One core, two shells: Bacterial and eukaryotic ribosomes

Nature Structural and Molecular Biology

Volumn 19, Issue 6, 2012, Pages 560-567

  Melnikov, Sergey ^a,b   Ben Shem, Adam ^a,c   Garreau De Loubresse, Nicolas ^a,b   Jenner, Lasse ^a,c   Yusupova, Gulnara ^a,d   Yusupov, Marat ^a,d  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c INSERM   (France)

^d CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MESSENGER RNA; PEPTIDES AND PROTEINS; RIBOSOME RNA; RNA 28S; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSFER RNA;

BACTERIUM; CELL FUNCTION; CELL STRUCTURE; CRYSTAL STRUCTURE; ESCHERICHIA COLI; EUKARYOTE; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; RIBOSOME; SACCHAROMYCES CEREVISIAE; TETRAHYMENA THERMOPHILA; THERMUS THERMOPHILUS; X RAY CRYSTALLOGRAPHY;

ANIMALS; BACTERIA; EUKARYOTIC CELLS; HUMANS; MODELS, MOLECULAR; PROTEIN BIOSYNTHESIS; RIBOSOMAL PROTEINS; RIBOSOMES; RNA, RIBOSOMAL;

BACTERIA (MICROORGANISMS); EUKARYOTA;

EID: 84861908221     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2313     Document Type: Review

References (84)

