[Cancer Research 60, 4752-4755, September 1, 2000]
© 2000 American Association for Cancer Research
XAGE-1, A New Gene That Is Frequently Expressed in Ewing’s Sarcoma1
Xiu Fen Liu,
Lee J. Helman,
Choy Yeung,
Tapan K. Bera,
Byungkook Lee and
Ira Pastan2
Laboratory of Molecular Biology, Division of Basic Sciences, NIH, National Cancer Institute, Bethesda, Maryland 20892-4255 [X. F. L., T. K. B., B. L., I. P.], and Pediatric Oncology Branch, Division of Clinical Sciences, National Cancer Institute, Bethesda, Maryland 20892 [L. J. H., C. Y.]
 |
ABSTRACT
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Our previous expressed sequence tag database analysis indicates that
XAGE-1 is frequently found in Ewing’s sarcoma and
alveolar rhabdomyosarcoma (U. Brinkmann et al., Cancer
Res., 59: 1445–1448, 1999). Using Northern blots
and RNA dot blots, we have now found that XAGE-1 is
highly expressed in normal testis, in seven of eight Ewing’s cell
lines, in four of nine Ewing’s sarcoma patient samples, and in one of
one alveolar rhabdomyosarcoma patient sample. The gene is located on
the X chromosome. The full-length cDNA contains 611 bp and predicts a
protein of Mr 16,300 with a potential
transmembrane domain at the NH2 terminus.
XAGE-1 shares homology with GAGE/PAGE proteins in the
COOH-terminal end. These findings could be valuable for cancer
diagnosis and cancer immunotherapy.
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Introduction
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Large numbers of
ESTs3
have been cloned from various tissues and cancers (1
, 2)
. Each cDNA clone or EST sequence is generated from a
single transcript. The frequency and distribution of the many different
transcripts in a given tissue depends on the level of gene expression.
Therefore, a particular gene expression pattern can be frequently
predicted by analysis of the frequency and specificity of various EST
sequences. We previously reported a computer screening strategy that
identified genes that are preferentially expressed in prostate or
prostate tumors (3, 4, 5)
. From this screen, numerous genes
were identified including a novel gene, PAGE4 (previously
named PAGE1) (6)
, and a set of XAGE
genes (7)
, which are related to the GAGE/MAGE family of
melanoma associated CT antigens.
CT antigens are a distinct class of differentiation antigens that have
a restricted pattern of expression in normal tissues
(8, 9, 10)
. CT antigens are currently viewed as attractive
candidates for cancer vaccines. Some thoroughly studied CT antigens are
MAGE, BAGE, GAGE, and LAGE/NY-ESO-1 (9, 10, 11, 12, 13, 14, 15, 16, 17)
. These genes
are primarily expressed in the primitive germ cells, spermatogonia, in
the normal testis. Malignant transformation is often associated with
activation or derepression of silent CT genes, and this results in the
expression of CT antigens in a variable proportion of a wide range of
human tumors. Recently, several additional members were added to the CT
antigen family. These include various PAGEs, PRAME, SSX, SCP-1, CT7,
MAGEC1, and MAGED1 (6
, 11
, 18, 19, 20, 21, 22)
. Identification of new
CT antigens or new family members is still being actively pursued in
the cancer research field.
Previously, we identified three related genes that we termed
XAGEs by homology walking using the dbEST database
(7)
. ESTs of the XAGE group were found in cDNA
libraries from testis, Ewing’s sarcoma, alveolar rhabdomyosarcoma,
fetal tissues, and germ cell tumors by database analysis. In this
study, we describe the isolation of a full-length cDNA of
XAGE-1 and analysis of the expression of the
XAGE-1 gene. We found that the gene is highly expressed in
normal testis, with aberrant expression in sarcomas of various types.
Although XAGE-1 did not show overall homology with any polypeptide
recorded in the data bank, it has strong homology with members of
GAGE/PAGE family in the COOH terminus of the predicted protein,
indicating that XAGE-1 belongs to a new family of CT antigens.
