Structural insights into the assembly of the 30S ribosomal subunit in vivo: Functional role of S5 and location of the 17S rRNA precursor sequence

Protein and Cell

Volumn 5, Issue 5, 2014, Pages 394-407

  Yang, Zhixiu ^a   Guo, Qiang ^a   Goto, Simon ^b   Chen, Yuling ^a   Li, Ningning ^a   Yan, Kaige ^a   Zhang, Yixiao ^a   Muto, Akira ^b   Deng, Haiteng ^a   Himeno, Hyouta ^b   Lei, Jianlin ^a   Gao, Ning ^a  

^a TSINGHUA UNIVERSITY   (China)

^b HIROSAKI UNIVERSITY   (Japan)

Author keywords

cryo EM; quantitative mass spectrometry; RbfA; ribosome assembly; RsgA

Indexed keywords

RIBOSOME RNA; ESCHERICHIA COLI PROTEIN; GUANOSINE TRIPHOSPHATASE; INORGANIC SALT; RBFA PROTEIN, E COLI; RIBOSOMAL PROTEIN S5; RIBOSOME PROTEIN; RSGA PROTEIN, E COLI;

ARTICLE; CRYSTAL STRUCTURE; ESCHERICHIA COLI; IMAGE PROCESSING; MASS SPECTROMETRY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; QUALITY CONTROL; SEQUENCE ANALYSIS; STRUCTURAL HOMOLOGY; TEMPERATURE; CHEMISTRY; CRYOELECTRON MICROSCOPY; GENETICS; METABOLISM; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SMALL RIBOSOMAL SUBUNIT; ULTRASTRUCTURE;

ESCHERICHIA COLI;

CRYOELECTRON MICROSCOPY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GTP PHOSPHOHYDROLASES; MASS SPECTROMETRY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RIBOSOMAL PROTEINS; RIBOSOME SUBUNITS, SMALL, BACTERIAL; RNA, RIBOSOMAL; SALTS;

EID: 84899495597     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-014-0044-1     Document Type: Article

References (66)

