The relation of serum anti-(GalNAc beta) and -para — forssman disaccharide IgG levels to the progression and histological grading of gastrointestinal cancer
Earlier we found two unusual IgG-antibody specificities to GalNAc? and GalNAcβ1-3GalNAcβ (Para — Forssman disaccharide, PFdi) carbohydrate ligands in human serum. The aim of the study was to evaluate whether elevated antibody levels are related to the progression of gastrointestinal cancer and the h...
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Інститут експериментальної патології, онкології і радіобіології ім. Р.Є. Кавецького НАН України
2007
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| Назва видання: | Experimental Oncology |
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| Цитувати: | The relation of serum anti-(GalNAc beta) and -para — forssman disaccharide IgG levels to the progression and histological grading of gastrointestinal cancer / E.P. Smorodin, O.A. Kurtenkov, B.L. Sergeyev, V.I. Chuzmarov, V.P. Afanasyev // Experimental Oncology. — 2007. — Т. 29, № 1. — С. 61-66. — Бібліогр.: 23 назв. — англ. |
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irk-123456789-1385622018-06-20T03:04:30Z The relation of serum anti-(GalNAc beta) and -para — forssman disaccharide IgG levels to the progression and histological grading of gastrointestinal cancer Smorodin, E.P. Kurtenkov, O.A. Sergeyev, B.L. Chuzmarov, V.I. Afanasyev, V.P. Original contributions Earlier we found two unusual IgG-antibody specificities to GalNAc? and GalNAcβ1-3GalNAcβ (Para — Forssman disaccharide, PFdi) carbohydrate ligands in human serum. The aim of the study was to evaluate whether elevated antibody levels are related to the progression of gastrointestinal cancer and the histopathological grading. Methods: Specific IgG levels were tested in 159 patients with gastric cancer, 88 patients with colorectal cancer and 96 blood donors by the ELISA using synthetic polyacrylamide (PAA) conjugates, GalNAcβ-PAA and PFdi-PAA. Biochemical and haematological analyses were performed using automatic equipment. Results: The anti-PFdi IgG levels were significantly higher in patients with gastric and colorectal cancer than in donors: in stages II–IV, P = 0.0002 – 0.04 (U-test). The elevated anti-PFdi IgG level was associated with the advanced gastric cancer: in stages II, III, IV vs stage I (P = 0.004 – 0.06) and in case of the tumor size T2 + T3 vs T1 (stages I, II; P = 0.03). Differences in anti-GalNAcβ IgG level were insignificant. No relation between antibody levels and the regional and distant metastases of gastric or colorectal cancer was found. The lower anti-GalNAcβ IgG level was associated with lower-differentiated carcinomas (P = 0.01 – 0.04). Prolonged postoperative changes in the levels of both antibodies during the follow-up were established. An elevation of both antibody levels in patients with gastrointestinal cancer was revealed after a surgical removal of G3-tumors (P = 0.003 – 0.01). The anti-PFdi IgG levels correlated with the levels of the C-reactive protein: r = 0.50, P = 0.003. The anti-GalNAcβ IgG levels correlated with the percentage of peripheral blood monocytes: r = 0.42, P = 0.002. Conclusion: The association of the anti-PFdi IgG level with cancer progression suggests the implication of antibodies in the pathogenesis of gastrointestinal cancer. Further studies are required to identify natural targets of antibodies, their relation to other diseases, prognostic significance in cancer. В сыворотке крови человека ранее выявлены IgG-антитела к углеводородным лигандам GalNAcβ и GalNAcβ1-3GalNAcβ (дисахарид Пара — Форсманна, PFdi). Цель исследования — выяснение связи повышенного уровня антител с прогрессией и гистологическими особенностями опухолей желудочно-кишечного тракта. Методы: обследовали 159 больных раком желудка, 88 — раком кишечника и 96 здоровых людей — доноров крови. Уровень специфических IgG-антител определяли методом ИФА с использованием синтетических конъюгатов полиакриламида (ПАА), GalNAcβ-ПАА и PFdi-ПАА. Уделение биохимических и гематологических показателей проводили с использованием автоматических анализаторов. Результаты: уровень анти-PFdi IgG у пациентов со злокачественными новообразованиями в стадиях II–IV (P = 0,0002 – 0,04) достоверно выше, чем у доноров. Повышенный уро вень анти-PFdi IgG ассоциировался с прогрессией рака желудка (в стадиях II–IV по сравнению со стадией I P = 0,004 – 0,06) и увеличением размера опухоли (T2 + T3 по сравнению с T1, стадии I, II; P = 0.03). Различия в уровнях анти- β IgG незначительные. Не выявлено взаимосвязи между уровнем антител и метастазированием опухолей желудка и кишечника. Более низкий уровень анти- β IgG определяли у больных с менее дифференцированными опухолями (P = 0,01 – 0,04). В период послеоперационного наблюдения отмечали изменения уровня обоих типов антител. После хирургического удаления опухолей органов желудочно-кишечного тракта (стадия дифференцировки G3) повышался уровень как анти-PFdi IgG, так и анти- βIgG (P = 0,003 – 0,01). Уровень анти-PFdi IgG коррелировал с уровнем С-реактивного белка (r = 0,50, P = 0,003), а уровень анти-GalNAcβ IgG — с относительным количеством моноцитов в периферической крови (r = 0,42, P = 0,002). Выводы: установлена зависимость уровня анти-PFdi IgG от опухолевой прогрессии, что подтверждает их участие в патогенезе злокачественных новообразований органов желудочно-кишечного тракта. Необходимы дальнейшие исследования по определению природных мишеней для антител, роли в развитии других заболеваний и прогностическом значении при онкологической патологии. 2007 Article The relation of serum anti-(GalNAc beta) and -para — forssman disaccharide IgG levels to the progression and histological grading of gastrointestinal cancer / E.P. Smorodin, O.A. Kurtenkov, B.L. Sergeyev, V.I. Chuzmarov, V.P. Afanasyev // Experimental Oncology. — 2007. — Т. 29, № 1. — С. 61-66. — Бібліогр.: 23 назв. — англ. 1812-9269 http://dspace.nbuv.gov.ua/handle/123456789/138562 en Experimental Oncology Інститут експериментальної патології, онкології і радіобіології ім. Р.Є. Кавецького НАН України |
