Cryo-EM structures of the late-stage assembly intermediates of the bacterial 50S ribosomal subunit

Nucleic Acids Research

Volumn 41, Issue 14, 2013, Pages 7073-7083

  Li, Ningning ^a   Chen, Yuling ^a   Guo, Qiang ^a   Zhang, Yixiao ^a   Yuan, Yi ^a   Ma, Chengying ^a   Deng, Haiteng ^a   Lei, Jianlin ^a   Gao, Ning ^a  

^a TSINGHUA UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL RNA; RIBOSOME RNA; RNA 50S; RNA 5S; RNA PRECURSOR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIUM MUTANT; BIOCHEMICAL COMPOSITION; CONTROLLED STUDY; GENE INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN STABILITY; RNA ISOLATION; RNA STRUCTURE; RNA TRANSLATION; SEQUENCE HOMOLOGY;

CRYOELECTRON MICROSCOPY; GTP PHOSPHOHYDROLASES; MODELS, MOLECULAR; RIBOSOME SUBUNITS, LARGE, BACTERIAL; RNA, RIBOSOMAL, 23S;

EID: 84881491558     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt423     Document Type: Article

References (73)

1. Kaczanowska M. and Ryden-Aulin M. (2007) Ribosome biogenesis and the translation process in Escherichia coli. Microbiol. Mol. Biol. Rev., 71, 477-494
2. Traub P. and Nomura M. (1968) Structure and function of E. coli ribosomes. V. Reconstitution of functionally active 30S ribosomal particles from RNA and proteins. Proc. Natl Acad. Sci. USA, 59, 777-784
3. Nierhaus K.H. and Dohme F. (1974) Total reconstitution of functionally active 50S ribosomal subunits from Escherichia coli. Proc. Natl Acad. Sci. USA, 71, 4713-4717
4. Mizushima S. and Nomura M. (1970) Assembly mapping of 30S ribosomal proteins from E. coli. Nature, 226, 1214
5. Rohl R. and Nierhaus K.H. (1982) Assembly map of the large subunit (50S) of Escherichia coli ribosomes. Proc. Natl Acad. Sci. USA, 79, 729-733
6. Shajani Z., Sykes M.T. and Williamson J.R. (2011) Assembly of bacterial ribosomes. Annu. Rev. Biochem., 80, 501-526
7. Britton R.A. (2009) Role of GTPases in bacterial ribosome assembly. Annu. Rev. Microbiol., 63, 155-176
8. Karbstein K. (2007) Role of GTPases in ribosome assembly. Biopolymers, 87, 1-11
9. Strunk B.S. and Karbstein K. (2009) Powering through ribosome assembly. RNA, 15, 2083-2104
10. Kobayashi K., Ehrlich S.D., Albertini A., Amati G., Andersen K.K., Arnaud M., Asai K., Ashikaga S., Aymerich S., Bessieres P. et al. (2003) Essential Bacillus subtilis genes. Proc. Natl Acad. Sci. USA, 100, 4678-4683
11. Morimoto T., Loh P.C., Hirai T., Asai K., Kobayashi K., Moriya S. and Ogasawara N. (2002) Six GTP-binding proteins of the Era/Obg family are essential for cell growth in Bacillus subtilis. Microbiology, 148, 3539-3552
12. Anand B., Verma S.K. and Prakash B. (2006) Structural stabilization of GTP-binding domains in circularly permuted GTPases: Implications for RNA binding. Nucleic Acids Res., 34, 2196-2205
13. Leipe D.D., Wolf Y.I., Koonin E.V. and Aravind L. (2002) Classification and evolution of P-loop GTPases and related ATPases. J. Mol. Biol., 317, 41-72
14. Reynaud E.G., Andrade M.A., Bonneau F., Ly T.B., Knop M., Scheffzek K. and Pepperkok R. (2005) Human Lsg1 defines a family of essential GTPases that correlates with the evolution of compartmentalization. BMC Biol., 3, 21
15. Uicker W.C., Schaefer L. and Britton R.A. (2006) The essential GTPase RbgA (YlqF) is required for 50S ribosome assembly in Bacillus subtilis. Mol. Microbiol., 59, 528-540
16. Matsuo Y., Morimoto T., Kuwano M., Loh P.C., Oshima T. and Ogasawara N. (2006) The GTP-binding protein YlqF participates in the late step of 50 S ribosomal subunit assembly in Bacillus subtilis. J. Biol. Chem., 281, 8110-8117
