Molecular Insights into Replication Initiation by Qβ Replicase Using Ribosomal Protein S1

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2014 Aug 15

PMID 25122749

Citations 31

Authors

Daijiro Takeshita

Seisuke Yamashita

Kozo Tomita

Affiliations

Soon will be listed here.

Abstract

Ribosomal protein S1, consisting of six contiguous OB-folds, is the largest ribosomal protein and is essential for translation initiation in Escherichia coli. S1 is also one of the three essential host-derived subunits of Qβ replicase, together with EF-Tu and EF-Ts, for Qβ RNA replication in E. coli. We analyzed the crystal structure of Qβ replicase, consisting of the virus-encoded RNA-dependent RNA polymerase (β-subunit), EF-Tu, EF-Ts and the N-terminal half of S1, which is capable of initiating Qβ RNA replication. Structural and biochemical studies revealed that the two N-terminal OB-folds of S1 anchor S1 onto the β-subunit, and the third OB-fold is mobile and protrudes beyond the surface of the β-subunit. The third OB-fold mainly interacts with a specific RNA fragment derived from the internal region of Qβ RNA, and its RNA-binding ability is required for replication initiation of Qβ RNA. Thus, the third mobile OB-fold of S1, which is spatially anchored near the surface of the β-subunit, primarily recruits the Qβ RNA toward the β-subunit, leading to the specific and efficient replication initiation of Qβ RNA, and S1 functions as a replication initiation factor, beyond its established function in protein synthesis.

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References

Salah P, Bisaglia M, Aliprandi P, Uzan M, Sizun C, Bontems F . Probing the relationship between Gram-negative and Gram-positive S1 proteins by sequence analysis. Nucleic Acids Res. 2009; 37(16):5578-88. PMC: 2760812. DOI: 10.1093/nar/gkp547. View

Klovins J, Berzins V, van Duin J . A long-range interaction in Qbeta RNA that bridges the thousand nucleotides between the M-site and the 3' end is required for replication. RNA. 1998; 4(8):948-57. PMC: 1369672. DOI: 10.1017/s1355838298980177. View

Wower I, Zwieb C, Guven S, Wower J . Binding and cross-linking of tmRNA to ribosomal protein S1, on and off the Escherichia coli ribosome. EMBO J. 2000; 19(23):6612-21. PMC: 305868. DOI: 10.1093/emboj/19.23.6612. View

Bear D, Ng R, Van Derveer D, Johnson N, Thomas G, SCHLEICH T . Alteration of polynucleotide secondary structure by ribosomal protein S1. Proc Natl Acad Sci U S A. 1976; 73(6):1824-8. PMC: 430399. DOI: 10.1073/pnas.73.6.1824. View

Yamashita S, Takeshita D, Tomita K . Translocation and rotation of tRNA during template-independent RNA polymerization by tRNA nucleotidyltransferase. Structure. 2014; 22(2):315-25. DOI: 10.1016/j.str.2013.12.002. View

Krissinel E, Henrick K . Inference of macromolecular assemblies from crystalline state. J Mol Biol. 2007; 372(3):774-97. DOI: 10.1016/j.jmb.2007.05.022. View

Adams P, Grosse-Kunstleve R, Hung L, Ioerger T, McCoy A, Moriarty N . PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr. 2002; 58(Pt 11):1948-54. DOI: 10.1107/s0907444902016657. View

Subramanian A . Structure and functions of ribosomal protein S1. Prog Nucleic Acid Res Mol Biol. 1983; 28:101-42. DOI: 10.1016/s0079-6603(08)60085-9. View

Hajnsdorf E, Boni I . Multiple activities of RNA-binding proteins S1 and Hfq. Biochimie. 2012; 94(7):1544-53. DOI: 10.1016/j.biochi.2012.02.010. View

10.

Takeshita D, Yamashita S, Tomita K . Mechanism for template-independent terminal adenylation activity of Qβ replicase. Structure. 2012; 20(10):1661-9. DOI: 10.1016/j.str.2012.07.004. View

11.

Sukhodolets M, Garges S . Interaction of Escherichia coli RNA polymerase with the ribosomal protein S1 and the Sm-like ATPase Hfq. Biochemistry. 2003; 42(26):8022-34. DOI: 10.1021/bi020638i. View

12.

McCoy A, Grosse-Kunstleve R, Adams P, Winn M, Storoni L, Read R . Phaser crystallographic software. J Appl Crystallogr. 2009; 40(Pt 4):658-674. PMC: 2483472. DOI: 10.1107/S0021889807021206. View

13.

Frazao C, McVey C, Amblar M, Barbas A, Vonrhein C, Arraiano C . Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex. Nature. 2006; 443(7107):110-4. DOI: 10.1038/nature05080. View

14.

Sorensen M, Fricke J, Pedersen S . Ribosomal protein S1 is required for translation of most, if not all, natural mRNAs in Escherichia coli in vivo. J Mol Biol. 1998; 280(4):561-9. DOI: 10.1006/jmbi.1998.1909. View

15.

Bycroft M, Hubbard T, Proctor M, Freund S, Murzin A . The solution structure of the S1 RNA binding domain: a member of an ancient nucleic acid-binding fold. Cell. 1997; 88(2):235-42. DOI: 10.1016/s0092-8674(00)81844-9. View

16.

Schuppli D, Miranda G, Qiu S, Weber H . A branched stem-loop structure in the M-site of bacteriophage Qbeta RNA is important for template recognition by Qbeta replicase holoenzyme. J Mol Biol. 1998; 283(3):585-93. DOI: 10.1006/jmbi.1998.2123. View

17.

Wahba A, Miller M, Niveleau A, Landers T, Carmichael G, Weber K . Subunit I of G beta replicase and 30 S ribosomal protein S1 of Escherichia coli. Evidence for the identity of the two proteins. J Biol Chem. 1974; 249(10):3314-6. View

18.

Sillers I, Moore P . Position of protein S1 in the 30 S ribosomal subunit of Escherichia coli. J Mol Biol. 1981; 153(3):761-80. DOI: 10.1016/0022-2836(81)90417-4. View

19.

Vasilyev N, Kutlubaeva Z, Ugarov V, Chetverina H, Chetverin A . Ribosomal protein S1 functions as a termination factor in RNA synthesis by Qβ phage replicase. Nat Commun. 2013; 4:1781. DOI: 10.1038/ncomms2807. View

20.

Murshudov G, Skubak P, Lebedev A, Pannu N, Steiner R, Nicholls R . REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr D Biol Crystallogr. 2011; 67(Pt 4):355-67. PMC: 3069751. DOI: 10.1107/S0907444911001314. View