articles
NATURE CELL BIOLOGY VOL 3 APRIL 2001 http://cellbio.nature.com 384
Skp1 forms multiple protein
complexes, including RAVE,
a regulator of V-ATPase assembly
Jae Hong Seol*, Anna Shevchenko†, Andrej Shevchenko†‡ and Raymond J. Deshaies*§
*Division of Biology and Howard Hughes Medical Institute, California Institute of Technology, Pasadena, California 91125, USA
†Protein and Peptide Group, European Molecular Biology Laboratory, Meyerhofstrasse 1, 69012 Heidelberg, Germany
‡e-mail: shevchenko@embl-heidelberg.de
§e-mail: deshaies@its.caltech.edu
SCF ubiquitin ligases are composed of Skp1, Cdc53, Hrt1 and one member of a large family of substrate receptors
known as F-box proteins (FBPs). Here we report the identification, using sequential rounds of epitope tagging, affini-
ty purification and mass spectrometry, of 16 Skp1 and Cdc53-associated proteins in budding yeast, including all
components of SCF, 9 FBPs, Yjr033 (Rav1) and Ydr202 (Rav2). Rav1, Rav2 and Skp1 form a complex that we have
named ‘regulator of the (H
+
)-ATPase of the vacuolar and endosomal membranes’ (RAVE), which associates with the
V
1
domain of the vacuolar membrane (H
+
)-ATPase (V-ATPase). V-ATPases are conserved throughout eukaryotes, and
have been implicated in tumour metastasis and multidrug resistance, and here we show that RAVE promotes glu-
cose-triggered assembly of the V-ATPase holoenzyme. Previous systematic genome-wide two-hybrid screens yielded
17 proteins that interact with Skp1 and Cdc53, only 3 of which overlap with those reported here. Thus, our results
provide a distinct view of the interactions that link proteins into a comprehensive cellular network.
S
CF ubiquitin ligases regulate a wide range of cellular process-
es, including immunity, signalling, cell division and transcrip-
tion
1
. SCF contains four subunits — Skp1, Cdc53 (also known
as cullin 1 or Cul1), an F-box protein, and the newly discovered
RING-H2 protein Hrt1 (also known as Roc1 or Rbx1; refs 2–5). A
remarkable property of SCF ubiquitin ligases is that their specifici-
ty can be programmed through an array of distinct substrate recep-
tors
6,7
. These receptors are recruited to SCF by the conserved F-box
Control
Cdc53–Myc
9
Skp1–Myc
9
S4
S6
M
r
(K)
M
r
(K)
a b
Control
RCY1–Myc
9
YBR280–Myc
9
RAV1–Myc
9
RAV2–Myc
9
Control
RCY1–Myc
9
YBR280–Myc
9
RAV1–Myc
9
RAV2–Myc
9
Control
RCY1–Myc
9
YBR280–Myc
9
RAV1–Myc
9
RAV2–Myc
9
Anti-Skp1 Anti-Cdc53 Anti-Myc
250
98
64
50
36
30
C1
C2
C3
C4
C5
C6
250
98
64
50
36
30
16
6
S1
S2
S3
S5
S7
S8
S9
S10
S11
S12
S13
Figure 1 Identification of proteins associated with Cdc53 and Skp1. a,
Proteins immunoprecipitated with an anti-Myc antibody (9E10) from 35 mg of wild-
type, CDC53–Myc
9
and SKP1–Myc
9
cell extracts were eluted with SDS, separated
in an 8–16% gradient SDS–polyacrylamide gel and visualized by silver staining.
Specific bands present only in Cdc53–Myc
9
or Skp1–Myc
9
immunoprecipitates were
identified by mass spectrometry. b, Extracts (6 mg) from untagged control,
RCY1–Myc
9
, YBR280–Myc
9
, RAV1–Myc
9
and RAV2–Myc
9
cells were immunoprecipi-
tated with 9E10, fractionated by SDS–PAGE, and immunoblotted with antibodies
against Myc, Cdc53 or Skp1 as indicated.
© 2001 Macmillan Magazines Ltd