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J. Biol. Chem., Vol. 275, Issue 31, 23608-23614, August 4, 2000
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From the Institut Jacques Monod, CNRS-UMRC9922, Université
Paris 6 and Paris 7-Denis Diderot, 2 Place Jussieu,
75251 Paris cedex 05, France
Uracil uptake by Saccharomyces
cerevisiae is mediated by the FUR4-encoded uracil
permease. The modification of uracil permease by phosphorylation at the
plasma membrane is a key mechanism for regulating endocytosis of this
protein. This modification in turn facilitates its ubiquitination and
internalization. Following endocytosis, the permease is targeted to the
lysosome/vacuole for proteolysis. We have previously shown that uracil
permease is phosphorylated at several serine residues within a well
characterized N-terminal PEST sequence. In this report, we provide
evidence that lysine residues 38 and 41, adjacent to the PEST sequence, are the target sites for ubiquitination of the permease. Conservative substitutions at both Lys38 and Lys41 give
variant permeases that are phosphorylated but fail to internalize. The
PEST sequence contains potential phosphorylation sites conforming to
the consensus sequences for casein kinase 1. Casein kinase 1 (CK1)
protein kinases, encoded by the redundant YCKI and
YCK2 genes, are located at the plasma membrane. Either
alone supports growth, but loss of function of both is lethal. Here, we
show that in CK1-deficient cells, the permease is poorly phosphorylated and poorly ubiquitinated. Moreover, CK1 overproduction rescued the
defective endocytosis of a mutant permease in which the serine phosphoacceptors were replaced by threonine (a less effective phosphoacceptor), which suggests that Yck activity may play a direct
role in phosphorylating the permease. Permease internalization was not
greatly affected in CK1-deficient cells, despite the low level of
ubiquitination of the protein. This may be due to CK1 having a second
counteracting role in endocytosis as shown by the higher turnover of
variant permeases with unphosphorylatable versions of the PEST sequence.
Casein Kinase I-dependent Phosphorylation within a
PEST Sequence and Ubiquitination at Nearby Lysines Signal
Endocytosis of Yeast Uracil Permease*
*
This work was supported by a special grant of the CNRS
(program "Biologie Cellulaire," project no. 96105) and a grant of
the Association pour la Recherche sur le Cancer (project no. 9773).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.
To whom correspondence should be addressed. Tel.: 33 1 44 27 63 86; Fax: 33 1 44 27 59 94; E-mail: grimal@ijm.jussieu.fr.
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