Programmed Ribosomal −1 Frameshifting as a Tradition: The Bacterial Transposable Elements of the IS3 Family

  • Olivier Fayet
  • Marie-Françoise Prère
Part of the Nucleic Acids and Molecular Biology book series (NUCLEIC, volume 24)


Insertion sequences (ISs) are small ubiquitous DNA transposable elements coding for one or two proteins that are found in the genome of most bacteria where they play an important role in genetic plasticity. Based on protein similarity, the ISs were grouped in 19 families, the largest being the IS3 family. Interestingly, most of its 418 members possess two overlapping genes and very likely use programmed ribosomal −1 frameshifting (PRF-1) to generate their transposase, the protein required for transposition, as was experimentally demonstrated for a few (e.g., IS3, IS150, IS911, IS3411). A systematic comparison of the IS3 family members was carried out to reveal the main features of the frameshift-programming signals present in their mRNA. The mandatory component is a short sequence where the shift from frame 0 to frame −1 occurs (Z-ZZN or more frequently X-XXZ-ZZN, the 0 frame codons are underlined). In the IS, there is a clear preference for the A-AA[A/G] and U-UU[U/C] tetramers (20%), and for the A-AAA-AA[A/G] heptamers (55%). The slippery motif is accompanied in 87% of the cases by one or two stimulatory elements. Like in eukaryotic viruses, it can be a structure formed by folding of the mRNA downstream of the motif. This is either a stem loop (60%) or a pseudoknot (13%). However, it can also be an upstream Shine–Dalgarno-like sequence (SD) that acts through pairing with 16S ribosomal RNA (in 56% of the IS). The two types of stimulators are both present in 42% of the IS and are both absent in 13% of them. Several lessons can be drawn from this comparative analysis and from more detailed analyses of frameshift signals of a few IS: (i) PRF-1 is a 2 (and perhaps 3) tRNA story and if ISs use a restricted set of frameshift motifs it is because prokaryotic ribosomes are less tolerant to near-cognate tRNA pairing than eukaryotic ribosomes. (ii) ISs have more flexibility in the design of their frameshift regions (use of 0, 1, or 2 stimulators) than eukaryotic viruses. (iii) The nucleotides immediately 3 to the slippery motif modulate frameshifting and thus must play a role in frame maintenance possibly through yet to identify interactions with the ribosome.


Insertion Sequence Infectious Bronchitis Virus Stem Loop Site Codon Prokaryotic Ribosome 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The help of Mick Chandler and Patricia Siguier with the IS database has been greatly appreciated. This work was funded by the Centre National de la Recherche Scientifique (CNRS), the University of Toulouse, and by a grant to OF from the Agence National pour la Recherche (#ANR-05-BLAN-0048-01)


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Authors and Affiliations

  1. 1.Laboratoire de Microbiologie et Génétique MoléculairesUniversité de ToulouseToulouseFrance
  2. 2.Laboratoire de Microbiologie et Génétique MoléculairesCentre national de la Recherche Scientifique, UMR5100ToulouseFrance

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