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J. Biol. Chem., Vol. 280, Issue 12, 11902-11910, March 25, 2005

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Proline Metabolism in Procyclic Trypanosoma brucei Is Down-regulated in the Presence of Glucose^*

Nadia Lamour, Loïc Rivière¶||, Virginie Coustou¶||, Graham H. Coombs, Michael P. Barrett**, and Frédéric Bringaud¶||

From the Institute of Biomedical and Life Sciences, Division of Infection & Immunity, University of Glasgow, Glasgow G12 8QQ, United Kingdom and the ^¶Laboratoire de Génomique Fonctionnelle des Trypanosomatides, UMR-5162 CNRS, Université Victor Segalen Bordeaux 2, 33076 Bordeaux Cedex, France

Proline metabolism has been studied in procyclic form Trypanosoma brucei. These parasites consume six times more proline from the medium when glucose is in limiting supply than when this carbohydrate is present as an abundant energy source. The sensitivity of procyclic T. brucei to oligomycin increases by three orders of magnitude when the parasites are obliged to catabolize proline in medium depleted in glucose. This indicates that oxidative phosphorylation is far more important to energy metabolism in this latter case than when glucose is available and the energy needs of the parasite can be fulfilled by substrate level phosphorylation alone. A gene encoding proline dehydrogenase, the first enzyme of the proline catabolic pathway, was cloned. RNA interference studies revealed the loss of this activity to be conditionally lethal. Proline dehydrogenase defective parasites grew as wild-type when glucose was available, but, unlike wild-type cells, they failed to proliferate using proline. In parasites grown in the presence of glucose, proline dehydrogenase activity was markedly lower than when glucose was absent from the medium. Proline uptake too was shown to be diminished when glucose was abundant in the growth medium. Wild-type cells were sensitive to 2-deoxy-D-glucose if grown using proline as the principal carbon source, but not in glucose-rich medium, indicating that this non-catabolizable glucose analogue might also stimulate repression of proline utilization. These results indicate that the ability of trypanosomes to use proline as an energy source can be regulated depending upon the availability of glucose.

Received for publication, December 20, 2004 , and in revised form, January 21, 2005.

^* 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 University of Glasgow studentship.

^|| These authors were supported by the CNRS, the Conseil Régional d'Aquitaine, the Ministère de l'Education Nationale de la Recherche et de la Technologie (Action Microbiologie), and the European Commission (INCO-DEV program, ICA4CT-2001-10075).

^** To whom correspondence may be addressed. Tel./Fax: 44-141-330-6904; E-mail: m.barrett{at}bio.gla.ac.uk.

To whom correspondence may be addressed. Tel.: 33-5-57-57-46-32; Fax: 33-5-57-57-4804; E-mail: bringaud{at}u-bordeaux2.fr.

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