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Materials and Methods
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Tissues and Cell Lines.
Ewing’s tumor tissue was obtained from frozen specimens obtained from
patients treated at the National Cancer Institute. Rhabdomyosarcoma
tumor tissue was obtained from the Cooperative Human Tissue Network,
Children’s Cancer Group. All alveolar rhabdomyosarcoma tumor
specimens were found to express the PAX-3-FKHR fusion transcript by
RT-PCR.4
Osteosarcoma cell lines were obtained from the American Type Culture
Collection. Ewing’s sarcoma cell lines RD-ES, TC-32, TC-71, and 5838
have been described previously, and all contain EWS-FLI-1 fusion
transcripts (23)
.4
LD, LG, JM, and
SB are cell lines established in our laboratories (by
L. J. H.) directly from tumor specimens. The cell line JM does
not express an EWS-ETS fusion transcript.
Northern Blots and RNA Dot Blot.
RNA was extracted either from tumor tissue using Trizol (Life
Technologies, Inc.) or from cell lines using RNAeasy (Qiagen). Total
RNA (20 µg) was used for Northern blot analysis of sarcoma tumors.
The multiple tissue mRNA dot blot and the normal tissue Northern blot
were purchased from Clontech (Palo Alto, CA). The 450-bp probe used for
hybridization was generated from EST clone af89d01.s1 by digestion with
EcoRI and NotI. The hybridization was conducted
as follows: the RNA-containing membranes were blocked for 3 h at
45°C in hybridization solution. Probes labeled with
32P either by random primer extension or by end
labeling (Lofstrand Labs Limited) were added to the membrane and
hybridized for 15 h at 45°C. Membranes were washed twice with
2x SSC/0.1% SDS at room temperature and twice with 0.1x SSC/0.1%
SDS at 65°C. The membranes were exposed to X-ray film for 1–2 days
before development
The Southern blot of human chromosomes (Oncor, Gaithersburg, MD) was
conducted using the same probe and the same hybridization conditions
used for Northern blot.
RT-PCR was performed on cDNA from 24 different human tissues using
human rapid-scan gene expression panels (Origene, Inc., Rockville, MD).
The thermocycling protocol was initial denaturation at 94°C for 3 min
and 35 cycles of denaturation at 94°C for 1 min, annealing at 65°C
for 1 min, and elongation at 72°C for 3 min. The PCR reactions were
analyzed on agarose gels, and specific products were cloned into TA
vectors (Invitrogen) and sequenced on an automated capillary sequencer
using Perkin-Elmer’s dRhodamine terminator cycle sequencing kit
(Perkin-Elmer Applied System).
The primers used were as follows: (a) xa-1,
5'-CAGCTTGTCTTCATTTAAACTTGTGGTTGC-3'; (b) xa-2,
5'-TCCCAGGAGCCCAGTAATGGAGA-3'; (c) xa-8,
5'-ACCTGGGAAGGAGCATAGGA-3'; and (d) xa-10,
5'-CTTTATTGAGATAGTTTAAGTCAAATATCTAA-3'. The oligonucleotides were
synthesized by Sigma-Genosys.
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Results
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Restricted Expression in Normal Tissues.
To determine the relative expression of XAGE-1 mRNA in
different tissues and tumors, we first conducted a mRNA dot blot
(Clontech) analysis using a full insert of EST af89d01.s1 as a
labeling probe. Among the 61 different samples of normal tissues and 7
fetal tissues including lung, brain, liver, heart, and spleen, the
expression of XAGE-1 was detected only in testis (Fig. 1A)
. This result indicates that XAGE-1, like other
CT antigens, is present in testis.
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Fig. 1. Specific expression of XAGE-1.