1. Adilakshmi T, Bellur DL, Woodson SA (2008) Concurrent nucleation of 16S folding and induced fit in 30S ribosome assembly. Nature 455: 1268-1272.
2. Blaha G, Stelzl U, Spahn CM, Agrawal RK, Frank J, Nierhaus KH (2000) Preparation of functional ribosomal complexes and effect of buffer conditions on tRNA positions observed by cryoelectron microscopy. Methods Enzymol 317: 292-309.
3. Boehringer D, O'Farrell HC, Rife JP, Ban N (2012) Structural insights into methyltransferase KsgA function in 30S ribosomal subunit biogenesis. J Biol Chem 287: 10453-10459.
4. Bunner AE, Beck AH, Williamson JR (2010) Kinetic cooperativity in Escherichia coli 30S ribosomal subunit reconstitution reveals additional complexity in the assembly landscape. Proc Natl Acad Sci USA 107: 5417-5422.
5. Bylund GO, Wipemo LC, Lundberg LA, Wikstrom PM (1998) RimM and RbfA are essential for efficient processing of 16S rRNA in Escherichia coli. J Bacteriol 180: 73-82.
6. Calidas D, Culver GM (2011) Interdependencies govern multidomain architecture in ribosomal small subunit assembly. RNA 17: 263-277.
7. Chen SS, Williamson JR (2013) Characterization of the ribosome biogenesis landscape in E. coli using quantitative mass spectrometry. J Mol Biol 425: 767-779.
8. Clatterbuck Soper SF, Dator RP, Limbach PA, Woodson SA (2013) In vivo X-ray footprinting of pre-30S ribosomes reveals chaperone-dependent remodeling of late assembly intermediates. Mol Cell 52: 506-516.
9. Culver GM, Noller HF (1999) Efficient reconstitution of functional Escherichia coli 30S ribosomal subunits from a complete set of recombinant small subunit ribosomal proteins. RNA 5: 832-843.
10. Culver GM, Heilek GM, Noller HF (1999) Probing the rRNA environment of ribosomal protein S5 across the subunit interface and inside the 30 S subunit using tethered Fe(II). J Mol Biol 286: 355-364.
11. Daigle DM, Brown ED (2004) Studies of the interaction of Escherichia coli YjeQ with the ribosome in vitro. J Bacteriol 186: 1381-1387.
12. Dammel CS, Noller HF (1993) A cold-sensitive mutation in 16S rRNA provides evidence for helical switching in ribosome assembly. Genes Dev 7: 660-670.
13. Dammel CS, Noller HF (1995) Suppression of a cold-sensitive mutation in 16S rRNA by overexpression of a novel ribosome-binding factor, RbfA. Genes Dev 9: 626-637.
14. Datta PP, Wilson DN, Kawazoe M, Swami NK, Kaminishi T, Sharma MR, Booth TM, Takemoto C, Fucini P, Yokoyama S et al (2007) Structural aspects of RbfA action during small ribosomal subunit assembly. Mol Cell 28: 434-445.
15. Davies BW, Kohrer C, Jacob AI, Simmons LA, Zhu J, Aleman LM, Rajbhandary UL, Walker GC (2010) Role of Escherichia coli YbeY, a highly conserved protein, in rRNA processing. Mol Microbiol 78: 506-518.
16. Dunkle JA, Xiong L, Mankin AS, Cate JH (2010) Structures of the Escherichiacoli ribosome with antibiotics bound near the peptidyl transferase center explain spectra of drug action. Proc Natl Acad Sci USA 107: 17152-17157.
17. Dutca LM, Culver GM (2008) Assembly of the 5′ and 3′ minor domains of 16S ribosomal RNA as monitored by tethered probing from ribosomal protein S20. J Mol Biol 376: 92-108.
18. Goto S, Kato S, Kimura T, Muto A, Himeno H (2011) RsgA releases RbfA from 30S ribosome during a late stage of ribosome biosynthesis. EMBO J 30: 104-114.
19. Grondek JF, Culver GM (2004) Assembly of the 30S ribosomal subunit: positioning ribosomal protein S13 in the S7 assembly branch. RNA 10: 1861-1866.
20. Guo Q, Yuan Y, Xu Y, Feng B, Liu L, Chen K, Sun M, Yang Z, Lei J, Gao N (2011) Structural basis for the function of a small GTPase RsgA on the 30S ribosomal subunit maturation revealed by cryoelectron microscopy. Proc Natl Acad Sci USA 108: 13100-13105.
21. Guo Q, Goto S, Chen Y, Feng B, Xu Y, Muto A, Himeno H, Deng H, Lei J, 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.
22. Hase Y, Yokoyama S, Muto A, Himeno H (2009) Removal of a ribosome small subunit-dependent GTPase confers salt resistance on Escherichia coli cells. RNA 15: 1766-1774.
23. Hase Y, Tarusawa T, Muto A, Himeno H (2013) Impairment of ribosome maturation or function confers salt resistance on Escherichia coli cells. PloS One 8: e65747.
24. Himeno H, Hanawa-Suetsugu K, Kimura T, Takagi K, Sugiyama W, Shirata S, Mikami T, Odagiri F, Osanai Y, Watanabe D et al (2004) A novel GTPase activated by the small subunit of ribosome. Nucleic Acids Res 32: 5303-5309.
25. Holmes KL, Culver GM (2004) Mapping structural differences between 30S ribosomal subunit assembly intermediates. Nat Struct Mol Biol 11: 179-186.
26. Holmes KL, Culver GM (2005) Analysis of conformational changes in 16 S rRNA during the course of 30 S subunit assembly. J Mol Biol 354: 340-357.
27. Ito T, Wittmann HG (1973) Amino acid replacements in proteins S5 and S12 of two Escherichia coli revertants from streptomycin dependence to independence. Mol Gen Genet 127: 19-32.
28. Jacob AI, Kohrer C, Davies BW, RajBhandary UL, Walker GC (2013) Conserved bacterial RNase YbeY plays key roles in 70S ribosome quality control and 16S rRNA maturation. Mol Cell 49: 427-438.
29. Jelenc PC (1980) Rapid purification of highly active ribosomes from Escherichia coli. Anal Biochem 105: 369-374.
30. Jiang M, Datta K, Walker A, Strahler J, Bagamasbad P, Andrews PC, Maddock JR (2006) The Escherichia coli GTPase CgtAE is involved in late steps of large ribosome assembly. J Bacteriol 188: 6757-6770.
