Beyond ribosome rescue: tmRNA and co-translational processes

FEBS Letters

Volumn 584, Issue 2, 2010, Pages 413-419

  Hayes, Christopher S ^a   Keiler, Kenneth C ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Ribosome pausing; SmpB; tmRNA; trans Translation; Translation

Indexed keywords

MESSENGER RNA; POLYPEPTIDE; TRANSFER RNA;

BACTERIUM; CARBOXY TERMINAL SEQUENCE; GENETIC CONSERVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; REVIEW; RIBOSOME; RNA TRANSLATION; TRANSLATION REGULATION;

BACTERIA; PROTEIN BIOSYNTHESIS; PROTEIN FOLDING; RIBOSOMES; RNA, BACTERIAL;

BACTERIA (MICROORGANISMS);

EID: 71549151293     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2009.11.023     Document Type: Review

References (65)

1. Komine Y., Kitabatake M., Yokogawa T., Nishikawa K., and Inokuchi H. A tRNA-like structure is resent in 10Sa RNA, a small stable RNA from Escherichia coli. Proc. Natl. Acad. Sci. USA 91 (1994) 9223-9227
2. Ushida C., Himeno H., Watanabe T., and Muto A. tRNA-like structures in 10Sa RNAs of Mycoplasma capricolum and Bacillus subtilis. Nucleic Acids Res. 22 (1994) 3392-3396
3. Li Z., Pandit S., and Deutscher M.P. 3′ exoribonucleolytic trimming is a common feature of the maturation of small, stable RNAs in Escherichia coli. Proc. Natl. Acad. Sci. USA 95 (1998) 2856-2861
4. Lin-Chao S., Wei C.L., and Lin Y.T. RNase E is required for the maturation of ssrA RNA and normal ssrA RNA peptide-tagging activity. Proc. Natl. Acad. Sci. USA 96 (1999) 12406-12411
5. Barends S., Wower J., and Kraal B. Kinetic parameters for tmRNA binding to alanyl-tRNA synthetase and elongation factor Tu from Escherichia coli. Biochemistry 39 (2000) 2652-2658
6. Rudinger-Thirion J., Giege R., and Felden B. Aminoacylated tmRNA from Escherichia coli interacts with prokaryotic elongation factor Tu. RNA 5 (1999) 989-992
7. Felden B., Himeno H., Muto A., McCutcheon J.P., Atkins J.F., and Gesteland R.F. Probing the structure of the Escherichia coli 10Sa RNA (tmRNA). RNA 3 (1997) 89-103
8. Tu G.F., Reid G.E., Zhang J.G., Moritz R.L., and Simpson R.J. C-terminal extension of truncated recombinant proteins in Escherichia coli with a 10Sa RNA decapeptide. J. Biol. Chem. 270 (1995) 9322-9326
9. Williams K.P., and Bartel D.P. Phylogenetic analysis of tmRNA secondary structure. RNA 2 (1996) 1306-1310
10. Karzai A.W., Susskind M.M., and Sauer R.T. SmpB, a unique RNA-binding protein essential for the peptide-tagging activity of SsrA (tmRNA). EMBO J. 18 (1999) 3793-3799
11. Bessho Y., Tamura S., Hori H., Tanaka H., Ohama T., and Osawa S. Planarian mitochondria sequence heterogeneity: Relationships between the type of cytochrome c oxidase subunit I gene sequence, karyotype and genital organ. Mol. Ecol. 6 (1997) 129-136
12. Shimizu Y., and Ueda T. 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 (2006) 15987-15996
13. Ivanova N., Pavlov M.Y., Bouakaz E., Ehrenberg M., and Schiavone L.H. Mapping the interaction of SmpB with ribosomes by footprinting of ribosomal RNA. Nucleic Acids Res. 33 (2005) 3529-3539
14. Kurita D., Sasaki R., Muto A., and Himeno H. Interaction of SmpB with ribosome from directed hydroxyl radical probing. Nucleic Acids Res. 35 (2007) 7248-7255
15. Sundermeier T.R., and Karzai A.W. Functional SmpB-ribosome interactions require tmRNA. J. Biol. Chem. 282 (2007) 34779-34786
16. Valle M., Gillet R., Kaur S., Henne A., Ramakrishnan V., and Frank J. Visualizing tmRNA entry into a stalled ribosome. Science 300 (2003) 127-130
17. Flynn J.M., Levchenko I., Seidel M., Wickner S.H., Sauer R.T., and Baker T.A. Overlapping recognition determinants within the ssrA degradation tag allow modulation of proteolysis. Proc. Natl. Acad. Sci. USA 98 (2001) 10584-10589
18. Gottesman S., Roche E., Zhou Y., and Sauer R.T. The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system. Genes Dev. 12 (1998) 1338-1347
19. Ivanova N., Pavlov M.Y., and Ehrenberg M. tmRNA-induced release of messenger RNA from stalled ribosomes. J. Mol. Biol. 350 (2005) 897-905
