LETTERS
High-density array comparative genomic hybridization (CGH)
1
showed amplification of chromosome 1q22 centered on the
RAB25 small GTPase
2
, which is implicated in apical vesicle
trafficking
3
, in approximately half of ovarian and breast
cancers. RAB25 mRNA levels were selectively increased in
stage III and IV serous epithelial ovarian cancers compared to
other genes within the amplified region, implicating RAB25 as
a driving event in the development of the amplicon. Increased
DNA copy number or RNA level of RAB25 was associated with
markedly decreased disease-free survival or overall survival in
ovarian and breast cancers, respectively. Forced expression of
RAB25 markedly increased anchorage-dependent and
anchorage-independent cell proliferation, prevented apoptosis
and anoikis, including that induced by chemotherapy, and
increased aggressiveness of cancer cells in vivo. The inhibition
of apoptosis was associated with a decrease in expression of
the proapoptotic molecules, BAK and BAX, and activation of
the antiapoptotic phosphatidylinositol 3 kinase (PI3K) and
AKT pathway, providing potential mechanisms for the effects
of RAB25 on tumor aggressiveness. Overall, these studies
implicate RAB25, and thus the RAB family of small G
proteins, in aggressiveness of epithelial cancers.
Ovarian cancer remains the fifth most frequent cause of cancer death
in women. An improved understanding of the genetic aberrations in
ovarian cancer may identify new etiologic, prognostic or therapeutic
targets that can improve patient management. Several genes located
at sites of DNA copy number aberrations in ovarian cancer, including
PIK3CA
4
, ERBB2 (ref. 5), MYC
6
, EEF1A2 (ref. 7), AKT2 (ref. 8) and
NCOA3 (ref. 9), have been implicated in the pathophysiology of ovar-
ian cancer. Importantly, chromosome CGH analyses reveal other
regions of recurrent abnormality in ovarian cancer, which may
encode additional genes contributing to tumor behavior
10–12
. In par-
ticular, chromosome 1q is frequently increased in copy number in
ovarian
11,12
and breast
13
cancers and Wilms
14
tumors; a high relapse
rate in invasive ductal breast carcinomas
13
and Wilms tumors
14
are
associated with increased DNA copy number on chromosome 1q, but
the driver of the regional copy number increase at 1q has not been
identified.
Using array CGH
1
to more precisely define region(s) of recurrent
copy number increase on chromosome 1q, we delineated an increase
(at least 1.3-fold) in DNA copy number in a 1.1-Mb region located on
chromosome 1q22 in 28 of 52 (54%) of advanced serous epithelial
ovarian cancers (Fig. 1a). Notably, ovarian cancer patients with ele-
vated 1q22 (at least 1.5 copies of RAB25) either did not enter a disease-
free state following surgery and chemotherapy or showed very short
disease-free survival, implicating gene(s) in this region as potential
oncogenes regulating the behavior of ovarian cancers (Fig. 1b).
The minimal region of copy number increase on 1q22 encompassed
the region from position 152,377,895 to 153,495,551, which contains a
total of 34 genes, including 22 known genes and 12 hypothetical pro-
teins based on the July 2003 human reference sequence. Based on
expression levels from our microarray data sets
15
, the Gene Expression
Omnibus and the Stanford Microarray Database, we eliminated 18 can-
didates that did not show a significant difference in RNA levels between
normal ovarian epithelium (NOE) and ovarian cancers. We analyzed
mRNA expression levels of the remaining 16 open reading frames
located in this region using real-time quantitative PCR to identify
potential drivers of the copy number increase at 1q22. Although mRNA
levels of several of the genes in this region were modestly elevated in a
fraction of ovarian cancers as compared to NOE or benign ovarian
tumors, RAB25 mRNA levels were markedly increased in 55 of 62
(88.7%) of ovarian cancers (P < 0.001; Fig. 1c,d). This observation was
confirmed in an independent ovarian cancer data set
16
wherein RAB25
transcript levels were increased in 35 of 44 (80%) ovarian cancer sam-
ples compared to NOE. The increase in RAB25 expression was stage
dependent, with stage III and stage IV cancers showing higher levels
(P < 0.01; Fig. 1d) than early stage cancers, suggesting a potential role of
RAB25 in tumor progression. Sequencing of the open reading frame in
8 ovarian cancer samples did not identify mutations in RAB25, suggest-
ing that mutation of RAB25 rarely or never occurs in ovarian cancer.
Linear regression analysis of 21 epithelial ovarian cancers for which
both CGH and expression levels were available showed a direct rela-
tionship between copy number and expression of RAB25 (Fig. 1e) with
1
Department of Molecular Therapeutics, University of Texas MD Anderson Cancer Center, Houston, Texas 77054, USA.
2
Lawrence Berkley National Laboratory,
Berkeley, California 94720, USA.
3
Department of Obstetrics and Gynecology, University of British Columbia, Vancouver, British Columbia V6H 3V5, Canada.
4
Department of Pathology,
6
Department of Gynecological Oncology, University of Texas MD Anderson Cancer Center, Houston, Texas, 77030, USA.
5
Department of
Obstetrics and Gynecology, University of California, San Francisco, San Francisco, California 94143, USA.
7
Department of Obstetrics and Gynecology, School of
Medicine, New York University, New York, New York 10016, USA. Correspondence should be addressed to G.B.M. (gmills@mdanderson.org).
Published online 24 October 2004; doi:10.1038/nm1125
The RAB25 small GTPase determines aggressiveness of
ovarian and breast cancers
Kwai Wa Cheng
1
, John P Lahad
1
, Wen-lin Kuo
2
, Anna Lapuk
2
, Kyosuke Yamada
2
, Nelly Auersperg
3
, Jinsong Liu
4
,
Karen Smith-McCune
5
, Karen H Lu
6
, David Fishman
7
, Joe W Gray
2
& Gordon B Mills
1
NATURE MEDICINE VOLUME 10 | NUMBER 11 | NOVEMBER 2004 1251
© 2004 Nature Publishing Group http://www.nature.com/naturemedicine