Trans-translation exposed: Understanding the structures and functions of tmRNA-SmpB

Frontiers in Microbiology

Volumn 5, Issue MAR, 2014, Pages

  Giudice, Emmanuel ^a   Macé, Kevin ^a   Gillet, Reynald ^a,b  

^a UNIVERSITÉ DE RENNES 1   (France)

^b INSTITUT UNIVERSITAIRE DE FRANCE   (France)

Author keywords

Ribosome; SmpB; Structure; tmRNA; Trans translation

Indexed keywords

ELONGATION FACTOR TU; ENDONUCLEASE; EXORIBONUCLEASE; GUANOSINE TRIPHOSPHATE; MESSENGER RNA; RIBOSOME PROTEIN; RIBOSOME PROTEIN S1; RNA BINDING PROTEIN; SMALL PROTEIN B; TRANSFER MESSENGER RNA; UNCLASSIFIED DRUG;

BACTERIAL GENOME; CELL SURVIVAL; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; HYDROLYSIS; NONHUMAN; PROTEIN SYNTHESIS REGULATION; REVIEW; RNA PROCESSING; RNA TRANSLATION; RNA TRANSPORT; TRANS TRANSLATION;

EID: 84897941600     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2014.00113     Document Type: Review

References (80)

1. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., and McCammon, J. A. (2001). Electrostatics of nanosystems: application to microtubules and the ribosome. Proc. Natl. Acad. Sci. U.S.A. 98, 10037-10041. doi: 10.1073/pnas.181342398.
2. Barends, S., Bjork, K., Gultyaev, A. P., de Smit, M. H., Pleij, C. W., and Kraal, B. (2002). Functional evidence for D- and T-loop interactions in tmRNA. FEBS Lett. 514, 78-83. doi: 10.1016/S0014-5793(02)02306-2.
3. Bessho, Y., Shibata, R., Sekine, S., Murayama, K., Higashijima, K., Hori-Takemoto, C., et al. (2007). Structural basis for functional mimicry of long-variable-arm tRNA by transfer-messenger RNA. Proc. Natl. Acad. Sci. U.S.A. 104, 8293-8298. doi: 10.1073/pnas.0700402104.
4. Bordeau, V., and Felden, B. (2002). Ribosomal protein S1 induces a conformational change of tmRNA; more than one protein S1 per molecule of tmRNA. Biochimie 84, 723-729. doi: 10.1016/S0300-9084(02)01442-6.
5. Bugaeva, E. Y., Surkov, S., Golovin, A. V., Ofverstedt, L. G., Skoglund, U., Isaksson, L. A., et al. (2009). Structural features of the tmRNA-ribosome interaction. RNA 15, 2312-2320. doi: 10.1261/rna.1584209.
6. 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. doi: 10.1016/S0092-8674(00)81844-9.
7. Cheng, K., Ivanova, N., Scheres, S. H., Pavlov, M. Y., Carazo, J. M., Hebert, H., et al. (2010). tmRNA.SmpB complex mimics native aminoacyl-tRNAs in the A site of stalled ribosomes. J. Struct. Biol. 169, 342-348. doi: 10.1016/j.jsb.2009.10.015.
8. Cheng, Z. F., and Deutscher, M. P. (2002). Purification and characterization of the Escherichia coli exoribonuclease RNase R. Comparison with RNase II. J. Biol. Chem. 277, 21624-21629. doi: 10.1074/jbc.M202942200.
9. Crandall, J., Rodriguez-Lopez, M., Pfeiffer, M., Mortensen, B., and Buskirk, A. (2010). rRNA mutations that inhibit transfer-messenger RNA activity on stalled ribosomes. J. Bacteriol. 192, 553-559. doi: 10.1128/JB.01178-09.
10. Dong, G., Nowakowski, J., and Hoffman, D. W. (2002). Structure of small protein B: the protein component of the tmRNA-SmpB system for ribosome rescue. EMBO J. 21, 1845-1854. doi: 10.1093/emboj/21.7.1845.
11. Felden, B., and Gillet, R. (2011). SmpB as the handyman of tmRNA during trans-translation. RNA Biol. 8, 440-449. doi: 10.4161/rna.8.3.15387.
12. Felden, B., Hanawa, K., Atkins, J. F., Himeno, H., Muto, A., Gesteland, R. F., et al. (1998). Presence and location of modified nucleotides in Escherichia coli tmRNA: structural mimicry with tRNA acceptor branches. EMBO J. 17, 3188-3196. doi: 10.1093/emboj/17.11.3188.
