Abstract
A high-resolution structure of the eukaryotic ribosome has been determined, leading to increased interest in studying protein biosynthesis and its regulation in the cell. New functional complexes of the full ribosome crystals obtained from the bacteria Escherichia coli and Thermus thermophilus and the yeast Saccharomyces cerevisiae have permitted the identification of precise residue positions in different states of the ribosome function. This knowledge, together with electron microscopy studies, has improved the understanding of how basic ribosome processes, including mRNA decoding, peptide bond formation, mRNA and tRNA translocation, and co-translational transport and modifications of the nascent peptide are regulated.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Agrawal RK, Penczek P, Grassucci RA, Frank J (1998) Visualization of elongation factor G on the Escherichia coli 70S ribosome: the mechanism of translocation. Proc Natl Acad Sci USA 95:6134–6138
Aitken CE, Lorsch JR (2012) A mechanistic overview of translation initiation in eukaryotes. Nat Struct Mol Biol 19:568–576
Ban N, Freeborn B, Nissen P, Penczek P, Grassucci RA, Sweet R, Frank J, Moore PB, Steitz TA (1998) A 9 Å resolution X-ray crystallographic map of the large ribosomal subunit. Cell 93:1105–1115
Ban N, Nissen P, Hansen J, Capel M, Moore PB, Steitz TA (1999) Placement of protein and RNA structures into a 5 Å-resolution map of the 50S ribosomal subunit. Nature (Lond) 400:841–847
Ban N, Nissen P, Hansen J, Moore PB, Steitz TA (2000) The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289:905–920
Becker T, Bhushan S, Jarasch A, Armache JP, Funes S, Jossinet F, Gumbart J, Mielke T, Berninghausen O, Schulten K et al (2009) Structure of monomeric yeast and mammalian Sec61 complexes interacting with the translating ribosome. Science 326:1369–1373
Ben-Shem A, Jenner L, Yusupova G, Yusupov M (2010) Crystal structure of the eukaryotic ribosome. Science 330:1203–1209
Ben-Shem A, Garreau de Loubresse N, Melnikov S, Jenner L, Yusupova G, Yusupov M (2011) The structure of the eukaryotic ribosome at 3.0 Å resolution. Science 334:1524–1529
Bingel-Erlenmeyer R, Kohler R, Kramer G, Sandikci A, Antolic S, Maier T, Schaffitzel C, Wiedmann B, Bukau B, Ban N (2008) A peptide deformylase-ribosome complex reveals mechanism of nascent chain processing. Nature (Lond) 452:108–111
Blaha G, Stanley RE, Steitz TA (2009) Formation of the first peptide bond: the structure of EF-P bound to the 70S ribosome. Science 325:966–970
Blanchard SC, Gonzalez RL, Kim HD, Chu S, Puglisi JD (2004) tRNA selection and kinetic proofreading in translation. Nat Struct Mol Biol 11:1008–1014
Carter AP, Clemons WM, Brodersen DE, Morgan-Warren RJ, Wimberly BT, Ramakrishnan V (2000) Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature (Lond) 407:340–348
Cate JH, Yusupov MM, Yusupova GZ, Earnest TN, Noller HF (1999) X-ray crystal structures of 70S ribosome functional complexes. Science 285:2095–2104
Clemons WM Jr, May JL, Wimberly BT, McCutcheon JP, Capel MS, Ramakrishnan V (1999) Structure of a bacterial 30S ribosomal subunit at 5.5 Å resolution. Nature (Lond) 400:833–840
Cornish PV, Ermolenko DN, Noller HF, Ha T (2008) Spontaneous intersubunit rotation in single ribosomes. Mol Cell 30:578–588
Demeshkina N, Jenner L, Westhof E, Yusupov M, Yusupova G (2012) A new understanding of the decoding principle on the ribosome. Nature (Lond) 484:256–259
Dunkle JA, Wang L, Feldman MB, Pulk A, Chen VB, Kapral GJ, Noeske J, Richardson JS, Blanchard SC, Cate JH (2011) Structures of the bacterial ribosome in classical and hybrid states of tRNA binding. Science 332:981–984
