[CANCER RESEARCH 48, 5342-5347, September 15, 1988]
Blood Group-related Antigens in Human Germ Cell Tumors
Robert J. Motzer, Victor E. Reuter,1 Carlos Cordon-Cardo, and George J. Bosl
Genitourinary Section, Solid Tumor Service, Department of Medicine fR. J. M., G. J. B.], and the Department of Pathology /K E. R., C. C-C.],
Memorial Sloan-Kettering Cancer Center, and the Department of Medicine, Cornell University Medical College, New York, New York 10021
ABSTRACT
With the use of immunohistochemical techniques, seven mouse mono
clonal antibodies and the lectin from Ulex europaeus, detecting blood
group antigens of the ABH and Lewis systems, have been used to define
the distribution of these antigenic structures in germ cell tumors. The
reagents used recognize the following blood group antigens: A, B, II,
Lewis", Lewis'", X (Lewis"), Y (Lewis'), and type I precursor antigen.
Tumors from 29 patients were studied. Tumors studied consisted of pure
embryonal carcinoma for eight patients, pure yolk sac tumor for two
patients, embryonal carcinoma plus yolk sac tumor in one patient, and
yolk sac tumor plus seminoma in one patient. Also studied were nine
classic seminomas and a group of six patients with tumors classified as
seminomas that exhibited atypical histológica!features. One patient had
an anaplastic carcinoma arising from the mediastinum which could not
be conclusively identified as a germ cell tumor morphologically and was
analyzed separately.
All embryonal carcinomas and yolk sac tumors exhibited strong positivity for type I precursor structure as detected by the K-21 monoclonal
antibody. In marked contrast, there was non staining in classic seminomas
but heterogeneous staining in five of six atypical seminomas. The majority
of embryonal carcinomas and all yolk sac tumors studied demonstrated
strong positivity for blood group antigen H. For seminoma, however, only
one of the atypical cases and two of the classic cases (occasional cells)
stained for H. Focal expression of the Y antigen was identified in 5 of 17
seminomas and in the majority of embryonal carcinomas and yolk sac
tumors. Two yolk sac tumors and two classic seminomas expressed blood
group X. The remaining blood group antigens were not expressed by
seminomas while they were variably expressed by embryonal carcinoma
and yolk sac tumors. These data suggest that K-21 and blood group
antigen H may be distinguishing markers of nonseminomatous germ cell
tumor irr.vM.vseminoma. If so, it is possible that the heterogeneous
expression of blood group substances in seminomas with atypical his
tologies is an indication of differentiation towards nonseminomatous germ
cell tumor.
and in body fluids and secretions (4, 5). A, B, and H antigens
are synthesized from erythrocytes and integrated on their cell
membrane (6). The site of synthesis for Lewis antigens is
uncertain, however, and they are absorbed onto erythrocytes
from plasma and likewise may reside on epithelial cells (6-8).
A, B, H, and Lewis antigen structures are synthesized from two
distinct precursor structures, type I [containing Gal(l —>
3)GlcNAc-] and type 2 [containing Gal(l -»4)GlcNAc-] (9).
The synthesis and expression of these antigens are regulated by
several independent genes (10, 11). Modifications of blood
group antigens identified by immunohistochemical
methods
have been demonstrated in several tumors and may have clinical
implications. These include the loss of antigen expression in
bladder cancer, correlating with invasiveness (2-4), enhance
ment of expression in colon cancer (15), and elevated serum
levels of Lewis antigens in patients with colon cancer (16). To
define the distribution of blood group antigens in human GCT,
an immunohistochemical analysis was performed using mouse
monoclonal antibodies and Ulex europaeus lectin with speci
ficities for A, B, H, Le", Leb, X, Y, and precursor type I antigens.
MATERIALS
AND METHODS
Patients
Tumors from 29 patients were chosen for analysis based on (a)
confirmed histológica! diagnosis of GCT and (b) availability of tissue
blocks embedded in paraffin. Patient characteristics are summarized in
Table 1. Patients 15 and 17-21 had Stage I seminoma, and the
remainder of patients had advanced GCT. Two patients (Patients 22
and 27) with pure seminoma at biopsy had an elevated serum afetoprotein level.
