The tmRNA-tagging mechanism and the control of gene expression: A review

Wiley Interdisciplinary Reviews: RNA

Volumn 2, Issue 2, 2011, Pages 233-246

  Barends, Sharief ^a   Barend, Kraal ^b   van Wezel, Gilles P ^b  

^a ProteoNic   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATE; MESSENGER RNA; PROTEIN EF; PROTEIN SMPB; PROTEIN TU; RIBONUCLEOPROTEIN; TRANSFER RNA; UNCLASSIFIED DRUG; BACTERIAL RNA; TMRNA;

CAULOBACTER CRESCENTUS; CELL CYCLE; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; RNA TRANSLATION; STREPTOMYCES COELICOLOR; STREPTOMYCES LIVIDANS; ANIMAL; BACTERIUM; BIOLOGICAL MODEL; CHEMISTRY; CONFORMATION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN SYNTHESIS; PROTEIN TRANSPORT;

BACTERIA (MICROORGANISMS);

ANIMALS; BACTERIA; BASE SEQUENCE; GENE EXPRESSION REGULATION; HUMANS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PROTEIN BIOSYNTHESIS; PROTEIN TRANSPORT; PROTEOLYSIS; RNA, BACTERIAL;

EID: 84857768741     PISSN: 17577004     EISSN: 17577012     Source Type: Journal    
DOI: 10.1002/wrna.48     Document Type: Review

References (119)

1. Ray BK, Apirion D. Characterization of 10S RNA: a new stable RNA molecule from Escherichia coli. Mol Gen Genet 1979, 174:25-32.
2. Chauhan AK, Apirion D. The gene for a small stable RNA (10Sa RNA) of Escherichia coli. Mol Microbiol 1989, 3:1481-1485.
3. Komine Y, Kitabatake M, Yokogawa T, Nishikawa K, Inokuchi H. A tRNA-like structure is present in 10Sa RNA, a small stable RNA from Escherichia coli. Proc Natl Acad Sci USA 1994, 91:9223-9227.
4. Ushida C, Himeno H, Watanabe T, Muto A. tRNA-like structures in 10Sa RNAs of Mycoplasma capricolum and Bacillus subtilis. Nucleic Acids Res 1994, 22:3392-3396.
5. Oh BK, Apirion D. 10Sa RNA, a small stable RNA of Escherichia coli, is functional. Mol Gen Genet 1991, 229:52-56.
6. Retallack DM, Friedman DI. A role for a small stable RNA in modulating the activity of DNA-binding proteins. Cell 1995, 83:227-235.
7. Tu GF, Reid GE, Zhang JG, Moritz JG, Simpson RJ. C-terminal extension of truncated recombinant proteins in Escherichia coli with a 10Sa RNA decapeptide. J Biol Chem 1995, 270:9322-9326.
8. Keiler KC, Waller PR, Sauer RT. Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA. Science 1996, 271:990-993.
9. Jentsch S. When proteins receive deadly messages at birth. Science 1996, 271:955-956.
10. Keiler KC, Shapiro L, Williams KP. tmRNAs that encode proteolysis-inducing tags are found in all known bacterial genomes: a two-piece tmRNA functions in Caulobacter. Proc Natl Acad Sci USA 2000, 97:7778-7783.
11. Williams KP. Descent of a split RNA. Nucleic Acids Res 2002, 30:2025-2030.
12. Felden B, Hanawa K, Atkins JF, Himeno H, Muto A, Gesteland RF, McCloskey JA, Crain PF. Presence and location of modified nucleotides in Escherichia coli tmRNA: structural mimicry with tRNA acceptor branches. Embo J 1998, 17:3188-3196.
13. Barends S, Bjork K, Gultyaev AP, de Smit MH, Pleij CW, Kraal B. Functional evidence for D- and T-loop interactions in tmRNA. FEBS Lett 2002, 514:78-83.
14. Moore SD, Sauer RT. Ribosome rescue: tmRNA tagging activity and capacity in Escherichia coli. Mol Microbiol 2005, 58:456-466.
15. de la Cruz J, Vioque A. Increased sensitivity to protein synthesis inhibitors in cells lacking tmRNA. RNA 2001, 7:1708-1716.
