Ribosomal protein S7: A new RNA-binding motif with structural similarities to a DNA architectural factor

Structure

Volumn 5, Issue 9, 1997, Pages 1199-1208

  Hosaka, Harumi ^a   Nakagawa, Atsushi ^a   Tanaka, Isao ^a   Harada, Nao ^b   Sano, Kazunari ^b   Kimura, Makoto ^b   Yao, Min ^c,d   Wakatsuki, Soichi ^c  

^a HOKKAIDO UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

^d MAC Science Co Ltd   (Japan)

Author keywords

Decoding center; Ribosomal protein S7; RNA architectural factor; RNA binding protein; X ray structure

Indexed keywords

BACTERIA (MICROORGANISMS); GEOBACILLUS STEAROTHERMOPHILUS;

EID: 0031572233     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(97)00270-0     Document Type: Article

References (74)

1. Gornicki, P., Nurse, K., Hellmann, W., Boublik, M. & Ofengand, J. (1984). High resolution localization of the tRNA anticodon interaction site on the Escherichia coli 30S ribosomal subunit. J. Biol. Chem. 259, 10493-10498.
2. Stark, H., et al., & van Heel, M. (1995). The 70S Escherichia coli ribosome at 23 Å resolution: fitting the ribosomal RNA. Structure 3, 815-821.
3. Frank, J., et al., & Agrawal, R.K. (1995). A model of protein synthesis based on cryo-electron microscopy of the E. coli ribosome. Nature 376, 441-444.
4. Agrawal, R.K., et al., & Frank, J. (1996). Direct visualization of A-, P-, and E-site transfer RNAs in the Escherichia coli ribosome. Science 271, 1000-1002.
5. Stark, H., et al., & van Heel, M. (1997). Arrangement of tRNAs in pre-and post-translocational ribosomes revealed by electron cryomicroscopy. Cell 88, 19-28.
6. Brimacombe, R. (1995). The structure of ribosomal RNA: a three-dimensional jigsaw puzzle. Eur. J. Biochem. 230, 365-383.
7. Capel, M.S., et al., & Sillers, I.Y. (1987). A complete mapping of the proteins in the small ribosomal subunit of Escherichia coli. Science 238, 1403-1406.
8. Brimacombe, R., Atmadja, J., Stiege, W. & Schüler, D. (1988). A detailed model of the three-dimensional structure of Escherichia coli 16 S ribosomal RNA in situ in the 30 S subunit. J. Mol. Biol. 199, 115-136.
9. Schüler, D. & Brimacombe, R. (1988). The Escherichia coli 30S ribosomal subunit; an optimized three-dimensional fit between the ribosomal proteins and the 16S RNA. EMBO J. 7, 1509-1513.
10. Pondkowinski, J. & Gornicki, P. (1989). Ribosomal proteins S7 and L1 are located close to the decoding site of E. coli ribosome - affinity labeling studies with modified tRNAs carrying photoreactive probes attached adjacent to the 3′-end of the anticodon. Nucleic Acids Res. 17, 8767-8782.
11. Nowotny, V. & Nierhaus, K.H. (1988). Assembly of the 30S subunit from Escherichia coli ribosomes occurs via two assembly domains which are initiated by S4 and S7. Biochemistry 27, 7051-7055.
12. Mandiyan, V., Tumminia, S., Wall, J.S., Hainfeld, J.F. & Boublik, M. (1989). Protein-induced conformational changes in 16 S ribosomal RNA during the initial assembly steps of the Escherichia coli 30 S ribosomal subunit. J. Mol. Biol. 210, 323-336.
13. Phe. FEBS Lett. 243, 299-302.
14. Abdurashidova, G.G., Tsvetkova, E.A. & Budowsky, E.I. (1990). Determination of tRNA nucleotide residues directly interacting with proteins in the post- and pretranslocated ribosomal complexes. FEBS Lett. 269, 398-401.
15. Phe to 30S-subunit protein S7 at the ribosomal A and P sites. Biochimie 74, 381-389.