Tissues
INTRODUCTION
The current successful treatment of GCT2 has been a major
advance in medical oncology. With cisplatin-based chemother
apy, 70-80% of patients with advanced GCT are cured of their
disease (1). However, certain problems in the diagnosis and
management of patients with advanced GCT persist.
Occasional seminomas exhibit pleomorphism and an in
creased mitotic index and may be difficult to distinguish from
embryonal carcinoma by light microscopy (2). There are limi
tations in the usefulness of criteria designed to identify patients
with poor prognostic features and to select appropriate therapy
(3). A better understanding of the biological characteristics of
these tumors may aid in their classification and in selection of
therapy and provide additional insight into the histogenesis of
GCT.
Blood group antigens are formed by sequential addition of
saccharides to the carbohydrate side chains of lipids and pro
teins and are found on erythrocytes, on certain epithelial cells,
Received 9/25/87; revised 2/26/88, 5/25/88; accepted 6/3/88.
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.
1To whom requests for reprints should be addressed, at Memorial Hospital,
1275 York Avenue. New York, NY 10021.
2 The abbreviation used is: GCT, germ cell tumors.
The study group included cases of easily identifiable classic pure
seminoma (9 cases), embryonal carcinoma (8 cases), or yolk sac tumor
(2 cases). Six tumors were classified as seminomas but contained
histologically atypical features (see "Results" and "Discussion"). Three
additional cases exhibited mixed histologies. One patient had a me
diastinal tumor interpreted as anaplastic carcinoma. Tissues from all
patients were obtained within 1-2 h of resection, fixed in buffered 10%
formaldehyde, dehydrated in graded alcohols and xylol, and embedded
in paraffin. The tumor tissue analyzed was obtained by biopsy prior to
chemotherapy or radiotherapy for all patients except Patient 11. The
tumor from this patient was obtained by incomplete resection of a
mediastinal mass following partial response to chemotherapy. The
histology of all cases as well as their immunoreactivity were reviewed
and interpreted by a reference pathologist (V. R.).
Reagents
Purified agglutinin I from U. europaeus (Vector, Burlingame, CA)
served to identify the H antigen. Mouse antibodies were used to detect
the other blood group antigens as summarized in Table 2(17, 18-22).
The antibodies were used either as undiluted culture supernatants or
after purification from mouse ascites fluid at approximately 20 Mg/ml.
Immunoperoxidase. Formalin-fixed, paraffin-embedded sections were
deparaffinized and treated for 15 min in 1% hydrogen peroxide in
phosphate-buffered saline in order to remove endogenous peroxidase
activity. Tissue sections were washed in phosphate-buffered saline and
incubated with the appropriate blocking serum for 20 min, drained.
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BLOOD GROUP ANTIGENS IN GCT
Table 1 Patient characteristics
of
pretreatment
siteTTTTTTTTTTMEDTRPTTTTTTTTTRPTTRPSCNTAX.
métastasesRPMarker
markersHCG
Patient1234567891011121314151617181920212223242526272829Age2524282523282922382818272729313032223232502136293524262820Blood
typeBAAOOOOOOABAAAOOOOAABA0OABAAABAOPrimary
siterTTTTTTTTTMEDTTTTTTTTTTTHPTTRPTTMEDTissue
25HCG=
=
179HCG
onlyRPRPSCNRPLungRPLungRPRPRPLungSCNRPMEDRPRPRPNon
9.3LDH
=
314LDH
=
476HCG
=
YSECECEC
+
SECYSYS
+
SYSSSSssssssssssssCarcinomaSites
+
23,800LDH
=
849HCG
=
56LDH=
278LDH
=
675LDH
=
331HCG
=
2.1HCG
=
380AFP
=
634LDH
=
376AFP=
=
10,360LDH
768HCG=
=
125AFP
83AFP=
150HCG
= 8.