13. Frazao, C., McVey, C. E., Amblar, M., Barbas, A., Vonrhein, C., Arraiano, C. M., et al. (2006). Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex. Nature 443, 110-114. doi: 10.1038/nature05080.
14. Fu, J., Hashem, Y., Wower, I., Lei, J., Liao, H. Y., Zwieb, C., et al. (2010). Visualizing the transfer-messenger RNA as the ribosome resumes translation. EMBO J. 29, 3819-3825. doi: 10.1038/emboj.2010.255.
15. Gagnon, M. G., Seetharaman, S. V., Bulkley, D., and Steitz, T. A. (2012). Structural basis for the rescue of stalled ribosomes: structure of YaeJ bound to the ribosome. Science 335, 1370-1372. doi: 10.1126/science.1217443.
16. Gaudin, C., Zhou, X., Williams, K. P., and Felden, B. (2002). Two-piece tmRNA in cyanobacteria and its structural analysis. Nucleic Acids Res. 30, 2018-2024. doi: 10.1093/nar/30.9.2018.
17. Ge, Z., Mehta, P., Richards, J., and Karzai, A. W. (2010). Non-stop mRNA decay initiates at the ribosome. Mol. Microbiol. 78, 1159-1170. doi: 10.1111/j.1365-2958.2010.07396.x.
18. Gillet, R., Kaur, S., Li, W., Hallier, M., Felden, B., and Frank, J. (2007). Scaffolding as an organizing principle in trans-translation. The roles of small protein B and ribosomal protein S1. J. Biol. Chem. 282, 6356-6363. doi: 10.1074/jbc.M609658200.
19. Giudice, E., and Gillet, R. (2013). The task force that rescues stalled ribosomes in bacteria. Trends Biochem. Sci. 38, 403-411. doi: 10.1016/j.tibs.2013.06.002.
20. Gutmann, S., Haebel, P. W., Metzinger, L., Sutter, M., Felden, B., and Ban, N. (2003). Crystal structure of the transfer-RNA domain of transfer-messenger RNA in complex with SmpB. Nature 424, 699-703. doi: 10.1038/nature01831.
21. Hajnsdorf, E., and Boni, I. V. (2012). Multiple activities of RNA-binding proteins S1 and Hfq. Biochimie 94, 1544-1553. doi: 10.1016/j.biochi.2012.02.010.
22. Hong, S. J., Tran, Q. A., and Keiler, K. C. (2005). Cell cycle-regulated degradation of tmRNA is controlled by RNase R and SmpB. Mol. Microbiol. 57, 565-575. doi: 10.1111/j.1365-2958.2005.04709.x.
23. Hou, Y. M., and Schimmel, P. (1988). A simple structural feature is a major determinant of the identity of a transfer RNA. Nature 333, 140-145. doi: 10.1038/333140a0.
24. Jacob, Y., Sharkady, S. M., Bhardwaj, K., Sanda, A., and 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. doi: 10.1074/jbc.M409277200.
25. Janssen, B. D., and Hayes, C. S. (2012). The tmRNA ribosome-rescue system. Adv. Protein Chem. Struct. Biol. 86, 151-191. doi: 10.1016/B978-0-12-386497-0.00005-0.
26. Karzai, A. W., Roche, E. D., and Sauer, R. T. (2000). The SsrA-SmpB system for protein tagging, directed degradation and ribosome rescue. Nat. Struct. Biol. 7, 449-455. doi: 10.1038/75843.
27. Karzai, A. W., Susskind, M. M., and Sauer, R. T. (1999). SmpB, a unique RNA-binding protein essential for the peptide-tagging activity of SsrA (tmRNA). EMBO J. 18, 3793-3799. doi: 10.1093/emboj/18.13.3793.
28. Kaur, S., Gillet, R., Li, W., Gursky, R., and Frank, J. (2006). Cryo-EM visualization of transfer messenger RNA with two SmpBs in a stalled ribosome. Proc. Natl. Acad. Sci. U.S.A. 103, 16484-16489. doi: 10.1073/pnas.0607438103.
29. Kavaliauskas, D., Nissen, P., and Knudsen, C. R. (2012). The busiest of all ribosomal assistants: elongation factor Tu. Biochemistry 51, 2642-2651. doi: 10.1021/bi300077s.
30. Keiler, K. C., Shapiro, L., and Williams, K. P. (2000). tmRNAs that encode proteolysis-inducing tags are found in all known bacterial genomes: A two-piece tmRNA functions in Caulobacter. Proc. Natl. Acad. Sci. U.S.A. 97, 7778-7783. doi: 10.1073/pnas.97.14.7778.