16. Fujihara A, Tomatsu H, Inagaki S, Tadaki T, Ushida C, Himeno H, Muto A. Detection of tmRNA-mediated trans-translation products in Bacillus subtilis. Genes Cells 2002, 7:343-350.
17. Karzai AW, Susskind MM, Sauer RT. SmpB, a unique RNA-binding protein essential for the peptide-tagging activity of SsrA (tmRNA). Embo J 1999, 18:3793-3799.
18. Sundermeier TR, Dulebohn DP, Cho HJ, Karzai AW. A previously uncharacterized role for small protein B (SmpB) in transfer messenger RNA-mediated trans-translation. Proc Natl Acad Sci USA 2005, 102:2316-2321.
19. Bessho Y, Shibata R, Sekine S, Murayama K, Higashijima K, Hori-Takemoto C, Shirouzu M, Kuramitsu S, Yokoyama S. Structural basis for functional mimicry of long-variable-arm tRNA by transfer-messenger RNA. Proc Natl Acad Sci USA 2007, 104:8293-8298.
20. Qi H, Shimizu Y, Ueda T. Ribosomal protein S1 is not essential for the trans-translation machinery. J Mol Biol 2007, 368:845-852.
21. Takada K, Takemoto C, Kawazoe M, Konno T, Hanawa-Suetsugu K, Lee S, Shirouzu M, Yokoyama S, Muto A, Himeno H. In vitro trans-translation of Thermus thermophilus: ribosomal protein S1 is not required for the early stage of trans-translation. RNA 2007, 13:503-510.
22. Wower IK, Zwieb CW, Guven SA, Wower J. Binding and cross-linking of tmRNA to ribosomal protein S1, on and off the Escherichia coli ribosome. Embo J 2000, 19:6612-6621.
23. Gillet R, Kaur S, Li W, Hallier M, Felden B, Frank J. Scaffolding as an organizing principle in trans-translation. The roles of small protein B and ribosomal protein S1. J Biol Chem 2007, 282:6356-6363.
24. Valle M, Gillet R, Kaur S, Henne A, Ramakrishnan V, Frank J. Visualizing tmRNA entry into a stalled ribosome. Science 2003, 300:127-130.
25. Hong SJ, Tran QA, Keiler KC. Cell cycle-regulated degradation of tmRNA is controlled by RNase R and SmpB. Mol Microbiol 2005, 57:565-575.
26. Richards J, Mehta P, Karzai AW, Nase R. Degrades non-stop mRNAs selectively in an SmpB-tmRNA-dependent manner. Mol Microbiol 2006, 62:1700-1712.
27. Barends S, Karzai AW, Sauer RT, Wower J, Kraal B. Simultaneous and functional binding of SmpB and EF-Tu-TP to the alanyl acceptor arm of tmRNA. J Mol Biol 2001, 314:9-21.
28. Ivanova N, Pavlov MY, Felden B, Ehrenberg M. Ribosome rescue by tmRNA requires truncated mRNAs. J Mol Biol 2004, 338:33-41.
29. Keiler KC. Biology of trans-translation. Annu Rev Microbiol 2008, 62:133-151.
30. Roche ED, Sauer RT. SsrA-mediated peptide tagging caused by rare codons and tRNA scarcity. EMBO J 1999, 18:4579-4589.
31. Collier J, Binet E, Bouloc P. Competition between SsrA tagging and translational termination at weak stop codons in Escherichia coli. Mol Microbiol 2002, 45:745-754.
32. Hayes CS, Bose B, Sauer RT. Stop codons preceded by rare arginine codons are efficient determinants of SsrA tagging in Escherichia coli. Proc Natl Acad Sci USA 2002, 99:3440-3445.
33. Roche ED, Sauer RT. Identification of endogenous SsrA-tagged proteins reveals tagging at positions corresponding to stop codons. J Biol Chem 2001, 276:28509-28515.
34. Hayes CS, Sauer RT. Cleavage of the A site mRNA codon during ribosome pausing provides a mechanism for translational quality control. Mol Cell 2003, 12:903-911.
35. Sunohara T, Abo T, Inada T, Aiba H. The C-terminal amino acid sequence of nascent peptide is a major determinant of SsrA tagging at all three stop codons. RNA 2002, 8:1416-1427.
36. Sunohara T, Jojima K, Tagami H, Inada T, Aiba H. Ribosome stalling during translation elongation induces cleavage of mRNA being translated in Escherichia coli. J Biol Chem 2004, 279:15368-15375.
