A dominant negative mutant of the E. coli RNA helicase DbpA blocks assembly of the 50S ribosomal subunit

Nucleic Acids Research

Volumn 37, Issue 19, 2009, Pages 6503-6514

  Sharpe Elles, Lisa M ^a,c   Sykes, Michael T ^b   Williamson, James R ^b   Uhlenbeck, Olke C ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c WASHBURN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL RNA; PEPTIDYLTRANSFERASE; PROTEIN DBPA; RNA 23S; RNA HELICASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM MUTANT; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SUBSTRATE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; RIBOSOME SUBUNIT; RNA CONFORMATION;

DEAD-BOX RNA HELICASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MUTATION; RIBOSOMAL PROTEINS; RIBOSOME SUBUNITS, LARGE, BACTERIAL; RNA, RIBOSOMAL;

ESCHERICHIA COLI;

EID: 71049181356     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp711     Document Type: Article

References (60)

1. Sieber,G. and Nierhaus,K.H. (1978) Kinetic and thermodynamic parameters of the assembly in vitro of the large subunit from Escherichia coli ribosomes. Biochemistry, 17, 3505-3511.
2. Spillmann,S., Dohme,F. and Nierhaus,K.H. (1977) Assembly in vitro of the 50S subunit from Escherichia coli ribosomes: Proteins essential for the first heat-dependent conformational change. J. Mol. Biol., 115 513-523.
3. Mangiarotti,G., Apirion,D., Schlessinger,D. and Silengo,L. (1968) Biosynthetic precursors of 30S and 50S ribosomal particles in Escherichia coli. Biochemistry, 7, 456-472.
4. Nierhaus,K.H., Bordasch,K. and Homann,H.E. (1973) In vivo assembly of Escherichia coli ribosomal proteins. J. Mol. Biol., 74, 587-597.
5. Hayes,F. and Hayes,D.H. (1971) Biosynthesis of ribosomes in E. coli. I. Properties of ribosomal precursor particles and their RNA components. Biochimie, 53, 369-382.
6. Osawa,S., Otaka,E., Itoh,T. and Fukui,T. (1969) Biosynthesis of 50s ribosomal subunit in Escherichia coli. J. Mol. Biol., 40, 321-351.
7. Lindahl,L. (1975) Intermediates and time kinetics of the in vivo assembly of Escherichia coli ribosomes. J. Mol. Biol., 92 15-37.
8. Dohme,F. and Nierhaus,K.H. (1976) Total reconstitution and assembly of 50 S subunits from Escherichia coli Ribosomes in vitro. J. Mol. Biol. 107, 585-599.
9. 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.
10. Traub,P. and Nomura,M. (1969) Mechanism of assembly of 30 s ribosomes studied in vitro. J. Mol. Biol., 40, 391-404.
11. Homann,H.E. and Nierhaus,K.H. (1971) Ribosomal proteins. Protein compositions of biosynthetic precursors and artifical subparticles from ribosomal subunits in Escherichia coli K 12. Eur. J. Biochem. 20, 249-257.
12. Nierhaus,K.H. (1991) The assembly of prokaryotic ribosomes. Biochimie 73, 739-755.
13. Held,W.A., Ballou,B., Mizushima,S. and Nomura,M. (1974) Assembly mapping of 30 S ribosomal proteins from Escherichia coli further studies. J. Biol. Chem., 249, 3103-3111.
14. 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.
15. Williamson,J.R. (2003) After the ribosome structures: How are the subunits assembled? RNA, 9, 165-167.
16. Kaczanowska,M. and Rydén-Aulin,M. (2007) Ribosome biogenesis and the translation process in Escherichia coli. Microbiol. Mol. Biol. Rev. 71, 477-494.
17. Wilson,D.N. and Nierhaus,K.H. (2007) The weird and wonderful world of bacterial ribosome regulation. Crit. Rev. Biochem. Mol. Biol., 42, 187-219.
18. Ban,N., Nissen,P., Hansen,J., Moore,P.B. and Steitz,T.A. (2000) The complete atomic structure of the large ribosomal subunit at 2.4A resolution. Science, 289, 905-920.
