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Analysis of tetra- and hepta-nucleotides motifs promoting -1 ribosomal frameshifting in Escherichia coli.

Sharma V, Prère MF, Canal I, Firth AE, Atkins JF, Baranov PV, Fayet O - Nucleic Acids Res. (2014)

Bottom Line: Depending on the signal, the frameshifting frequency can vary over a wide range, from less than 1% to more than 50%.While motif efficiency varies widely, a major distinctive rule of bacterial -1 frameshifting is that the most efficient motifs are those allowing cognate re-pairing of the A site tRNA from ZZN to ZZZ.The outcome of the genomic search is a set of 69 gene clusters, 59 of which constitute new candidates for functional utilization of -1 frameshifting.

View Article: PubMed Central - PubMed

Affiliation: School of Biochemistry and Cell biology, University College Cork, Cork, Ireland.

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Distribution of Z_ZZ.N and X_XX.Z_ZZ.N motifs in mobile elements from the IS1 and IS3 families. These two families were selected because biologically relevant -1 frameshifting was demonstrated in both (4,10). The sequences of the IS from these 2 families (63 entries for the IS1 family and 494 for the IS3 family), obtained from the ISFinder database (October 2012), were examined for the presence of potential frameshift signals (i.e. existence of 2 overlapping ORFs, with the second being in the -1 frame relative to the first and presence of a Z_ZZ.N or X_XX.Z_ZZ.N motif in the overlap region; the Z_ZZN motifs scored in panel B are those which are not part of an X_XX.Z_ZZ.N heptamer). The relative frameshifting frequencies of the motifs found are indicated in the right-hand panels. All values were normalized relative to that of the best motif (A_AA.G or C_CC.A_AA.G), using data from Figures 3 and 4.
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Figure 5: Distribution of Z_ZZ.N and X_XX.Z_ZZ.N motifs in mobile elements from the IS1 and IS3 families. These two families were selected because biologically relevant -1 frameshifting was demonstrated in both (4,10). The sequences of the IS from these 2 families (63 entries for the IS1 family and 494 for the IS3 family), obtained from the ISFinder database (October 2012), were examined for the presence of potential frameshift signals (i.e. existence of 2 overlapping ORFs, with the second being in the -1 frame relative to the first and presence of a Z_ZZ.N or X_XX.Z_ZZ.N motif in the overlap region; the Z_ZZN motifs scored in panel B are those which are not part of an X_XX.Z_ZZ.N heptamer). The relative frameshifting frequencies of the motifs found are indicated in the right-hand panels. All values were normalized relative to that of the best motif (A_AA.G or C_CC.A_AA.G), using data from Figures 3 and 4.

Mentions: From the above experimental study, we concluded that a majority of heptamers (and nearly half of the tetramers) were capable of eliciting -1 frameshifting at substantial levels (at least twice the background level). To determine the range of motifs used in genes utilizing frameshifting for their expression, we carried out an analysis of IS mobile genetics elements known, or suspected, to use this mode of translational control. We focused on the members of the IS1 and IS3 families available in the ISFinder database in October 2012 (9). As shown in Figure 5, both tetramers and heptamers are found, but with a marked preference for heptamers (87 against 403). Among the five tetramers, the three most shift-prone motifs, A_AA.G and U_UU.[U,C], predominate and the less efficient A_AA.A motif is also well represented. Only 16 different heptamers are found with 72% of them being either A_AA.A_AA.G or A_AA.A_AA.A. The next most frequent are A_AA.A_AA.C and G_GG.A_AA.C, both of low efficiency, followed by the more efficient G_GG.A_AA.G, U_UU.U_UU.C and G_GG.A_AA.A. To conclude, it appears that genes known or suspected to use PRF-1 to express a biologically important protein do not necessarily utilize high efficiency motifs. However, this conclusion is based on one category of genes where two overlapping genes code for the proteins required for transposition of two types of IS elements. There, the purpose of frameshifting is to provide the ‘right’ amount of a fusion protein which has the transposase function (18,52); this amount is what keeps transposition of the IS at a level without negative effect on the bacterial host. If the ‘right’ amount is a low amount, then the use of low-efficiency motifs, with or without flanking stimulators, is a way to achieve this goal as illustrated by the IS1 element (53).