17. Schaefer L., Uicker W.C., Wicker-Planquart C., Foucher A.E., Jault J.M. and Britton R.A. (2006) Multiple GTPases participate in the assembly of the large ribosomal subunit in Bacillus subtilis. J. Bacteriol., 188, 8252-8258
18. Matsuo Y., Oshima T., Loh P.C., Morimoto T. and Ogasawara N. (2007) Isolation and characterization of a dominant negative mutant of Bacillus subtilis GTP-binding protein, YlqF, essential for biogenesis and maintenance of the 50 S ribosomal subunit. J. Biol. Chem., 282, 25270-25277
19. Thompson A., Schafer J., Kuhn K., Kienle S., Schwarz J., Schmidt G., Neumann T., Johnstone R., Mohammed A.K. and Hamon C. (2003) Tandem mass tags: A novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal. Chem., 75, 1895-1904
20. Guo Q., Goto S., Chen Y., Feng B., Xu Y., Muto A., Himeno H., Deng H., Lei J. and Gao N. (2013) Dissecting the in vivo assembly of the 30S ribosomal subunit reveals the role of RimM and general features of the assembly process. Nucleic Acids Res., 41, 2609-2620
21. Shaikh T.R., Gao H., Baxter W.T., Asturias F.J., Boisset N., Leith A. and Frank J. (2008) SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs. Nat. Protoc., 3, 1941-1974
22. Scheres S.H. (2012) A Bayesian view on cryo-EM structure determination. J. Mol. Biol., 415, 406-418
23. Fernandez J.J., Luque D., Caston J.R. and Carrascosa J.L. (2008) Sharpening high resolution information in single particle electron cryomicroscopy. J. Struct. Biol., 164, 170-175
24. Schuwirth B.S., Borovinskaya M.A., Hau C.W., Zhang W., Vila-Sanjurjo A., Holton J.M. and Cate J.H. (2005) Structures of the bacterial ribosome at 3.5 A resolution. Science, 310, 827-834
25. Selmer M., Dunham C.M., Murphy F.V., Weixlbaumer A., Petry S., Kelley A.C., Weir J.R. and Ramakrishnan V. (2006) Structure of the 70S ribosome complexed with mRNA and tRNA. Science, 313, 1935-1942
26. Jossinet F. and Westhof E. (2005) Sequence to Structure (S2S): Display, manipulate and interconnect RNA data from sequence to structure. Bioinformatics, 21, 3320-3321
27. Rother M., Rother K., Puton T. and Bujnicki J.M. (2011) ModeRNA: A tool for comparative modeling of RNA 3D structure. Nucleic Acids Res., 39, 4007-4022
28. Kiefer F., Arnold K., Kunzli M., Bordoli L. and Schwede T. (2009) The SWISS-MODEL Repository and associated resources. Nucleic Acids Res., 37, D387-D392
29. Eswar N., Webb B., Marti-Renom M.A., Madhusudhan M.S., Eramian D., Shen M.Y., Pieper U. and Sali A. (2006) Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinform., Chapter 5, Unit 5.6
30. Trabuco L.G., Villa E., Mitra K., Frank J. and Schulten K. (2008) Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics. Structure, 16, 673-683
31. Delano W.L(2008) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA, USA
32. LeBarron J., Mitra K. and Frank J. (2007) Displaying 3D data on RNA secondary structures: ColoRNA. J. Struct. Biol., 157, 262-270
33. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C. and Ferrin T.E. (2004) UCSF Chimera-A visualization system for exploratory research and analysis. J. Comput. Chem., 25, 1605-1612
34. Jiang M., Sullivan S.M., Walker A.K., Strahler J.R., Andrews P.C. and Maddock J.R. (2007) Identification of novel Escherichia coli ribosome-Associated proteins using isobaric tags and multidimensional protein identification techniques. J. Bacteriol., 189, 3434-3444
35. Herold M. and Nierhaus K.H. (1987) Incorporation of six additional proteins to complete the assembly map of the 50 S subunit from Escherichia coli ribosomes. J. Biol. Chem., 262, 8826-8833