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Digital Library of Periodicals of National Academy of Sciences of Ukraine |
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DSpace DC |
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English |
| topic |
Original contributions Original contributions |
| spellingShingle |
Original contributions Original contributions Smorodin, E.P. Kurtenkov, O.A. Sergeyev, B.L. Chuzmarov, V.I. Afanasyev, V.P. The relation of serum anti-(GalNAc beta) and -para — forssman disaccharide IgG levels to the progression and histological grading of gastrointestinal cancer Experimental Oncology |
| description |
Earlier we found two unusual IgG-antibody specificities to GalNAc? and GalNAcβ1-3GalNAcβ (Para — Forssman disaccharide, PFdi) carbohydrate ligands in human serum. The aim of the study was to evaluate whether elevated antibody levels are related to the progression of gastrointestinal cancer and the histopathological grading. Methods: Specific IgG levels were tested in 159 patients with gastric cancer, 88 patients with colorectal cancer and 96 blood donors by the ELISA using synthetic polyacrylamide (PAA) conjugates, GalNAcβ-PAA and PFdi-PAA. Biochemical and haematological analyses were performed using automatic equipment. Results: The anti-PFdi IgG levels were significantly higher in patients with gastric and colorectal cancer than in donors: in stages II–IV, P = 0.0002 – 0.04 (U-test). The elevated anti-PFdi IgG level was associated with the advanced gastric cancer: in stages II, III, IV vs stage I (P = 0.004 – 0.06) and in case of the tumor size T2 + T3 vs T1 (stages I, II; P = 0.03). Differences in anti-GalNAcβ IgG level were insignificant. No relation between antibody levels and the regional and distant metastases of gastric or colorectal cancer was found. The lower anti-GalNAcβ IgG level was associated with lower-differentiated carcinomas (P = 0.01 – 0.04). Prolonged postoperative changes in the levels of both antibodies during the follow-up were established. An elevation of both antibody levels in patients with gastrointestinal cancer was revealed after a surgical removal of G3-tumors (P = 0.003 – 0.01). The anti-PFdi IgG levels correlated with the levels of the C-reactive protein: r = 0.50, P = 0.003. The anti-GalNAcβ IgG levels correlated with the percentage of peripheral blood monocytes: r = 0.42, P = 0.002. Conclusion: The association of the anti-PFdi IgG level with cancer progression suggests the implication of antibodies in the pathogenesis of gastrointestinal cancer. Further studies are required to identify natural targets of antibodies, their relation to other diseases, prognostic significance in cancer. |
| format |
Article |
| author |
Smorodin, E.P. Kurtenkov, O.A. Sergeyev, B.L. Chuzmarov, V.I. Afanasyev, V.P. |
| author_facet |
Smorodin, E.P. Kurtenkov, O.A. Sergeyev, B.L. Chuzmarov, V.I. Afanasyev, V.P. |
| author_sort |
Smorodin, E.P. |
| title |
The relation of serum anti-(GalNAc beta) and -para — forssman disaccharide IgG levels to the progression and histological grading of gastrointestinal cancer |
| title_short |
The relation of serum anti-(GalNAc beta) and -para — forssman disaccharide IgG levels to the progression and histological grading of gastrointestinal cancer |
| title_full |
The relation of serum anti-(GalNAc beta) and -para — forssman disaccharide IgG levels to the progression and histological grading of gastrointestinal cancer |
| title_fullStr |
The relation of serum anti-(GalNAc beta) and -para — forssman disaccharide IgG levels to the progression and histological grading of gastrointestinal cancer |
| title_full_unstemmed |
The relation of serum anti-(GalNAc beta) and -para — forssman disaccharide IgG levels to the progression and histological grading of gastrointestinal cancer |
| title_sort |
relation of serum anti-(galnac beta) and -para — forssman disaccharide igg levels to the progression and histological grading of gastrointestinal cancer |
| publisher |
Інститут експериментальної патології, онкології і радіобіології ім. Р.Є. Кавецького НАН України |
| publishDate |
2007 |
| topic_facet |
Original contributions |
| url |
http://dspace.nbuv.gov.ua/handle/123456789/138562 |
| citation_txt |
The relation of serum anti-(GalNAc beta) and -para — forssman disaccharide IgG levels to the progression and histological grading of gastrointestinal cancer / E.P. Smorodin, O.A. Kurtenkov, B.L. Sergeyev, V.I. Chuzmarov, V.P. Afanasyev // Experimental Oncology. — 2007. — Т. 29, № 1. — С. 61-66. — Бібліогр.: 23 назв. — англ. |
| series |
Experimental Oncology |
| work_keys_str_mv |
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| fulltext |
Experimental Oncology ���� ������� ����� ��arc��� ������ ������� ����� ��arc��� ���arc��� ���� �� ��
T�e immunopat�ological role of antibodies remains
poorly understood until t�e relevant autoantigen and
t�e exogenous immunogen are unknown. Normal
individuals as well as individuals wit� autoimmune
diseases and cancer produce antibodies reacting wit�
a variety of carbo�ydrate determinants [�]. Human
natural anticarbo�ydrate antibodies belong mostly
to t�e Ig�-class and t�eir individual p�ysiological
level is sustained by immune �omeostasis. In some
patients wit� cancer�� t�e unusually �ig� levels of t�e
IgG antibody to t�e mucin-type carbo�ydrate epitopes
were found [�]. T�is may be explained by an adap-
tive immune response indicating an antibody class
switc�ing to IgG and undergoing affinity maturation.