Fischer N, Konevega AL, Wintermeyer W, Rodnina MV, Stark H (2010) Ribosome dynamics and tRNA movement by time-resolved electron cryomicroscopy. Nature (Lond) 466:329–333
Fourmy D, Recht MI, Blanchard SC, Puglisi JD (1996) Structure of the A site of Escherichia coli 16S ribosomal RNA complexed with an aminoglycoside antibiotic. Science 274:1367–1371
Frank J, Agrawal RK (2000) A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature (Lond) 406:318–322
Frank J, Verschoor A, Li Y, Zhu J, Lata RK, Radermacher M, Penczek P, Grassucci R, Agrawal RK, Srivastava S (1995) A model of the translational apparatus based on a three-dimensional reconstruction of the Escherichia coli ribosome. Biochem Cell Biol 73:757–765
Frank J, Gao H, Sengupta J, Gao N, Taylor DJ (2007) The process of mRNA-tRNA translocation. Proc Natl Acad Sci USA 104:19671–19678
Fu J, Munro JB, Blanchard SC, Frank J (2011) Cryoelectron microscopy structures of the ribosome complex in intermediate states during tRNA translocation. Proc Natl Acad Sci USA 108:4817–4821
Gagnon MG, Seetharaman SV, Bulkley D, Steitz TA (2012) Structural basis for the rescue of stalled ribosomes: structure of YaeJ bound to the ribosome. Science 335:1370–1372
Gao YG, Selmer M, Dunham CM, Weixlbaumer A, Kelley AC, Ramakrishnan V (2009) The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science 326:694–699
Gavrilova LP, Kostiashkina OE, Koteliansky VE, Rutkevitch NM, Spirin AS (1976) Factor-free (“non-enzymic”) and factor-dependent systems of translation of polyuridylic acid by Escherichia coli ribosomes. J Mol Biol 101:537–552
Gerbi SA (1986) The evolution of eukaryotic ribosomal DNA. Biosystems 19:247–258
Hajnsdorf E, Boni IV (2012) Multiple activities of RNA-binding proteins S1 and Hfq. Biochimie 94:1544–1553
Hansen JL, Schmeing TM, Moore PB, Steitz TA (2002) Structural insights into peptide bond formation. Proc Natl Acad Sci USA 99:11670–11675
Harel M, Shoham M, Frolow F, Eisenberg H, Mevarech M, Yonath A, Sussman JL (1988) Crystallization of halophilic malate dehydrogenase from Halobacterium marismortui. J Mol Biol 200:609–610
Harms J, Schluenzen F, Zarivach R, Bashan A, Gat S, Agmon I, Bartels H, Franceschi F, Yonath A (2001) High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell 107:679–688
Horan LH, Noller HF (2007) Intersubunit movement is required for ribosomal translocation. Proc Natl Acad Sci USA 104:4881–4885
Jackson RJ, Hellen CU, Pestova TV (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11:113–127
Jenner L, Demeshkina N, Yusupova G, Yusupov M (2010a) Structural aspects of messenger RNA reading frame maintenance by the ribosome. Nat Struct Mol Biol 17:555–560
Jenner L, Demeshkina N, Yusupova G, Yusupov M (2010b) Structural rearrangements of the ribosome at the tRNA proofreading step. Nat Struct Mol Biol 17:1072–1078
Jin H, Kelley AC, Loakes D, Ramakrishnan V (2010) Structure of the 70S ribosome bound to release factor 2 and a substrate analog provides insights into catalysis of peptide release. Proc Natl Acad Sci USA 107:8593–8598
Jin H, Kelley AC, Ramakrishnan V (2011) Crystal structure of the hybrid state of ribosome in complex with the guanosine triphosphatase release factor 3. Proc Natl Acad Sci USA 108:15798–15803
Klinge S, Voigts-Hoffmann F, Leibundgut M, Arpagaus S, Ban N (2011) Crystal structure of the eukaryotic 60S ribosomal subunit in complex with initiation factor 6. Science 334:941–948
