Molecular insights into replication initiation by Qβ replicase using ribosomal protein S1

Nucleic Acids Research

Volumn 42, Issue 16, 2014, Pages 10809-10822

  Takeshita, Daijiro ^a   Yamashita, Seisuke ^a   Tomita, Kozo ^a  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR TS; ELONGATION FACTOR TU; Q BETA REPLICASE; RIBOSOMAL PROTEIN S1; RIBOSOME PROTEIN; RNA POLYMERASE BETA SUBUNIT; UNCLASSIFIED DRUG; ESCHERICHIA COLI PROTEIN; PROTEIN BINDING; PROTEIN SUBUNIT; QBETA RIBONUCLEIC ACID; RIBOSOMAL PROTEIN S1, E COLI; VIRUS RNA;

ARTICLE; CRYSTAL STRUCTURE; ESCHERICHIA COLI; IN VITRO STUDY; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SYNTHESIS; RNA BINDING; RNA REPLICATION; STRUCTURE ANALYSIS; VIRUS REPLICATION; BINDING SITE; BIOSYNTHESIS; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN SUBUNIT;

ESCHERICHIA COLI;

BINDING SITES; ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN SUBUNITS; Q BETA REPLICASE; RIBOSOMAL PROTEINS; RNA, VIRAL;

EID: 84908332956     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku745     Document Type: Article

References (54)