As a rule�� t�e serum IgG antibodies affinity-purified on
synt�etic sorbents ex�ibited a low specificity to tumor-
associated mucins�� possibly due to t�e presence of a
clustered form of carbo�ydrates in mucins [3�� 4]. As in
immunoassays or t�e purification of antibodies poly-
acrylamide �PAA��-glycoconjugates wit� a low epitope
density ������ mol. %�� were used�� t�e specificity of
t�e antibodies examined may be directed to glycolipids
�natural targets wit� non-clustered sacc�arides��.
PAA-glycoconjugates are �omogenous antigens
wit� a single reiterative epitope t�at enables t�e detec-
tion of epitope-specific antibodies [5]. In immunoas-
says�� synt�etic glycoconjugate-models �ave certain
advantages over natural antigens containing usually
different determinants. T�e �ig� reproducibility of anti-
body detection by t�e ELISA and t�e low background in
t�e control make PAA-conjugates a promising tool for
comparative investigations [��� �]. T�e measurement
of antibodies to glycolipids is tec�nically demanding
and different laboratories �ave demonstrated t�at
t�e immunoassays varied widely in sensitivity and t�e
criteria employed for a positive test [��].
Taking into consideration t�e �ig� frequency of �u-
man antibodies to glycolipids and t�eir possible role in
t�e pat�ogenesis of cancer [8]�� we tested t�e serum of
patients by t�e ELISA using a set of PAA-β-glycocon-
jugates�� and found two populations of IgG antibodies
t�at were specific to GalNAcβ and GalNAcβ�-3GalNAcβ
ligands [3] �t�e latter is an outer disacc�aride of Para —
Forssman glycolipid�� PFdi��. T�e aim of t�e present study
was to evaluate w�et�er serum antibody levels are re-
lated to t�e progression of gastrointestinal cancer and
t�e �istopat�ological grading. T�e level of anti-PFdi IgG
was found to be associated wit� t�e advanced cancer
and t�at of anti-GalNAcβ IgG was associated wit� t�e
�istopat�ological grading.
MATERIALS AND METHODS
Subjects. T�e investigation was carried out in ac-
cordance wit� t�e ICH GCP Standards and approved
THE RELATION OF SERUM ANTI-(GalNAc bETA) AND -PARA —
FORSSMAN DISACCHARIDE IgG LEVELS TO THE PROGRESSION AND
HISTOLOGICAL GRADING OF GASTROINTESTINAL CANCER
E.P. Smorodin1, *, O.A. Kurtenkov1, B.L. Sergeyev1, V.I. Chuzmarov2, V.P. Afanasyev2
1Department of Oncology & Immunology, National Institute for Health Development, Tallinn, Estonia
2North-Estonian Regional Hospital Oncological Centre, Tallinn, Estonia
Earlier we found two unusual IgG-antibody specificities to GalNAcβ and GalNAcβ1-3GalNAcβ (Para — Forssman disaccharide,
PFdi) carbohydrate ligands in human serum. The aim of the study was to evaluate whether elevated antibody levels are related to the
progression of gastrointestinal cancer and the histopathological grading. Methods: Specific IgG levels were tested in 159 patients with
gastric cancer, 88 patients with colorectal cancer and 96 blood donors by the ELISA using synthetic polyacrylamide (PAA) conjugates,
GalNAcβ-PAA and PFdi-PAA. Biochemical and haematological analyses were performed using automatic equipment. Results: The
anti-PFdi IgG levels were significantly higher in patients with gastric and colorectal cancer than in donors: in stages II–IV, P =
0.0002 – 0.04 (U-test). The elevated anti-PFdi IgG level was associated with the advanced gastric cancer: in stages II, III, IV vs
stage I (P = 0.004 – 0.06) and in case of the tumor size T2 + T3 vs T1 (stages I, II; P = 0.03). Differences in anti-GalNAcβ IgG
level were insignificant. No relation between antibody levels and the regional and distant metastases of gastric or colorectal cancer
was found. The lower anti-GalNAcβ IgG level was associated with lower-differentiated carcinomas (P = 0.01 – 0.04). Prolonged
postoperative changes in the levels of both antibodies during the follow-up were established. An elevation of both antibody levels in
patients with gastrointestinal cancer was revealed after a surgical removal of G3-tumors (P = 0.003 – 0.01). The anti-PFdi IgG
levels correlated with the levels of the C-reactive protein: r = 0.50, P = 0.003. The anti-GalNAcβ IgG levels correlated with the
percentage of peripheral blood monocytes: r = 0.42, P = 0.002. Conclusion: The association of the anti-PFdi IgG level with cancer
progression suggests the implication of antibodies in the pathogenesis of gastrointestinal cancer. Further studies are required to
identify natural targets of antibodies, their relation to other diseases, prognostic significance in cancer.