Korostelev A, Asahara H, Lancaster L, Laurberg M, Hirschi A, Zhu J, Trakhanov S, Scott WG, Noller HF (2008) Crystal structure of a translation termination complex formed with release factor RF2. Proc Natl Acad Sci USA 105:19684–19689
Korostelev A, Zhu J, Asahara H, Noller HF (2010) Recognition of the amber UAG stop codon by release factor RF1. EMBO J 29:2577–2585
Lake JA (1976) Ribosome structure determined by electron microscopy of Escherichia coli small subunits, large subunits and monomeric ribosomes. J Mol Biol 105:131–139
Laurberg M, Asahara H, Korostelev A, Zhu J, Trakhanov S, Noller HF (2008) Structural basis for translation termination on the 70S ribosome. Nature (Lond) 454:852–857
Lecompte O, Ripp R, Thierry JC, Moras D, Poch O (2002) Comparative analysis of ribosomal proteins in complete genomes: an example of reductive evolution at the domain scale. Nucleic Acids Res 30:5382–5390
Maguire BA, Beniaminov AD, Ramu H, Mankin AS, Zimmermann RA (2005) A protein component at the heart of an RNA machine: the importance of protein l27 for the function of the bacterial ribosome. Mol Cell 20:427–435
Melnikov S, Ben-Shem A, Garreau de Loubresse N, Jenner L, Yusupova G, Yusupov M (2012) One core, two shells: bacterial and eukaryotic ribosomes. Nat Struct Mol Biol 19:560–567
Moazed D, Noller HF (1986) Transfer RNA shields specific nucleotides in 16S ribosomal RNA from attack by chemical probes. Cell 47:985–994
Moazed D, Noller HF (1989) Intermediate states in the movement of transfer RNA in the ribosome. Nature (Lond) 342:142–148
Moazed D, Noller HF (1990) Binding of tRNA to the ribosomal A and P sites protects two distinct sets of nucleotides in 16 S rRNA. J Mol Biol 211:135–145
Nissen P, Hansen J, Ban N, Moore PB, Steitz TA (2000) The structural basis of ribosome activity in peptide bond synthesis. Science 289:920–930
Ogle JM, Brodersen DE, Clemons WM Jr, Tarry MJ, Carter AP, Ramakrishnan V (2001) Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 292:897–902
Ogle JM, Murphy FV, Tarry MJ, Ramakrishnan V (2002) Selection of tRNA by the ribosome requires a transition fro m an open to a closed form. Cell 111:721–732
Pai RD, Zhang W, Schuwirth BS, Hirokawa G, Kaji H, Kaji A, Cate JH (2008) Structural insights into ribosome recycling factor interactions with the 70S ribosome. J Mol Biol 376:1334–1347
Passmore LA, Schmeing TM, Maag D, Applefield DJ, Acker MG, Algire MA, Lorsch JR, Ramakrishnan V (2007) The eukaryotic translation initiation factors eIF1 and eIF1A induce an open conformation of the 40S ribosome. Mol Cell 26:41–50
Peisker K, Braun D, Wolfle T, Hentschel J, Funfschilling U, Fischer G, Sickmann A, Rospert S (2008) 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
Pestka S (1968) Studies on the formation of transfer ribonucleic acid-ribosome complexes. 3. The formation of peptide bonds by ribosomes in the absence of supernatant enzymes. J Biol Chem 243:2810–2820
Petry S, Brodersen DE, Murphy FVT, Dunham CM, Selmer M, Tarry MJ, Kelley AC, Ramakrishnan V (2005) Crystal structures of the ribosome in complex with release factors RF1 and RF2 bound to a cognate stop codon. Cell 123:1255–1266
Polikanov YS, Blaha GM, Steitz TA (2012) How hibernation factors RMF, HPF, and YfiA turn off protein synthesis. Science 336:915–918
Powers T, Noller HF (1994) Selective perturbation of G530 of 16 S rRNA by translational miscoding agents and a streptomycin-dependence mutation in protein S12. J Mol Biol 235:156–172
Rabl J, Leibundgut M, Ataide SF, Haag A, Ban N (2011) Crystal structure of the eukaryotic 40S ribosomal subunit in complex with initiation factor 1. Science 331:730–736