Analysis of tetra- and hepta-nucleotides motifs promoting -1 ribosomal frameshifting in Escherichia coli.

Sharma V, Prère MF, Canal I, Firth AE, Atkins JF, Baranov PV, Fayet O - Nucleic Acids Res. (2014)

Distribution of Z_ZZ.N and X_XX.Z_ZZ.N motifs in mobile elements from the IS1 and IS3 families. These two families were selected because biologically relevant -1 frameshifting was demonstrated in both (4,10). The sequences of the IS from these 2 families (63 entries for the IS1 family and 494 for the IS3 family), obtained from the ISFinder database (October 2012), were examined for the presence of potential frameshift signals (i.e. existence of 2 overlapping ORFs, with the second being in the -1 frame relative to the first and presence of a Z_ZZ.N or X_XX.Z_ZZ.N motif in the overlap region; the Z_ZZN motifs scored in panel B are those which are not part of an X_XX.Z_ZZ.N heptamer). The relative frameshifting frequencies of the motifs found are indicated in the right-hand panels. All values were normalized relative to that of the best motif (A_AA.G or C_CC.A_AA.G), using data from Figures 3 and 4.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4066793&req=5

Figure 5: Distribution of Z_ZZ.N and X_XX.Z_ZZ.N motifs in mobile elements from the IS1 and IS3 families. These two families were selected because biologically relevant -1 frameshifting was demonstrated in both (4,10). The sequences of the IS from these 2 families (63 entries for the IS1 family and 494 for the IS3 family), obtained from the ISFinder database (October 2012), were examined for the presence of potential frameshift signals (i.e. existence of 2 overlapping ORFs, with the second being in the -1 frame relative to the first and presence of a Z_ZZ.N or X_XX.Z_ZZ.N motif in the overlap region; the Z_ZZN motifs scored in panel B are those which are not part of an X_XX.Z_ZZ.N heptamer). The relative frameshifting frequencies of the motifs found are indicated in the right-hand panels. All values were normalized relative to that of the best motif (A_AA.G or C_CC.A_AA.G), using data from Figures 3 and 4.
Mentions: From the above experimental study, we concluded that a majority of heptamers (and nearly half of the tetramers) were capable of eliciting -1 frameshifting at substantial levels (at least twice the background level). To determine the range of motifs used in genes utilizing frameshifting for their expression, we carried out an analysis of IS mobile genetics elements known, or suspected, to use this mode of translational control. We focused on the members of the IS1 and IS3 families available in the ISFinder database in October 2012 (9). As shown in Figure 5, both tetramers and heptamers are found, but with a marked preference for heptamers (87 against 403). Among the five tetramers, the three most shift-prone motifs, A_AA.G and U_UU.[U,C], predominate and the less efficient A_AA.A motif is also well represented. Only 16 different heptamers are found with 72% of them being either A_AA.A_AA.G or A_AA.A_AA.A. The next most frequent are A_AA.A_AA.C and G_GG.A_AA.C, both of low efficiency, followed by the more efficient G_GG.A_AA.G, U_UU.U_UU.C and G_GG.A_AA.A. To conclude, it appears that genes known or suspected to use PRF-1 to express a biologically important protein do not necessarily utilize high efficiency motifs. However, this conclusion is based on one category of genes where two overlapping genes code for the proteins required for transposition of two types of IS elements. There, the purpose of frameshifting is to provide the ‘right’ amount of a fusion protein which has the transposase function (18,52); this amount is what keeps transposition of the IS at a level without negative effect on the bacterial host. If the ‘right’ amount is a low amount, then the use of low-efficiency motifs, with or without flanking stimulators, is a way to achieve this goal as illustrated by the IS1 element (53).

Bottom Line: Depending on the signal, the frameshifting frequency can vary over a wide range, from less than 1% to more than 50%.While motif efficiency varies widely, a major distinctive rule of bacterial -1 frameshifting is that the most efficient motifs are those allowing cognate re-pairing of the A site tRNA from ZZN to ZZZ.The outcome of the genomic search is a set of 69 gene clusters, 59 of which constitute new candidates for functional utilization of -1 frameshifting.

View Article: PubMed Central - PubMed

Affiliation: School of Biochemistry and Cell biology, University College Cork, Cork, Ireland.

Show MeSH
Related in: MedlinePlus