Key Words: GalNAc beta1-3GalNAc beta, Para — Forssman, polyacrylamide-glycoconjugates, IgG antibodies, gastric cancer,
colorectal cancer.
Received: January 15, 2007.
*Correspondence: Fax: +372-6593901
E-mail: evgeni.smorodin@tai.ee
Abbreviations used: A – absorbance; CRP – C-reactive protein;
PAA – polyacrylamide; Pfdi – Para — Forssman disaccharide;
TF – Thomsen-Friedenreich antigen; αGal — Galα1-3Galβ; Tn —
GalNAcα; TBS – Tris-buffer/0.05% Tween-20.
Exp Oncol �����
���� ��� �����
�� Experimental Oncology ���� ������� ����� ��arc���
by Tallinn �edical Researc� Et�ics Committee. T�e
informed consent from t�e subjects under study was
obtained. Blood transfusion donors and patients wit�
gastric�� colon or rectal cancer wit� a verified diagnosis
��istology and tumor staging by t�e pTN� system�� were
examined [�]. T�e median age of donors was 5� years
�range 3� to �5 years��; t�at of gastric cancer patients��
5� years �range �8 to ��4 years��; and of colorectal cancer
patients�� �� years �range 4� to ��5 years��. In all cases��
except special investigations �t�e effect of a surgical
removal of t�e tumor or t�e follow-up study���� blood
samples were taken before t�e surgical operation. T�e
gastrectomy and extended D� limp�adenectomy�� but
not spleenectomy�� for gastric cancer and t�e resection
of local lesions for colorectal cancer were performed.
T�e patients w�o received c�emo- or X-ray-t�erapy
were excluded from t�e study. Concomitant diseases
in patients were examined based on t�e �istory of t�e
disease and a personal conversation.
Glycoconjugates. T�e glycoconjugates wit�
polyacrylet�anolamide �PAA�� — GalNAcβ-PAA and
GalNAcβ�-3GalNAcβ-PAA were received from Lec-
tinity�� Russia. T�e epitope density was �� mol. %.
Tris��ydroxymet�yl��aminomet�ane-PAA �Tris-PAA��
was used as a negative control.
The determination of epitope-specific antibody
levels in sera. T�e venous blood serum was kept at
���� °C. In t�e ELISA�� t�e serum frozen/t�awed once
was used. T�e met�od was performed as described
in [�]. Briefly�� PAA-glycoconjugates �5 µg/ml�� in �.�5
� carbonate buffer�� pH �.��� were applied to t�e Nunc-
Immuno plate ��axiSorp�� and �eld overnig�t at 4 °C.
After was�ing wit� Tris-buffer/�.�5% Tween-�� �TBS����
t�e serum diluted to �:�5��:4�� in TBS/�.�5% casein/
5 m� EDTA-disodium salt was added. T�e dilution of
sera wit� a buffer containing 5 m� EDTA reduces t�e
background significantly�� but influences weakly t�e
specific antibody binding [�]. After incubation for 3 �
at �� °C�� t�e plate was was�ed and incubated wit� t�e
goat anti-�uman IgG-alkaline p�osp�atase conjugate
for �.5 � at �� °C. T�e absorbance �A�� at 4�5 nm of
t�e reaction wit� a p-nitrop�enylp�osp�ate disodium
salt �� mg/ml in t�e glycine-buffer�� pH ��.3�� �� °C��
� ��� was measured using a Labsystem �ultiscan
�CC/34� �Finland��. T�e ratio of t�e mean Atest/Acontrol
was calculated�� w�ere Atest is t�e absorbance wit� t�e
PAA-glycoconjugate and Acontrol�� wit� t�e Tris-PAA. T�e
variation coefficient was 3%.
Clinical analysis of blood samples. T�e bioc�emi-
cal and �aematological analyses were performed in
Nort�-Estonian Regional Hospital Oncological Centre
using automatic equipment: a Hitac�i ��� and Elecsys
������ Roc�e Diagnostics; Sysmex XE-������ Sysmex
Corporation. Blood samples were taken from patients
before and/or after a surgical operation during t�e
planned visits to t�e p�ysician for �ealt� control. T�e
antibody levels were correlated wit� t�e levels of t�e
C-reactive protein �CRP���� tumor markers �CA��-���
CEA���� alanine aminotransferase�� glucose�� �aemo-
globin�� circulating red blood cells �count���� leukocytes
�count���� neutrop�ils �%���� monocytes �%���� lymp�ocytes
�%���� platelets �count�� and eosinop�ils �%��. T�e CRP
concentration was determined by using a turbidimetri-
cal met�od and tumor markers by an electroc�emilu-
minescense immunoassay.
Statistical methods. T�e �ann — W�itney U-test��
�D Cartesian box plots grap� and regression analysis
were used in t�e study. T�e differences were con-
sidered significant w�en P < �.�5. T�e grap�s were
plotted by means of a SigmaPlot ���� program and
Statgrap�ics Plus 5.�.
RESULTS
The relation of antibody levels to cancer. T�e
subjects were analysed by age�� gender and AB��H��
blood group p�enotype to assess t�e possible influen-
ce of t�ese parameters in t�e comparative study. In
donors as well as in patients wit� cancer t�e levels of
anti-GalNAcβ and -PFdi IgG antibodies were not related
to age and gender. T�e relation between antibody le-
vels and t�e blood group p�enotype in donors was not
observed eit�er. T�e �ig�er anti-PFdi IgG levels for t�e
A-blood group as compared to t�ose for B or � groups
were revealed in cancer patients �P = �.�3��. T�erefore��
t�e influence of t�e blood group was taken into account:
an approximately equal ratio of A/B and A/� was c�osen
for t�e comparison of cancer patients wit� donors as
well as for analysis by stage of cancer.
