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J. Biol. Chem., Vol. 283, Issue 29, 20421-20432, July 18, 2008

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Apical Loop-Internal Loop RNA Pseudoknots

A NEW TYPE OF STIMULATOR OF-1 TRANSLATIONAL FRAMESHIFTING IN BACTERIA^*

From the Laboratoire de Microbiologie et Génétique Moléculaire, UMR5100, Centre National de la Recherche Scientifique and Université Paul Sabatier, 118 route de Narbonne, 31062 Toulouse cedex 9, France

Nearly all members of a widespread family of bacterial transposable elements related to insertion sequence 3 (IS3), therefore called the IS3 family, very likely use programmed -1 ribosomal frameshifting to produce their transposase, a protein required for mobility. Comparative analysis of the potential frameshift signals in this family suggested that most of the insertion sequences from the IS51 group contain in their mRNA an elaborate pseudoknot that could act as a recoding stimulator. It results from a specific intramolecular interaction between an apical loop and an internal loop from two stem-loop structures. Directed mutagenesis, chemical probing, and gel mobility assays of the frameshift region of one element from the IS51 group, IS3411, provided clear evidences of the existence of the predicted structure. Modeling was used to generate a three-dimensional molecular representation of the apical loop-internal loop complex. We could demonstrate that mutations affecting the stability of the structure reduce both frameshifting and transposition, thus establishing the biological importance of this new type of RNA structure for the control of transposition level.

Received for publication, April 14, 2008 , and in revised form, May 8, 2008.

^* This work was supported by Research Grant NT05-1_44848 from the Agence National de la Recherche (Programme Blanc) and by funds from the Centre National de la Recherche Scientifique and the Université Paul Sabatier of Toulouse. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental text, Table S1, and Figs. S1-S3.

¹ These authors contributed equally to this work.

² Present address: IFR QUASAV 149, Laboratoire RCIM UPRES EA 2647/USC INRA, UFR Sciences, Université d'Angers, 2 boulevard Lavoisier, 49045 Angers cedex, France.

³ To whom correspondence should be addressed: Université Paul Sabatier, CNRS UMR5100, bat. IBCG, 118 route de Narbonne, 31062 Toulouse Cedex 9, France. Tel.: 33-5-6133-5875; Fax: 33-5-6133-5886; E-mail: Olivier.Fayet{at}ibcg.biotoul.fr.

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