Ratje AH, Loerke J, Mikolajka A, Brunner M, Hildebrand PW, Starosta AL, Donhofer A, Connell SR, Fucini P, Mielke T et al (2010) Head swivel on the ribosome facilitates translocation by means of intra-subunit tRNA hybrid sites. Nature (Lond) 468:713–716
Rodnina MV, Wintermeyer W (2001) Fidelity of aminoacyl-tRNA selection on the ribosome: kinetic and structural mechanisms. Annu Rev Biochem 70:415–435
Rodnina MV, Gromadski KB, Kothe U, Wieden HJ (2005) Recognition and selection of tRNA in translation. FEBS Lett 579:938–942
Schmeing TM, Ramakrishnan V (2009) What recent ribosome structures have revealed about the mechanism of translation. Nature (Lond) 461:1234–1242
Schmeing TM, Voorhees RM, Kelley AC, Gao YG, Murphy FVT, Weir JR, Ramakrishnan V (2009) The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA. Science 326:688–694
Schmeing TM, Voorhees RM, Kelley AC, Ramakrishnan V (2011) How mutations in tRNA distant from the anticodon affect the fidelity of decoding. Nat Struct Mol Biol 18:432–436
Schuette JC, Murphy FVT, Kelley AC, Weir JR, Giesebrecht J, Connell SR, Loerke J, Mielke T, Zhang W, Penczek PA et al (2009) GTPase activation of elongation factor EF-Tu by the ribosome during decoding. EMBO J 28:755–765
Schuwirth BS, Borovinskaya MA, Hau CW, Zhang W, Vila-Sanjurjo A, Holton JM, Cate JH (2005) Structures of the bacterial ribosome at 3.5 Å resolution. Science 310:827–834
Seidelt B, Innis CA, Wilson DN, Gartmann M, Armache JP, Villa E, Trabuco LG, Becker T, Mielke T, Schulten K et al (2009) Structural insight into nascent polypeptide chain-mediated translational stalling. Science 326:1412–1415
Selmer M, Dunham CM, Murphy FVT, Weixlbaumer A, Petry S, Kelley AC, Weir JR, Ramakrishnan V (2006) Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313:1935–1942
Sengupta J, Agrawal RK, Frank J (2001) Visualization of protein S1 within the 30S ribosomal subunit and its interaction with messenger RNA. Proc Natl Acad Sci USA 98:11991–11996
Serdyuk IN, Agalarov SC, Sedelnikova SE, Spirin AS, May RP (1983) Shape and compactness of the isolated ribosomal 16 S RNA and its complexes with ribosomal proteins. J Mol Biol 169:409–425
Shine J, Dalgarno L (1974) 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
Smith TF, Lee JC, Gutell RR, Hartman H (2008) The origin and evolution of the ribosome. Biol Direct 3:16
Song H, Mugnier P, Das AK, Webb HM, Evans DR, Tuite MF, Hemmings BA, 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
Spahn CM, Beckmann R, Eswar N, Penczek PA, Sali A, Blobel G, Frank J (2001) Structure of the 80S ribosome from Saccharomyces cerevisiae: tRNA–ribosome and subunit–subunit interactions. Cell 107:373–386
Stark H, Orlova EV, Rinke-Appel J, Junke N, Mueller F, Rodnina M, Wintermeyer W, Brimacombe R, van Heel M (1997a) Arrangement of tRNAs in pre- and posttranslocational ribosomes revealed by electron cryomicroscopy. Cell 88:19–28
Stark H, Rodnina MV, Rinke-Appel J, Brimacombe R, Wintermeyer W, van Heel M (1997b) Visualization of elongation factor Tu on the Escherichia coli ribosome. Nature (Lond) 389:403–406
Stark H, Rodnina MV, Wieden HJ, Zemlin F, Wintermeyer W, van Heel M (2002) Ribosome interactions of aminoacyl-tRNA and elongation factor Tu in the codon-recognition complex. Nat Struct Biol 9:849–854
Steitz TA (2008) A structural understanding of the dynamic ribosome machine. Nat Rev Mol Cell Biol 9:242–253
Trakhanov SD, Yusupov M, Agalarov S, Garber M, Ryazantzev S, Tischenko S, Shirokov V (1987) Crystallization of 70S ribosomes and 30S ribosomal subunits from Thermus thermophilus. FEBS Lett 220:319–322