Hig� levels of antibodies�� particularly anti-PFdi
IgG�� were found in t�e serum of patients wit� cancer
�Fig. ���. T�e anti-PFdi antibody level was significantly
�ig�er in patients wit� gastrointestinal cancer�� espe-
cially in stages II�IV�� t�an in donors�� w�ereas t�e diffe-
rence in t�e level of anti-GalNAcβ IgG was insignificant
�Table ���. An asymmetrical distribution of anti-PFdi IgG
values was c�aracteristic of more advanced cancer
�Fig. ��� boxes ��� 3 and 4��. T�e median values in stage I
of gastric cancer were very close to t�ose in donors
�Table ��� ����� but t�e median in stages II and IV was
significantly �ig�er �Table ���. Taken toget�er�� stages
I and II were analyzed for tumor size: t�e differences
in T� vs T� + T3 remained significant. A similar stage-
dependent c�ange of median values was observed
for colorectal cancer but differences were significant
only between stages I and II: P = �.�4�� �tumor size
status in stage I was T� + T� vs T3 + T4 in stage II��.
T�e level of anti-GalNAcβ IgG was not related to t�e
stage of gastric or colorectal cancer. T�ese results and
our previous data [��] s�ow t�at t�e levels of serum
anti-carbo�ydrate antibodies in patients wit� cancer
are eit�er directly or inversely associated wit� tumor
progression �PFdi�� TF�� αGal�� or do not depend on it
�GalNAc� Tn���� �Table 3�� summarized data��.
Table 1. Analysis of serum IgG antibody levels in donors and cancer patients
Serum Anti-GalNAcβ Anti-PFdi
n Median P n Median P
Donors 96 1.34 107 1.36
Gastric cancer, all stages
Stages II, III, IV
159 1.37 0.30 160
121
1.61
1.88
0.001
0.0002
Colorectal cancer, all
Stages II, III, IV
88 1.38 0.17 88
69
1.63
1.72
0.074
0.04
Total cancer, all stages 247 1.37 0.22 248 1.62 0.003
Experimental Oncology ���� ������� ����� ��arc��� �3���� ������� ����� ��arc��� �3�arc��� �3�� �3 �3
Table 2. The relation between the anti-PFdi IgG level and the stage and size
status of the tumor in patients with gastric cancer
Stage, size n Median Comparison, P
I 39 1.38 I vs II, 0.029
II 42 1.76 I vs III, 0.056
III 44 1.49 I vs IV, 0.004
IV 35 2.26 III vs IV, 0.065
T1 (I) 31 1.24 T1 vs T2 + T3,
0.027T2 + T3 (I, II) 50 1.68
Table 3. The association of the serum anticarbohydrate IgG level with the
progression and histopathological grading of cancer
Antibodies
Tumor progression Histopathological grading*
Gastric can-
cer
Breast cancer Gastrointesti-
nal cancer
Breast cancer
Tn [10] No No No No
GalNAcβ No ND Direct ND
TF [10] Inverse No Direct No
αGal [10] Direct Inverse No Direct
PFdi Direct ND No ND
*Direct association: lower levels are associated with lower-differentiated
carcinomas (the comparison is shown in Table 4).
ND: not determined.
Fig. 1. Binding of t�e serum IgG-antibody wit� PFdi-PAA ���
and GalNAcβ-PAA ��� adsorbed onto immunoplates in patients
wit� gastric cancer. Lig�t symbols s�ow t�e control binding wit�
Tris-PAA�� respectively
Fig. 2. T�e distribution of anti-PFdi IgG levels in donors and
patients. Donors: box No �; gastrointestinal cancer in stage
I: box No �; gastric cancer in stages II�IV: No 3; colorectal
cancer in stages II�IV: No 4. T�e lower boundary of t�e box
indicates t�e �5t� percentile data�� a line wit�in t�e box marks
t�e median�� and t�e upper boundary of t�e box indicates t�e
��5t� percentile. Bars above and below t�e box indicate t�e ��t�
and ��t� percentiles
No relation between t�e levels of anti-GalNAcβ or
anti-PFdi antibodies and regional lymp� node metasta-
ses �stages II and III�� and distant metastases �stages III
vs IV�� in patients wit� gastric or colorectal cancer
was observed. T�e relation between antibody levels
and t�e �istopat�ological grading was found only for
anti-GalNAcβ IgG: t�e median for lower-differentiated
carcinomas was significantly lower �Table 4��.
T�e effect of t�e surgical removal of tumors on anti-
body levels was investigated: blood samples from eac�
patient were taken before and after surgery at intervals
of t�ree to sixteen mont�s. T�e postoperative level of
antibodies was increased in 8����% of patients �av-
ing G3-tumors�� differences were significant. Differen-
ces in pre- vs postoperative levels of anti-GalNAcβ or
anti-PFdi IgG were not significant for G� + G�-tumors
�Table 5�� Fig. 3��.
T�e follow-up study of sixty-eig�t patients wit�
gastrointestinal cancer carried out since ���4 �as
s�own bot� t�e stimulation and suppression of t�e
immune response to take place. A long-term �ig�
anti-PFdi IgG level was also observed but a common
trend towards t�e decline of antibody levels occurred
during t�e last period of observation �Fig. 4��.
Fig. 3. Difference in postoperative and preoperative antibody
levels �∆�� in patients wit� gastrointestinal cancer �stages I�� II�� III��.