37. Pedersen K, Zavialov AV, Pavlov MY, Elf J, Gerdes K, Ehrenberg M. The bacterial toxin RelE displays codon-specific cleavage of mRNAs in the ribosomal A site. Cell 2003, 112:131-140.
38. Christensen SK, Gerdes K. RelE toxins from bacteria and Archaea cleave mRNAs on translating ribosomes, which are rescued by tmRNA. Mol Microbiol 2003, 48:1389-1400.
39. Neubauer C, Gao YG, Andersen KR, Dunham CM, Kelley AC, Hentschel J, Gerdes K, Ramakrishnan V, Brodersen DE. The structural basis for mRNA recognition and cleavage by the ribosome-dependent endonuclease RelE. Cell 2009, 139:1084-1095.
40. Baik S, Inoue K, Ouyang M, Nouye M. Significant bias against the ACA triplet in the tmRNA sequence of Escherichia coli K-12. J Bacteriol 2009, 191:6157-6166.
41. Garza-Sanchez F, Gin JG, Hayes CS. Amino acid starvation and colicin D treatment induce A-site mRNA cleavage in Escherichia coli. J Mol Biol 2008, 378:505-519.
42. Hayes CS, Keiler KC. Beyond ribosome rescue: tmRNA and co-translational processes. FEBS Lett 2010, 584:413-419.
43. Holberger LE, Hayes CS. Ribosomal protein S12 and aminoglycoside antibiotics modulate A-site mRNA cleavage and transfer-messenger RNA activity in Escherichia coli. J Biol Chem 2009, 284:32188-32200.
44. Cheng K, Ivanova N, Scheres SH, Pavlov MY, Carazo JM, Hebert H, Ehrenberg M, Lindahl M. tmRNA. SmpB complex mimics native aminoacyl-tRNAs in the A site of stalled ribosomes. J Struct Biol 2010, 169:342-348.
45. Weis F, Bron P, Rolland JP, Thomas D, Felden B, Gillet R. Accommodation of tmRNA-SmpB into stalled ribosomes: a cryo-EM study. RNA 2009, 16:299-306.
46. Shpanchenko OV, Golovin AV, Bugaeva EY, Isaksson LA, Dontsova OA. Structural aspects of trans-translation. IUBMB Life 62:120-124.
47. Williams KP, Martindale KA, Bartel DP. Resuming translation on tmRNA: a unique mode of determining a reading frame. Embo J 1999, 18:5423-5433.
48. Konno T, Kurita D, Takada K, Muto A, Himeno H. A functional interaction of SmpB with tmRNA for determination of the resuming point of trans-translation. RNA 2007, 13:1723-1731.
49. Lee S, Ishii M, Tadaki T, Muto A, Himeno H. 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 2001, 7:999-1012.
50. Miller MR, Healey DW, Robison SG, Dewey JD, Buskirk AR. The role of upstream sequences in selecting the reading frame on tmRNA. BMC Biol 2008, 6:29.
51. Watts T, Cazier D, Healey D, Buskirk A. SmpB contributes to reading frame selection in the translation of transfer-messenger RNA. J Mol Biol 2009, 391:275-281.
52. Nonin-Lecomte S, Germain-Amiot N, Gillet R, Hallier M, Ponchon L, Dardel F, Felden B. Ribosome hijacking: a role for small protein B during trans-translation. EMBO Rep 2009, 10:160-165.
53. Kurita D, Muto A, Himeno H. Role of the C-terminal tail of SmpB in the early stage of trans-translation. RNA 2010, 16:980-990.
54. Komarova AV, Tchufistova LS, Supina EV, Boni IV. Protein S1 counteracts the inhibitory effect of the extended Shine-Dalgarno sequence on translation. RNA 2002, 8:1137-1147.
55. Herman C, Thevenet D, Bouloc P, Walker GC, D'Ari R. Degradation of carboxy-terminal-tagged cytoplasmic proteins by the Escherichia coli protease HflB (FtsH). Genes Dev 1998, 12:1348-1355.
56. Gottesman S, Roche E, Zhou Y, Sauer RT. The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system. Genes Dev 1998, 12:1338-1347.
