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J. Biol. Chem., Vol. 278, Issue 31, 28787-28792, August 1, 2003

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Involvement of a Mate Chaperone (TorD) in the Maturation Pathway of Molybdoenzyme TorA^*

Marianne Ilbert , Vincent Méjean, Marie-Thérèse Giudici-Orticoni , Jean-Pierre Samama ¶ and Chantal Iobbi-Nivol ||

From the Laboratoire de Chimie Bactérienne and Laboratoire de Bioénergétique et Ingénierie des Protéines, Institut de Biologie Structurale et Microbiologie, CNRS, 31, chemin Joseph Aiguier, 13402 Marseille Cedex 20, France and ^¶Département de Biologie et de Génomique Structurales, Institut de Génétique et de Biologie Moléculaire et Cellulaire, BP 10142, 1, rue Laurent Fries, 67404 Illkirch, France

As many prokaryotic molybdoenzymes, the trimethylamine oxide reductase (TorA) of Escherichia coli requires the insertion of a bis(molybdopterin guanine dinucleotide)molybdenum cofactor in its catalytic site to be active and translocated to the periplasm. We show in vitro that the purified apo form of TorA was activated weakly when an appropriate bis(molybdopterin guanine dinucleotide)molybdenum source was provided, whereas addition of the TorD chaperone increased apoTorA activation up to 4-fold, allowing maturation of most of the apoprotein. We demonstrate that TorD alone is sufficient for the efficient activation of apoTorA by performing a minimal in vitro assay containing only the components for the cofactor synthesis, apoTorA and TorD. Interestingly, incubation of apoTorA with TorD before cofactor addition led to a significant increase of apoTorA activation, suggesting that TorD acts on apoTorA before cofactor insertion. This result is consistent with the fact that TorD binds to apoTorA and probably modifies its conformation in the absence of cofactor. Therefore, we propose that TorD is involved in the first step of TorA maturation to make it competent to receive the cofactor.

Received for publication, March 18, 2003 , and in revised form, May 5, 2003.

^* This work was supported by grants from the CNRS and the Université de la Méditerranée. 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 Ministère del'Education nationale, de la Recherche et de la Technologie fellowship.

^|| To whom correspondence should be addressed. Tel.: 33-4-91-16-44-27; Fax: 33-4-91-71-89-14; E-mail iobbi{at}ibsm.cnrs-mrs.fr.

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