Boxes No � and �: anti-GalNAcβ IgG; No 3 and 4: anti-PFdi IgG.
Lig�t boxes: patients wit� G� and G� tumors; dark boxes: patients
wit� G3 tumors. T�e markings are t�e same as s�own in Fig. ���
t�e upper bar for t�e last box equals ��.�� �not s�own��
Fig. 4. C�anges of t�e anti-PFdi IgG level during t�e follow-up.
Patients wit� gastric cancer. T�e zero point s�ows t�e preopera-
tive antibody level. — stage III�� pT3N���G��3 ; — II�� pT3N���G� ;
— II�� pT3N���G� ; — II�� pT3N���G3. T�e preoperative antibody
level was not analysed in t�e last case
Table 4. The relation between the anti-GalNAcβ IgG level and the histo-
pathological grading
Patients Grade n Median Comparison, P
Gastric cancer, all stages
Stages I, II
G1 + G2
G3
G1
G2 + G3
G1 + G2
G3
G1
G2 + G3
59
98
23
134
35
45
17
63
1.58
1.32
1.76
1.35
1.53
1.28
1.95
1.32
G1 + G2 vs G3,
0.010
G1 vs G2 + G3,
0.040
G1 + G2 vs G3,
0.008
G1 vs G2 + G3,
0.022
Colorectal cancer, all stages G1 + G2
G3
62
25
1.39
1.23
G1 + G2 vs G3,
0.04 2
�4 Experimental Oncology ���� ������� ����� ��arc���
Table 5. The effect of the tumor removal on the serum antibody level in
patients with gastrointestinal cancer
Antibodies Grade n Median of difference* P
GalNAcβ G1 + G2 18 –0.15 0.21
G3 14 0.32 0.009
PFdi G1 + G2 18 0.09 0.77
G3 14 0.46 0.003
*Postoperative minus preoperative antibody level.
The relation of antibody levels to blood parame-
ters and other diseases. T�e anti-PFdi IgG level was
found to correlate wit� CRP �Fig. 5��. In a follow-up study��
anti-GalNAcβ IgG levels correlated wit� t�e monocytes
percentage �r = �.4��� P = �.����� n = 5���. T�e correlation
wit� tumor markers and ot�er parameters �see �aterials
and �et�ods�� was not establis�ed.
Fig. 5. T�e correlation between t�e levels of anti-PFdi IgG and
CRP. Y = �.���X + �.��4; r = �.5��� P = �.��3�� n = 34
T�e autoimmune and r�eumatic manifestations or
paraneoplastic syndromes may be observed in pa-
tients wit� malignancies [��]. According to preliminary
examinations based on t�e �istory of t�e disease and
a personal conversation�� we did not register diagnoses
of paraneoplastic neurological disease syndromes��
dermatomiositis or systemic lupus eryt�ematosus in
t�e subgroup of patients wit� a �ig� level of anti-PFdi
IgG �Atest/Acontrol ≥ ��� dilution �:�5�� n = 54��. Postopera-
tive infectious complications were not related to �ig�
antibody levels eit�er. Concomitant r�eumatic symp-
toms were marked in �% of patients�� type � diabetes
in 4% of cases. T�e direct association of t�e levels
of anti-PFdi antibodies wit� t�e secondary anaemia
is scarcely probable because t�eir �ig� levels were
frequently observed in patients wit� a normal count
of eryt�rocytes. T�e relation of antibodies to ot�er
diseases will require furt�er study.
DISCUSSION
T�e significantly �ig�er anti-PFdi IgG level in
patients wit� cancer as compared wit� donors was
observed. In t�is respect�� t�e anti-PFdi antibodies
differ from antibodies to ot�er carbo�ydrate antigens
�TF�� Tn and Forssman�� w�ose level was significantly
lower in patients wit� gastrointestinal cancer [��� ��].
Besides�� for gastric cancer t�e anti-PFdi IgG level was
significantly �ig�er in stages II�IV t�an in stage I and
correlated wit� t�e level of CRP. As reported lately�� t�e
level of CRP was increased in gastric and colorectal
cancer. T�e increased level of CRP in one-t�ird of
patients wit� colorectal cancer was associated wit� a
larger size and advanced stage of t�e tumor [�3�� �4].
In t�is respect�� t�e relation of t�e anti-PFdi IgG level to
tumor progression resembles t�at of an acute-p�ase
protein CRP. However�� t�e elevation of bot� parame-
ters may be due to different pat�ological conditions
accompanying tumor progression �inflammation��
autoimmunity�� �epatic dysfunction and ot�ers��.
T�e anti-GalNAcβ IgG level was associated wit� t�e
�istopat�ological grading of gastric and colorectal car-
cinomas �Table 4��. Interestingly�� a similar difference in
anti-TF for gastrointestinal cancer and in anti-αGal IgG
for breast cancer was observed earlier as well �Table 3��.
We �ypot�esized t�at t�e immunosuppression occurs in
patients wit� low-differentiated carcinoma. T�e effect of
t�e tumor removal on antibody levels was investigated in
t�e follow-up. T�e postoperative level of antibodies was
elevated in patients �aving G3-tumors �Table 5�� Fig. 3��.