31. Keiler, K. C., Waller, P. R., and Sauer, R. T. (1996). Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271, 990-993. doi: 10.1126/science.271.5251.990.
32. Komine, Y., Kitabatake, M., Yokogawa, T., Nishikawa, K., and Inokuchi, H. (1994). A tRNA-like structure is present in 10Sa RNA, a small stable RNA from Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 91, 9223-9227. doi: 10.1073/pnas.91.20.9223.
33. Kurita, D., Muto, A., and Himeno, H. (2010). Role of the C-terminal tail of SmpB in the early stage of trans-translation. RNA 16, 980-990. doi: 10.1261/rna.1916610.
34. Kurita, D., Sasaki, R., Muto, A., and Himeno, H. (2007). Interaction of SmpB with ribosome from directed hydroxyl radical probing. Nucleic Acids Res. 35, 7248-7255. doi: 10.1093/nar/gkm677.
35. Lee, S., Ishii, M., Tadaki, T., Muto, A., and Himeno, H. (2001). Determinants on tmRNA for initiating efficient and precise trans-translation: some mutations upstream of the tag-encoding sequence of Escherichia coli tmRNA shift the initiation point of trans-translation in vitro. RNA 7, 999-1012. doi: 10.1017/S1355838201010342.
36. Li, Z., Pandit, S., and Deutscher, M. P. (1998). 3' exoribonucleolytic trimming is a common feature of the maturation of small, stable RNAs in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 95, 2856-2861. doi: 10.1073/pnas.95.6.2856.
37. Liang, W., and Deutscher, M. P. (2012). Transfer-messenger RNA-SmpB protein regulates ribonuclease R turnover by promoting binding of HslUV and Lon proteases. J. Biol. Chem. 287, 33472-33479. doi: 10.1074/jbc.M112.375287.
38. Liang, W., and Deutscher, M. P. (2013). Ribosomes regulate the stability and action of the exoribonuclease RNase R. J. Biol. Chem. 288, 34791-34798. doi: 10.1074/jbc.M113.519553.
39. Lin-Chao, S., Wei, C. L., and Lin, Y. T. (1999). RNase E is required for the maturation of ssrA RNA and normal ssrA RNA peptide-tagging activity. Proc. Natl. Acad. Sci. U.S.A. 96, 12406-12411. doi: 10.1073/pnas.96.22.12406.
40. Matos, R. G., Barbas, A., Gomez-Puertas, P., and Arraiano, C. M. (2011). Swapping the domains of exoribonucleases RNase II and RNase R: conferring upon RNase II the ability to degrade ds RNA. Proteins 79, 1853-1867. doi: 10.1002/prot.23010.
41. Miller, M. R., and Buskirk, A. R. (2014). An unusual mechanism for EF-Tu activation during tmRNA-mediated ribosome rescue. RNA 20, 228-235. doi: 10.1261/rna.042226.113.
42. Miller, M. R., Healey, D. W., Robison, S. G., Dewey, J. D., and Buskirk, A. R. (2008). The role of upstream sequences in selecting the reading frame on tmRNA. BMC Biol. 6:29. doi: 10.1186/1741-7007-6-29.
43. Miller, M. R., Liu, Z., Cazier, D. J., Gebhard, G. M., Herron, S. R., Zaher, H. S., et al. (2011). The role of SmpB and the ribosomal decoding center in licensing tmRNA entry into stalled ribosomes. RNA 17, 1727-1736. doi: 10.1261/rna.2821711.
44. Moore, S. D., and Sauer, R. T. (2007). The tmRNA system for translational surveillance and ribosome rescue. Annu. Rev. Biochem. 76, 101-124. doi: 10.1146/annurev.biochem.75.103004.142733.
45. Moreira, R. N., Domingues, S., Viegas, S. C., Amblar, M., and Arraiano, C. M. (2012). Synergies between RNA degradation and trans-translation in Streptococcus pneumoniae: cross regulation and co-transcription of RNase R and SmpB. BMC Microbiol. 12:268. doi: 10.1186/1471-2180-12-268.
46. Nameki, N., Tadaki, T., Himeno, H., and Muto, A. (2000). Three of four pseudoknots in tmRNA are interchangeable and are substitutable with single-stranded RNAs. FEBS Lett. 470, 345-349. doi: 10.1016/S0014-5793(00)01349-1.
