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Originally published In Press as doi:10.1074/jbc.M102945200 on August 10, 2001

J. Biol. Chem., Vol. 276, Issue 47, 43949-43957, November 23, 2001
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Ubiquitin Is Required for Sorting to the Vacuole of the Yeast General Amino Acid Permease, Gap1*

Oriane SoetensDagger , Johan-Owen De CraeneDagger , and Bruno André§

From the Laboratoire de Physiologie Cellulaire, Université Libre de Bruxelles CP300, Institut de Biologie et de Médecine Moléculaires, 12 rue des Professeurs Jeneer et Brachet, 6041 Gosselies, Belgium

In yeast, ubiquitin plays a central role in proteolysis of a multitude of proteins and serves also as a signal for endocytosis of many plasma membrane proteins. We showed previously that ubiquitination of the general amino acid permease (Gap1) is essential to its endocytosis followed by vacuolar degradation. These processes occur when NH<UP><SUB>4</SUB><SUP>+</SUP></UP>, a preferential source of nitrogen, is added to cells growing on proline or urea, i.e. less favored nitrogen sources. In this study, we show that Gap1 is ubiquitinated on two lysine residues in the cytosolic N terminus (positions 9 and 16). A mutant Gap1 in which both lysines are mutated (Gap1K9K16) remains fully stable at the plasma membrane after NH<UP><SUB>4</SUB><SUP>+</SUP></UP> addition. Furthermore, each of the two lysines harbors a poly-ubiquitin chain in which ubiquitin is linked to the lysine 63 of the preceding ubiquitin. The Gap1K9 and Gap1K16 mutants, in which a single lysine is mutated, are down-regulated in response to NH<UP><SUB>4</SUB><SUP>+</SUP></UP> although more slowly. In proline-grown cells lacking Npr1, a protein kinase involved in the control of Gap1 trafficking, newly synthesized Gap1 is sorted from the Golgi to the vacuole without passing through the plasma membrane (accompanying article, De Craene, J.-O., Soetens, O., and André, B. (2001) J. Biol. Chem. 276, 43939-43948). We show here that ubiquitination of Gap1 is also required for this direct sorting to the vacuole. In an npr1Delta mutant, neosynthesized Gap1K9K16 is rerouted to and accumulates at the plasma membrane. Finally, Bul1 and Bul2, two proteins interacting with Npi1/Rsp5, are essential to ubiquitination and down-regulation of cell-surface Gap1, as well as to sorting of neosynthesized Gap1 to the vacuole, as occurs in an npr1Delta mutant. Our results reveal a novel role of ubiquitin in the control of Gap1 trafficking, i.e. direct sorting from the late secretory pathway to the vacuole. This result reinforces the growing evidence that ubiquitin plays an important role not only in internalization of plasma membrane proteins but also in their sorting in the endosomes and/or trans-Golgi.

* This work was supported by Grant FRSM 3.4602.94 from the Fund for Medical Scientific Research, Belgium and Grant 98/30-223 from the Communauté Française de Belgique (Actions de Recherches Concertées (ARC)).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Dagger These authors equally contributed to this work.

§ To whom correspondence should be addressed. E-mail: bran@ulb.ac.be.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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