The roles of ribosomal proteins in the structure assembly, and evolution of the large ribosomal subunit

Journal of Molecular Biology

Volumn 340, Issue 1, 2004, Pages 141-177

  Klein, D J ^a   Moore, P B ^a   Steitz, T A ^a,b  

^a YALE UNIVERSITY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

23 S RNA; evolution; protein RNA interactions; r proteins, ribosomal proteins; ribosome; ribosome assembly; RRM, RNA recognition motif

Indexed keywords

ARGININE; LYSINE; PHOSPHATE; PROTEIN SUBUNIT; RIBOSOME PROTEIN; RNA;

ARTICLE; BINDING AFFINITY; BINDING SITE; ELECTRICITY; EVOLUTION; GENETIC TRANSCRIPTION; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

HALOARCULA; HALOARCULA MARISMORTUI; INSERTION SEQUENCES;

EID: 2942615089     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.03.076     Document Type: Article

References (83)

1. Moore P.B. The three-dimensional structure of the ribosome and its components. Annu. Rev. Biophys. Biomol. Struct. 27:1998;35-58
2. Ban N., Nissen P., Hansen J., Moore P.B., Steitz T.A. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science. 289:2000;905-920
3. Wimberly B.T., Brodersen D.E., Clemons W.M. Jr, Morgan-Warren R.J., Carter A.P., Vonrhein C., Hartsch T., Ramakrishnan V. Structure of the 30 S ribosomal subunit. Nature. 407:2000;327-339
4. Schluenzen F., Tocilj A., Zarivach R., Harms J., Gluehmann M., Janell D., et al. Structure of functionally activated small ribosomal subunit at 3.3 angstroms resolution. Cell. 102:2000;615-623
5. Harms J., Schluenzen F., Zarivach R., Bashan A., Gat S., Agmon I., et al. High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell. 107:2001;679-688
6. Yusupov M.M., Yusupova G.Z., Baucom A., Lieberman K., Earnest T.N., Cate J.H., Noller H.F. Crystal structure of the ribosome at 5.5 Å resolution. Science. 292:2001;883-896
7. Vila-Sanjurjo A., Ridgeway W.K., Seymaner V., Zhang W., Santoso S., Yu K., Cate J.H. X-ray crystal structures of the WT and a hyper-accurate ribosome from Escherichia coli. Proc. Natl Acad. Sci. USA. 100:2003;8682-8687
8. Nissen P., Hansen J., Ban N., Moore P.B., Steitz T.A. The structural basis of ribosome activity in peptide bond synthesis. Science. 289:2000;920-930
9. Schmeing T.M., Seila A.C., Hansen J.L., Freeborn B., Soukup J.K., Scaringe S.A., et al. A pre-translocational intermediate in protein synthesis observed in crystals of enzymatically active 50 S subunits. Nature Struct. Biol. 9:2002;225-230
10. Ogle J.M., Brodersen D.E., Clemons W.M. Jr, Tarry M.J., Carter A.P., Ramakrishnan V. Recognition of cognate transfer RNA by the 30 S ribosomal subunit. Science. 292:2001;897-902
11. Carter A.P., Clemons W.M., Brodersen D.E., Morgan-Warren R.J., Wimberly B.T., Ramakrishnan V. Functional insights from the structure of the 30 S ribosomal subunit and its interactions with antibiotics. Nature. 407:2000;340-348
12. Brodersen D.E., Clemons W.M. Jr, Carter A.P., Morgan-Warren R.J., Wimberly B.T., Ramakrishnan V. The structural basis for the action of the antibiotics tetracycline, pactamycin, and hygromycin B on the 30 S ribosomal subunit. Cell. 103:2000;1143-1154
13. Schlunzen F., Zarivach R., Harms J., Bashan A., Tocilj A., Albrecht R., Yonath A., Franceschi F. Structural basis for the interaction of antibiotics with the peptidyl transferase centre in eubacteria. Nature. 413:2001;814-821
14. Pioletti M., Schlunzen F., Harms J., Zarivach R., Gluhmann M., Avila H., et al. Crystal structures of complexes of the small ribosomal subunit with tetracycline, edeine and IF3. EMBO J. 20:2001;1829-1839
15. Hansen J.L., Ippolito J.A., Ban N., Nissen P., Moore P.B., Steitz T.A. The structures of four macrolide antibiotics bound to the large ribosomal subunit. Mol. Cell. 10:2002;117-128