36. Korepanov A.P., Korobeinikova A.V., Shestakov S.A., Garber M.B. and Gongadze G.M. (2012) Protein L5 is crucial for in vivo assembly of the bacterial 50S ribosomal subunit central protuberance. Nucleic Acids Res., 40, 9153-9159
37. Horne J.R. and Erdmann V.A. (1972) Isolation and characterization of 5S RNA-protein complexes from Bacillus stearothermophilus and Escherichia coli ribosomes. Mol. Gen. Genet., 119, 337-344
38. Barkan A., Klipcan L., Ostersetzer O., Kawamura T., Asakura Y. and Watkins K.P. (2007) The CRM domain: An RNA binding module derived from an ancient ribosome-Associated protein. RNA, 13, 55-64
39. Beringer M. and Rodnina M.V. (2007) The ribosomal peptidyl transferase. Mol. Cell, 26, 311-321
40. Ali I.K., Lancaster L., Feinberg J., Joseph S. and Noller H.F. (2006) Deletion of a conserved, central ribosomal intersubunit RNA bridge. Mol. Cell, 23, 865-874
41. Komoda T., Sato N.S., Phelps S.S., Namba N., Joseph S. and Suzuki T. (2006) The A-site finger in 23 S rRNA acts as a functional attenuator for translocation. J. Biol. Chem., 281, 32303-32309
42. Sergiev P.V., Kiparisov S.V., Burakovsky D.E., Lesnyak D.V., Leonov A.A., Bogdanov A.A. and Dontsova O.A. (2005) The conserved A-site finger of the 23S rRNA: Just one of the intersubunit bridges or a part of the allosteric communication pathway? J. Mol. Biol., 353, 116-123
43. Yassin A. and Mankin A.S. (2007) Potential new antibiotic sites in the ribosome revealed by deleterious mutations in RNA of the large ribosomal subunit. J. Biol. Chem., 282, 24329-24342
44. Dohme F. and Nierhaus K.H. (1976) Role of 5S RNA in assembly and function of the 50S subunit from Escherichia coli. Proc. Natl Acad. Sci. USA, 73, 2221-2225
45. Charollais J., Dreyfus M. and Iost I. (2004) CsdA, a cold-shock RNA helicase from Escherichia coli, is involved in the biogenesis of 50S ribosomal subunit. Nucleic Acids Res., 32, 2751-2759
46. El Hage A. and Alix J.H. (2004) Authentic precursors to ribosomal subunits accumulate in Escherichia coli in the absence of functional DnaK chaperone. Mol. Microbiol., 51, 189-201
47. Charollais J., Pflieger D., Vinh J., Dreyfus M. and Iost I. (2003) The DEAD-box RNA helicase SrmB is involved in the assembly of 50S ribosomal subunits in Escherichia coli. Mol. Microbiol., 48, 1253-1265
48. Hager J., Staker B.L., Bugl H. and Jakob U. (2002) Active site in RrmJ, a heat shock-induced methyltransferase. J. Biol. Chem., 277, 41978-41986
49. Jiang M., Datta K., Walker A., Strahler J., Bagamasbad P., Andrews P.C. and Maddock J.R. (2006) The Escherichia coli GTPase CgtAE is involved in late steps of large ribosome assembly. J. Bacteriol., 188, 6757-6770
50. Teraoka H. and Nierhaus K.H. (1978) Protein L16 induces a conformational change when incorporated into a L16-deficient core derived from Escherichia coli ribosomes. FEBS Lett., 88, 223-226
51. Frank J. and Agrawal R.K. (2000) A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature, 406, 318-322
52. Valle M., Zavialov A., Sengupta J., Rawat U., Ehrenberg M. and Frank J. (2003) Locking and unlocking of ribosomal motions. Cell, 114, 123-134
53. 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
54. Reblova K., Razga F., Li W., Gao H., Frank J. and Sponer J. (2010) Dynamics of the base of ribosomal A-site finger revealed by molecular dynamics simulations and Cryo-EM. Nucleic Acids Res., 38, 1325-1340