47. Neubauer, C., Gillet, R., Kelley, A. C., and Ramakrishnan, V. (2012). Decoding in the absence of a codon by tmRNA and SmpB in the ribosome. Science 335, 1366-1369. doi: 10.1126/science.1217039.
48. Nonin-Lecomte, S., Germain-Amiot, N., Gillet, R., Hallier, M., Ponchon, L., Dardel, F., et al. (2009). Ribosome hijacking: a role for small protein B during trans-translation. EMBO Rep. 10, 160-165. doi: 10.1038/embor.2008.243.
49. Ogle, J. M., Murphy, F. V., Tarry, M. J., and Ramakrishnan, V. (2002). Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell 111, 721-732. doi: 10.1016/S0092-8674(02)01086-3.
50. Oh, B. K., Chauhan, A. K., Isono, K., and Apirion, D. (1990). Location of a gene (ssrA) for a small, stable RNA (10Sa RNA) in the Escherichia coli chromosome. J. Bacteriol. 172, 4708-4709.
51. Pyrkov, T. V., Chugunov, A. O., Krylov, N. A., Nolde, D. E., and Efremov, R. G. (2009). PLATINUM: a web tool for analysis of hydrophobic/hydrophilic organization of biomolecular complexes. Bioinformatics 25, 1201-1202. doi: 10.1093/bioinformatics/btp111.
52. Ramadoss, N. S., Alumasa, J. N., Cheng, L., Wang, Y., Li, S., Chambers, B. S., et al. (2013). Small molecule inhibitors of trans-translation have broad-spectrum antibiotic activity. Proc. Natl. Acad. Sci. U.S.A. 110, 10282-10287. doi: 10.1073/pnas.1302816110.
53. Ramrath, D. J., Yamamoto, H., Rother, K., Wittek, D., Pech, M., Mielke, T., et al. (2012). The complex of tmRNA-SmpB and EF-G on translocating ribosomes. Nature 485, 526-529. doi: 10.1038/nature11006.
54. Ranaei-Siadat, E., Fabret, C., Seijo, B., Dardel, F., Grosjean, H., and Nonin-Lecomte, S. (2013). RNA-methyltransferase TrmA is a dual-specific enzyme responsible for C5-methylation of uridine in both tmRNA and tRNA. RNA Biol. 10, 572-578. doi: 10.4161/rna.24327.
55. Ray, B. K., and Apirion, D. (1979). Characterization of 10S RNA: a new stable rna molecule from Escherichia coli. Mol. Gen. Genet. 174, 25-32. doi: 10.1007/BF00433301.
56. Richards, J., Mehta, P., and Karzai, A. W. (2006). RNase R degrades non-stop mRNAs selectively in an SmpB-tmRNA-dependent manner. Mol. Microbiol. 62, 1700-1712. doi: 10.1111/j.1365-2958.2006.05472.x.
57. Saguy, M., Gillet, R., Metzinger, L., and Felden, B. (2005). tmRNA and associated ligands: a puzzling relationship. Biochimie 87, 897-903. doi: 10.1016/j.biochi.2005.03.014.
58. Schmeing, T. M., Voorhees, R. M., Kelley, A. C., Gao, Y. G., Murphy, F. V. T., Weir, J. R., et al. (2009). The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA. Science 326, 688-694. doi: 10.1126/science.1179700.
59. Sharkady, S. M., and Williams, K. P. (2004). A third lineage with two-piece tmRNA. Nucleic Acids Res. 32, 4531-4538. doi: 10.1093/nar/gkh795.
60. Shi, W., Zhang, X., Jiang, X., Yuan, H., Lee, J. S., Barry, C. E., et al. (2011). Pyrazinamide inhibits trans-translation in Mycobacterium tuberculosis. Science 333, 1630-1632. doi: 10.1126/science.1208813.
61. Shimizu, Y., and Ueda, T. (2006). SmpB triggers GTP hydrolysis of elongation factor Tu on ribosomes by compensating for the lack of codon-anticodon interaction during trans-translation initiation. J. Biol. Chem. 281, 15987-15996. doi: 10.1074/jbc.M512165200.
62. Shpanchenko, O. V., Zvereva, M. I., Ivanov, P. V., Bugaeva, E. Y., Rozov, A. S., Bogdanov, A. A., et al. (2005). Stepping transfer messenger RNA through the ribosome. J. Biol. Chem. 280, 18368-18374. doi: 10.1074/jbc.M409094200.