It is notewort�y t�at t�is p�enomenon was observed for
ot�er anti-carbo�ydrate antibodies �anti-TF�� -Tn and -
αGal IgG�� w�ose postoperative level was increased in a
majority of patients wit� gastrointestinal low-differentia-
ted carcinomas �a manuscript in preparation��. T�e levels
of Forssman antibodies in t�e sera of patients �ave been
reported to be also elevated significantly after a radical
resection of t�e tumor [���� �5]. T�e total levels of IgG
and ot�er isotype antibodies remained unc�anged after
gastrectomy [��]. Taken toget�er�� t�ese results may
be interpreted as a common suppressive influence of
carcinomas �low-differentiated mainly�� on t�e produc-
tion of anti-carbo�ydrate antibodies. Alt�oug� t�e
postoperative elevation of anti-PFdi IgG levels �as well
as anti-αGal IgG�� unpublis�ed data�� was observed�� t�e
relation between t�eir levels and �istopat�ological grad-
ing was not registered for gastric and colorectal cancer
�Table 3��. Per�aps�� t�e direct association of t�e level of
t�ese antibodies wit� tumor progression does not allow
a statistical evaluation of t�eir relation to grading.
T�e terminal β-linked GalNAc residues are specific li-
gands of t�e C-type lectin of �uman macrop�ages�� w�ose
recognition and targeting modulates immune response
[���]. We observed t�e correlation of anti-GalNAcβ IgG
levels wit� t�e percentage of perip�eral blood monocytes
t�at mig�t reflect t�e adaptive immune response and t�e
production of specific IgG antibodies.
The putative natural antigens. T�e specificity of t�e
antibodies examined in t�e ELISA using PAA-conjugates
wit� a low epitope density may be directed to glycolipids.
Usually�� an external oligosacc�aride in carbo�ydrate moie-
ty is an immunodominant. Probably�� t�e Para — Forssman
glycolipid is a natural cross-reactive ligand to antibodies��
w�ic� we named “anti-PFdi”�� because it contains a ter-
minated GalNAcβ�-3GalNAcβ disacc�aride�� t�e same
as in PFdi-PAA [�8�� ��]. T�e serum anti-PFdi IgG did
not react wit� t�e Forssman disacc�aride �GalNAcα�-
3GalNAc� and ot�er ligands [3]. It is in agreement wit�
vice versa investigations: t�e lack of t�e cross-reactivity
between Forssman and Para — Forssman glycolipids was
observed earlier for anti-Forssman antibodies [�8]. We
did not find any literature data about t�e expression of
t�e Para — Forssman antigen in �uman tissues�� except
in eryt�rocytes�� w�ere it is present in low amounts [�8].
Experimental Oncology ���� ������� ����� ��arc��� �5���� ������� ����� ��arc��� �5�arc��� �5�� �5 �5
Human natural anti-Para — Forssman antibodies ap-
peared to �ave been described earlier neit�er. W�et�er
t�e Para — Forssman antigen is expressed in �uman
gastric carcinoma similarly to t�e Forssman antigen
remains to be clarified [��].
T�e natural ligand for anti-GalNAcβ antibodies
may be glycolipid wit� a terminated GalNAcβ resi-
due�� for example GA��� an x� glycolipid or a P antigen.
T�e serum anti-GalNAcβ IgG reacted weakly wit� Tn
�GalNAc� and ot�er ligands [3]. T�e IgG antibodies
affinity-purified on GalNAcβ-sep�arose from �uman
serum were specific and did not s�ow any reactivity to
Tn and t�e ot�er GalNAc-ligands tested earlier [3]�� but
reacted weakly wit� synt�etic GA� �GalNAcβ�-4Galβ�-
4Glc� �unpublis�ed observations��. T�e specificity of
purified antibodies to PAA-glycoconjugates and t�eir
reactivity to tumor-derived glycolipids�� as well as t�e
c�aracterization of carbo�ydrate moiety wit� monoclo-
nal antibodies will be subjected to furt�er study.
T�e exogenous origin of an antigenic stimulus
s�ould not be neglected eit�er. A widespread �uman
parasite Giardia intestinalis mig�t be related to t�e
production of anti-PF antibodies because its cyst wall
antigen contains t�e �-3��-GalNAc-�omopolymer
[��]. Alt�oug� t�e polymer is �ig�ly insoluble�� its de-
graded products �oligomers���� if t�ey form�� could be
potential immunogens.
T�e Helicobacter pylori infection is one of t�e
main reasons for gastric disorders and its relation to
cancer is well documented [��]. T�ere is evidence
t�at t�e cancer-related TF-epitope is expressed in
surface membrane glycoconjugates of H. pylori and
is associated wit� a modulation of t�e natural immune
response to a TF-antigen in infected subjects [�3]. No
correlation or only a tendency to correlation between
t�e levels of anti-GalNAcβ or anti-PFdi IgG and serum
IgG antibodies against H. pylori cell surface antigens
was observed in donors and cancer patients. T�e treat-
ment of H. pylori-infected patients wit� gastric ulcer
�a standard one-week triple t�erapy�� did not influence
t�e level of antibodies�� irrespective of t�e efficacy of
t�erapy. T�e origin of immunogens remains unclear
and needs furt�er exploration.
T�us�� significant differences in antibody levels
were found owing to t�e application of t�e �ig�ly
reproducible immunoassay wit� synt�etic �omoge-
neous neoantigens. T�e �ig� anti-PFdi antibody level
in patients and its association wit� advanced cancer
as well as prolonged postoperative c�anges during
t�e follow-up suggest t�e presence of adaptive antibo-
dies t�at are involved in tumor pat�ogenesis directly
or indirectly. A furt�er monitoring of patients and t�e
survival analysis are now underway to evaluate t�e
prognostic significance of antibodies.
