Understanding ribosome assembly: The structure of in vivo assembled immature 30S subunits revealed by cryo-electron microscopy

RNA

Volumn 17, Issue 4, 2011, Pages 697-709

  Jomaa, Ahmad ^a   Stewart, Geordie ^a   Martín Benito, Jaime ^b   Zielke, Ryszard ^c   Campbell, Tracey L ^a   Maddock, Janine R ^c   Brown, Eric D ^a   Ortega, Joaquin ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

17S rRNA; 30S subunit; GTPase; Ribosome assembly; rRNA processing; YjeQ protein

Indexed keywords

MESSENGER RNA; RIBOSOME PROTEIN; RIBOSOME RNA; RNA 17S; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; GENE; GENE DELETION; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN RNA BINDING; RNA PROCESSING; RNA STRUCTURE; SMALL RIBOSOMAL SUBUNIT; YJEQ GENE;

CRYOELECTRON MICROSCOPY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE DELETION; GTP PHOSPHOHYDROLASES; PROTEIN STRUCTURE, SECONDARY; RIBOSOME SUBUNITS, SMALL, BACTERIAL; RNA, RIBOSOMAL;

EID: 79952996835     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.2509811     Document Type: Article

References (56)

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. Aebi U, Pollard TD. 1987. A glow discharge unit to render electron microscope grids and other surfaces hydrophilic. J Electron Microsc Tech 7: 29-33.
3. 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. (Pubitemid 30659939)
4. Borovinskaya MA, Pai RD, Zhang W, Schuwirth BS, Holton JM, Hirokawa G, Kaji H, Kaji A, Cate JH. 2007. Structural basis for aminoglycoside inhibition of bacterial ribosome recycling. Nat Struct Mol Biol 14: 727-732. (Pubitemid 47220057)
5. Brown ED. 2005. Conserved P-loop GTPases of unknown function in bacteria: an emerging and vital ensemble in bacterial physiology. Biochem Cell Biol 83: 738-746.
6. Bubunenko M, Korepanov A, Court DL, Jagannathan I, Dickinson D, Chaudhuri BR, Garber MB, Culver GM. 2006. 30S ribosomal subunits can be assembled in vivo without primary binding ribosomal protein S15. RNA 12: 1229-1239. (Pubitemid 43990548)
7. Campbell TL, Brown ED. 2008. Genetic interaction screens with ordered overexpression and deletion clone sets implicate the Escherichia coli GTPase YjeQ in late ribosome biogenesis. J Bacteriol 190: 2537-2545.
8. Campbell TL, Daigle DM, Brown ED. 2005. Characterization of the Bacillus subtilis GTPase YloQ and its role in ribosome function. Biochem J 389: 843-852.
9. Chen X, Walker AK, Strahler JR, Simon ES, Tomanicek-Volk SL, Nelson BB, Hurley MC, Ernst SA, Williams JA, Andrews PC. 2006. Organellar proteomics: Analysis of pancreatic zymogen granule membranes. Mol Cell Proteomics 5: 306-312. (Pubitemid 43329308)
10. Connolly K, Culver G. 2009. Deconstructing ribosome construction. Trends Biochem Sci 34: 256-263.
11. Culver GM. 2003. Assembly of the 30S ribosomal subunit. Biopolymers 68: 234-249. (Pubitemid 36222402)
12. Daigle DM, Brown ED. 2004. Studies of the interaction of Escherichia coli YjeQ with the ribosome in vitro. J Bacteriol 186: 1381-1387.
13. Daigle DM, Rossi L, Berghuis AM, Aravind L, Koonin EV, Brown ED. 2002. YjeQ, an essential, conserved, uncharacterized protein from Escherichia coli, is an unusual GTPase with circularly permuted G-motifs and marked burst kinetics. Biochemistry 41: 11109-11117.
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. (Pubitemid 350030563)
15. Frank J. 2003. Toward an understanding of the structural basis of translation. Genome Biol 4: 237. doi: 10.1186/gb-2003-4-12-237.
16. Gao H, Valle M, Ehrenberg M, Frank J. 2004. Dynamics of EF-G interaction with the ribosome explored by classification of a heterogeneous cryo-EM dataset. J Struct Biol 147: 283-290. (Pubitemid 39140735)
17. 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.
18. 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. (Pubitemid 34014868)
19. Hayes F, Vasseur M. 1976. Processing of the 17-S Escherichia coli precursor RNA in the 27-S pre-ribosomal particle. Eur J Biochem 61: 433-442.
20. 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. (Pubitemid 39445517)
21. Holmes KL, Culver GM. 2004. Mapping structural differences between 30S ribosomal subunit assembly intermediates. Nat Struct Mol Biol 11: 179-186. (Pubitemid 38146522)
22. Hosokawa K, Nomura M. 1965. Incomplete ribosomes produced in chloramphenicol- and puromycin-inhibited Escherichia coli. J Mol Biol 12: 225-241.
23. Hosokawa K, Fujimura RK, Nomura M. 1966. Reconstitution of functionally active ribosomes from inactive subparticles and proteins. Proc Natl Acad Sci 55: 198-204.
24. 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. (Pubitemid 44497887)
25. Jiang M, Sullivan SM, Walker AK, Strahler JR, Andrews PC, Maddock JR. 2007. Identification of novel Escherichia coli ribosome-associated proteins using isobaric tags and multidimensional protein identification techniques. J Bacteriol 189: 3434-3444. (Pubitemid 46668807)
