A single base change in the Shine-Dalgarno region of 16S rRNA of Escherichia coli affects translation of many proteins.

Jacob, William F.; Santer, Melvin; Dahĺberg, Albert E.

doi:10.1073/pnas.84.14.4757

Cited by 180 publications

(113 citation statements)

References 42 publications

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“…Base pairing between the SD signal and a complementary region at the 3Ј end of 16S rRNA has been directly proven in E. coli by introducing point mutations into the 'anti-SD' region of rRNA and demonstrating convincingly that a correlation between translational efficiency and 'strength' of SD:anti-SD interactions exists ( Fig. 1A; Hui and deBoer, 1987;Jacob et al, 1987).…”

Section: Basic Mechanism Of Translation Initiation In Prokaryotesmentioning

confidence: 91%

Functional importance of RNA interactions in selection of translation initiation codons

Sprengart

Porter

1997

Molecular Microbiology

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SummaryRNA base pairing between the initiation codon and anticodon loop of initiator tRNA is essential but not sufficient for the selection of the 'correct' mRNA translational start site by ribosomes. In prokaryotes, additional RNA interactions between small ribosomal subunit RNA and mRNA sequences just upstream of the start codon can efficiently direct the ribosome to the initiation site. Although there is presently no proof for a similar important ribosomal RNA interaction in eukaryotes, the 5Ј non-coding regions of their mRNAs and 'consensus sequences' surrounding initiation codons have been shown to be strong determinants for initiation-site selection, but the exact mechanisms are not yet understood. Intramolecular base pairing in mRNA and participation of translation initiation factors can strongly influence the formation of mRNA-small ribosomal subunit-initiator tRNA complexes and modulate translational activities in both prokaryotes and eukaryotes. Only recently has it been appreciated that alternative mechanisms may also contribute to the selection of initiation codons in all organisms. Although direct proof is currently lacking, there is accumulating evidence that additional cis-acting mRNA elements and trans-acting proteins may form specific 'bridging' interactions with ribosomes during translation initiation.

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Section: Basic Mechanism Of Translation Initiation In Prokaryotesmentioning

confidence: 91%

Functional importance of RNA interactions in selection of translation initiation codons

Sprengart

Porter

1997

Molecular Microbiology

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“…One might then wonder why the SD sequence is considered to be the universal mechanism for translation initiation in prokaryotes. One possible reason is the large proportion of genes having the SD sequence in the well studied species (5)(6)(7)(8). Those species in which the functionality of the SD sequence was confirmed by experimental evidences, such as E. coli, B. subtilis, or M. jannaschii, tend to show large positive values of dR SD (53.7, 78.0, and 44.9, respectively).…”

Section: Discussionmentioning

confidence: 99%

Dynamic evolution of translation initiation mechanisms in prokaryotes

Nakagawa

Niimura²,

Miura³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

128

167

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It is generally believed that prokaryotic translation is initiated by the interaction between the Shine-Dalgarno (SD) sequence in the 5′ UTR of an mRNA and the anti-SD sequence in the 3′ end of a 16S ribosomal RNA. However, there are two exceptional mechanisms, which do not require the SD sequence for translation initiation: one is mediated by a ribosomal protein S1 (RPS1) and the other used leaderless mRNA that lacks its 5′ UTR. To understand the evolutionary changes of the mechanisms of translation initiation, we examined how universal the SD sequence is as an effective initiator for translation among prokaryotes. We identified the SD sequence from 277 species (249 eubacteria and 28 archaebacteria). We also devised an SD index that is a proportion of SD-containing genes in which the differences of GC contents are taken into account. We found that the SD indices varied among prokaryotic species, but were similar within each phylum. Although the anti-SD sequence is conserved among species, loss of the SD sequence seems to have occurred multiple times, independently, in different phyla. For those phyla, RPS1-mediated or leaderless mRNA-used mechanisms of translation initiation are considered to be working to a greater extent. Moreover, we also found that some species, such as Cyanobacteria, may acquire new mechanisms of translation initiation. Our findings indicate that, although translation initiation is indispensable for all protein-coding genes in the genome of every species, its mechanisms have dynamically changed during evolution. dynamic evolution | Shine-Dalgarno sequence | ribosomal protein S1T ranslation initiation is fundamentally important for all protein-coding genes in the genome of every organism. Initiation, rather than elongation, is usually the rate-limiting step in translation, and proceeds at very different efficiencies depending on the sequences in the 5′ UTRs of mRNAs (1). In prokaryotes (for both eubacteria and archaebacteria), the Shine-Dalgarno (SD) sequence in an mRNA is well known as the initiator element of translation (2, 3). The SD sequence, typically GGAGG, is located approximately 10 nucleotides upstream of the initiator codon. The SD sequence pairs with a complementary sequence (CCUCC) in the 3′ end of a 16S rRNA. In the 16S rRNA, the sequence is called the anti-SD sequence in the 3′ tail of which region is single-stranded. The interaction between the SD and the anti-SD sequences (called the SD interaction) augments initiation by anchoring the small (30S) ribosomal subunit around the initiation codon to form a preinitiation complex (4). The importance of the SD interaction for efficient initiation of translation has been experimentally verified for both eubacteria and archaebacteria. Alterations of the SD sequence or the anti-SD sequence strongly inhibit protein synthesis, both in eubacteria including Escherichia coli (5) and Bacillus subtilis (6, 7) and in archaebacteria such as Methanocaldococcus jannaschii (8). For this reason, the SD interaction is thought to be the universal m...

