The role of SmpB and the ribosomal decoding center in licensing tmRNA entry into stalled ribosomes

RNA

Volumn 17, Issue 9, 2011, Pages 1727-1736

  Miller, Mickey R ^a   Liu, Zhu ^a   Cazier, Deanna J ^a   Gebhard, Grant M ^a   Herron, Steven R ^a   Zaher, Hani S ^b   Green, Rachel ^b   Buskirk, Allen R ^a  

^a Brigham Young University   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Decoding; EF Tu; Ribosome; SmpB; tmRNA

Indexed keywords

CELL PROTEIN; PEPTIDYLTRANSFERASE; SMPB PROTEIN; TRANSFER MESSENGER RNA; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ACTIVATION; MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; RIBOSOME; RNA STRUCTURE; RNA TRANSLATION; RNA TRANSPORT; TRANSLATION INITIATION;

AMINO ACID SEQUENCE; ANTICODON; CIRCULAR DICHROISM; CODON; ESCHERICHIA COLI; IMMUNOBLOTTING; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PEPTIDE ELONGATION FACTOR G; PEPTIDE ELONGATION FACTOR TU; RIBOSOMES; RNA, BACTERIAL; RNA, MESSENGER; RNA, TRANSFER; RNA-BINDING PROTEINS; TRANSFER RNA AMINOACYLATION;

EID: 84860389001     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.2821711     Document Type: Article

References (42)