26. Kimura T, Takagi K, Hirata Y, Hase Y, Muto A, Himeno H. 2008. Ribosome-small-subunit-dependent GTPase interacts with tRNA-binding sites on the ribosome. J Mol Biol 381: 467-477.
27. 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. (Pubitemid 29233959)
28. Ludtke SJ, Baldwin PR, Chiu W. 1999. EMAN: Semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128: 82-97. (Pubitemid 30013436)
29. Mangiarotti G, Turco E, Ponzetto A, Altruda F. 1974. Precursor 16S RNA in active 30S ribosomes. Nature 247: 147-148.
30. Mindell JA, Grigorieff N. 2003. Accurate determination of local defocus and specimen tilt in electron microscopy. J Struct Biol 142: 334-347. (Pubitemid 36638267)
31. Mitra K, Frank J. 2006. RIBOSOME DYNAMICS: Insights from atomic structure modeling into cryo-electron microscopy maps. Annu Rev Biophys Biomol Struct 35: 299-317. (Pubitemid 43877380)
32. Mizushima S, Nomura M. 1970. Assembly mapping of 30S ribosomal proteins from E. coli. Nature 226: 1214.
33. 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.
34. Poot RA, van den Worm SH, Pleij CW, van Duin J. 1998. Base complementarity in helix 2 of the central pseudoknot in 16S rRNA is essential for ribosome functioning. Nucleic Acids Res 26: 549-553. (Pubitemid 28291583)
35. Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, Hattan S, Khainovski N, Pillai S, Dey S, Daniels S, et al. 2004. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 3: 1154-1169.
36. 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 107: 4567-4572.
37. Scheres SH, Valle M, Carazo JM. 2005a. Fast maximum-likelihood refinement of electron microscopy images. Bioinformatics 21: 243-244.
38. Scheres SH, Valle M, Nunez R, Sorzano CO, Marabini R, Herman GT, Carazo JM. 2005b. Maximum-likelihood multi-reference refinement for electron microscopy images. J Mol Biol 348: 139-149. (Pubitemid 40461846)
39. Scheres SH, Gao H, Valle M, Herman GT, Eggermont PP, Frank J, Carazo JM. 2007. Disentangling conformational states of macromolecules in 3D-EM through likelihood optimization. Nat Methods 4: 27-29. (Pubitemid 46029470)
40. Scheres SH, Nunez-Ramirez R, Sorzano CO, Carazo JM, Marabini R. 2008. Image processing for electron microscopy single-particle analysis using XMIPP. Nat Protoc 3: 977-990. (Pubitemid 351818686)
41. Schluenzen F, Tocilj A, Zarivach R, Harms J, Gluehmann M, Janell D, Bashan A, Bartels H, Agmon I, Franceschi F, et al. 2000. Structure of functionally activated small ribosomal subunit at 3.3 Å resolution. Cell 102: 615-623.
42. 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. (Pubitemid 41567336)
43. 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 98: 11991-11996. (Pubitemid 32959814)
44. Sharma MR, Barat C, Wilson DN, Booth TM, Kawazoe M, Hori-Takemoto C, Shirouzu M, Yokoyama S, Fucini P, Agrawal RK. 2005. Interaction of Era with the 30S ribosomal subunit implications for 30S subunit assembly. Mol Cell 18: 319-329. (Pubitemid 41350537)
45. Siibak T, Peil L, Xiong L, Mankin A, Remme J, Tenson T. 2009. Erythromycin- and chloramphenicol-induced ribosomal assembly defects are secondary effects of protein synthesis inhibition. Antimicrob Agents Chemother 53: 563-571.
46. Srivastava AK, Schlessinger D. 1990. Mechanism and regulation of bacterial ribosomal RNA processing. Annu Rev Microbiol 44: 105-129.
47. Sykes MT, Williamson JR. 2009. A complex assembly landscape for the 30S ribosomal subunit. Annu Rev Biophys 38: 197-215.
48. Talkington MW, Siuzdak G, Williamson JR. 2005. An assembly landscape for the 30S ribosomal subunit. Nature 438: 628-632. (Pubitemid 41740567)
49. Traub P, Nomura M. 1968a. Structure and function of E. coli ribosomes. V. Reconstitution of functionally active 30S ribosomal particles from RNA and proteins. Proc Natl Acad Sci 59: 777-784.
50. Traub P, Nomura M. 1968b. Structure and function of Escherichia coli ribosomes. I. Partial fractionation of the functionally active ribosomal proteins and reconstitution of artificial subribosomal particles. J Mol Biol 34: 575-593.
51. Traub P, Nomura M. 1969. Studies on the assembly of ribosomes in vitro. Cold Spring Harb Symp Quant Biol 34: 63-67.
52. 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. (Pubitemid 34760585)
53. Wilson DN, Nierhaus KH. 2007. The weird and wonderful world of bacterial ribosome regulation. Crit Rev Biochem Mol Biol 42: 187-219. (Pubitemid 46911961)
54. 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 407: 327-339.
55. Wriggers W, Milligan RA, McCammon JA. 1999. Situs: A package for docking crystal structures into low-resolution maps from electron microscopy. J Struct Biol 125: 185-195. (Pubitemid 29402603)
56. 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. (Pubitemid 32422479)