57. Choy JS, Aung LL, Karzai AW. Lon protease degrades transfer-messenger RNA-tagged proteins. J Bacteriol 2007, 189:6564-6571.
58. Gur E, Sauer RT. Evolution of the ssrA degradation tag in Mycoplasma: specificity switch to a different protease. Proc Natl Acad Sci USA 2008, 105:16113-16118.
59. Barends S, Karzai AW, Sauer RT, Wower J, Kraal B. Simultaneous and functional binding of SmpB and EF-Tu-GTP to the alanyl acceptor arm of tmRNA. J Mol Biol 2001, 314:9-21.
60. Levchenko I, Seidel M, Sauer RT, Baker TA. A specificity-enhancing factor for the ClpXP degradation machine. Science 2000, 289:2354-2356.
61. Flynn JM, Levchenko I, Seidel M, Wickner SH, Sauer RT, Baker TA. Overlapping recognition determinants within the ssrA degradation tag allow modulation of proteolysis. Proc Natl Acad Sci USA 2001, 98:10584-10589.
62. Park EY, Song HK. A degradation signal recognition in prokaryotes. J Synchrot Radiat 2008, 15:246-249.
63. Song HK, Eck MJ. Structural basis of degradation signal recognition by SspB, a specificity-enhancing factor for the ClpXP proteolytic machine. Mol Cell 2003, 12:75-86.
64. Lies M, Maurizi MR. Turnover of endogenous SsrA-tagged proteins mediated by ATP-dependent proteases in Escherichia coli. J Biol Chem 2008, 283:22918-22929.
65. Barends S, Zehl M, Bialek S, de Waal E, Traag BA, Willemse J, Jensen ON, Vijgenboom E, van Wezel GP. Transfer-messenger RNA controls the translation of cell-cycle and stress proteins in Streptomyces. EMBO Rep 2010, 11:119-125.
66. Milla ME, Brown BM, Sauer RT. P22 Arc repressor: enhanced expression of unstable mutants by addition of polar C-terminal sequences. Protein Sci 1993, 2:2198-2205.
67. Withey JH, Friedman DI. The biological roles of trans-translation. Curr Opin Microbiol 2002, 5:154-159.
68. Asano K, Kurita D, Takada K, Konno T, Muto A, Himeno H. Competition between trans-translation and termination or elongation of translation. Nucleic Acids Res 2005, 33:5544-5552.
69. Zhang Y, Zhang J, Hara H, Kato I, Inouye M. Insights into the mRNA cleavage mechanism by MazF, an mRNA interferase. J Biol Chem 2005, 280:3143-3150.
70. Zhang Y, Zhang J, Hoeflich KP, Ikura M, Qing G, Inouye M. MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coli. Mol Cell 2003, 12:913-923.
71. Zhang Y, Zhu L, Zhang J, Inouye M. Characterization of ChpBK, an mRNA interferase from Escherichia coli. J Biol Chem 2005, 280:26080-26088.
72. Garza-Sanchez F, Shoji S, Fredrick K, Hayes CS. RNase II is important for A-site mRNA cleavage during ribosome pausing. Mol Microbiol 2009, 73:882-897.
73. Abo T, Inada T, Ogawa K, Aiba H. SsrA-mediated tagging and proteolysis of LacI and its role in the regulation of lac operon. EMBO J 2000, 19:3762-3769.
74. Retallack DM, Johnson LL, Friedman DI. Role for 10Sa RNA in the growth of lambda-P22 hybrid phage. J Bacteriol 1994, 176:2082-2089.
75. Keiler KC, Shapiro L. tmRNA in Caulobacter crescentus is cell cycle regulated by temporally controlled transcription and RNA degradation. J Bacteriol 2003, 185:1825-1830.
76. Keiler KC, Shapiro L. TmRNA is required for correct timing of DNA replication in Caulobacter crescentus. J Bacteriol 2003, 185:573-580.
77. Quon KC, Yang B, Domian IJ, Shapiro L, Marczynski GT. Negative control of bacterial DNA replication by a cell cycle regulatory protein that binds at the chromosome origin. Proc Natl Acad Sci USA 1998, 95:120-125.
78. Wortinger M, Sackett MJ, Brun YV. CtrA mediates a DNA replication checkpoint that prevents cell division in Caulobacter crescentus. EMBO J 2000, 19:4503-4512.