16. Döring, T., Mitchell, P., Osswald, M., Bochkariov, D. & Brimacombe, R. (1994). The decoding region of 16S RNA; a cross-linking study of the ribosomal A,P and E sites using tRNA derivatized at position 32 in the anticodon loop. EMBO J. 13, 2677-2685.
17. Stade, K., Rinke-Appel, J. & Brimacombe, R. (1989). Site-directed cross-linking of mRNA analogues to the Escherichia coli ribosome; identification of 30S ribosomal components that can be cross-linked to the mRNA at various points 5′ with respect to the decoding site. Nucleic Acids Res. 17, 9889-9908.
18. Dean, D., Yates, J.L. & Nomura, M. (1981). Identification of ribosomal protein S7 as a repressor of translation within the str operon of E. coli. Cell 24, 413-419.
19. Saito, K. & Nomura, M. (1994). Post-transcriptional regulation of the str operon in Escherichia coli. Structural and mutational analysis of the target site for translational repressor S7. J. Mol. Biol. 235, 125-139.
20. Bernstein, F.C. (1978). The protein data bank: a computer-based archival file for macromolecular structures. J. Mol. Biol. 112, 535-542.
21. Holm, L. & Sander, C. (1993). Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123-138.
22. Moore, P.B. (1988). The ribosome returns. Nature 331, 223-227.
23. Powers, T., Changchien, L.M., Craven, G.R. & Noller, H.F. (1988). Probing the assembly of the 3′ major domain of 16 S ribosomal RNA. Quaternary interactions involving ribosomal proteins S7, S9 and S19. J. Mol. Biol. 200, 309-319.
24. Ehresmann, B., Reinbolt, J., Backendorf, C., Tritsch, D. & Ebel, J. (1976). Studies of the binding sites of Escherichia coli ribosomal protein S7 with 16S RNA by ultraviolet irradiation. FEBS Lett. 67, 316-319.
25. Urlaub, H., Kruft, V., Bischof, O., Müller, E.C. & Wittmann-Liebold, B. (1995). Protein-rRNA binding features and their structural and functional implications in ribosomes as determined by cross-linking studies. EMBO J. 14, 4578-4588.
26. Bischof, O., Kruft, V. & Wittmann-Liebold, B. (1994). Analysis of the puromycin binding site in the 70 S ribosome of Escherichia coli at the peptide level. J. Biol. Chem. 269, 18315-18319.
27. Möller, K., Zwieb, C. & Brimacombe, R. (1978). Identification of the oligonucleotide and oligopeptide involved in an RNA-protein crosslink induced by ultraviolet irradiation of Escherichia coli 30S ribosomal subunits. J. Mol. Biol. 126, 489-506.
28. Zwieb, C. & Brimacombe, R. (1979). RNA-protein cross-linking in Escherichia coli 30S ribosomal subunits: precise localization of the nucleotide in 16S RNA which is coupled to protein S7 by ultraviolet irradiation. Nucleic Acids Res. 6, 1775-1790.
29. Wower, I. & Brimacombe, R. (1983). The localization of multiple sites on 16S RNA which are cross-linked to proteins S7 and S8 in Escherichia coli 30S ribosomal subunits by treatment with 2-iminothiolane. Nucleic Acids Res. 11, 1419-1437.
30. Urlaub, H., Thiede, B., Müller, E.C., Brimacombe, R. & Wittmann-Liebold, B. (1997). Identification and sequence analysis of contact sites between ribosomal proteins and rRNA in Escherichia coli 30S subunits by a new approach using matrix-assisted laser desorption/ionization-mass spectrometry combined with N-terminal microsequencing. J. Biol. Chem. 272, 14547-14555.
31. Dragon, F. & Brakier-Gingras, L. (1993). Interaction of Escherichia coli ribosomal protein S7 with 16S rRNA. Nucleic Acids Res. 21, 1199-1203.
32. Dragon, F., Payant, C. & Brakier-Gingras, L. (1994). Mutational and structural analysis of the RNA binding site for Escherichia coli ribosomal protein S7. J. Mol. Biol. 244, 74-85.