19. Yusupov,M.M., Yusupova,G.Z., Baucom,A., Lieberman,K., Earnest,T.N., Cate,J.H.D. and Noller,H.F. (2001) Crystal structure of the ribosome at 5.5A resolution. Science, 292, 883-896.
20. Nicol,S.M. and Fuller-Pace,F.V. (1995) The "DEAD box" protein DbpA interacts specifically with the peptidyltransferase center in 23S rRNA. Proc. Natl Acad. Sci. USA, 92, 11681-11685.
21. Tsu,C.A. and Uhlenbeck,O.C. (1998) Kinetic analysis of the RNA-dependent adenosinetriphosphatase activity of DbpA, an Escherichia coli DEAD protein specific for 23S ribosomal RNA. Biochemistry, 37, 16989-16996.
22. Karginov,F.V., Caruthers,J.M., Hu,Y., McKay,D.B. and Uhlenbeck,O.C. (2005) YxiN is a modular protein combining a DEx(D/H) core and a specific RNA-binding domain. J. Biol. Chem., 280, 35499-35505.
23. Kossen,K., Karginov,F.V. and Uhlenbeck,O.C. (2002) The carboxy-terminal domain of the DExDH protein YxiN is sufficient to confer specificity for 23S rRNA. J. Mol. Biol., 324, 625-636.
24. Wang,S., Hu,Y., Overgaard,M.T., Karginov,F.V., Uhlenbeck,O.C. and McKay,D.B. (2006) The domain of the Bacillus subtilis DEAD-box helicase YxiN that is responsible for specific binding of 23S rRNA has an RNA recognition motif fold. RNA, 12, 959-967.
25. Boddeker,N., Stade,K. and Franceschi,F. (1997) Characterization of DbpA, an Escherichia coli DEAD box protein with ATP independent RNA unwinding activity. Nucleic Acids Res., 25, 537-545.
26. Baba,T., Ara,T., Hasegawa,M., Takai,Y., Okumura,Y., Baba,M., Datsenko,K.A., Tomita,M., Wanner,B.L. and Mori,H. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: The Keio collection. Mol. Syst. Biol., 2, 2006.0008.
27. Iost,I. and Dreyfus,M. (2006) DEAD-box RNA helicases in Escherichia coli. Nucleic Acids Res., 34, 4189-4197.
28. Sharpe Elles,L.M. and Uhlenbeck,O.C. (2008) Mutation of the arginine finger in the active site of Escherichia coli DbpA abolishes ATPase and helicase activity and confers a dominant slow growth phenotype. Nucleic Acids Res., 36, 41-50.
29. Karginov,F.V. and Uhlenbeck,O.C. (2004) Interaction of Escherichia coli DbpA with 23S rRNA in different functional states of the enzyme. Nucleic Acids Res., 32, 3028-3032.
30. Zhang,Y., Buchholz,F., Muyrers,J.P.P. and Stewart,A.F. (1998) A new logic for DNA engineering using recombination in Escherichia coli. Nat. Genet., 20, 123-128.
31. Diges,C.M. and Uhlenbeck,O.C. (2001) Escherichia coli DbpA is an RNA helicase that requires hairpin 92 of 23S rRNA. EMBO J., 20 5503-5512.
32. Tsu,C.A., Kossen,K. and Uhlenbeck,O.C. (2001) The Escherichia coli DEAD protein DbpA recognizes a small RNA hairpin in 23S rRNA. RNA, 7 702-709.
33. 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.
34. Fahlman,R.P., Dale,T. and Uhlenbeck,O.C. (2004) Uniform binding of aminoacylated transfer RNAs to the ribosomal A and P sites. Mol. Cell 16, 799-805.
35. Lowe,T.M. and Eddy,S.R. (1999) A computational screen for methylation guide snoRNAs in yeast. Science, 283, 1168-1171.
36. Nierhaus,K.H. and Montejo,V. (1973) A protein involved in the peptidyltransferase activity of Escherichia coli ribosomes. Proc. Natl Acad. Sci. USA, 70, 1931-1935.
37. Sperling,E., Bunner,A.E., Sykes,M.T. and Williamson,J.R. (2008) Quantitative analysis of isotope distributions in proteomic mass spectrometry using least-squares Fourier transform convolution. Anal. Chem., 80, 4906-4917.
38. Fuller-Pace,F.V., Nicol,S.M., Reid,A.D. and Lane,D.P. (1993) DbpA: A DEAD box protein specifically activated by 23s rRNA. EMBO J., 12, 3619-3626.