1. Gruschke, S. & Ott, M. The polypeptide tunnel exit of the mitochondrial ribosome is tailored to meet the specific requirements of the organelle. Bioessays 32, 1050-1057 (2010).
2. Twiss, J.L. & Fainzilber, M. Ribosomes in axons-scrounging from the neighbors? Trends Cell Biol. 19, 236-243 (2009).
3. Ban, N., Nissen, P., Hansen, J., Moore, P.B. & Steitz, T.A. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science 289, 905-920 (2000).
4. Wimberly, B.T. et al. Structure of the 30S ribosomal subunit. Nature 407, 327-339 (2000).
5. Yusupov, M.M. et al. Crystal structure of the ribosome at 5.5 A resolution. Science 292, 883-896 (2001).
6. Harms, J. et al. High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell 107, 679-688 (2001).
7. Selmer, M. et al. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313, 1935-1942 (2006).
8. Schuwirth, B.S. et al. Structures of the bacterial ribosome at 3.5 A resolution. Science 310, 827-834 (2005).
9. Dube, P. et al. Correlation of the expansion segments in mammalian rRNA with the fine structure of the 80 S ribosome; a cryoelectron microscopic reconstruction of the rabbit reticulocyte ribosome at 21 A resolution. J. Mol. Biol. 279, 403-421 (1998).
10. Spahn, C.M. et al. Structure of the 80S ribosome from Saccharomyces cerevisiae-tRNA-ribosome and subunit-subunit interactions. Cell 107, 373-386 (2001). Reports a 15-Å resolution map of yeast ribosome, providing the first structural comparison between bacterial and eukaryotic ribosomes.
11. Sengupta, J. et al. Identification of the versatile scaffold protein RACK1 on the eukaryotic ribosome by cryo-EM. Nat. Struct. Mol. Biol. 11, 957-962 (2004).
12. Halic, M., Becker, T., Frank, J., Spahn, C.M. & Beckmann, R. Localization and dynamic behavior of ribosomal protein L30e. Nat. Struct. Mol. Biol. 12, 467-468 (2005).
13. Chandramouli, P. et al. Structure of the mammalian 80S ribosome at 8.7 A resolution. Structure 16, 535-548 (2008).
14. Taylor, D.J. et al. Comprehensive molecular structure of the eukaryotic ribosome. Structure 17, 1591-1604 (2009). Summarizes advances in eukaryotic ribosome modeling over almost a decade.
15. Armache, J.P. et al. Cryo-EM structure and rRNA model of a translating eukaryotic 80S ribosome at 5.5-A resolution. Proc. Natl. Acad. Sci. USA 107, 19748-19753 (2010).
16. Armache, J.P. et al. Localization of eukaryote-specific ribosomal proteins in a 5.5-A cryo-EM map of the 80S eukaryotic ribosome. Proc. Natl. Acad. Sci. USA 107, 19754-19759 (2010). References 15 and 16 describe several principles of evolution of the 80S ribosome, show co-evolution of rRNA and proteins and changes in the functional centers of the ribosome, and describe the behavior of dynamic RNA expansions.
17. Balagopal, V. & Parker, R. Stm1 modulates translation after 80S formation in Saccharomyces cerevisiae. RNA 17, 835-842 (2011).
18. Rabl, J., Leibundgut, M., Ataide, S.F., Haag, A. & Ban, N. Crystal structure of the eukaryotic 40S ribosomal subunit in complex with initiation factor 1. Science 331, 730-736 (2011). The X-ray structure of the small ribosomal subunit from T. thermophila reports the location and architecture of eukaryote-specific proteins and rRNA expansions.
19. Klinge, S., Voigts-Hoffmann, F., Leibundgut, M., Arpagaus, S. & Ban, N. Crystal structure of the eukaryotic 60S ribosomal subunit in complex with initiation factor 6. Science 334, 941-948 (2011). The X-ray structure of the large ribosomal subunit from T. thermophila reports the location and architecture of eukaryote-specific proteins and rRNA expansions.
20. Ben-Shem, A. et al. The structure of the eukaryotic ribosome at 3.0 A resolution. Science 334, 1524-1529 (2011). X-ray structure of the complete 80S ribosome from S. cerevisiae reports the precise location, architecture and registry of all eukaryote-specific proteins and almost all eukaryote-specific rRNA moieties, and describes interactions between ribosomal subunits.
21. Ye, Y. & Godzik, A. Flexible structure alignment by chaining aligned fragment pairs allowing twists. Bioinformatics 19 (suppl. 2), ii246-ii255 (2003).
22. Tu, D., Blaha, G., Moore, P.B. & Steitz, T.A. Structures of MLSBK antibiotics bound to mutated large ribosomal subunits provide a structural explanation for resistance. Cell 121, 257-270 (2005).
23. Smith, T.F., Lee, J.C., Gutell, R.R. & Hartman, H. The origin and evolution of the ribosome. Biol. Direct 3, 16 (2008).
24. Lecompte, O., Ripp, R., Thierry, J.C., Moras, D. & Poch, O. Comparative analysis of ribosomal proteins in complete genomes: an example of reductive evolution at the domain scale. Nucleic Acids Res. 30, 5382-5390 (2002).
25. Gerbi, S.A. The evolution of eukaryotic ribosomal DNA. Biosystems 19, 247-258 (1986).
