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J Biol Chem, Vol. 275, Issue 5, 3037-3041, February 4, 2000

Enkephalins Are Transported by a Novel Eukaryotic Peptide Uptake System^*

Melinda Hauser, Amy M. Donhardt, David Barnes, Fred Naider^§, and Jeffrey M. Becker^¶

From the  Department of Microbiology and Biochemistry, Molecular and Cellular Biology, University of Tennessee, Knoxville, Tennessee 37996-0845 and the ^§ Department of Chemistry, College of Staten Island, City University of New York, Staten Island, New York 10314

We have identified an oligopeptide transporter in the yeast Saccharomyces cerevisiae which mediates the uptake of tetra- and pentapeptides, including the endogenous opioids leucine enkephalin (Tyr-Gly-Gly-Phe-Leu) and methionine enkephalin (Tyr-Gly-Gly-Phe-Met). The transporter is encoded by the gene OPT1. Yeast expressing OPT1 can utilize enkephalins to satisfy amino acid auxotrophic requirements for growth. The transport of radiolabeled leucine enkephalin exhibits saturable kinetics, with a K_m of 310 µM. Transport activity is optimum at acidic pH and sensitive to reagents which uncouple oxidative phosphorylation, suggesting an energy dependence on the proton gradient. Growth, transport, and chromatographic data indicate that leucine enkephalin is not hydrolyzed in the extracellular medium and as such is translocated intact across the cell membrane. The system is specific for tetra- and pentapeptides and can be inhibited by the opioid receptor antagonists naloxone and naltrexone. To date, this is the first example of a eukaryotic transport system which can use enkephalins as a substrate, opening the possibility that a homologue exists in higher eukaryotes.

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