79. Domian IJ, Quon KC, Shapiro L. Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle. Cell 1997, 90:415-424.
80. Hong SJ, Lessner FH, Mahen EM, Keiler KC. Proteomic identification of tmRNA substrates. Proc Natl Acad Sci USA 2007, 104:17128-17133.
81. Cheng L, Keiler KC. Correct timing of dnaA transcription and initiation of DNA replication requires trans translation. J Bacteriol 2009, 191:4268-4275.
82. Russell JH, Keiler KC. Subcellular localization of a bacterial regulatory RNA. Proc Natl Acad Sci USA 2009, 106:16405-16409.
83. Abe T, Sakaki K, Fujihara A, Ujiie H, Ushida C, Himeno H, Sato T, Muto A. tmRNA-dependent trans-translation is required for sporulation in Bacillus subtilis. Mol Microbiol 2008, 69:1491-1498.
84. Stragier P, Kunkel B, Kroos L, Losick R. Chromosomal rearrangement generating a composite gene for a developmental transcription factor. Science 1989, 243:507-512.
85. van Wezel GP, McKenzie NL, Nodwell JR. Chapter 5. Applying the genetics of secondary metabolism in model actinomycetes to the discovery of new antibiotics. Methods Enzymol 2009, 458:117-141.
86. Hopwood DA. Streptomyces in Nature and Medicine: The Antibiotic Makers. New York: Oxford University Press; 2007.
87. Rigali S, Titgemeyer F, Barends S, Mulder S, Thomae AW, Hopwood DA, van Wezel GP. Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep 2008, 9:670-675.
88. Paget MS, Molle V, Cohen G, Aharonowitz Y, Buttner MJ. Defining the disulphide stress response in Streptomyces coelicolor A3(2): identification of the sigmaR regulon. Mol Microbiol 2001, 42:1007-1020.
89. Braud S, Lavire C, Bellier A, Mazodier P. Effect of SsrA (tmRNA) tagging system on translational regulation in Streptomyces. Arch Microbiol 2006, 184:343-352.
90. Paleckova P, Bobek J, Felsberg J, Mikulik K. Activity of translation system and abundance of tmRNA during development of Streptomyces aureofaciens producing tetracycline. Folia Microbiol (Praha) 2006, 51:517-524.
91. Paleckova P, Felsberg J, Bobek J, Mikulik K. tmRNA abundance in Streptomyces aureofaciens, S. griseus and S. collinus under stress-inducing conditions. Folia Microbiol (Praha) 2007, 52:463-470.
92. Yang C, Glover JR. The SmpB-tmRNA tagging system plays important roles in Streptomyces coelicolor growth and development. PLoS ONE 2009, 4:e4459.
93. Flardh K, Buttner MJ. Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat Rev Microbiol 2009, 7:36-49.
94. Bentley SD, Chater KF, Cerdeno-Tarraga AM, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D, et al. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 2002, 417:141-147.
95. Chater KF. Streptomyces inside-out: a new perspective on the bacteria that provide us with antibiotics. Phil Trans R Soc Lond B Biol Sci 2006, 361:761-768.
96. Leskiw BK, Bibb MJ, Chater KF. The use of a rare codon specifically during development? Mol Microbiol 1991, 5:2861-2867.
97. Rigali S, Nothaft H, Noens EE, Schlicht M, Colson S, Muller M, Joris B, Koerten HK, Hopwood DA, Titgemeyer F, et al. The sugar phosphotransferase system of Streptomyces coelicolor is regulated by the GntR-family regulator DasR and links N-acetylglucosamine metabolism to the control of development. Mol Microbiol 2006, 61:1237-1251.
98. van Wezel GP, Woudt LP, Vervenne R, Verdurmen ML, Vijgenboom E, Bosch L. Cloning and sequencing of the tuf genes of Streptomyces coelicolor A3(2). Biochim Biophys Acta 1994, 1219:543-547.
99. van Wezel GP, Takano E, Vijgenboom E, Bosch L, Bibb MJ. The tuf3 gene of Streptomyces coelicolor A3(2) encodes an inessential elongation factor Tu that is apparently subject to positive stringent control. Microbiology 1995, 141(Pt 10):2519-2528.