20LDH=
557NoneLDH
=
1,073NoneNoneNoneNoneNoneAFP
=
2,977LDH
=
930HCG
=
9LDH =
532HCG
=
5LDH =
343LDH
=
3,680LDH
=
794HCG
=
57AFP=
60LDH=
825AFP
=
LN.HistologyECECECECECEC
560LDH
=
= 14.460
" T, testis; RP, retroperitoneal; MED, mediastinum; SCN, supraclavicular lymph node; AX. LN., axillary lymph node; HCG, human chorionic gonadotropi level
as measured in ng/ml; AFP, serum «-fetoprotein level as measured in ng/ml; LDH, serum láclatedehydrogenase level as measured in units/liter; EC, embryonal
carcinoma; YS, yolk sac tumor; S, seminoma.
Table 2 Derivation and specificity of mouse monoclonal antibodies identifying
blood group antigens"
Purified agglutinin I from U. europaeus (Vector Laboratories) was used to
detect H antigen.
Antibody
(immunoglobulin
subclass)K21
lineTERA-1
cell
(IgM)
HT-29
T36 (IgG3)
SK-RC-7
S8 (IgM)
SK-CO-10
T174(IgGl)
SK-CO-10
T218(IgM)
P12(IgM)
Human placenta
F3 (IgM)Immunizing SK-LU-3Blood
" Mouse monoclonal antibodies distributed by
group
specificityPrecursor
were finally washed with distilled water, counterstained with hematoxylin, and mounted with Permount.
Method for Staining with I rctin. Formalin-fixed, paraffin-embedded
sections were prepared as above. The U. europaeus lectin was incubated
for 2 h at room temperature, followed by rabbit anli-Ulex lectin antibody
(Vector) at a dilution of 1:1000 overnight at 4°C.Immunoperoxidase
methods were performed as described above using biotinylated goat
anti-rabbit immunoglobulins as secondary reagents.
Controls. Negative controls included replacement of the primary
antibody with normal blocking serum.
I
A
21
B
22
Lewis'
20
Lewis"
20
Lewis*
18,20
Lewis"Refs.18,27 19,20
Cambridge Research Labora
RESULTS
tories (CRL, Cambridge, MA).
and incubated with appropriately diluted primary antibody overnight
at 4°C.The avidin-biotin method was used as described by Hsu et al.
(23). The secondary antibodies were biotinylated (Vector) and incubated
on section for 30 min. For the final reaction diaminobenzidine was
used as chromogen, incubating tissue sections for 5 min with 5 mg of
diaminobenzidine tetrahydrochloride (Sigma, St. Louis, MO) in 100
ml of water containing 100 n\ of 0.3% hydrogen peroxide. Sections
The tumors from Patients 1-5, 7, 8, and 10 were interpreted
as embryonal carcinoma. Patients 11 and 13 had yolk sac tumor
only in the tissue analyzed. Patients 14-28 had pure seminoma.
The seminoma from Patients 14-22 had a classic morphology;
in contrast, seminoma from Patients 23-28 had atypical fea
tures including increased mitotic index, nuclear pleomorphism
and crowding, increased nucleancytoplasmic ratio, prominent
nucleolus, and indistinct cytoplasmic membranes. Three pa
tients had mixed GCT: Patient 9, embryonal carcinoma plus
yolk sac tumor; Patient 12, yolk sac tumor plus seminoma
5343
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BLOOD GROUP ANTIGENS IN GCT
(atypical). The morphologies of tumors from Patient 2 (em
bryonal carcinoma), Patient 14 (classical seminoma), and Pa
tient 28 (seminoma with some atypical features) are demon
strated in Figs. 1 (left), 2 (left), and 3 (left), respectively. The
tumor of patient 29 could not conclusively be identified as a
GCT. Thus, this patient was considered separately for analysis
of immunoreactivity.
GCT Tumor Immunoreactivity
The immunophenotypic characterizations of the study cases
are summarized in Table 3.
Precursor Type I Antigen. All of the embryonal carcinomas
and yolk sac tumors uniformly expressed precursor structure,
with the single exception of the tumor in Patient 12, which
expressed the antigen in <50% of tumor cells. All of the classic
seminomas (Patients 14-22), one atypical seminoma (Patient
24) and the seminomatous component of a mixed tumor (Pa
tient 9) expressed no immunoreactivity for precursor antigen.
