RsgA releases RbfA from 30S ribosome during a late stage of ribosome biosynthesis

EMBO Journal

Volumn 30, Issue 1, 2011, Pages 104-114

  Goto, Simon ^a,b   Kato, Shingo ^a   Kimura, Takatsugu ^a   Muto, Akira ^a   Himeno, Hyouta ^a  

^a HIROSAKI UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

GTPase; RbfA; ribosome assembly; ribosome maturation; RsgA

Indexed keywords

BACTERIAL PROTEIN; GUANOSINE TRIPHOSPHATASE; RBFA PROTEIN; RNA 16S; RSGA PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE MUTATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN SECRETION; RIBOSOME; RIBOSOME BIOSYNTHESIS; RIBOSOME SUBUNIT; RNA SYNTHESIS;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GTP PHOSPHOHYDROLASES; MUTATION; PROTEIN BINDING; RIBOSOMAL PROTEINS; RIBOSOME SUBUNITS, SMALL, BACTERIAL; RIBOSOMES;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 78650899879     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.291     Document Type: Article

References (60)

1. Absalon C, Hamze K, Blanot D, Frehel C, Carballido-Lopez R, Holland BI, Heijenoort Jv, Séror SJ (2008) The GTPase CpgA is implicated in the deposition of the peptidoglycan sacculus in Bacillus subtilis. J Bacteriol 190: 3786-3790
2. Arigoni F, Talabot F, Peitsch M, Edgerton MD, Meldrum E, Allet E, Fish R, Jamotte T, Curchod ML, Loferer H (1998) A genome-based approach for the identification of essential bacterial genes. Nat Biotechnol 16: 851-856
3. Britton RA (2009) Role of GTPases in bacterial ribosome assembly. Annu Rev Microbiol 63: 155-176
4. Bylund GO, Lövgren JM, Wikström PM (2001) Characterization of mutations in the metY-nusA-infB operon that suppress the slow growth of a DrimM mutant. J Bacteriol 183: 6095-6106
5. Bylund GO, Wipemo LC, Lundberg LA, Wikström PM (1998) RimM and RbfA are essential for efficient processing of 16S rRNA in Escherichia coli. J Bacteriol 180: 73-82
6. 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
7. 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
8. Campbell TL, Henderson J, Heinrichs DE, Brown ED (2006) The yjeQ gene is required for virulence of Staphylococcus aureus. Infect Immun 74: 4918-4921
9. Cladière L, Hamze K, Madec E, Levdikov VM, Wilkinson AJ, Holland IB, Séror SJ (2006) The GTPase, CpgA(YloQ), a putative translation factor, is implicated in morphogenesis in Bacillus subtilis. Mol Genet Genomics 275: 409-420
10. Connolly K, Culver G (2009) Deconstructing ribosome construction. Trends Biochem Sci 34: 256-263
11. Dagley S, Turnock G, Wild DG (1963) The accumulation of ribonu-cleic acid by a mutant of Escherichia coli. Biochem J 88: 555-566
12. Dagley S, White AE, Wild DG, Sykes J (1962) Synthesis of protein and ribosomes by bacteria. Nature 194: 25-27
13. Daigle DM, Brown ED (2004) Studies of the interaction of Escherichia coli YjeQ with the ribosome in vitro. J Bacteriol 186: 1381-1387
14. 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
15. 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
16. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645
17. Datta PP, Wilson DN, Kawazoe M, Swami NK, Kaminishi T, Sharma MR, Booth TM, Takemoto C, Fucini P, Yokoyama S, Agrawal RK (2007) Structural aspects of RbfA action during small ribosomal subunit assembly. Mol Cell 28: 434-445
18. 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
19. Hedges J, West M, Johnson AW (2005) Release of the export adapter, Nmd3p, from the 60S ribosomal subunit requires Rpl10p and the cytoplasmic GTPase Lsg1p. EMBO J 24: 567-579
20. Held WA, Nomura M (1973) Rate determining step in the recon-stitution of Escherichia coli 30S ribosomal subunits. Biochemistry 12: 3273-3281
21. Himeno H, Hanawa-Suetsugu K, Kimura T, Takagi K, Sugiyama W, Shirata S, Mikami T, Odagiri F, Osanai Y, Watanabe D, Goto S, Kalachnyuk L, Ushida C, Muto A (2004) A novel GTPase activated by the small subunit of ribosome. Nucleic Acids Res 32: 5303-5309
22. Hosokawa K, Nomura M (1965) Incomplete ribosomes produced in chloramphenicol- and puromycin-inhibited Escherichia coli. J Mol Biol 12: 225-241
23. Huang YJ, Swapna GV, Rajan PK, Ke H, Xia B, Shukla K, Inouye M, Montelione GT (2003) Solution NMR structure of ribosome-bind-ing factor A (RbfA), a cold-shock adaptation protein from Escherichia coli. J Mol Biol 327: 521-536
24. Hunt A, Rawlins JP, Thomaides HB, Errington J (2006) Functional analysis of 11 putative essential genes in Bacillus subtilis. Microbiology 152: 2895-2907
25. Hwang J, Inouye M (2006) The tandem GTPase, Der, is essential for the biogenesis of 50S ribosomal subunits in Escherichia coli. Mol Microbiol 61 : 1660-1672
26. Inoue K, Alsina J, Chen J, Inouye M (2003) Suppression of defective ribosome assembly in a rbfA deletion mutant by overexpression of Era, an essential GTPase in Escherichia coli. Mol Microbiol 48: 10 0 5 - 101 6