100. Bucca G, Brassington AM, Hotchkiss G, Mersinias V, Smith CP. Negative feedback regulation of dnaK, clpB and lon expression by the DnaK chaperone machine in Streptomyces coelicolor, identified by transcriptome and in vivo DnaK-depletion analysis. Mol Microbiol 2003, 50:153-166.
101. Wickner S, Hoskins J, McKenney K. Function of DnaJ and DnaK as chaperones in origin-specific DNA binding by RepA. Nature 1991, 350:165-167.
102. Kahmann JD, Sass HJ, Allan MG, Seto H, Thompson CJ, Grzesiek S. Structural basis for antibiotic recognition by the TipA class of multidrug-resistance transcriptional regulators. EMBO J 2003, 22:1824-1834.
103. Noens EE, Mersinias V, Traag BA, Smith CP, Koerten HK, van Wezel GP. SsgA-like proteins determine the fate of peptidoglycan during sporulation of Streptomyces coelicolor. Mol Microbiol 2005, 58:929-944.
104. Noens EE, Mersinias V, Willemse J, Traag BA, Laing E, Chater KF, Smith CP, Koerten HK, van Wezel GP. Loss of the controlled localization of growth stage-specific cell-wall synthesis pleiotropically affects developmental gene expression in an ssgA mutant of Streptomyces coelicolor. Mol Microbiol 2007, 64:1244-1259.
105. Traag BA, Kelemen GH, Van Wezel GP. Transcription of the sporulation gene ssgA is activated by the IclR-type regulator SsgR in a whi-independent manner in Streptomyces coelicolor A3(2). Mol Microbiol 2004, 53:985-1000.
106. Wang G, Inaoka T, Okamoto S, Ochi K. A novel insertion mutation in Streptomyces coelicolor ribosomal S12 protein results in paromomycin resistance and antibiotic overproduction. Antimicrob Agents Chemother 2009, 53:1019-1026.
107. Arsene F, Tomoyasu T, Bukau B. The heat shock response of Escherichia coli. Int J Food Microbiol 2000, 55:3-9.
108. Musatovova O, Dhandayuthapani S, Baseman JB. Transcriptional heat shock response in the smallest known self-replicating cell, Mycoplasma genitalium. J Bacteriol 2006, 188:2845-2855.
109. Manteca A, Mader U, Connolly BA, Sanchez J. A proteomic analysis of Streptomyces coelicolor programmed cell death. Proteomics 2006, 6:6008-6022.
110. Ranquet C, Gottesman S. Translational regulation of the Escherichia coli stress factor RpoS: a role for SsrA and Lon. J Bacteriol 2007, 189:4872-4879.
111. Fredriksson A, Ballesteros M, Peterson CN, Persson O, Silhavy TJ, Nystrom T. Decline in ribosomal fidelity contributes to the accumulation and stabilization of the master stress response regulator sigmaS upon carbon starvation. Genes Dev 2007, 21:862-874.
112. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P. CRISPR provides acquired resistance against viruses in prokaryotes. Science 2007, 315:1709-1712.
113. Brouns SJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJ, Snijders AP, Dickman MJ, Makarova KS, Koonin EV, van der Oost J. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 2008, 321:960-964.
114. van der Oost J, Brouns SJ. RNAi: prokaryotes get in on the act. Cell 2009, 139:863-865.
115. Montero CI, Lewis DL, Johnson MR, Conners SB, Nance EA, Nichols JD, Kelly RM. Colocation of genes encoding a tRNA-mRNA hybrid and a putative signaling peptide on complementary strands in the genome of the hyperthermophilic bacterium Thermotoga maritima. J Bacteriol 2006, 188:6802-6807.
116. Dulebohn D, Choy J, Sundermeier T, Okan N, Karzai AW. Trans-translation: the tmRNA-mediated surveillance mechanism for ribosome rescue, directed protein degradation, and nonstop mRNA decay. Biochemistry 2007, 46:4681-4693.
117. Karzai AW, Roche ED, Sauer RT. The SsrA-SmpB system for protein tagging, directed degradation and ribosome rescue. Nat Struct Biol 2000, 7:449-455.
118. Moore SD, Sauer RT. The tmRNA system for translational surveillance and ribosome rescue. Annu Rev Biochem 2007, 76:101-124.
119. Withey JH, Friedman DI. A salvage pathway for protein structures: tmRNA and trans-translation. Annu Rev Microbiol 2003, 57:101-123.