63. Someya, T., Nameki, N., Hosoi, H., Suzuki, S., Hatanaka, H., Fujii, M., et al. (2003). Solution structure of a tmRNA-binding protein, SmpB, from Thermus thermophilus. FEBS Lett. 535, 94-100. doi: 10.1016/S0014-5793(02)03880-2.
64. 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. doi: 10.1006/jmbi.1998.1909.
65. Stagg, S. M., Frazer-Abel, A. A., Hagerman, P. J., and Harvey, S. C. (2001). Structural studies of the tRNA domain of tmRNA. J. Mol. Biol. 309, 727-735. doi: 10.1006/jmbi.2001.4632.
66. Stepanov, V. G., and Nyborg, J. (2003). tmRNA from Thermus thermophilus. Interaction with alanyl-tRNA synthetase and elongation factor Tu. Eur. J. Biochem. 270, 463-475. doi: 10.1046/j.1432-1033.2003.03401.x.
67. Subramanian, A. R. (1983). Structure and functions of ribosomal protein S1. Prog. Nucleic Acid Res. Mol. Biol. 28, 101-142. doi: 10.1016/S0079-6603(08)60085-9.
68. Sundermeier, T. R., Dulebohn, D. P., Cho, H. J., and Karzai, A. W. (2005). A previously uncharacterized role for small protein B (SmpB) in transfer messenger RNA-mediated trans-translation. Proc. Natl. Acad. Sci. U.S.A. 102, 2316-2321. doi: 10.1073/pnas.0409694102.
69. Tanner, D. R., Dewey, J. D., Miller, M. R., and Buskirk, A. R. (2006). Genetic analysis of the structure and function of transfer messenger RNA pseudoknot 1. J. Biol. Chem. 281, 10561-10566. doi: 10.1074/jbc.M600167200.
70. Ushida, C., Himeno, H., Watanabe, T., and Muto, A. (1994). tRNA-like structures in 10Sa RNAs of Mycoplasma capricolum and Bacillus subtilis. Nucleic Acids Res. 22, 3392-3396. doi: 10.1093/nar/22.16.3392.
71. Valle, M., Gillet, R., Kaur, S., Henne, A., Ramakrishnan, V., and Frank, J. (2003). Visualizing tmRNA entry into a stalled ribosome. Science 300, 127-130. doi: 10.1126/science.1081798.
72. Watts, T., Cazier, D., Healey, D., and Buskirk, A. (2009). SmpB contributes to reading frame selection in the translation of transfer-messenger RNA. J. Mol. Biol. 391, 275-281. doi: 10.1016/j.jmb.2009.06.037.
73. Weis, F., Bron, P., Giudice, E., Rolland, J. P., Thomas, D., Felden, B., et al., (2010a) tmRNA-SmpB: a journey to the centre of the bacterial ribosome. EMBO J. 29, 3810-3818. doi: 10.1038/emboj.2010.252.
74. Weis, F., Bron, P., Rolland, J. P., Thomas, D., Felden, B., and Gillet, R. (2010b) Accommodation of tmRNA-SmpB into stalled ribosomes: a cryo-EM study. RNA 16, 299-306. doi: 10.1261/rna.1757410.
75. Williams, K. P., Martindale, K. A., and Bartel, D. P. (1999). Resuming translation on tmRNA: a unique mode of determining a reading frame. EMBO J. 18, 5423-5433. doi: 10.1093/emboj/18.19.5423.
76. 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. doi: 10.1093/emboj/19.23.6612.
77. Wower, I. K., Zwieb, C., and Wower, J. (2004). Contributions of pseudoknots and protein SmpB to the structure and function of tmRNA in trans-translation. J. Biol. Chem. 279, 54202-54209. doi: 10.1074/jbc.M410488200.
78. Wower, I. K., Zwieb, C., and Wower, J. (2005). Transfer-messenger RNA unfolds as it transits the ribosome. RNA 11, 668-673. doi: 10.1261/rna.7269305.
79. Wower, I. K., Zwieb, C., and Wower, J. (2009). Escherichia coli tmRNA lacking pseudoknot 1 tags truncated proteins in vivo and in vitro. RNA 15, 128-137. doi: 10.1261/rna.1192409.
80. Zvereva, M. I., Ivanov, P. V., Teraoka, Y., Topilina, N. I., Dontsova, O. A., Bogdanov, A. A., et al. (2001). Complex of transfer-messenger RNA and elongation factor Tu. Unexpected modes of interaction. J. Biol. Chem. 276, 47702-47708. doi: 10.1074/jbc.M106786200.