27. Inoue K, Chen J, Tan Q, Inouye M (2006) Era and RbfA have overlapping function in ribosome biogenesis in Escherichia coli. J Mol Microbiol Biotechnol 11 : 41-52
28. Inoue T, Shingaki R, Hirose S, Waki K, Mori H, Fukui K (2007) Genome-wide screening of genes required for swarming motility in Escherichia coli K-12. J Bacteriol 189: 950-957
29. 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
30. Kaczanowska M, Rydén-Aulin M (2007) Ribosome biogenesis and the translation process in Escherichia coli. Microbiol Mol Biol Rev 71: 477-494
31. Karbstein K (2007) Role of GTPases in ribosome assembly. Biopolymers 87: 1-11
32. Karbstein K, Jonas S, Doudna JA (2005) An essential GTPase promotes assembly of preribosomal RNA processing complexes. Mol Cell 20: 633-643
33. 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
34. Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, Toyonaga H, Mori H (2005) Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res 12: 291-299
35. Kressler D, Hurt E, Bassler J (2010) Driving ribosome assembly. Biochim Biophys Acta 1803: 673-683
36. Levdikov VM, Blagova EV, Brannigan JA, Cladière L, Antson AA, Isupov MN, Séror SJ, Wilkinson AJ (2004) The crystal structure of YloQ, a circularly permuted GTPase essential for Bacillus subtilis viability. J Mol Biol 340: 767-782
37. Loh PC, Morimoto T, Matsuo Y, Oshima T, Ogasawara N (2007) The GTP-binding protein YqeH participates in biogenesis of the 30S ribosome subunit in Bacillus subtilis. Genes Genet Syst 82: 281-289
38. Lowry CV, Dahlberg JE (1971) Structural differences between the 16S ribosomal RNA of E. coli and its precursor. Nat New Biol 232: 52-54
39. Mangiarotti G, Turco E, Perlo C, Altruda F (1975) Role of precursor 16S RNA in assembly of E. coli 30S ribosomes. Nature 253: 569-571
40. Matsuo Y, Morimoto T, Kuwano M, Loh PC, Oshima T, 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
41. Neidhardt FC, Eidlic L (1963) Characterization of the RNA formed under conditions of relaxed amino acid control in Escherichia coli. Biochim Biophys Acta 68: 380-388
42. Nichols CE, Johnson C, Lamb HK, Lockyer M, Charles IG, Hawkins AR, Stammers DK (2007) Structure of the ribosomal interacting GTPase YjeQ from the enterobacterial species Salmonella typhimur-ium. Acta Crystallogr Sect F Struct Biol Cryst Commun 63: 922-928
43. Nierhaus KH, Dohme F (1974) Total reconstitution of functionally active 50S ribosomal subunits from Escherichia coli. Proc Natl Acad Sci USA 71: 4713-4717
44. Nomura M, Erdmann VA (1970) Reconstitution of 50S ribosomal subunits from dissociated molecular components. Nature 228: 744-748
45. Sato A, Kobayashi G, Hayashi H, Yoshida H, Wada A, Maeda M, Hiraga S, Takeyasu K, Wada C (2005) The GTP binding protein Obg homolog ObgE is involved in ribosome maturation. Genes Cells 10: 393-408
46. Senger B, Lafontaine DL, Graindorge JS, Gadal O, Camasses A, Sanni A, Garnier JM, Breitenbach M, Hurt E, Fasiolo F (2001) The nucle(ol)ar Tif6p and Efl1p are required for a late cytoplasmic step of ribosome synthesis. Mol Cell 8: 1363-1373
47. 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
48. Shin DH, Lou Y, Jancarik J, Yokota H, Kim R, Kim SH (2004) Crystal structure of YjeQ from Thermotoga maritima contains a circularly permuted GTPase domain. Proc Natl Acad Sci USA 101 : 13198-13203
49. 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
50. Strunk BS, Karbstein K (2009) Powering through ribosome assembly. RNA 15: 2083-2104
51. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4: 41
52. Tatusov RL, Koonin EV, Lipman DJ (1997) A genomic perspective on protein families. Science 278: 631-637
53. 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
54. Uicker WC, Schaefer L, Britton RA (2006) The essential GTPase RbgA (YlqF) is required for 50S ribosome assembly in Bacillus subtilis. Mol Microbiol 59: 528-540
55. Uicker WC, Schaefer L, Koenigsknecht M, Britton RA (2007) The essential GTPase YqeH is required for proper ribosome assembly in Bacillus subtilis. J Bacteriol 189: 2926-2929
56. Wicker-Planquart C, Foucher AE, Louwagie M, Britton RA, Jault JM (2008) Interactions of an essential Bacillus subtilis GTPase, YsxC, with ribosomes. J Bacteriol 190: 681-690
57. Wilson DN (2009) The A-Z of bacterial translation inhibitors. Crit Rev Biochem Mol Biol 44: 393-433
58. Wilson DN, Nierhaus KH (2007) The weird and wonderful world of bacterial ribosome regulation. Crit Rev Biochem Mol Biol 42: 187-219
59. 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
60. Young RA, Steitz JA (1978) Complementary sequences 1700 nucleo-tides apart form a ribonuclease III cleavage site in Escherichia coli ribosomal precursor RNA. Proc Natl Acad Sci USA 75: 3593-3597