Local absence of secondary structure permits translation of mrnas that lack ribosome-binding sites

PLoS Genetics

Volumn 7, Issue 6, 2011, Pages

  Scharff, Lars B ^a   Childs, Liam ^a   Walther, Dirk ^a   Bock, Ralph ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; BACTERIAL RNA; RNA 16S;

ARTICLE; BACTERIAL GENETICS; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; ESCHERICHIA COLI; GENE CONSTRUCT; GENE IDENTIFICATION; GENETIC ASSOCIATION; MOLECULAR RECOGNITION; NONHUMAN; PROMOTER REGION; REPORTER GENE; RIBOSOME; RNA BINDING; RNA STRUCTURE; RNA TRANSLATION; SEQUENCE ANALYSIS; START CODON; STRUCTURE ANALYSIS; TRANSLATION INITIATION; 5' UNTRANSLATED REGION; BACTERIAL GENE; BACTERIUM; CHEMISTRY; CONFORMATION; GENETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR COMPUTER; PROTEIN SYNTHESIS;

PROKARYOTA;

5' UNTRANSLATED REGIONS; BACTERIA; BINDING SITES; CLONING, MOLECULAR; CODON, INITIATOR; COMPUTERS, MOLECULAR; GENES, BACTERIAL; NUCLEIC ACID CONFORMATION; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, BACTERIAL; RNA, MESSENGER; RNA, RIBOSOMAL, 16S;

EID: 79959847578     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002155     Document Type: Article

References (36)