16. Hansen J.L., Moore P.B., Steitz T.A. Structures of five antibiotics bound at the peptidyl transferase center of the large ribosomal subunit. J. Mol. Biol. 330:2003;1061-1075
17. Brodersen D.E., Clemons W.M. Jr, Carter A.P., Wimberly B.T., Ramakrishnan V. Crystal structure of the 30 S ribosomal subunit from Thermus thermophilus: structure of the proteins and their interactions with 16 S RNA. J. Mol. Biol. 316:2002;725-768
18. Klein D.J., Schmeing T.M., Moore P.B., Steitz T.A. The kink-turn: a new RNA secondary structure motif. EMBO J. 20:2001;4214-4221
19. Hansen M.A., Kirpekar F., Ritterbusch W., Vester B. Posttranscriptional modifications in the A-loop of 23 S rRNAs from selected archaea and eubacteria. RNA. 8:2002;202-213
20. Belova L., Tenson T., Xiong L., McNicholas P.M., Mankin A.S. A novel site of antibiotic action in the ribosome: interaction of evernimicin with the large ribosomal subunit. Proc. Natl Acad. Sci. USA. 98:2001;3726-3731
21. Wimberly B.T., Guymon R., McCutcheon J.P., White S.W., Ramakrishnan V. A detailed view of a ribosomal active site: the structure of the L11-RNA complex. Cell. 97:1999;491-502
22. Conn G.L., Draper D.E., Lattman E.E., Gittis A.G. Crystal structure of a conserved ribosomal protein-RNA complex. Science. 284:1999;1171-1174
23. Nikulin A., Eliseikina I., Tishchenko S., Nevskaya N., Davydova N., Platonova O., et al. Structure of the L1 protuberance in the ribosome. Nature Struct. Biol. 10:2003;104-108
24. Ban N., Freeborn B., Nissen P., Penczek P., Grassucci R.A., Sweet R., et al. A 9 Å resolution X-ray crystallographic map of the large ribosomal subunit. Cell. 93:1998;1105-1115
25. Valle M., Zavialov A., Sengupta J., Rawat U., Ehrenberg M., Frank J. Locking and unlocking of ribosomal motions. Cell. 114:2003;123-134
26. Beckmann R., Spahn C.M., Eswar N., Helmers J., Penczek P.A., Sali A., Frank J., Blobel G. Architecture of the protein-conducting channel associated with the translating 80 S ribosome. Cell. 107:2001;361-372
27. Rould M.A., Perona J.J., Soll D., Steitz T.A. Structure of E. coli glutaminyl-tRNA synthetase complexed with tRNA(Gln) and ATP at 2.8 Å resolution. Science. 246:1989;1135-1142
28. Herold M., Nierhaus K.H. Incorporation of six additional proteins to complete the assembly map of the 50 S subunit from Escherichia coli ribosomes. J. Biol. Chem. 262:1987;8826-8833
29. Rao J.K., Argos P. Structural stability of halophilic proteins. Biochemistry. 20:1981;6536-6543
30. Elcock A.H., McCammon J.A. Electrostatic contributions to the stability of halophilic proteins. J. Mol. Biol. 280:1998;731-748
31. Oubridge C., Ito N., Evans P.R., Teo C.H., Nagai K. Crystal structure at 1.92 Å resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin. Nature. 372:1994;432-438
32. Murzin A.G., Brenner S.E., Hubbard T., Chothia C. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 247:1995;536-540
33. AEvarsson A., Brazhnikov E., Garber M., Zheltonosova J., Chirgadze Y., al-Karadaghi S., Svensson L.A., Liljas A. Three-dimensional structure of the ribosomal translocase: elongation factor G from Thermus thermophilus. EMBO J. 13:1994;3669-3677
34. Watenpaugh K.D., Sieker L.C., Jensen L.H. The structure of rubredoxin at 1.2 Å resolution. J. Mol. Biol. 131:1979;509-522
35. Hard T., Kellenbach E., Boelens R., Maler B.A., Dahlman K., Freedman L.P., et al. Solution structure of the glucocorticoid receptor DNA-binding domain. Science. 249:1990;157-160
36. Schmeing T.M., Moore P.B., Steitz T.A. Structures of deacylated tRNA mimics bound to the E site of the large ribosomal subunit. RNA. 9:2003;1345-1352
37. Zvereva M.I., Shpanchenko O.V., Dontsova O.A., Nierhaus K.H., Bogdanov A.A. Effect of point mutations at position 89 of the E. coli 5 S rRNA on the assembly and activity of the large ribosomal subunit. FEBS Letters. 421:1998;249-251