39. Peil,L., Virumae,K. and Remme,J. (2008) Ribosome assembly in Escherichia coli strains lacking the RNA helicase DeaD/CsdA or DbpA. FEBS J., 275, 3772-3782.
40. 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.
41. Srivastava,A.K. and Schlessinger,D. (1988) Coregulation of processing and translation: Mature 50 termini of Escherichia coli 23S ribosomal RNA form in polysomes. Proc. Natl Acad. Sci. USA, 85 7144-7148.
42. 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.
43. 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.
44. Sirdeshmukh,R. and Schlessinger,D. (1985) Why is processing of 23 S ribosomal RNA in Escherichia coli not obligate for its function? J. Mol. Biol., 186, 669-672.
45. Srivastava,A.K. and Schlessinger,D. (1990) Mechanism and regulation of bacterial ribosomal RNA processing. Ann. Rev. Microbio., 44, 105-129.
46. Ofengand,J. and del Campo,M. (2004) In Björk,G.R. (ed.), EcoSal - Escherichia coli and Salmonella: Cellular and Molecuclar Biology. ASM Press, Washington, DC.
47. Bakin,A. and Ofengand,J. (1993) Four newly located pseudouridylate residues in Escherichia coli 23S ribosomal RNA are all at the peptidyltransferase center: Analysis by the application of a new sequencing technique. Biochemistry, 32, 9754-9762.
48. Bügl,H., Fauman,E.B., Staker,B.L., Zheng,F., Kushner,S.R., Saper,M.A., Bardwell,J.C.A. and Jakob,U. (2000) RNA methylation under heat shock control. Mol. Cell, 6, 349-360.
49. 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.
50. Roth,H.E. and Nierhaus,K.H. (1980) Assembly map of the 50-S subunit from Escherichia coli ribosomes, covering the proteins present in the first reconstitution intermediate particle. Eur. J. Biochem., 103, 95-98.
51. Bharat,A., Jiang,M., Sullivan,S.M., Maddock,J.R. and Brown,E.D. (2006) Cooperative and critical roles for both G domains in the GTPase activity and cellular function of ribosome-associated Escherichia coli EngA. J. Bacteriol., 188, 7992-7996.
52. Sato,A., Kobayashi,G., Hayashi,H., Yoshida,H., Wada,A., Maeda,M., Hiraga,S., Takeyasu,K. and Wada,C. (2005) The GTP binding protein Obg homolog ObgE is involved in ribosome maturation. Genes Cells, 10, 393-408.
53. Caldas,T., Binet,E., Bouloc,P. and Richarme,G. (2000) Translational defects of Escherichia coli mutants deficient in the Um2552 23S ribosomal RNA methyltransferase RrmJ/FTSJ. Biochem. Biophys. Res. Commun., 271, 714-718.
54. Silverman,E., Edwalds-Gilbert,G. and Lin,R.-J. (2003) DExD/H-box proteins and their partners: Helping RNA helicases unwind. Gene, 312, 1-16.
55. Yang,Q., Del Campo,M., Lambowitz,A.M. and Jankowsky,E. (2007) DEAD-box proteins unwind duplexes by local strand separation. Mol. Cell, 28, 253-263.
56. Cordin,O., Banroques,J., Tanner,N.K. and Linder,P. (2006) The DEAD-box protein family of RNA helicases. Gene, 367, 17-37.
57. Jain,C. (2008) The E. coli RhlE RNA helicase regulates the function of related RNA helicases during ribosome assembly. RNA, 14, 381-389.
58. Nishimura,M., Yoshida,T., Shirouzu,M., Terada,T., Kuramitsu,S., Yokoyama,S., Ohkubo,T. and Kobayashi,Y. (2004) Solution structure of ribosomal protein L16 from Thermus thermophilus HB8. J. Mol. Biol. 344, 1369-1383.
59. Polach,K.J. and Uhlenbeck,O.C. (2002) Cooperative binding of ATP and RNA substrates to the DEAD/H Protein DbpA. Biochemistry, 41, 3693-3702.
60. Caldas,T., Binet,E., Bouloc,P., Costa,A., Desgres,J. and Richarme,G. (2000) The FtsJ/RrmJ heat shock protein of Escherichia coli is a 23S ribosomal RNA methyltransferase. J. Biol. Chem., 275, 16414-16419.