A, RNA dot blot hybridization. Human multiple tissue
master blot with 76 tissue-specific poly(A) RNA (Clontech) were
hybridized with XAGE-specific probe. A1, whole
brain; B1, cerebral cortex; C1, frontal
lobe; D1, parietal lobe; E1, occipital
lobe; F1, temporal lobe; G1, p.g.
of cerebral cortex; H1, pons; A2,
cerebellum left; B2, cerebellum right;
C2, corpus callosum; D2, amygdala;
E2, caudate nucleus; F2, hippocampus;
G2, medulla oblongata; H2, putamen;
A3, substantia; B3, nucleus accumbens;
C3, thalamus; D3, pituitary gland;
E3, spinal cord; A4, heart;
B4, aorta; C4, atrium left;
D4, atrium right; E4, ventricle left,
F4, ventricle right; G4, interventricular
septum; H4, apex of the heart; A5,
esophagus; B5, stomach; C5, duodenum;
D5, jejunum; E5, ileum;
F5, ileoceum; G5, appendix;
H5, colon ascending; A6, colon
transverse; B6, colon descending; C6,
colon rectum; A7, kidney; B7, skeletal
muscle; C7, spleen; D7, thymus;
E7, PBLs; F7, lymph node;
G7, bone marrow; H7, trachea;
A8, lung; B8, placenta;
C8, bladder; D8, uterus;
E8, prostate; F8, testis;
G8, ovary; A9, liver; B9,
pancreas; C9, adrenal gland; D9, thyroid,
gland; E9, salivary gland; F9, mammary
gland. B, RT-PCR analysis. Twenty-four different
sources of cDNA (Origene) were amplified by using primers xa-1 and xa-2
under the conditions described in "Materials and Methods." After
the PCR cycles, 5 µl of 25 µl of the high-concentration (1000x)
reactions were analyzed in agarose gel and visualized by staining with
ethidium bromide. C, four different concentrations from
lung, testis, and PBLs amplified in A were run together
to compare the relative level of XAGE-1expression.
F3–H3, D6–H6, H8, G9, and
H9 are empty.
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To verify the specificity of XAGE-1 expression, we conducted
a RT-PCR analysis by using the human rapid-scan panel with primers xa-1
and xa-2. We detected a 275-bp fragment in testis among the 24
different tissues analyzed (Fig. 1B)
. Unexpectedly, the
275-bp fragment was also present at lower amounts in normal lung and
PBLs. Extremely weak expression of XAGE-1 was detected in
bone marrow, spleen, and skin. To compare the relative level of
XAGE-1 in testis, lung, and PBLs, different dilutions of
cDNA were analyzed in the same rapid-scan panel as shown in Fig. 1C
. The mRNA present in testis was about 10–100 times
higher than that in the lung and more than 100 times higher than that
in PBLs.
Because XAGE-1 is highly abundant in testis and is expressed
at a low level in lung and PBLs, we attempted to determine the
transcript size in these different tissues. Northern blot analysis was
conducted using the same probe used for the RNA dot blot. As shown in
Fig. 2A
, a single band of 700 bp was revealed in the testis.
However, no signal was detected in lung and PBLs. This result is
probably due to the low level of XAGE-1 expression in lung
and PBLs because the Northern blot analysis is much less sensitive than
RT-PCR in detecting the expression of XAGE-1. These results
are consistent with the RNA dot blot analysis described above (Fig. 1A)
.
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Fig. 2. Northern blot analysis of the XAGE-1 gene.
A, Northern blot (Clontech) of 16 different normal
tissues probed separately with xage-1 and actin probe.
B, the expression of XAGE-1 in Ewing’s
sarcoma cell lines (left panel) and osteosarcoma cell
lines (right panel). C, the expression of
XAGE-1 in patient tumor samples. Lanes
1–9, Ewing’s sarcoma patients; Lane
10, normal muscle; Lane
11, alveolar rhabdomyosarcoma; Lane
12, fetal muscle; Lanes
13–15, embryonal rhabdomyosarcoma. Total RNA was probed
separately with xage-1 probe and actin probe.
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XAGE-1 Expression in Ewing’s Sarcoma,
Rhabdomyosarcoma, and Osteosarcoma.