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“…The degree of complementarity between the SD sequence within the 5Ј untranslated leader of prokaryotic mRNA and the ASD sequence near the 3Ј end of the 16S rRNA is a major determinant of the efficiency by which leadered mRNAs are translated (Hui and de Boer, 1987;Jacob et al, 1987;Ringquist et al, 1992). Some naturally leaderless messages, although lacking a conventional SD-ASD interaction, are highly expressed [e.g.…”

Section: Discussionmentioning

confidence: 99%

“…The RBS of conventionally leadered Escherichia coli mRNA extends approximately Ϯ 15 nucleotides relative to the start codon (Steitz, 1969;Steitz and Jakes, 1975;Steitz and Steege, 1977), contains non-random sequence using statistical analysis (Scherer et al, 1980;Stormo et al, 1982), and is responsible for establishing a 1000-fold range of translational efficiencies (Ray and Pearson, 1974;. Highly efficient initiation regions include some or all of the following mRNA elements: a polypyrimidine tract for ribosomal protein S1 interaction (Boni et al, 1990;Zhang and Deutscher, 1991;Tzareva et al, 1994); a Shine-Dalgarno (SD) sequence with basepairing complementarity to the anti-SD (ASD) of the 16S rRNA (Shine and Dalgarno, 1974;Hui and de Boer, 1987;Jacob et al, 1987); a cognate start codon for initiator fMet-tRNA anticodon interaction (Ringquist et al, 1992;Vollenoweth and Rabinowitz, 1992); and base-specific enhancer sequences upstream (Olins and Rangwala, 1989) or downstream (Sprengart et al, 1990; of the start codon. The relative importance and interdependence of these mRNA elements as well as the temporal order of their recognition by initiating ribosomes is less well understood.…”

Section: Introductionmentioning

confidence: 99%

An AUG initiation codon, not codon–anticodon complementarity, is required for the translation of unleadered mRNA in Escherichia coli

Etten

Janssen

1998

Molecular Microbiology

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SummaryWe determined the in vivo translational efficiency of 'unleadered' lacZ compared with a conventionally leadered lacZ with and without a Shine-Dalgarno (SD) sequence in Escherichia coli and found that changing the SD sequence of leadered lacZ from the consensus 5Ј-AGGA-3Ј to 5Ј-UUUU-3Ј results in a 15-fold reduction in translational efficiency; however, removing the leader altogether results in only a twofold reduction. An increase in translation coincident with the removal of the leader lacking a SD sequence suggests the existence of stronger or novel translational signals within the coding sequence in the absence of the leader. We examined, therefore, a change in the translational signals provided by altering the AUG initiation codon to other naturally occurring initiation codons (GUG, UUG, CUG) in the presence and absence of a leader and find that mRNAs lacking leader sequences are dependent upon an AUG initiation codon, whereas leadered mRNAs are not. This suggests that mRNAs lacking leader sequences are either more dependent on perfect codon-anticodon complementarity or require an AUG initiation codon in a sequence-specific manner to form productive initiation complexes. A mutant initiator tRNA with compensating anticodon mutations restored expression of leadered, but not unleadered, mRNAs with UAG start codons, indicating that codon-anticodon complementarity was insufficient for the translation of mRNA lacking leader sequences. These data suggest that a cognate AUG initiation codon specifically serves as a stronger and different translational signal in the absence of an untranslated leader.

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A single base change in the Shine-Dalgarno region of 16S rRNA of Escherichia coli affects translation of many proteins.

Cited by 180 publications

References 42 publications

Functional importance of RNA interactions in selection of translation initiation codons

Functional importance of RNA interactions in selection of translation initiation codons

Dynamic evolution of translation initiation mechanisms in prokaryotes

An AUG initiation codon, not codon–anticodon complementarity, is required for the translation of unleadered mRNA in Escherichia coli

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