38. Beauclerk A.A., Cundliffe E. The binding site for ribosomal protein L2 within 23 S ribosomal RNA of Escherichia coli. EMBO J. 7:1988;3589-3594
39. Chothia C., Janin J. Principles of protein-protein recognition. Nature. 256:1975;705-708
40. Egebjerg J., Christiansen J., Garrett R.A. Attachment sites of primary binding proteins L1, L2 and L23 on 23 S ribosomal RNA of Escherichia coli. J. Mol. Biol. 222:1991;251-264
41. Ostergaard P., Phan H., Johansen L.B., Egebjerg J., Ostergaard L., Porse B.T., Garrett R.A. Assembly of proteins and 5 S rRNA to transcripts of the major structural domains of 23 S rRNA. J. Mol. Biol. 284:1998;227-240
42. Leffers H., Egebjerg J., Andersen A., Christensen T., Garrett R.A. Domain VI of Escherichia coli 23 S ribosomal RNA. Structure, assembly and function. J. Mol. Biol. 204:1988;507-522
43. Egebjerg J., Leffers H., Christensen A., Andersen H., Garrett R.A. Structure and accessibility of domain I of Escherichia coli 23 S RNA in free RNA, in the L24-RNA complex and in 50 S subunits. Implications for ribosomal assembly. J. Mol. Biol. 196:1987;125-136
44. 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. Nucl. Acids Res. 30:2002;931-941
45. Rozhdestvensky T.S., Tang T.H., Tchirkova I.V., Brosius J., Bachellerie J.P., Huttenhofer A. 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. Nucl. Acids Res. 31:2003;869-877
46. Steitz T.A., Moore P.B. RNA, the first macromolecular catalyst: the ribosome is a ribozyme. Trends Biochem. Sci. 28:2003;411-418
47. Luger K., Mader A.W., Richmond R.K., Sargent D.F., Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature. 389:1997;251-260
48. Rossmann M.G., Johnson J.E. Icosahedral RNA virus structure. Annu. Rev. Biochem. 58:1989;533-569
49. Liljas A. Comparative biochemistry and biophysics of ribosomal proteins. Int. Rev. Cytol. 124:1991;103-136
50. Vidovic I., Nottrott S., Hartmuth K., Luhrmann R., Ficner R. Crystal structure of the spliceosomal 15.5 kD protein bound to a U4 snRNA fragment. Mol. Cell. 6:2000;1331-1342
51. Chao J.A., Prasad G.S., White S.A., Stout C.D., Williamson J.R. Inherent protein structural flexibility at the RNA-binding interface of L30e. J. Mol. Biol. 326:2003;999-1004
52. Song H., Mugnier P., Das A.K., Webb H.M., Evans D.R., Tuite M.F., Hemmings B.A., Barford D. The crystal structure of human eukaryotic release factor eRF1-mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell. 100:2000;311-321
53. Golden B.L., Ramakrishnan V., White S.W. Ribosomal protein L6: structural evidence of gene duplication from a primitive RNA binding protein. EMBO J. 12:1993;4901-4908
54. Davies C., White S.W., Ramakrishnan V. The crystal structure of ribosomal protein L14 reveals an important organizational component of the translational apparatus. Structure. 4:1996;55-66
55. Unge J., Berg A., Al-Kharadaghi S., Nikulin A., Nikonov S., Davydova N., et al. The crystal structure of ribosomal protein L22 from Thermus thermophilus: insights into the mechanism of erythromycin resistance. Structure. 6:1998;1577-1586
56. Mogridge J., Legault P., Li J., Van Oene M.D., Kay L.E., Greenblatt J. Independent ligand-induced folding of the RNA-binding domain and two functionally distinct antitermination regions in the phage lambda N protein. Mol. Cell. 1:1998;265-275
57. Lu M., Steitz T.A. Structure of Escherichia coli ribosomal protein L25 complexed with a 5 S rRNA fragment at 1.8-Å resolution. Proc. Natl Acad. Sci. USA. 97:2000;2023-2028
58. Weeks K.M., Crothers D.M. Major groove accessibility of RNA. Science. 261:1993;1574-1577
59. Battiste J.L., Mao H., Rao N.S., Tan R., Muhandiram D.R., Kay L.E., Frankel A.D., Williamson J.R. Alpha helix-RNA major groove recognition in an HIV-1 rev peptide-RRE RNA complex. Science. 273:1996;1547-1551