Analysis of the EST database predicts that XAGE-1 is
present in Ewing’s sarcoma and alveolar rhabdomyosarcoma. To confirm
the database prediction experimentally, we first determined whether
XAGE-1 was present in the various Ewing’s cell lines by
Northern blot analysis. A single band of 700 bp was detected in seven
of eight cell lines (Fig. 2B)
. XAGE-1 was not
expressed in cell line JM, which is a mouse xenograft tumor derived
from a Ewing’s sarcoma that has lost the chromosome translocation
t(11;22).4 Cell line 5838 had an extra
band with a size of 1.2 kb. This band might be due to alternate
splicing or use of an alternate polyadenalytion signal in the
XAGE-1 gene. XAGE-1 was present in two of five
osteosarcoma cell lines, with the SAOS cell line showing relatively low
XAGE-1 expression (Fig. 2B)
.
To address whether XAGE-1 was present in human patient
samples, we conducted a Northern blot hybridization analysis. Of nine
patients with Ewing’s sarcoma, four (patients 5–8) expressed
XAGE-1 with a single 700-bp band (Fig. 2C)
.
Patients 1 and 5–9 expressed the EWS-FLI-1 transcript, an
indication of chromosome translocation (Ref. 24
; data not
shown). We noticed that XAGE-1 was not expressed in all of
the patient samples with the chromosome translocation. However, samples
that did not express either an EWS-FLI-1 or an
EWS-ERG fusion transcript also did not express
XAGE-1 (Fig. 2
C, Lanes 2–4). The correlation
between the absence of XAGE-1 expression and the absence of
chromosome translocation needs further study. XAGE-1 was
also expressed in one of one patient sample with alveolar
rhabdomyosarcoma and in one of three patient samples of embryonal
rhabdomyosarcoma but not in the normal controls (Fig. 2C)
. Together, these data indicate that
XAGE-1 is expressed in nearly half of the sarcoma patient
samples.
Chromosome Localization of XAGE-1.
Most of the CT antigens are localized on the X chromosome, with the
exception of SCP-1, which is located on chromosome 1 (8
, 20) . To find where XAGE-1 is localized, Southern blot
hybridization was performed on a human chromosome blot using the same
probe used for dot blot and Northern blot. We detected only one strong
band on the X chromosome, and no other cross-hybridizing bands were
found on the blot (data not shown). This result indicates that the
XAGE-1 gene is located on the X chromosome and that there is
not a very strong homology with the other predicted XAGE
members, XAGE-2 and XAGE-3, because under
stringent hybridization conditions, XAGE-2 and
XAGE-3 were not detected.
Full-length cDNA of XAGE-1 and Putative Peptide
Sequences.
To obtain the full-length XAGE-1 cDNA sequence, rapid
amplification of cDNA ends-PCR was performed using primers localized in
the EST contig and total RNA from Ewing’s sarcoma cell line TC-71. The
longest rapid amplification of cDNA ends product contains an additional
184 nucleotides at the 5' end compared with the EST contig sequence.
The correct cDNA sequence was confirmed by sequencing the PCR product
from primers xa-8 and xa-10. The XAGE-1 cDNA is 611 bp in
length, excluding the poly(A) tail, and contains 438 nucleotides
in the coding region, flanked by 85 bp in the 5'-untranslated region
and 88 bp in the 3'-untranslated region (Fig. 3A)
.
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Fig. 3. Sequence of XAGE-1. A, the
nucleotide and amino acid sequence of XAGE-1. The polyadenylation
signal is italicized and bold. The
translational stop codons are indicated in bold. Primers
are showed by arrows. B, Hoop/Woods
hydrophilicity plot. A potential membrane-spanning region was noticed
in the NH2-terminal end.
