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J. Biol. Chem., Vol. 279, Issue 52, 54193-54201, December 24, 2004

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SsrA Tagging of Escherichia coli SecM at Its Translation Arrest Sequence^*

Justine Collier, Chantal Bohn, and Philippe Bouloc

From the Laboratoire des Réseaux de Régulations et Biogenèse de l'Enveloppe Bactérienne, Institut de Génétique et Microbiologie, Université Paris-Sud, CNRS, UMR8621, Btiment 400, F-91405 Orsay Cedex, France

SecM is expressed from the secM-secA operon and activates the expression of secA in response to secretion defects. The 3'-end of secM encodes an "arrest sequence," which can interact with the ribosomal exit tunnel, preventing complete secM translation under secretion-defective conditions. In a cis-acting manner, ribosome stalling enhances secA translation. Pro¹⁶⁶ is the last residue incorporated when SecM elongation is arrested. We report that secretion deficiencies lead to SsrA tagging of SecM after Pro¹⁶⁶, Gly¹⁶⁵, and likely Arg¹⁶³. Northern blot analysis revealed the presence of a truncated secM transcript, likely issued from a secM-secA cleavage. The level of secM transcripts was decreased either when secM translation was totally prevented or when Pro¹⁶⁶ was mutated. However, the accumulation of a truncated secM transcript required secM translation and was prevented when the SecM arrest sequence was inactivated by a point mutation changing Pro¹⁶⁶ to Ala. We suggest that ribosome pausing at the site encoding the arrest sequence is required for formation of the truncated secM mRNA. SsrA tagging affected neither the presence of the secM mRNA nor secA expression, even under translocation-defective conditions. It is therefore likely that SsrA tagging of SecM occurs only after cleavage of secM-secA mRNA within the secM open reading frame encoding the SecM arrest sequence. Accumulation of transcripts expressing arrested SecM generated growth inhibition that was alleviated by the SsrA tagging system. Therefore, SsrA tagging of SecM would rescue ribosomes to avoid excessive jamming of the translation apparatus on stop-less secM mRNA.

Received for publication, December 22, 2003 , and in revised form, October 18, 2004.

^* This work was supported in part by Actions Concertées Incitatives Microbiologie Grant MIC 0324 and by Direction Générale de l'Armement Grant CR251090. 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.

Supported by a grant from the Fondation pour la Recherche Médicale. To whom correspondence may be addressed: Dept. of Developmental Biology, Beckman Center, Stanford University School of Medicine, Stanford, CA 94305. Tel.: 650-725-7678; Fax: 650-725-7739; E-mail: justinec{at}stanford.edu. To whom correspondence may be addressed. Tel.: 33-1-6915-7016; Fax: 33-1-6915-6678; E-mail: bouloc{at}infobiogen.fr.

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