1. McCarthy JEG, Brimacombe R, (1994) Prokaryotic translation initiation: the interactive pathway leading to initiation. Trends Genet 10: 402-407.
2. Kozak M, (1999) Initiation of translation in prokaryotes and eukaryotes. Gene 234: 187-208.
3. Apel W, Schulze WX, Bock R, (2010) Identification of protein stability determinants in chloroplasts. Plant J 63: 636-650.
4. Drechsel O, Bock R, (2010) Selection of Shine-Dalgarno sequences in plastids. Nucleic Acids Res 39: 1427-1438.
5. Fargo DC, Zhang M, Gillham NW, Boynton JE, (1998) Shine-Dalgarno-like sequences are not required for translation of chloroplast mRNAs in Chlamydomonas reinhardtii chloroplasts or in Escherichia coli. Mol Gen Genet 257: 271-282.
6. Skorski P, Leroy P, Fayet O, Dreyfus M, Hermann-Le Denmat S, (2006) The highly efficient translation initiation region from the Escherichia coli rpsA gene lacks a Shine-Dalgarno element. J Bacteriol 188: 6277-6285.
7. Nakagawa S, Niimura Y, Miura K-I, Gojobori T, (2010) Dynamic evolution of translation initiation mechanisms in prokaryotes. Proc Natl Acad Sci USA 107: 6382-6387.
8. Hazle T, Bonen L, (2007) Comparative analysis of sequences preceding protein-coding mitochondrial genes in flowering plants. Mol Biol Evol 24: 1101-1112.
9. Boni IV, Isaeva DM, Musychenko ML, Tzareva NV, (1991) Ribosome-messenger recognition: mRNA target sites for ribosomal protein S1. Nucleic Acids Res 19: 155-162.
10. Komarova AV, Tchufistova LS, Dreyfus M, Boni IV, (2005) AU-rich sequences within 5′ untranslated leaders enhance translation and stabilize mRNA in Escherichia coli. J Bacteriol 187: 1344-1349.
11. Komarova AV, Tchufistova LS, Supina EV, Boni IV, (2002) Protein S1 counteracts the inhibitory effect of the extended Shine-Dalgarno sequence on translation. RNA 8: 1137-1147.
12. Bailey TL, Elkan C, (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proceedings of the Second International Conference on Intelligent Systems for Molecular Biology pp. 28-36.
13. Linhart C, Halperin Y, Shamir R, (2008) Transcription factor and microRNA motif discovery: The Amadeus platform and a compendium of metazoan target sets. Genome Res 18: 1180-1189.
14. Reeder J, Giegerich R, (2005) Consensus shapes: an alternative to the Sankoff algorithm for RNA consensus structure prediction. Bioinformatics 21: 3516-3523.
15. Nakamoto T, (2006) A unified view of the initiation of protein synthesis. Biochem Biophys Res Commun 341: 675-678.
16. Ricard B, Salser W, (1975) Secondary structures formed by random RNA sequences. Biochem Biophys Res Commun 63: 548-554.
17. Ricard B, Salser W, (1976) Optical measurements reveal base-pairing in T4-specific mRNAs. Biochim Biophys Acta 425: 196-201.
18. Gralla J, DeLisi C, (1974) mRNA is expected to form stable secondary structures. Nature 248: 330-332.
19. Kudla G, Murray AW, Tollervey D, Plotkin JB, (2009) Coding-sequence determinants of gene expression in Escherichia coli. Science 324: 255-258.
20. Hofacker IL, Fontana W, Stadler PF, Bonhoeffer LS, Tacker M, et al. (1994) Fast folding and comparison of RNA secondary structures. Monatshefte f Chemie 125: 167-188.
21. Hüttenhofer A, Noller HF, (1994) Footprinting mRNA-ribosome complexes with chemical probes. EMBO J 13: 3892-3901.
22. Wikström PM, Lind LK, Berg DE, (1992) Importance of mRNA folding and start codon accessibility in the expression of genes in a ribosomal protein operon of Escherichia coli. J Mol Biol 224: 949-966.
23. Kertesz M, Wan Y, Mazor E, Rinn JL, Nutter RC, et al. (2010) Genome-wide measurement of RNA secondary structure in yeast. Nature 467: 103-107.
24. Studer SM, Joseph S, (2006) Unfolding of mRNA secondary structure by the bacterial translation initiation complex. Mol Cell 22: 105-115.
25. Jones CN, Wilkinson KA, Hung KT, Weeks KM, Spremulli LL, (2008) Lack of secondary structure characterizes the 5′ ends of mammalian mitochondrial mRNAs. RNA 14: 862-871.
26. Christian BE, Spremulli LL, (2010) Preferential selection of the 5′-terminal start codon on leaderless mRNAs by mammalian mitochondrial ribosomes. J Biol Chem 285: 28379-28386.
27. Kaberdina AC, Szaflarski W, Nierhaus KH, Moll I, (2009) An unexpected type of ribosomes induced by kasugamycin: a look into ancestral times of protein synthesis. Mol Cell 33: 227-236.
28. Pruitt KD, Harrow J, Harte RA, Wallin C, Diekhans M, et al. (2009) The consensus coding sequence (CCDS) project: Identifying a common protein-coding gene set for the human and mouse genomes. Genome Res 19: 1316-1323.
29. Bailey TL, Gribskov M, (1998) Combining evidence using p-values: application to sequence homology searches. Bioinformatics 14: 48-54.
30. Starmer J, Stomp A, Vouk M, Bitzer D, (2006) Predicting Shine-Dalgarno sequence locations exposes genome annotation errors. PLoS Comput Biol 2: e57 doi:10.1371/journal.pcbi.0020057.
31. Neupert J, Karcher D, Bock R, (2008) Design of simple synthetic RNA thermometers for temperature-controlled gene expression in Escherichia coli. Nucleic Acids Res 36: e124.
32. Hayashi K, Morooka N, Yamamoto Y, Fujita K, Isono K, et al. (2006) Highly accurate genome sequences of Escherichia coli K-12 strains MG1655 and W3110. Mol Syst Biol 2: e0007.
33. Neupert J, Bock R, (2009) Designing and using synthetic RNA thermometers for temperature-controlled gene expression in bacteria. Nature Protoc 4: 1262-1273.
34. Bernhart SH, Hofacker IL, Stadler PF, (2006) Local base pairing probabilities in large RNAs. Bioinformatics 22: 614-615.
35. Sharp PM, Li W-H, (1987) The codon adaptation index- a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15: 1281-1295.
36. Dong H, Nilsson L, Kurland CG, (1996) Co-variation of tRNA abundance and codon usage in Escherichia coli at different growth rates. J Mol Biol 260: 649-663.