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The longest open reading frame indicates that the putative XAGE-1
protein consists of 146 amino acid residues with a molecular weight of
16,300. Hydrophilicity analysis (Fig. 3B)
indicates a
hydrophobic sequence in the NH2-terminal end,
suggesting the possibility of a transmembrane domain. Analysis of the
protein sequence reveals no possible posttranslational modifications by
searching GCG Lite. This putative protein did not show overall
sequence homology with any peptide recorded in the data banks. However,
alignment of the amino acid sequence of XAGE-1 with PAGE4
(6)
and PAGE1 [Ref. 25
(renamed GAGE9; Ref.
15
)] reveals a striking homology in the
COOH-terminal end of these proteins (Fig. 4)
, suggesting that XAGE-1 encodes a distinct protein that
could share structural or functional features with other GAGE/PAGE
family members.
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Discussion
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XAGE-1 is a human X-linked gene that is strongly
expressed in normal testis, Ewing’s sarcoma, and alveolar
rhabdomyosarcoma. It is also expressed in normal lung and PBLs, but at
much lower levels. XAGE-1 expression in lung and lymphocytes
was not predicted by EST database analysis, probably because of its
weak expression and the small size of lung and PBL libraries. The
expression pattern of XAGE-1 in Ewing’s sarcoma, lung,
PBLs, and bone marrow is interesting. At present, it is unclear in
which cell type Ewing’s sarcoma originates and why it metastasizes to
the lung. The high level of XAGE-1 expression in many
Ewing’s sarcomas suggests that the tumor could arise in cells in the
bone or bone marrow that normally express XAGE-1 or
metastasize to the region where XAGE-1 is expressed.
Additional experiments using in situ hybridization or
immunohistochemistry should provide information about this possible
relationship.
Until now, there has been no report on the expression of CT antigens in
Ewing’s sarcoma and alveolar rhabdomyosarcoma. We found
XAGE-1 expressed in seven of eight Ewing’s sarcoma cell
lines, 44% (four of nine) of Ewing’s sarcoma tumor specimens, and one
of one alveolar rhabdomyosarcoma tumor sample. We are currently
screening the expression of XAGE-1 in other tumor cell
types. Our preliminary data indicate that the XAGE-1 gene is
activated in many tumor cell lines and other tumor types. Studies on
the XAGE-1 gene may provide more information on this cancer
antigen family that may be of use in the diagnosis or immunotherapy of
cancer.
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ACKNOWLEDGMENTS
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We thank Drs. C. Wolfgang and K. Egland for critical reading of
the manuscript. We also thank R. Mann for editorial assistance.
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FOOTNOTES
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The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
1 Supported in part by the Children’s Cancer
Group/Cooperative Human Tissue Network, which is funded by the National
Cancer Institute. 
2 To whom requests for reprints should be
addressed, at Laboratory of Molecular Biology, Division of Basic
Sciences, NIH, National Cancer Institute, Building 37, Room 4E16, 37
Convent Drive 4255, Bethesda, MD 20892-4255. Phone: (301) 496-4797;
Fax: (301) 402-1344; E-mail: pasta{at}helix.nih.gov
3 The abbreviations used are: EST, expressed
sequence tag; CT, cancer-testis; RT-PCR, reverse transcription-PCR;
PBL, peripheral blood leukocyte.
4 Unpublished observations.
Received 4/11/00.
Accepted 7/19/00.
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G. Cronwright, K. Le Blanc, C. Gotherstrom, P. Darcy, M. Ehnman, and B. Brodin
Cancer/Testis Antigen Expression in Human Mesenchymal Stem Cells: Down-regulation of SSX Impairs Cell Migration and Matrix Metalloproteinase 2 Expression
Cancer Res.,
March 15, 2005;
65(6):
2207 - 2215.
[Abstract]
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K. A. Egland, V. Kumar, P. Duray, and I. Pastan
Characterization of Overlapping XAGE-1 Transcripts Encoding a Cancer Testis Antigen Expressed in Lung, Breast, and Other Types of Cancers
Mol. Cancer Ther.,
May 1, 2002;
1(7):
441 - 450.
[Abstract]
[Full Text]
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ABSTRACT
Introduction