1. Subramanian,A.R. (1983) Structure and functions of ribosomal protein S1. Prog. Nucleic Acid Res. Mol. Biol. 28, 102-138.
2. Farwell,M.A., Robert,M.W. and Rabinowitz,J.C. (1992) The effect of ribosomal protein S1 from Escherichia coli and Micrococcus luteus on protein synthesis in vitro by E. coli and Bacillus subtilis. Mol. Microbiol. 6, 3375-3383.
3. Boni,I.V., Isaeva,D.M., Musychenko,M.L. and Tzareva,N.V. (1991) Ribosome-messenger recognition: mRNA target sites for ribosomal protein S1. Nucleic Acids Res. 19, 155-162.
4. Tedin,K., Resch,A. and Blasi,U. (1997) Requirements for ribosomal protein S1 for translation initiation of mRNAs with and without a 5′ leader sequence. Mol. Microbiol. 25, 189-199.
5. Sorensen,M.A., Fricke,J. and Pedersen,S. (1998) Ribosomal protein S1 is required for translation of most, if not all, natural mRNAs in Escherichia coli in vivo. J. Mol. Biol. 280, 561-569.
6. Komarova,A.V., Tchufistova,L.S., Supina,E.V. and Boni,I.V. (2002) Protein S1 counteracts the inhibitory effect of the extended Shine-Dalgarno sequence on translation. RNA 8, 1137-1147.
7. Duval,M., Korepanov,A., Fuchsbauer,O., Fechter,P., Haller,A., Fabbretti,A., Choulier,L., Micura,R., Klaholz,B.P., Romby,P. et al. (2013) Escherichia coli ribosomal protein S1 unfolds structured mRNAs onto the ribosome for active translation initiation. PLoS Biol. 11, e1001731.
8. Hajnsdorf,E. and Boni,I.V. (2012) Multiple activities of RNA-binding protein S1 and Hfq. Biochimie 94, 1544-1553.
9. Wahba,A.J., Miller,M.J., Niveleau,A., Landers,T.A., Carmichael,G.G., Weber,K., Hawley,D.A. and Slobin,L.I. (1974) Subunit I of Q beta replicase and 30 S ribosomal protein S1 of Escherichia coli. Evidence for the identity of the two proteins. J. Biol. Chem. 249, 3314-3316.
10. Blumenthal,T. and Carmichael,G.G. (1979) RNA replication: function and structure of Qbeta-replicase. Annu. Rev. Biochem. 48, 525-548.
11. Kondo,M., Gallerani,R. and Weissmann,C. (1970) Subunit structure of Q-beta replicase. Nature 228, 525-527.
12. Blumenthal,T., Landers,T.A. and Weber,K. (1972) Bacteriophage Q replicase contains the protein biosynthesis elongation factors EF Tu and EF Ts. Proc. Natl Acad. Sci. U.S.A. 69, 1313-1317.
13. Kidmose,R.T., Vasiliev,N.N., Chetverin,A.B., Andersen,G.R. and Knudsen,C.R. (2010) Structure of the Qbeta replicase, an RNA-dependent RNA polymerase consisting of viral and host proteins. Proc. Natl Acad. Sci. U.S.A. 107, 10884-10889.
14. Takeshita,D. and Tomita,K. (2010) Assembly of Qβ viral RNA polymerase with host translational elongation factors EF-Tu and-Ts. Proc. Natl Acad. Sci. U.S.A. 107, 15733-15738.
15. Takeshita,D. and Tomita,K. (2012) Molecular basis for RNA polymerization by Qβ replicase. Nat. Struct. Mol. Biol. 19, 229-237.
16. Takeshita,D., Yamashita,S. and Tomita,K. (2012) Mechanism for template-independent terminal adenylation activity of Qβ replicase. Structure 20, 1661-1669.
17. Salah,P., Bisaglia,M., Aliprandi,P., Uzan,M., Sizun,C. and Bontems,F. (2009) Probing the relationship between Gram-negative and Gram-positive S1 proteins by sequence analysis. Nucleic Acids Res. 37, 5578-5588.
18. Klovins,J., Berzins,V. and van Duin,J. (1998) A long-range interaction in Qβ RNA that bridges the thousand nucleotides between the M-site and the 3′ end is required for replication. RNA 4, 948-957.
19. Klovins,J. and van Duin,J. (1999) A long-range pseudoknot in Qβ RNA is essential for replication. J. Mol. Biol. 294, 875-884.
20. Milojevic,T., Sonnleitner,E., Romeo,A., Djinovic-Carugo,K. and Blasi,U. (2013) False positive RNA binding activities after Ni-affinity purification from Escherichia coli. RNA Biol. 10, 1066-1069.
21. McGinness,K.E. and Sauer,R.T. (2004) Ribosomal protein S1 binds mRNA and tmRNA similarly but play distinct roles in translation of these molecules. Proc. Natl Acad. Sci. U.S.A. 101, 13454-13459.
22. Otwinowski,Z. and Minor,W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326.
23. McCoy,A.J., Grosse-Kunstleve,R.W., Adams,P.D., Winn,M.D., Storoni,L.C. and Read,R.J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674.
24. Emsley,P. and Cowtan,K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132.
25. Adams,P.D., Grosse-Kunstleve,R.W., Hung,L.W., Ioerger,T.R., McCoy,A.J., Moriarty,N.W., Read,R.J., Sacchettini,J.C., Sauter,N.K. and Terwilliger,T.C. (2002). PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. D Biol. Crystallogr. 58, 1948-1954.
26. Murshudov,G.N., Skubák,P., Lebedev,A.A., Pannu,N.S., Steiner,R.A., Nicholls,R.A., Winn,M.D., Long,F. and Vagin,A.A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367.
27. Blanc,E., Roversi,P., Vonrhein,C., Flensburg,C., Lea,S.M. and Bricogne,G. (2004) Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr. D Biol. Crystallogr. 60, 2210-2221.
28. Krissinel,E. and Henrick,K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797.