33. Davies, C., Ramakrishnan, V. & White, S.W. (1996). Structural evidence for specific S8-RNA and S8-protein interactions within the 30S ribosomal subunit: ribosomal protein S8 from Bacillus stearothermophilus at 1.9 Å resolution. Structure 4, 1093-1104.
34. Liljas, A. & Garber, M. (1995). Ribosomal proteins and elongation factors. Curr. Opin. Struct. Biol. 5, 721-727.
35. Nagai, K., Oubridge, C., Jessen, T.H., Li, J. & Evans, P.R. (1990). Crystal structure of the RNA-binding domain of the U1 small nuclear ribonucleoprotein A. Nature 348, 515-520.
36. Jaishree, T.N., Ramakrishnan, V. & White, S.W. (1996). Solution structure of prokaryotic ribosomal protein S17 by high-resolution NMR spectroscopy. Biochemistry 35, 2845-2853.
37. Bycroft, M., Hubbard, T.J.P., Proctor, M., Freund, S.M.V. & Murzin, A.G. (1997). The solution structure of the S1 RNA binding domain: a member of an ancient nucleic acid-binding fold. Cell 88, 235-242.
38. Schindelin, H., Marahiel, M.A. & Heinemann, U. (1993). Universal nucleic acid-binding domain revealed by crystal structure of the B. subtilis major cold-shock protein. Nature 364, 164-168.
39. Leijonmarck, M. & Liljas, A. (1987). Structure of the C-terminal domain of the ribosomal protein L7/L12 from Escherichia coli at 1.7 Å. J Mol. Biol. 195, 555-579.
40. Markus, M.A., Hinck, A.P., Huang, S., Draper, D.E. & Torchia, D.A. (1997). High resolution solution structure of ribosomal protein L11-C76, a helical protein with a flexible loop that becomes structured upon binding to RNA. Nat. Struct. Biol. 4, 70-77.
41. Chan, Y.-L., Suzuki, K., Olvera, J. & Wool, I.G. (1993). Zinc-finger-like motifs in rat ribosomal proteins S27 and S29. Nucleic Acids Res. 21, 649-655.
42. Herfurth, E., Briesemeister, U. & Wittmann-Liebold, B. (1994). Complete amino acid sequence of ribosomal protein S14 from Bacillus stearothermophilus and homology studies to other ribosomal proteins. FEBS Lett 351, 114-118.
43. Tanaka, I., Appelt, K., Dijk, J., White, S.W. & Wilson, K.S. (1984). 3 Å Resolution structure of a protein with histone-like properties in prokaryotes. Nature 310, 376-381.
44. Vis, H., Mariani, M., Vorgias, C.E., Wilson, K.S., Kaptein, R. & Boelens, R. (1995). Solution structure of the HU protein from Bacillus stearothermophilus. J. Mol. Biol. 254, 692-703.
45. Harrison, S.C. & Aggarwal, A.K. (1990). DNA recognition by proteins with the helix-turn-helix motif. Annu. Rev. Biochem. 59, 993-969.
46. McKay, D.B. & Steitz, T.A. (1981). Structure of catabolite gene activator protein at 2.9 Å resolution suggests binding to left-handed B-DNA. Nature 290, 744-749.
47. Anderson, W.F., Ohlendorf, D.H., Takeda, Y. & Matthews, B.W. (1981). Structure of the cro repressor from bacteriophage λ and its interaction with DNA. Nature, 290, 754-758.
48. Pabo, C.O. & Lewis, M. (1982). The operator-binding domain of λ repressor: structure and DNA recognition. Nature 298, 443-447.
49. Flashner, Y. & Gralla, J.D. (1988). DNA dynamic flexibility and protein recognition: differential stimulation by bacterial histone-like protein HU. Cell 54, 713-721.
50. Johnson, R.C., Bruist, M.F. & Simon, M.I. (1986). Host protein requirements for in vitro site-specific DNA inversion. Cell 46, 531-539.
51. Rice, P.A., Yang, S., Mizuuchi, K. & Nash, H.A. (1996). Crystal structure of an IHF-DNA complex: a protein-induced DNA U-turn. Cell 87, 1295-1306.