20. Keiler K.C., Waller P.R., and Sauer R.T. Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 271 (1996) 990-993
21. Mehta P., Richards J., and Karzai A.W. tmRNA determinants required for facilitating non-stop mRNA decay. RNA 12 (2006) 2187-2198
22. Richards J., Mehta P., and Karzai A.W. RNase R degrades non-stop mRNAs selectively in an SmpB-tmRNA-dependent manner. Mol. Microbiol. 62 (2006) 1700-1712
23. Yamamoto Y., Sunohara T., Jojima K., Inada T., and Aiba H. SsrA-mediated trans-translation plays a role in mRNA quality control by facilitating degradation of truncated mRNAs. RNA 9 (2003) 408-418
24. Gueneau de Novoa P., and Williams K.P. The tmRNA website: Reductive evolution of tmRNA in plastids and other endosymbionts. Nucleic Acids Res. 32 (2004) D104-108
25. Mao C., Bhardwaj K., Sharkady S.M., Fish R.I., Driscoll T., Wower J., Zwieb C., Sobral B.W., and Williams K.P. Variations on the tmRNA gene. RNA Biol. 6 (2009) 355-361
26. Moore S.D., and Sauer R.T. Ribosome rescue: tmRNA tagging activity and capacity in Escherichia coli. Mol. Microbiol. 58 (2005) 456-466
27. Huang C., Wolfgang M., Withey J., Koomey M., and Friedman D. Charged tmRNA but not tmRNA-mediated proteolysis is essential for Neisseria gonorrhoeae viability. EMBO J. 19 (2000) 1098-1107
28. Keiler K.C. Physiology of tmRNA: What gets tagged and why?. Curr. Opin. Microbiol. 10 (2007) 169-175
29. Ivanova N., Pavlov M.Y., Felden B., and Ehrenberg M. Ribosome rescue by tmRNA requires truncated mRNAs. J. Mol. Biol. 338 (2004) 33-41
30. Kobayashi K., Kuwana R., and Takamatsu H. kinA mRNA is missing a stop codon in the undomesticated Bacillus subtilis strain ATCC 6051. Microbiology 154 (2008) 54-63
31. Abo T., Inada T., Ogawa K., and Aiba H. SsrA-mediated tagging and proteolysis of LacI and its role in the regulation of lac operon. EMBO J. 19 (2000) 3762-3769
32. Ujiie H., Matsutani T., Tomatsu H., Fujihara A., Ushida C., Miwa Y., Fujita Y., Himeno H., and Muto A. Trans-translation is involved in the CcpA-dependent tagging and degradation of TreP in Bacillus subtilis. J. Biochem. 145 (2009) 59-66
33. Pedersen K., Zavialov A.V., Pavlov M.Y., Elf J., Gerdes K., and Ehrenberg M. The bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site. Cell 112 (2003) 131-140
34. Zhang Y., Zhang J., Hoeflich K.P., Ikura M., Qing G., and Inouye M. MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coli. Mol. Cell 12 (2003) 913-923
35. Zhang Y., Zhu L., Zhang J., and Inouye M. Characterization of ChpBK, an mRNA interferase from Escherichia coli. J. Biol. Chem. 280 (2005) 26080-26088
36. Christensen S.K., and Gerdes K. RelE toxins from bacteria and Archaea cleave mRNAs on translating ribosomes, which are rescued by tmRNA. Mol. Microbiol. 48 (2003) 1389-1400
37. Christensen S.K., Pedersen K., Hansen F.G., and Gerdes K. Toxin-antitoxin loci as stress-response-elements: ChpAK/MazF and ChpBK cleave translated RNAs and are counteracted by tmRNA. J. Mol. Biol. 332 (2003) 809-819
38. Garza-Sánchez F., Gin J.G., and Hayes C.S. Amino acid starvation and colicin D treatment induce A-site mRNA cleavage in Escherichia coli. J. Mol. Biol. 378 (2008) 505-519
39. Hayes C.S., Bose B., and Sauer R.T. Proline residues at the C terminus of nascent chains induce SsrA tagging during translation termination. J. Biol. Chem. 277 (2002) 33825-33832
40. Hayes C.S., Bose B., and Sauer R.T. Stop codons preceded by rare arginine codons are efficient determinants of SsrA tagging in Escherichia coli. Proc. Natl. Acad. Sci. USA 99 (2002) 3440-3445
41. Hayes C.S., and Sauer R.T. Cleavage of the A site mRNA codon during ribosome pausing provides a mechanism for translational quality control. Mol. Cell 12 (2003) 903-911
42. Li X., Hirano R., Tagami H., and Aiba H. Protein tagging at rare codons is caused by tmRNA action at the 3′ end of nonstop mRNA generated in response to ribosome stalling. RNA 12 (2006) 248-255