Of the remaining atypical seminomas, two (Patients 25 + 27)
had homogeneous expression of antigen, three (Patients 12, 23,
and 28) expressed antigen in <50% of tumor cells and one
(Patient 28) expressed antigen in only occasional tumor cells.
Examples of immunoreactivity to K-21 monoclonal antibody
are demonstrated for Patient 2 (embryonal carcinoma, K-21
positive), Patient 14 (seminoma, K-21 negative), and Patient
28 (seminoma, K-21 positive) in Figs. 1 (right), 2 (right), and 3
(right), respectively.
H Antigen. Expression of H antigen was noted in the endothelial cells and erythrocytes of all specimens studied. Homo
geneous tumor immunoreactivity was observed in 5 of 10 em
:-
bryonal carcinomas and all yolk sac tumors except for Patient
12 in whom there was immunoreactivity in approximately 50%
of tumor cells. Seminomas were nonreactive except for Patient
24 which expressed H antigen homogeneously and Patients 17
and 20 in which it was expressed in occasional cells.
A and B Antigens. A and B blood group antigen were present
on erythrocytes and endothelial cells of corresponding blood
type patients. Patients 2 and 11 expressed the appropriate blood
group type A on tumor cells analyzed, embryonal carcinoma,
and yolk sac tumor, respectively. The other non-O blood type
patients with embryonal carcinoma and yolk sac tumor (Pa
tients 1,3, 10, 12, and 13) had deletion of appropriate A or B
blood type on tumor analyzed. Nine patients (Patients 12, 1821, and 24-27) had deletion of appropriate A and/or B antigen
in seminoma. No tumor studied had anomalous expression of
these antigens or incompatible immunophenotype for ABH
isoantigens.
Lewis". Lewis" was expressed in 5 of 10 patients with em
bryonal carcinoma and 1 of 4 patients with yolk sac tumors.
No expression in seminoma was noted.
Lewisb. Immunoreactivity to Lewisb was present in 6 of 10
patients with embryonal carcinoma and 2 of 4 with yolk sac
tumor. No patients with seminoma expressed Lewisb in tumor.
Lewis". X antigen was expressed in tumors of 2 of 4 patients
with yolk sac histology. Two classic seminomas expressed X
focally. No embryonal carcinoma had immunoreactivity for the
X antigen.
Lewis'. The tumors in 7 of 10 patients with embryonal
carcinoma and 3 of 4 patients with yolk sac tumor expressed
Y. For seminoma, 2 of 9 classic tumors and 3 of 7 with atypical
morphological features expressed Y.
*S -'
*>
Fig. 1. Embryonal carcinoma from Patient 2 stained with hematoxylin and eosin (left) and with monoclonal antibody K-21 to precursor structure (right), /trrows,
cytoplasmic membrane staining.
5344
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BLOOD GROUP ANTIGENS IN GCT
. V-
mmlmffl'*tf&8&&$
Fig. 2. Seminoma from Patient 14 stained with hematoxylin and eosin (left) and with monoclonal antibody K-21 to precursor structure (right).
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* & * ' ^«*"
-, •• J!*
•
*o v <A''^®
%v>
.TSfc.v,£.^'."JfÃ-^ ^
>^. «^-f^t,^'
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•
T¡ »
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S -:
•
VJL ^
SSvSill-.v •/'•
#i*
-V•
JÄ1*
** 1w-'
-^
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••
èA ^S '* ""A^«^
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»
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Fig. 3. Seminoma from Patient 28 stained with hematoxylin and eosin (left) and with monoclonal antibody K-21 to precursor structure (right). Arrows, patchy
cytoplasmic membrane staining.
5345
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BLOOD GROUP ANTIGENS IN GCT
Table 3 Immunoreactirity of a panel of antibodies delecting blood group antigens
in GCT
H12345678910111261300OO•o••14
PS"
HistologyEmbryonal
carcinomaYolk
sacClassic
seminomaAtypical
O15
O16
O17
0'18
O
O
O
0
O19
O20
O'21
O
O
O
O22
O9
O23
O
O
O
differing expression of precursor antigen in seminoma as deter
mined by the monoclonal antibody K-21 remains to be defined
and requires studying a larger number of patients. However, it
is possible that the expression of K-21 in these tumors is an
early marker of differentiation toward nonseminomatous his
tology.