60. Ruff M., Krishnaswamy S., Boeglin M., Poterszman A., Mitschler A., Podjarny A., et al. Class II aminoacyl transfer RNA synthetases: crystal structure of yeast aspartyl-tRNA synthetase complexed with tRNA(Asp). Science. 252:1991;1682-1689
61. Steitz T.A. Structural studies of protein-nucleic acid interaction: the sources of sequence-specific binding. Quart. Rev. Biophys. 23:1990;205-280
62. Nierhaus K.H. The assembly of prokaryotic ribosomes. Biochimie. 73:1991;739-755
63. Eriksson A.E., Baase W.A., Zhang X.J., Heinz D.W., Blaber M., Baldwin E.P., Matthews B.W. Response of a protein structure to cavity-creating mutations and its relation to the hydrophobic effect. Science. 255:1992;178-183
64. Worbs M., Huber R., Wahl M.C. Crystal structure of ribosomal protein L4 shows RNA-binding sites for ribosome incorporation and feedback control of the S10 operon. EMBO J. 19:2000;807-818
65. Spillmann S., Dohme F., Nierhaus K.H. Assembly in vitro of the 50 S subunit from Escherichia coli ribosomes: proteins essential for the first heat-dependent conformational change. J. Mol. Biol. 115:1977;513-523
66. Lieberman K.R., Noller H.F. Ribosomal protein L15 as a probe of 50 S ribosomal subunit structure. J. Mol. Biol. 284:1998;1367-1378
67. Nowotny V., Nierhaus K.H. Initiator proteins for the assembly of the 50 S subunit from Escherichia coli ribosomes. Proc. Natl Acad. Sci. USA. 79:1982;7238-7242
68. Dabbs E.R. A spontaneous mutant of Escherichia coli with protein L24 lacking from the ribosome. Mol. Gen. Genet. 187:1982;453-458
69. Cabezon T., Herzog A., Petre J., Yaguchi M., Bollen A. Ribosomal assembly deficiency in an Escherichia coli thermosensitive mutant having an altered L24 ribosomal protein. J. Mol. Biol. 116:1977;361-374
70. Skinner R.H., Stark M.J., Dahlberg A.E. Mutations within the 23 S rRNA coding sequence of E. coli which block ribosome assembly. EMBO J. 4:1985;1605-1608
71. Bajaj M., Blundell T. Evolution and the tertiary structure of proteins. Annu. Rev. Biophys. Bioeng. 13:1984;453-492
72. Makarova K.S., Ponomarev V.A., Koonin E.V. Two C or not two C: recurrent disruption of Zn-ribbons, gene duplication, lineage-specific gene loss, and horizontal gene transfer in evolution of bacterial ribosomal proteins. Genome Biol. 2:2001;0033
73. Dabbs E.R. Mutant studies on the prokaryotic ribosome. Hardesty B., Kramer G. Structure, Function and Genetics of Ribosomes. 1986;733 Springer, New York
74. Noller H.F., Hoffarth V., Zimniak L. Unusual resistance of peptidyl transferase to protein extraction procedures. Science. 256:1992;1416-1419
75. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. D Biol. Crystallog. 54:1998;905-921
76. Jones T.A., Zou J.Y., Cowan S., Kjeldgaard M. Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 46:1991;110-119
77. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26:1993;283-291
78. Lovell S.C., Davis I.W., Arendall W.B., de Bakker P.I., Word J.M., Prisant M.G., Richardson J.S., Richardson D.C. Structure validation by C-alpha geometry: phi, psi, and C-beta deviation. Proteins: Struct. Funct. Genet. 50:2003;437-450
79. Lee B., Richards F.M. The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55:1971;379-400
80. Leffers H., Kjems J., Ostergaard L., Larsen N., Garrett R.A. Evolutionary relationships amongst archaebacteria. A comparative study of 23 S ribosomal RNAs of a sulphur-dependent extreme thermophile, an extreme halophile and a thermophilic methanogen. J. Mol. Biol. 195:1987;43-61
81. Gilbert D., Westhead D., Nagano N., Thornton J. Motif-based searching in TOPS protein topology databases. Bioinformatics. 15:1999;317-326
82. Carson M. RIBBONS 2.0. J. Appl. Crystallog. 24:1991;958-961
83. Holm L., Sander C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233:1993;123-138