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Volume 272, Number 25, Issue of June 20, 1997 pp. 15849-15855
©1997 by The American Society for Biochemistry and Molecular Biology, Inc.

Dynamic Compartmentation of Vacuolar Amino Acids in Penicillium cyclopium
CYTOSOLIC ADENYLATES ACT AS A CONTROL SIGNAL FOR EFFLUX INTO THE CYTOSOL

(Received for publication, December 18, 1996, and in revised form, April 1, 1997)

From the Martin-Luther-University Halle, College of Pharmacy, Department of Cell Physiology, 06120 Halle, Federal Republic of Germany

The regulation of amino acid transport from the vacuolar reservoir into the cytoplasm has been studied in hyphal cells of Penicillium cyclopium. To avoid artifacts caused by the isolation of vacuoles, efflux was examined "in situ," i.e. in cells whose plasma membranes were permeabilized for micromolecules by a treatment with nystatin. The ATP-dependent proton gradient and amino acid transport activities at the vacuolar membrane remained intact under these conditions. Accumulation of amino acids in the vacuole proved to be the result of a dynamic equilibrium of active, ATP-dependent uptake and energy-independent efflux. The latter was strongly accelerated after the vacuolar amino acid content had surpassed a threshold level.

Efflux of vacuolar amino acids was specifically controlled by extravacuolar adenylates: ATP, 5-adenylyl imidodiphosphate (an ATPase-resistant ATP-analogue), ADP, or AMP caused a strong inhibition in the concentration range around 200 µmol/liter, whereas both lower and higher concentrations allowed significant efflux rates. Estimates of the cytosolic adenylates (which consisted mainly of ATP) were close to 2 mmol/liter in glucose-metabolizing cells, which concentration allowed maximum rates of both vacuolar uptake and efflux. During 24 h of carbon and nitrogen starvation, the adenylate level decreased toward the efflux-inhibiting region around 200 µmol/liter, whereas 3-4 d of carbon and nitrogen starvation caused a further decline of the adenylate content, leading again to efflux-permitting concentrations. Thus, the cytosolic adenylate pool appears to effectively control the availability of vacuolar amino acids for the cellular metabolism.

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