52. Heilek, G.M. & Noller, H.F. (1996). Site-directed hydroxyl radical probing of the rRNA neighbourhood of ribosomal protein S5. Science 272, 1659-1662.
53. Harada, N., Sano, K., Kimura, M., Hosaka, H., Nakagawa, A. & Tanaka, I. (1997). Crystallization and preliminary X-ray crystallographic study of the ribosomal protein S7 from Bacillus stearothermophilus. J. Struct. Biol., in press.
54. Hendrickson, WA (1991). Determination of macromolecular structures from anomalous diffraction of synchrotron radiation. Science 254, 51-58.
55. Otwinowski, Z. & Minor, W. (1997). Processing of X-ray diffraction data collected in oscillations mode. Methods Enzymol. 276, 307-326.
56. Matthews, B.W. (1968). Solvent contents of protein crystals. J. Mol. Biol. 33, 491-497.
57. Knight, S. (1989). Ribulose 1,5-Bisphosphate Carboxylase/Oxygenase - A Structural Study. Thesis, Swedish University of Agricultural Sciences, Uppsala, Sweden.
58. Tickle, I. (1991). Refinement of single isomorphous replacement heavy-atom parameters in Patterson vs reciprocal space. In Isomorphous Replacement and Anomalous Scattering. Proceedings of the CCP4 Study Weekend, 25-26. January 1991. (Wolf, W., Evans, P.R. & Leslie, A.G.W., eds), pp. 87-95, SERC Daresbury Laboratory, Warrington, UK.
59. Otwinowski, Z. (1991). Maximum likelihood refinement of heavy-atom parameters. In Isomorphous Replacement and Anomalous Scattering. Proceedings of the CCP4 Study Weekend, 25-26. January 1991. (Wolf, W., Evans, P.R. & Leslie, A.G.W., eds), pp. 80-86, SERC Daresbury Laboratory, Warrington, UK.
60. Cowtan, K. & Main, P. (1996). Phase combination and cross validation in iterated density-modification calculations. Acra Cryst. D 52, 43-48.
61. de la Fortelle, E. & Bricogne, G. (1997). Maximum-likelihood heavy-atom parameter refinement in the MIR and MAD methods. Methods Enzymol. 276, 472-494.
62. 1 ATPase. Acta Cryst. D 52, 30-42.
63. Jones, T.A., Zou, J.Y., Cowan, S.W. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Cryst. A 47, 489-501
64. Brünger, A.T. (1993). X-PLOR Version 3.1 A system for X-ray Crystallography and NMR. Yale University Press, New Haven, CT, USA.
65. Brünger, A.T. (1992). Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355, 472-475.
66. Engh, R.A. & Huber, R. (1991). Accurate bond and angle parameters for X-ray protein structure refinement. Acta Cryst. A 47, 392-400.
67. Kraulis, P.J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 24, 946-950.
68. Merrit, E.A. & Murphy, M.E.P. (1994). Raster3D version 2.0, a program for photorealistic molecular graphics. Acta Cryst. D 50, 869-873.
69. Kabsch, W. & Sander, C. (1983). Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577-2637.
70. Nicholls, A., Sharp, K. & Honig, B. (1991). Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11, 281-296.
71. Brimacombe, R. (1991). RNA-protein interactions in the E .coli ribosome. Biochimie 73, 927-936.
72. Rinke-Appel, J., Juenke, N., Osswald, M. & Brimacombe, R. (1995). The ribosomal environment of tRNA: Crosslinks to rRNA from positions 8 and 20:1 in the central fold of tRNA located at the A, P, or E site. RNA 1, 1018-1028.
73. Osswald, M., Döring, T. & Brimacombe, R. (1995). The ribosomal neighbourhood of the central fold of tRNA: cross-links from position 47 of tRNA located at the A, P or E site. Nucleic Acids Res. 23, 4635-4641.
74. Mueller, F., et al., & Brimacombe, R. (1995). Getting closer to an understanding of the three-dimensional structure of ribosomal RNA. Biochem. Cell Biol. 73, 767-773.