Tu D, Blaha G, Moore PB, Steitz TA (2005) Structures of MLSBK antibiotics bound to mutated large ribosomal subunits provide a structural explanation for resistance. Cell 121:257–270
Valle M, Sengupta J, Swami NK, Grassucci RA, Burkhardt N, Nierhaus KH, Agrawal RK, Frank J (2002) Cryo-EM reveals an active role for aminoacyl-tRNA in the accommodation process. EMBO J 21:3557–3567
Valle M, Zavialov A, Li W, Stagg SM, Sengupta J, Nielsen RC, Nissen P, Harvey SC, Ehrenberg M, Frank J (2003) Incorporation of aminoacyl-tRNA into the ribosome as seen by cryo-electron microscopy. Nat Struct Biol 10:899–906
Vasiliev VD (1974) Morphology of the ribosomal 30S subparticle according to electron microscopic data. Acta Biol Med Ger 33:779–793
Voorhees RM, Weixlbaumer A, Loakes D, Kelley AC, Ramakrishnan V (2009) Insights into substrate stabilization from snapshots of the peptidyl transferase center of the intact 70S ribosome. Nat Struct Mol Biol 16:528–533
Weixlbaumer A, Petry S, Dunham CM, Selmer M, Kelley AC, Ramakrishnan V (2007) Crystal structure of the ribosome recycling factor bound to the ribosome. Nat Struct Mol Biol 14:733–737
Weixlbaumer A, Jin H, Neubauer C, Voorhees RM, Petry S, Kelley AC, Ramakrishnan V (2008) Insights into translational termination from the structure of RF2 bound to the ribosome. Science 322:953–956
Wimberly BT, Brodersen DE, Clemons WM Jr, Morgan-Warren RJ, Carter AP, Vonrhein C, Hartsch T, Ramakrishnan V (2000) Structure of the 30S ribosomal subunit. Nature (Lond) 407:327–339
Wittmann HG (1983) Architecture of prokaryotic ribosomes. Annu Rev Biochem 52:35–65
Yonath A, Mussig J, Wittmann HG (1982) Parameters for crystal growth of ribosomal subunits. J Cell Biochem 19:145–155
Yonath A, Tesche B, Lorenz S, Mussig J, Erdmann VA, Wittmann HG (1983) Several crystal forms of the Bacillus stearothermophilus 50 S ribosomal particles. FEBS Lett 154:15–20
Yoshizawa S, Fourmy D, Puglisi JD (1999) Recognition of the codon-anticodon helix by ribosomal RNA. Science 285:1722–1725
Yusupov MM, Trakhanov SD, Barinin VV, Boroviagin BD, Garber MB, Sedelnikova SE, Selivanova OM, Tischenko SV, Shirokov VA, Edintsov MM (1987) Crystallization of the 30S subunits of Thermus thermophilus ribosomes. Dokl Akad Nauk (USSR) 292:1271–1274
Yusupov MM, Yusupova GZ, Baucom A, Lieberman K, Earnest TN, Cate JH, Noller HF (2001) Crystal structure of the ribosome at 5.5 Å resolution. Science 292:883–896
Yusupova GZ, Yusupov MM, Cate JH, Noller HF (2001) The path of messenger RNA through the ribosome. Cell 106:233–241
Yusupova G, Jenner L, Rees B, Moras D, Yusupov M (2006) Structural basis for messenger RNA movement on the ribosome. Nature (Lond) 444:391–394
Zaher HS, Green R (2009) Fidelity at the molecular level: lessons from protein synthesis. Cell 136:746–762
Zaman S, Fitzpatrick M, Lindahl L, Zengel J (2007) Novel mutations in ribosomal proteins L4 and L22 that confer erythromycin resistance in Escherichia coli. Mol Microbiol 66:1039–1050
Zhou J, Lancaster L, Trakhanov S, Noller HF (2012) Crystal structure of release factor RF3 trapped in the GTP state on a rotated conformation of the ribosome. RNA 18:230–240
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer Japan
About this chapter
Cite this chapter
Yusupov, M. (2014). Recent Progress in Ribosome Structure Studies. In: Ito, K. (eds) Regulatory Nascent Polypeptides. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55052-5_2
Download citation
DOI: https://doi.org/10.1007/978-4-431-55052-5_2
Published:
Publisher Name: Springer, Tokyo
Print ISBN: 978-4-431-55051-8
Online ISBN: 978-4-431-55052-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)