26. Shasmal, M. & Sengupta, J. Structural diversity in bacterial ribosomes: mycobacterial 70S ribosome structure reveals novel features. PLoS ONE 7, e31742 (2012).
27. Gao, H., Ayub, M.J., Levin, M.J. & Frank, J. The structure of the 80S ribosome from Trypanosoma cruzi reveals unique rRNA components. Proc. Natl. Acad. Sci. USA 102, 10206-10211 (2005).
28. Forster, A.C. & Church, G.M. Towards synthesis of a minimal cell. Mol. Syst. Biol. 2, 45 (2006).
29. McIntosh, K.B. & Warner, J.R. Yeast ribosomes: variety is the spice of life. Cell 131, 450-451 (2007).
30. Gilbert, W.V. Functional specialization of ribosomes? Trends Biochem. Sci. 36, 127-132 (2011).
31. Vesper, O. et al. Selective translation of leaderless mRNAs by specialized ribosomes generated by MazF in Escherichia coli. Cell 147, 147-157 (2011).
32. Sato, N., Tachikawa, T., Wada, A. & Tanaka, A. Temperature-dependent regulation of the ribosomal small-subunit protein S21 in the cyanobacterium Anabaena variabilis M3. J. Bacteriol. 179, 7063-7071 (1997).
33. Forget, B.G. & Jordan, B. 5S RNA synthesized by Escherichia coli in presence of chloramphenicol: different 5′-terminal sequences. Science 167, 382-384 (1970).
34. Panina, E.M., Mironov, A.A. & Gelfand, M.S. Comparative genomics of bacterial zinc regulons: enhanced ion transport, pathogenesis, and rearrangement of ribosomal proteins. Proc. Natl. Acad. Sci. USA 100, 9912-9917 (2003).
35. Nanamiya, H. et al. Zinc is a key factor in controlling alternation of two types of L31 protein in the Bacillus subtilis ribosome. Mol. Microbiol. 52, 273-283 (2004).
36. Gunderson, J.H. et al. Structurally distinct, stage-specific ribosomes occur in Plasmodium. Science 238, 933-937 (1987).
37. Yusupova, G.Z., Yusupov, M.M., Cate, J.H. & Noller, H.F. The path of messenger RNA through the ribosome. Cell 106, 233-241 (2001).
38. Jenner, L.B., Demeshkina, N., Yusupova, G. & Yusupov, M. Structural aspects of messenger RNA reading frame maintenance by the ribosome. Nat. Struct. Mol. Biol. 17, 555-560 (2010).
39. Shine, J. & Dalgarno, L. The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc. Natl. Acad. Sci. USA 71, 1342-1346 (1974).
40. Yusupova, G., Jenner, L., Rees, B., Moras, D. & Yusupov, M. Structural basis for messenger RNA movement on the ribosome. Nature 444, 391-394 (2006).
41. Kaminishi, T. et al. A snapshot of the 30S ribosomal subunit capturing mRNA via the Shine-Dalgarno interaction. Structure 15, 289-297 (2007).
42. Korostelev, A. et al. Interactions and dynamics of the Shine Dalgarno helix in the 70S ribosome. Proc. Natl. Acad. Sci. USA 104, 16840-16843 (2007).
43. Hajnsdorf, E. & Boni, I.V. Multiple activities of RNA-binding proteins S1 and Hfq. Biochimie published online, doi:10.1016/j.biochi.2012.02. 010 (18 February 2012).
44. Sengupta, J., Agrawal, R.K. & Frank, J. Visualization of protein S1 within the 30S ribosomal subunit and its interaction with messenger RNA. Proc. Natl. Acad. Sci. USA 98, 11991-11996 (2001).
45. Tolan, D.R., Hershey, J.W. & Traut, R.T. Crosslinking of eukaryotic initiation factor eIF3 to the 40S ribosomal subunit from rabbit reticulocytes. Biochimie 65, 427-436 (1983).
46. Siridechadilok, B., Fraser, C.S., Hall, R.J., Doudna, J.A. & Nogales, E. Structural roles for human translation factor eIF3 in initiation of protein synthesis. Science 310, 1513-1515 (2005).
47. Yu, Y., Abaeva, I.S., Marintchev, A., Pestova, T.V. & Hellen, C.U. Common conformational changes induced in type 2 picornavirus IRESs by cognate trans-acting factors. Nucleic Acids Res. 39, 4851-4865 (2011).
48. Jackson, R.J., Hellen, C.U. & Pestova, T.V. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol. 11, 113-127 (2010).
49. Echeverría Aitken, C. & Lorsch, J.R. A mechanistic overview of translation initiation in eukaryotes. Nat. Struct. Mol. Biol. 19, 568-576 (2012). The reviews in references 48 and 49 summarize eukaryote-specific aspects of translation initiation.
50. Passmore, L.A. et al. The eukaryotic translation initiation factors eIF1 and eIF1A induce an open conformation of the 40S ribosome. Mol. Cell 26, 41-50 (2007).
51. Zaman, S., Fitzpatrick, M., Lindahl, L. & Zengel, J. Novel mutations in ribosomal proteins L4 and L22 that confer erythromycin resistance in Escherichia coli. Mol. Microbiol. 66, 1039-1050 (2007).
52. Bingel-Erlenmeyer, R. et al. A peptide deformylase-ribosome complex reveals mechanism of nascent chain processing. Nature 452, 108-111 (2008).
53. Peisker, K. et al. Ribosome-associated complex binds to ribosomes in close proximity of Rpl31 at the exit of the polypeptide tunnel in yeast. Mol. Biol. Cell 19, 5279-5288 (2008).
54. Ben-Shem, A., Jenner, L., Yusupova, G. & Yusupov, M. Crystal structure of the eukaryotic ribosome. Science 330, 1203-1209 (2010). The first X-ray structure of a eukaryotic (S. cerevisiae) ribosome.