29. Blumenthal,T. and Landers,T.A. (1973) The inhibition of nucleic acid-binding proteins by aurintricarboxylic acid. Biochem. Biophys. Res. Commun. 55, 680-688.
30. Zamora,H., Luce,R. and Biebricher,C.K. (1995) Design of artificial short-chained RNA species that are replicated by Q beta replicase. Biochemistry 34, 1261-1266.
31. Tomita,K., Fukai,S., Ishitani,R., Ueda,T., Takeuchi,N., Vassylyev,D.G. and Nureki,O. (2004) Structural basis for template-independent RNA polymerization. Nature 430, 700-704.
32. Yamashita,S., Takeshita,D. and Tomita,K. (2014) Translocation and rotation of tRNA during template-independent RNA polymerization by tRNA nucleotidyltransferase. Structure 22, 315-325.
33. Bycroft,M., Hubbard,T.J., Proctor,M., Freund,S.M. and Murzin,A.G. (1997) The solution structure of the S1 RNA binding domain: a member of an ancient nucleic acid-binding fold. Cell 88, 235-242.
34. Guerrier-Takada,C., Subramanian,A.R. and Cole,P.E. (1983) The activity of discrete fragments of ribosomal protein S1 in Q beta replicase function. J. Biol. Chem. 258, 13649-13652.
35. Sillers,I.Y. and Moore,P.B. (1981) Position of protein S1 in the 30 S ribosomal subunit of Escherichia coli. J. Mol. Biol. 153, 761-780.
36. Odom,O.W., Deng,H.Y., Subramanian,A.R. and Hardesty,B. (1984) Relaxation time, interthiol distance, and mechanism of action of ribosomal protein S1. Arch. Biochem. Biophys. 230, 178-193.
37. Walleczek,J., Albrecht-Ehrlich,R., St öffler,G. and Stöffler-Meilicke,M. (1990) Three-dimensional localization of the NH2-and carboxyl-terminal domain of ribosomal protein S1 on the surface of the 30 S subunit from Escherichia coli. J. Biol. Chem. 265, 11338-11344.
38. Meyer,F., Weber,H. and Weissmann,C. (1981) Interactions of Q beta replicase with Q beta RNA. J. Mol. Biol. 153, 631-660.
39. Barrera,I., Schuppli,D., Sogo,J.M. and Weber,H. (1993) Different mechanisms of recognition of bacteriophage Q beta plus and minus strand RNAs by Q beta replicase. J. Mol. Biol. 232, 512-521.
40. Miranda,G., Schuppli,D., Barrera,I., Hausherr,C., Sogo,J.M. and Weber,H. (1997) Recognition of bacteriophage Qbeta plus strand RNA as a template by Qbeta replicase: role of RNA interactions mediated by ribosomal proteins S1 and host factor. J. Mol. Biol. 267, 1089-1103.
41. Schuppli,D., Miranda,G., Qiu,S. and Weber,H. (1998) A branched stem-loop structure in the M-site of bacteriophage Qβ RNA is important for template recognition by Qβ replicase holoenzyme. J. Mol. Biol. 283, 585-593.
42. Frazão,C., McVey,C.E., Amblar,M., Barbas,A., Vonrhein,C., Arraiano,C.M. and Carrondo,M.A. (2006) Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex. Nature 443, 110-114.
43. Vasilyev,N.N., Kutlubaeva,Z.S., Ugarov,V.I., Chetverina,H.V. and Chetverin,A.B. (2013) Ribosomal protein S1 functions as a termination factor in RNA synthesis by Qβ phage replicase. Nat. Commun. 4, doi:10.1038/ncomms2807.
44. Kolb,A., Hermoso,J.M., Thomas,J.O. and Szer,W. (1977) Nucleic acid helix-unwinding properties of ribosomal protein S1 and the role of S1 in mRNA binding to ribosomes. Proc. Natl Acad. Sci. U.S.A. 74, 2379-2383.
45. Bear,D.G., Ng,R., Van Derveer,D., Johnson,N.P., Thomas,G., Schleich,T. and Noller,H.F. (1976) Alteration of polynucleotide secondary structure by ribosomal protein S1. Proc. Natl Acad. Sci. U.S.A. 73, 1824-1828.
46. Studer,S.M. and Joseph,S. (2006) Unfolding of mRNA secondary structure by the bacterial translation initiation complex. Mol. Cell 22, 105-215.
47. Qu,X., Lancaster,L., Noller,H.F., Bustamante,C. and Tinoco,I. Jr (2012) Ribosomal protein S1 unwinds double-stranded RNA in multiple steps. Proc. Natl Acad. Sci. U.S.A. 109, 14458-14463.
48. Skouv,J., Schnier,J., Rasmussen,M.D., Subramanian,A.R. and Pedersen,S. (1990) Ribosomal protein S1 of Escherichia coli is the effector for the regulation of its own synthesis. J. Biol. Chem. 265, 17044-17049.
49. Boni,I.V., Artamonova,V.S. and Dreyfus,M. (2000) The last RNA-binding repeat of the Escherichia coli ribosomal protein S1 is specifically involved in autogenous control. J. Bacteriol. 182, 5872-5879.
50. Sukhodolets,M.V. and Garges,S. (2003) Interaction of Escherichia coli RNA polymerase with the ribosomal protein S1 and the Sm-like ATPase Hfq. Biochemistry 42, 8022-8034.
51. Sukhodolets,M.V., Garges,S. and Adhya,S. (2006) Ribosomal protein S1 promotes transcriptional cycling. RNA 12, 1505-1513.
52. Wower,I.K., Zwieb,C.W., Guven,S.A. and Wower,J. (2000) Binding and cross-linking of tmRNA to ribosomal protein S1, on and off the Escherichia coli ribosome. EMBO J. 19, 6612-6621.
53. Karzai,A.W. and Sauer,R.T. (2001) Protein factors associated with the SsrA SmpB tagging and ribosome rescue complex. Proc. Natl Acad. Sci. U.S.A. 98, 3040-3044.
54. Weiner,A.M. and Maizels,N. (1987) tRNA-like structures tag the 3 ends of genomic RNA molecules for replication: Implications for the origin of protein synthesis. Proc. Natl Acad. Sci. U.S.A. 84, 7383-7387.