43. Li X., Yokota T., Ito K., Nakamura Y., and Aiba H. Reduced action of polypeptide release factors induces mRNA cleavage and tmRNA tagging at stop codons in Escherichia coli. Mol. Microbiol. 63 (2007) 116-126
44. Roche E.D., and Sauer R.T. SsrA-mediated peptide tagging caused by rare codons and tRNA scarcity. EMBO J. 18 (1999) 4579-4589
45. Roche E.D., and Sauer R.T. Identification of endogenous SsrA-tagged proteins reveals tagging at positions corresponding to stop codons. J. Biol. Chem. 276 (2001) 28509-28515
46. Garza-Sánchez F., Shoji S., Fredrick K., and Hayes C.S. RNase II is important for A-site mRNA cleavage during ribosome pausing. Mol. Microbiol. 73 (2009) 882-897
47. Cruz-Vera L.R., Rajagopal S., Squires C., and Yanofsky C. Features of ribosome-peptidyl-tRNA interactions essential for tryptophan induction of tna operon expression. Mol. Cell 19 (2005) 333-343
48. Pro in the A-site of SecM-arrested ribosomes inhibits the recruitment of transfer-messenger RNA. J. Biol. Chem. 281 (2006) 34258-34268
49. Szaflarski W., Vesper O., Teraoka Y., Plitta B., Wilson D.N., and Nierhaus K.H. New features of the ribosome and ribosomal inhibitors: Non-enzymatic recycling, misreading and back-translocation. J. Mol. Biol. 380 (2008) 193-205
50. Kuroha K., Horiguchi N., Aiba H., and Inada T. Analysis of nonstop mRNA translation in the absence of tmRNA in Escherichia coli. Genes Cell 14 (2009) 739-749
51. Janssen B.D., and Hayes C.S. Kinetics of paused ribosome recycling in Escherichia coli. J. Mol. Biol. 394 (2009) 251-267
52. Heurgue-Hamard V., Karimi R., Mora L., MacDougall J., Leboeuf C., Grentzmann G., Ehrenberg M., and Buckingham R.H. Ribosome release factor RF4 and termination factor RF3 are involved in dissociation of peptidyl-tRNA from the ribosome. EMBO J. 17 (1998) 808-816
53. Pavlov M.Y., Antoun A., Lovmar M., and Ehrenberg M. Complementary roles of initiation factor 1 and ribosome recycling factor in 70S ribosome splitting. EMBO J. 27 (2008) 1706-1717
54. Collier J., Binet E., and Bouloc P. Competition between SsrA tagging and translational termination at weak stop codons in Escherichia coli. Mol. Microbiol. 45 (2002) 745-754
55. Fujihara A., Tomatsu H., Inagaki S., Tadaki T., Ushida C., Himeno H., and Muto A. Detection of tmRNA-mediated trans-translation products in Bacillus subtilis. Genes Cell 7 (2002) 343-350
56. Hong S.J., Lessner F.H., Mahen E.M., and Keiler K.C. Proteomic identification of tmRNA substrates. Proc. Natl. Acad. Sci. USA 104 (2007) 17128-17133
57. Maki J.A., Schnobrich D.J., and Culver G.M. The DnaK chaperone system facilitates 30S ribosomal subunit assembly. Mol. Cell 10 (2002) 129-138
58. Miczak A., Kaberdin V.R., Wei C.L., and Lin-Chao S. Proteins associated with RNase E in a multicomponent ribonucleolytic complex. Proc. Natl. Acad. Sci. USA 93 (1996) 3865-3869
59. Munavar H., Zhou Y., and Gottesman S. Analysis of the Escherichia coli Alp phenotype: Heat shock induction in ssrA mutants. J. Bacteriol. (2005) 187-4751
60. Danese P.N., and Silhavy T.J. Targeting and assembly of periplasmic and outer-membrane proteins in Escherichia coli. Annu. Rev. Genet. 32 (1998) 59-94
61. van Stelten J., Silva F., Belin D., and Silhavy T.J. Effects of antibiotics and a proto-oncogene homolog on destruction of protein translocator SecY. Science 325 (2009) 753-756
62. Campo N., Tjalsma H., Buist G., Stepniak D., Meijer M., Veenhuis M., Westermann M., Muller J.P., Bron S., Kok J., et al. Subcellular sites for bacterial protein export. Mol. Microbiol. 53 (2004) 1583-1599
63. Russell J.H., and Keiler K.C. Subcellular localization of a bacterial regulatory RNA. Proc. Natl. Acad. Sci. USA 106 (2009) 16405-16409
64. Shiomi D., Yoshimoto M., Homma M., and Kawagishi I. Helical distribution of the bacterial chemoreceptor via colocalization with the Sec protein translocation machinery. Mol. Microbiol. 60 (2006) 894-906
65. Pomerantz R.T., and O'Donnell M. The replisome uses mRNA as a primer after colliding with RNA polymerase. Nature 456 (2008) 762-766