G., and Lilley, D. M. J. (2005) Induced fit of RNA on binding the L7Ae protein to the kink-turn motif. RNA 11 (in press).