55. Jenner, L., Demeshkina, N., Yusupova, G. & Yusupov, M. Structural rearrangements of the ribosome at the tRNA proofreading step. Nat. Struct. Mol. Biol. 17, 1072-1078 (2010).
56. Thiébeauld, O. et al. A new plant protein interacts with eIF3 and 60S to enhance virus-activated translation re-initiation. EMBO J. 28, 3171-3184 (2009).
57. Park, H.S., Himmelbach, A., Browning, K.S., Hohn, T. & Ryabova, L.A. A plant viral 'reinitiation' factor interacts with the host translational machinery. Cell 106, 723-733 (2001).
58. Nishimura, T., Wada, T. & Okada, K. A key factor of translation reinitiation, ribosomal protein L24, is involved in gynoecium development in Arabidopsis. Biochem. Soc. Trans. 32, 611-613 (2004).
59. Finley, D., Bartel, B. & Varshavsky, A. The tails of ubiquitin precursors are ribosomal proteins whose fusion to ubiquitin facilitates ribosome biogenesis. Nature 338, 394-401 (1989).
60. Panse, V.G. & Johnson, A.W. Maturation of eukaryotic ribosomes: acquisition of functionality. Trends Biochem. Sci. 35, 260-266 (2010).
61. Karbstein, K. Inside the 40S ribosome assembly machinery. Curr. Opin. Chem. Biol. 15, 657-663 (2011).
62. Klein, D.J., Moore, P.B. & Steitz, T.A. The roles of ribosomal proteins in the structure assembly, and evolution of the large ribosomal subunit. J. Mol. Biol. 340, 141-177 (2004).
63. Timsit, Y., Acosta, Z., Allemand, F., Chiaruttini, C. & Springer, M. The role of disordered ribosomal protein extensions in the early steps of eubacterial 50 S ribosomal subunit assembly. Int. J. Mol. Sci. 10, 817-834 (2009).
64. Pomeranz Krummel, D.A., Oubridge, C., Leung, A.K., Li, J. & Nagai, K. Crystal structure of human spliceosomal U1 snRNP at 5.5 A resolution. Nature 458, 475-480 (2009).
65. Houge, G. et al. Fine mapping of 28S rRNA sites specifically cleaved in cells undergoing apoptosis. Mol. Cell. Biol. 15, 2051-2062 (1995).
66. Houge, G., Doskeland, S.O., Boe, R. & Lanotte, M. Selective cleavage of 28S rRNA variable regions V3 and V13 in myeloid leukemia cell apoptosis. FEBS Lett. 315, 16-20 (1993).
67. Sweeney, R., Chen, L. & Yao, M.C. An rRNA variable region has an evolutionarily conserved essential role despite sequence divergence. Mol. Cell. Biol. 14, 4203-4215 (1994).
68. Beckmann, R. et al. Architecture of the protein-conducting channel associated with the translating 80S ribosome. Cell 107, 361-372 (2001).
69. Kondrashov, N. et al. Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. Cell 145, 383-397 (2011).
70. Strunk, B.S. et al. Ribosome assembly factors prevent premature translation initiation by 40S assembly intermediates. Science 333, 1449-1453 (2011).
71. Fitzgerald, K.D. & Semler, B.L. Bridging IRES elements in mRNAs to the eukaryotic translation apparatus. Biochim. Biophys. Acta 1789, 518-528 (2009).
72. Lorsch, J.R. & Dever, T.E. Molecular view of 43 S complex formation and start site selection in eukaryotic translation initiation. J. Biol. Chem. 285, 21203-21207 (2010).
73. Acker, M.G. & Lorsch, J.R. Mechanism of ribosomal subunit joining during eukaryotic translation initiation. Biochem. Soc. Trans. 36, 653-657 (2008).
74. Bengtson, M.H. & Joazeiro, C.A. Role of a ribosome-associated E3 ubiquitin ligase in protein quality control. Nature 467, 470-473 (2010).
75. Bokov, K. & Steinberg, S.V. A hierarchical model for evolution of 23S ribosomal RNA. Nature 457, 977-980 (2009).
76. Balagopal, V. & Parker, R. Stm1 modulates mRNA decay and Dhh1 function in Saccharomyces cerevisiae. Genetics 181, 93-103 (2009).
77. Warner, J.R. The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24, 437-440 (1999).
78. Strunk, B.S. & Karbstein, K. Powering through ribosome assembly. RNA 15, 2083-2104 (2009).
79. Wilson, D.N. & Beckmann, R. The ribosomal tunnel as a functional environment for nascent polypeptide folding and translational stalling. Curr. Opin. Struct. Biol. 21, 274-282 (2011).
80. Brandt, F., Carlson, L.A., Hartl, F.U., Baumeister, W. & Grunewald, K. The three-dimensional organization of polyribosomes in intact human cells. Mol. Cell 39, 560-569 (2010).
81. Brandt, F. et al. The native 3D organization of bacterial polysomes. Cell 136, 261-271 (2009).
82. Dunkle, J.A. et al. Structures of the bacterial ribosome in classical and hybrid states of tRNA binding. Science 332, 981-984 (2011).
83. Spahn, C.M. et al. Cryo-EM visualization of a viral internal ribosome entry site bound to human ribosomes: the IRES functions as an RNA-based translation factor. Cell 118, 465-475 (2004).
84. Jarasch, A. et al. The DARC site: a database of aligned ribosomal complexes. Nucleic Acids Res. 40, D495-D500 (2012). The paper describes a recently constructed publicly available database of all existing structures of ribosomes; all structures are aligned, and coordinates are available to download in Protein Data Bank (pdb) format.