1. Andersen E.S., Rosenblad M.A., Larsen N., Westergaard J.C., Burks J., Wower I.K., Wower J., Gorodkin J., Samuelsson T., Zwieb C. 2006. The tmRDB and SRPDB resources. Nucleic Acids Res 34: D163-D168.
2. Bessho Y., Shibata R., Sekine S., Murayama K., Higashijima K, Hori- Takemoto C, Shirouzu M, Kuramitsu S, Yokoyama S 2007. Structural basis for functional mimicry of long-variable-arm tRNA by transfer-messenger RNA. Proc Natl Acad Sci 104: 8293-8298. (Pubitemid 47175481)
3. Brunelle J.L., Youngman E.M., Sharma D., Green R. 2006. The interaction between C75 of tRNA and the A loop of the ribosome stimulates peptidyl transferase activity. RNA 12: 33-39. (Pubitemid 43037451)
4. Chadani Y., Ono K., Ozawa S., Takahashi Y., Takai K., Nanamiya H., Tozawa Y., Kutsukake K., Abo T. 2010. Ribosome rescue by Escherichia coli ArfA (YhdL) in the absence of trans-translation system. Mol Microbiol 78: 796-808.
5. Cochella L., Green R. 2005. An active role for tRNA in decoding beyond codon: Anticodon pairing. Science 308: 1178-1180. (Pubitemid 40696436)
6. Cochella L., Brunelle J.L., Green R. 2007. Mutational analysis reveals two independent molecular requirements during transfer RNA selection on the ribosome. Nat Struct Mol Biol 14: 30-36. (Pubitemid 46067420)
7. Cole C., Barber J.D., Barton G.J. 2008. The Jpred 3 secondary structure prediction server. Nucleic Acids Res 36: W197-W201.
8. Crooks G.E., Hon G., Chandonia J.M., Brenner S.E. 2004. WebLogo: A sequence logo generator. Genome Res 14: 1188-1190. (Pubitemid 38811555)
9. Daviter T., Gromadski K.B., Rodnina M.V. 2006. The ribosome's response to codon-anticodon mismatches. Biochimie 88: 1001-1011.
10. Fu J., Hashem Y., Wower I., Lei J., Liao H.Y., Zwieb C., Wower J., Frank J. 2010. Visualizing the transfer-messenger RNA as the ribosome resumes translation. EMBO J 29: 3819-3825.
11. Gromadski K.B., Rodnina M.V. 2004. Kinetic determinants of highfidelity tRNA discrimination on the ribosome. Mol Cell 13: 191-200. (Pubitemid 38183266)
12. Hallier M., Ivanova N., Rametti A., Pavlov M., Ehrenberg M., Felden B. 2004. Pre-binding of small protein B to a stalled ribosome triggers trans-translation. J Biol Chem 279: 25978-25985. (Pubitemid 38798739)
13. Hayes C.S., Bose B., Sauer R.T. 2002a. Proline residues at the C terminus of nascent chains induce SsrA tagging during translation termination. J Biol Chem 277: 33825-33832.
14. Hayes C.S., Bose B., Sauer R.T. 2002b. Stop codons preceded by rare arginine codons are efficient determinants of SsrA tagging in Escherichia coli. Proc Natl Acad Sci 99: 3440-3445. (Pubitemid 34252127)
15. Holberger L.E., Hayes C.S. 2009. Ribosomal protein S12 and aminoglycoside antibiotics modulate A-site mRNA cleavage and transfer-messenger RNA activity in Escherichia coli. J Biol Chem284: 32188-32200.
16. Ivanova N., Pavlov M.Y., Felden B., Ehrenberg M. 2004. Ribosome rescue by tmRNA requires truncated mRNAs. J Mol Biol 338: 33-41. (Pubitemid 38429784)
17. Jacob Y., Sharkady S.M., Bhardwaj K., Sanda A., Williams K.P. 2005. Function of the SmpB tail in transfer-messenger RNA translation revealed by a nucleus-encoded form. J Biol Chem 280: 5503-5509. (Pubitemid 40280027)
18. Kaur S., Gillet R., Li W., Gursky R., Frank J. 2006. Cryo-EM visualization of transfer messenger RNA with two SmpBs in a stalled ribosome. Proc Natl Acad Sci 103: 16484-16489. (Pubitemid 44715222)
19. Kurita D., Sasaki R., Muto A., Himeno H. 2007. Interaction of SmpB with ribosome from directed hydroxyl radical probing. Nucleic Acids Res 35: 7248-7255.
20. Kurita D., Muto A., Himeno H. 2010. Role of the C-terminal tail of SmpB in the early stage of trans-translation. RNA 16: 980-990.
21. Luo P., Baldwin R.L. 1997. Mechanism of helix induction by trifluoroethanol: A framework for extrapolating the helix-forming properties of peptides from trifluoroethanol/water mixtures back to water. Biochemistry 36: 8413-8421. (Pubitemid 27297553)
22. Moazed D., Noller H.F. 1991. Sites of interaction of the CCA end of peptidyl-tRNA with 23S rRNA. Proc Natl Acad Sci 88: 3725-3728. (Pubitemid 21916696)
23. Moore S.D., Sauer R.T. 2007. The tmRNA system for translational surveillance and ribosome rescue. Annu Rev Biochem 76: 101-124.
24. Nonin-Lecomte S., Germain-Amiot N., Gillet R., Hallier M., Ponchon L., Dardel F., Felden B. 2009. Ribosome hijacking: A role for small protein B during trans-translation. EMBO Rep 10: 160-165.
25. Ogle J.M., Ramakrishnan V. 2005. Structural insights into translational fidelity. Annu Rev Biochem 74: 129-177. (Pubitemid 40995504)
26. Ogle J.M., Brodersen D.E., Clemons W.M. Jr, Tarry M.J., Carter A.P., Ramakrishnan V. 2001. Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 292: 897-902. (Pubitemid 32422480)
27. Ogle J.M., Murphy F.V., Tarry M.J., Ramakrishnan V. 2002. Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell 111: 721-732. (Pubitemid 35446316)
28. Pape T., Wintermeyer W., Rodnina M. 1999. Induced fit in initial selection and proofreading of aminoacyl-tRNA on the ribosome. EMBO J 18: 3800-3807. (Pubitemid 29308859)
29. Powers T., Noller H.F. 1990. Dominant lethal mutations in a conserved loop in 16S rRNA. Proc Natl Acad Sci 87: 1042-1046.
30. Roche E.D., Sauer R.T. 2001. Identification of endogenous SsrA-tagged proteins reveals tagging at positions corresponding to stop codons. J Biol Chem 276: 28509-28515.
31. Schmeing T.M., Voorhees R.M., Kelley A.C., Gao Y.G., Murphy F.V. IV, Weir J.R., Ramakrishnan V. 2009. The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA. Science 326: 688-694.
32. Selmer M., Dunham C.M., Murphy F.V. IV, Weixlbaumer A., Petry S., Kelley A.C., Weir J.R., Ramakrishnan V. 2006. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313: 1935-1942. (Pubitemid 44497996)
33. Shimizu Y., Ueda T. 2006. SmpB triggers GTP hydrolysis of elongation factor Tu on ribosomes by compensating for the lack of codonanticodon interaction during trans-translation initiation. J Biol Chem 281: 15987-15996. (Pubitemid 43848492)
34. Shimizu Y., Inoue A., Tomari Y., Suzuki T., Yokogawa T., Nishikawa K., Ueda T. 2001. Cell-free translation reconstituted with purified components. Nat Biotechnol 19: 751-755. (Pubitemid 32729537)
35. Stark H., Rodnina M.V., Wieden H.J., Zemlin F., Wintermeyer W., Van Heel M. 2002. Ribosome interactions of aminoacyl-tRNA and elongation factor Tu in the codon-recognition complex. Nat Struct Biol 9: 849-854. (Pubitemid 35257786)
36. Sundermeier T.R., Dulebohn D.P., Cho H.J., Karzai A.W. 2005. A previously uncharacterized role for small protein B (SmpB) in transfer messenger RNA-mediated trans-translation. Proc Natl Acad Sci 102: 2316-2321. (Pubitemid 40279373)
37. Tanner D.R., Cariello D.A., Woolstenhulme C.J., Broadbent M.A., Buskirk A.R. 2009. Genetic identification of nascent peptides that induce ribosome stalling. J Biol Chem 284: 34809-34818.
38. Valle M., Zavialov A., Li W., Stagg S.M., Sengupta J., Nielsen R.C., Nissen P., Harvey S.C., Ehrenberg M., Frank J. 2003. Incorporation of aminoacyl-tRNA into the ribosome as seen by cryo-electron microscopy. Nat Struct Biol 10: 899-906. (Pubitemid 37386098)
39. Watts T., Cazier D., Healey D., Buskirk A. 2009. SmpB contributes to reading frame selection in the translation of transfer-messenger RNA. J Mol Biol 391: 275-281.
40. Weis F., Bron P., Giudice E., Rolland J.P., Thomas D., Felden B., Gillet R. 2010. tmRNA-SmpB: A journey to the centre of the bacterial ribosome. EMBO J 29: 3810-3818.
41. Youngman E.M., Green R. 2005. Affinity purification of in vivo-assembled ribosomes for in vitro biochemical analysis. Methods 36: 305-312. (Pubitemid 41074962)
42. Youngman E.M., Brunelle J.L., Kochaniak A.B., Green R. 2004. The active site of the ribosome is composed of two layers of conserved nucleotides with distinct roles in peptide bond formation and peptide release. Cell 117: 589-599. (Pubitemid 38692525)