31. Jomaa A, Stewart G, Martin-Benito J, Zielke R, Campbell TL, Maddock JR, Brown ED, Ortega J (2011) Understanding ribosome assembly: the structure of in vivo assembled immature 30S subunits revealed by cryo-electron microscopy. RNA 17: 697-709.
32. Jones PG, Inouye M (1996) RbfA, a 30S ribosomal binding factor, is a cold-shock protein whose absence triggers the cold-shock response. Mol Microbiol 21: 1207-1218.
33. Kirthi N, Roy-Chaudhuri B, Kelley T, Culver GM (2006) A novel single amino acid change in small subunit ribosomal protein S5 has profound effects on translational fidelity. RNA 12: 2080-2091.
34. Lei J, Frank J (2005) Automated acquisition of cryo-electron micrographs for single particle reconstruction on an FEI Tecnai electron microscope. J Struct Biol 150: 69-80.
35. Leong V, Kent M, Jomaa A, Ortega J (2013) Escherichia coli rimM and yjeQ null strains accumulate immature 30S subunits of similar structure and protein complement. RNA 19: 789-802.
36. Li Z, Pandit S, Deutscher MP (1999) RNase G (CafA protein) and RNase E are both required for the 5′ maturation of 16S ribosomal RNA. EMBO J 18: 2878-2885.
37. Maguire BA, Wondrack LM, Contillo LG, Xu Z (2008) A novel chromatography system to isolate active ribosomes from pathogenic bacteria. RNA 14: 188-195.
38. Mangiarotti G, Turco E, Ponzetto A, Altruda F (1974) Precursor 16S RNA in active 30S ribosomes. Nature 247: 147-148.
39. Mathews DH, Disney MD, Childs JL, Schroeder SJ, Zuker M, Turner DH (2004) Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc Natl Acad Sci USA 101: 7287-7292.
40. Mizushima S, Nomura M (1970) Assembly mapping of 30S ribosomal proteins from E. coli. Nature 226: 1214.
41. Mulder AM, Yoshioka C, Beck AH, Bunner AE, Milligan RA, Potter CS, Carragher B, Williamson JR (2010) Visualizing ribosome biogenesis: parallel assembly pathways for the 30S subunit. Science 330: 673-677.
42. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.
43. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kale L, Schulten K (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26: 1781-1802.
44. Piepersberg W, Bock A, Wittmann HG (1975) Effect of different mutations in ribosomal protein S5 of Escherichia coli on translational fidelity. Mol Gen Genet 140: 91-100.
45. Powers T, Daubresse G, Noller HF (1993) Dynamics of in vitro assembly of 16 S rRNA into 30 S ribosomal subunits. J Mol Biol 232: 362-374.
46. Ramaswamy P, Woodson SA (2009) S16 throws a conformational switch during assembly of 30S 5′ domain. Nat Struct Mol Biol 16: 438-445.
47. Rath BK, Frank J (2004) Fast automatic particle picking from cryo-electron micrographs using a locally normalized cross-correlation function: a case study. J Struct Biol 145: 84-90.
48. Rodnina MV, Wintermeyer W (1995) GTP consumption of elongation factor Tu during translation of heteropolymeric mRNAs. Proc Natl Acad Sci USA 92: 1945-1949.
49. Rohl R, Nierhaus KH (1982) Assembly map of the large subunit (50S) of Escherichia coli ribosomes. Proc Natl Acad Sci USA 79: 729-733.
50. Roy-Chaudhuri B, Kirthi N, Kelley T, Culver GM (2008) Suppression of a cold-sensitive mutation in ribosomal protein S5 reveals a role for RimJ in ribosome biogenesis. Mol Microbiol 68: 1547-1559.
51. Roy-Chaudhuri B, Kirthi N, Culver GM (2010) Appropriate maturation and folding of 16S rRNA during 30S subunit biogenesis are critical for translational fidelity. Proc Natl Acad Sci USA 107: 4567-4572.
52. Scheres SH (2012) A Bayesian view on cryo-EM structure determination. J Mol Biol 415: 406-418.
53. Schrodinger LLC (2010) The PyMOL molecular graphics system, version 1. 3r1.
54. Schultz SG, Solomon AK (1961) Cation transport in Escherichia coli. I. Intracellular Na and K concentrations and net cation movement. J Gen Physiol 45: 355-369.
55. 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.
56. Shaikh TR, Gao H, Baxter WT, Asturias FJ, Boisset N, Leith A, Frank J (2008a) SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs. Nat Protoc 3: 1941-1974.
57. Shaikh TR, Trujillo R, LeBarron JS, Baxter WT, Frank J (2008b) Particle-verification for single-particle, reference-based reconstruction using multivariate data analysis and classification. J Struct Biol 164: 41-48.
58. Shajani Z, Sykes MT, Williamson JR (2011) Assembly of bacterial ribosomes. Annu Rev Biochem 80: 501-526.
59. Stern S, Powers T, Changchien LM, Noller HF (1989) RNA-protein interactions in 30S ribosomal subunits: folding and function of 16S rRNA. Science 244: 783-790.
60. Sykes MT, Shajani Z, Sperling E, Beck AH, Williamson JR (2010) Quantitative proteomic analysis of ribosome assembly and turnover in vivo. J Mol Biol 403: 331-345.
61. Talkington MW, Siuzdak G, Williamson JR (2005) An assembly landscape for the 30S ribosomal subunit. Nature 438: 628-632.
62. Thompson A, Schafer J, Kuhn K, Kienle S, Schwarz J, Schmidt G, Neumann T, Johnstone R, Mohammed AK, 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.
63. Trabuco LG, Villa E, Mitra K, Frank J, Schulten K (2008) Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics. Structure 16: 673-683.
64. Traub P, 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.
65. Xia B, Ke H, Shinde U, Inouye M (2003) The role of RbfA in 16S rRNA processing and cell growth at low temperature in Escherichia coli. J Mol Biol 332: 575-584.
66. Young RA, Steitz JA (1978) Complementary sequences 1700 nucleotides apart form a ribonuclease III cleavage site in Escherichia coli ribosomal precursor RNA. Proc Natl Acad Sci USA 75: 3593-3597.