55. Piekna-Przybylska D., Przybylski P., Baudin-Baillieu A., Rousset J.P. and Fournier M.J. (2008) Ribosome performance is enhanced by a rich cluster of pseudouridines in the A-site finger region of the large subunit. J. Biol. Chem., 283, 26026-26036
56. Sharpe Elles L.M., Sykes M.T., Williamson J.R. and Uhlenbeck O.C. (2009) A dominant negative mutant of the E. coli RNA helicase DbpA blocks assembly of the 50S ribosomal subunit. Nucleic Acids Res., 37, 6503-6514
57. Hwang J. and Inouye M. (2006) The tandem GTPase, Der, is essential for the biogenesis of 50S ribosomal subunits in Escherichia coli. Mol. Microbiol., 61, 1660-1672
58. Wower I.K., Wower J. and Zimmermann R.A. (1998) Ribosomal protein L27 participates in both 50 S subunit assembly and the peptidyl transferase reaction. J. Biol. Chem., 273, 19847-19852
59. Maguire B.A. and Wild D.G. (1997) The roles of proteins L28 and L33 in the assembly and function of Escherichia coli ribosomes in vivo. Mol. Microbiol., 23, 237-245
60. Maguire B.A. and Wild D.G. (1997) The effects of mutations in the rpmB G operon of Escherichia coli on ribosome assembly and ribosomal protein synthesis. Biochim. Biophys. Acta, 1353, 137-147
61. Chen S.S. and Williamson J.R. (2013) Characterization of the ribosome biogenesis landscape in E. coli using quantitative mass spectrometry. J. Mol. Biol., 425, 767-779
62. Mulder A.M., Yoshioka C., Beck A.H., Bunner A.E., Milligan R.A., Potter C.S., Carragher B. and Williamson J.R. (2010) Visualizing ribosome biogenesis: Parallel assembly pathways for the 30S subunit. Science, 330, 673-677
63. Powers T., Daubresse G. and Noller H.F. (1993) Dynamics of in vitro assembly of 16 S rRNA into 30 S ribosomal subunits. J. Mol. Biol., 232, 362-374
64. de Narvaez C.C. and Schaup H.W. (1979) In vivo transcriptionally coupled assembly of Escherichia coli ribosomal subunits. J. Mol. Biol., 134, 1-22
65. Adilakshmi T., Bellur D.L. and Woodson S.A. (2008) Concurrent nucleation of 16S folding and induced fit in 30S ribosome assembly. Nature, 455, 1268-1272
66. Holmes K.L. and Culver G.M. (2004) Mapping structural differences between 30S ribosomal subunit assembly intermediates. Nat. Struct. Mol. Biol., 11, 179-186
67. Holmes K.L. and Culver G.M. (2005) Analysis of conformational changes in 16 S rRNA during the course of 30 S subunit assembly. J. Mol. Biol., 354, 340-357
68. Woodson S.A. (2011) RNA folding pathways and the selfassembly of ribosomes. Acc. Chem. Res., 44, 1312-1319
69. Achila D., Gulati M., Jain N. and Britton R.A. (2012) Biochemical characterization of ribosome assembly GTPase RbgA in Bacillus subtilis. J. Biol. Chem., 287, 8417-8423
70. Dutca L.M. and Culver G.M. (2008) Assembly of the 50 and 30 minor domains of 16S ribosomal RNA as monitored by tethered probing from ribosomal protein S20. J. Mol. Biol., 376, 92-108
71. Jomaa A., Stewart G., Martin-Benito J., Zielke R., Campbell T.L., Maddock J.R., Brown E.D. and Ortega J. (2011) Understanding ribosome assembly: The structure of in vivo assembled immature 30S subunits revealed by cryo-electron microscopy. RNA, 17, 697-709
72. Nanamiya H., Akanuma G., Natori Y., Murayama R., Kosono S., Kudo T., Kobayashi K., Ogasawara N., Park S.M., Ochi K. et al. (2004) Zinc is a key factor in controlling alternation of two types of L31 protein in the Bacillus subtilis ribosome. Mol. Microbiol., 52, 273-283
73. Schmalisch M., Langbein I. and Stulke J. (2002) The general stress protein Ctc of Bacillus subtilis is a ribosomal protein. J. Mol. Microbiol. Biotechnol., 4, 495-501