Seminoma and nonseminomatous GCT differed in expres
sion of the blood group antigen H. The majority of embryonal
carcinomas and all yolk sac tumors studied expressed H. Only
two classic seminomas and one atypical seminoma expressed
immunoreactivity for the blood group antigen H. It is interest
ing that the two classic seminomas that expressed H also
expressed Le" and Ley antigens (see Table 3, Patients 17 and
20). The higher proportion of H expression in yolk sac tumors
compared to embryonal carcinoma may be a function of cellular
differentiation since blood-forming elements are first produced
in the fetal yolk sac (29).
Seminoma and nonseminomatous GCT (embryonal carci
noma and yolk sac tumor) differed in expression of the blood
group antigens A, B, Lea, Leb, X, and Y. While embryonal
carcinoma and yolk sac tumor had a distribution of expression,
classic seminoma did not express these antigens with the two
exceptions commented above. In addition, three atypical semi
O24
O
seminomaOtherPatient
nomas expressed variable amounts of Y antigen.
•25 O
026
•
In conclusion, the monoclonal antibody K-21 detecting type
O27
O'
I
precursor
antigen may be an important cell surface marker
O28
•
for GCT. All embryonal carcinomas and yolk sac tumors
O12
»
O29
0
strongly expressed this antigen. This finding correlates with in
vivo studies on teratocarcinoma by Rettig et al. (18). Seminoma,
0
0AOeoo0ooooo00ooooo0o0ooooooooooo0B0ooo0oo0ooooooooo0o0ooooooooooo0Le"0••e00o0oe»0o0ooooo0ooooooooooooLe"••ee0â€
however, differs in expression of precursor antigen. The signif
" PS, precursor structure, type I chain. Immunoreactivities: •,homogeneous
staining: 0, <50% tumor cells positive; O', occasional cells staining; O, <50%
icance of heterogeneous expression in seminoma patients re
tumor cells positive.
mains to be defined by studying a larger number of tumors,
which also may add insight into the histogenesis of GCT.
DISCUSSION
Blood group-related antigens are a group of cell surface
carbohydrate structures which are present in the surface of RBC
as well as many other nonerythroid cells. These antigens are
formed by the sequential addition of sugar residues to precursor
structures and their expression is modulated during develop
ment and maturation as well as neoplastic transformation.
Andrews et al. (24) demonstrated modulation of specific surface
carbohydrate determinants, stage-specific embryonic antigens
1 and 3, during differentiation of cloned human embryonal
carcinoma cells. Damjanov et al. (25) also identified stagespecific embryonic antigen 3 in human embryonal carcinoma,
yolk sac tumor, and teratoma but not in seminoma. Williams
et al. (26), Fukudaef al. (27), and Rettig étal.(18) demonstrated
the presence of other carbohydrate determinants on the surface
of embryonal carcinoma cells, including the epitope recognized
by antibody K-21, a glycoprotein exhibiting specificity for blood
group precursor type I chain (27). Finally, Teshima et al. (28)
showed marked differences in cell surface carbohydrates on
germ cell tumor subtypes and commented on their potential
use in establishing a more precise classification of these tumors.
We have used a panel of monoclonal antibodies and the lectin
U. europaeus with specificities toward diverse blood grouprelated antigens to study human germ cell tumors. Type I
precursor antigen as detected by K-21 antibody was present in
all embryonal carcinomas and yolk sac tumors. In contrast, all
classic seminomas were negative for K-21. Six of the seven
atypical cases exhibited variable immunoreactivity with K-21.
Thus, K-21 reactivity in seminoma appeared to correlate with
atypical morphological features. The clinical significance of
ACKNOWLEDGMENTS
The authors gratefully acknowledge Mary Ellen McCroarty for tech
nical assistance.
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Blood Group-related Antigens in Human Germ Cell Tumors
Robert J. Motzer, Victor E. Reuter, Carlos Cordon-Cardo, et al.
Cancer Res 1988;48:5342-5347.
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