ACKNOWLEDGEMENTS
We are grateful to Professor N. Bovin for consulta-
tions and for providing us wit� synt�etic glycoconju-
gates�� to Dr. A. Lipping for providing us wit� �istological
data�� to T. Smorodina for subject searc��� to R. Syld
for correcting Englis� and to A. Kull for tec�nical as-
sistance. T�e study was supported by t�e Estonian
Science Foundation�� grants No 4��4� and No �����.
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Соотношение между уРоВнем IIgG �нтите�� �� G �нтите�� �� GGalNAc бет�
и диС�Х�Риду П�Р� — ФоРСм�нн� В СЫВоРот��е ��РоВи
и ПРоГРеССиеЙ, � т���же СтеПенью диФФеРенциРоВ��и
оПуХо��еЙ же��удоЧно-��ишеЧноГо тР���т�
В сыворотке крови человека ранее выявлены IgG-антитела к ��лево�оро�ны�� ли�ан�а�� GalNAcβ и GalNAcβ1-3GalNAcβIgG-антитела к ��лево�оро�ны�� ли�ан�а�� GalNAcβ и GalNAcβ1-3GalNAcβ-антитела к ��лево�оро�ны�� ли�ан�а�� GalNAcβ и GalNAcβ1-3GalNAcβGalNAcβ и GalNAcβ1-3GalNAcβ и GalNAcβ1-3GalNAcβGalNAcβ1-3GalNAcβ1-3GalNAcβGalNAcβ
(�исахари� Пара — Форс��анна, PFdi).PFdi).). Цель иссле�ования — выяснение связи повышенно�о �ровня антител с про�рессией
и �истоло�ически��и особенностя��и оп�холей жел��очно-кишечно�о тракта. Методы: обсле�овали 159 больных рако��
жел��ка, 88 — рако�� кишечника и 96 з�оровых лю�ей — �оноров крови. Уровень специфических IgG-антител опре�елялиIgG-антител опре�еляли-антител опре�еляли
��ето�о�� ИФА с использование�� синтетических конъю�атов полиакрила��и�а (ПАА), GalNAcβ-ПАА и PFdi-ПАА. �пре�елениеGalNAcβ-ПАА и PFdi-ПАА. �пре�еление-ПАА и PFdi-ПАА. �пре�елениеPFdi-ПАА. �пре�еление-ПАА. �пре�еление
биохи��ических и �е��атоло�ических показателей прово�или с использование�� авто��атических анализаторов. Результаты:
�ровень анти-PFdi IgG � пациентов со злокачественны��и новообразования��и в ста�иях II–IV (PFdi IgG � пациентов со злокачественны��и новообразования��и в ста�иях II–IV ( IgG � пациентов со злокачественны��и новообразования��и в ста�иях II–IV (IgG � пациентов со злокачественны��и новообразования��и в ста�иях II–IV ( � пациентов со злокачественны��и новообразования��и в ста�иях II–IV (II–IV (–IV (IV ( (P = 0,0002 – 0,04) �остоверно
выше, че�� � �оноров. Повышенный �ро вень анти-PFdi IgG ассоциировался с про�рессией рака жел��ка (в ста�иях II–IV поPFdi IgG ассоциировался с про�рессией рака жел��ка (в ста�иях II–IV по IgG ассоциировался с про�рессией рака жел��ка (в ста�иях II–IV поII–IV по–IV поIV по по
сравнению со ста�ией I (I ((P = 0,004 – 0,06) и �величение�� раз��ера оп�холи (T2 + T3 по сравнению с T1, ста�ии I, II;T2 + T3 по сравнению с T1, ста�ии I, II;2 + T3 по сравнению с T1, ста�ии I, II;T3 по сравнению с T1, ста�ии I, II;3 по сравнению с T1, ста�ии I, II;T1, ста�ии I, II;1, ста�ии I, II;I, II;, II;II;; P = 0.03).
Различия в �ровнях анти-GalNAcGalNAcβ IgG незначительные. �е выявлено взаи��освязи ��еж�� �ровне�� антител и ��етастазиро-IgG незначительные. �е выявлено взаи��освязи ��еж�� �ровне�� антител и ��етастазиро-незначительные. �е выявлено взаи��освязи ��еж�� �ровне�� антител и ��етастазиро-
вание�� оп�холей жел��ка и кишечника. Более низкий �ровень анти-GalNAcGalNAcβ IgG опре�еляли � больных с ��енее �ифферен-IgG опре�еляли � больных с ��енее �ифферен- опре�еляли � больных с ��енее �ифферен-
цированны��и оп�холя��и (P = 0,01 – 0,04). В перио� послеоперационно�о наблю�ения от��ечали из��енения �ровня обоих
типов антител. После хир�р�ическо�о ��аления оп�холей ор�анов жел��очно-кишечно�о тракта (ста�ия �ифференцировки
G3) повышался �ровень как анти-PFdi IgG, так и анти-GalNAc3) повышался �ровень как анти-PFdi IgG, так и анти-GalNAcPFdi IgG, так и анти-GalNAc IgG, так и анти-GalNAcGalNAcβ IgG (IgG ( (P = 0,003 – 0,01). Уровень анти-PFdi IgG коррелировалPFdi IgG коррелировал IgG коррелировал
с �ровне�� С-реактивно�о белка (r = 0,50, P = 0,003), а �ровень анти-GalNAcβ IgG — с относительны�� количество�� ��оно-GalNAcβ IgG — с относительны�� количество�� ��оно- IgG — с относительны�� количество�� ��оно-IgG — с относительны�� количество�� ��оно- — с относительны�� количество�� ��оно-
цитов в периферической крови (r = 0,42, P = 0,002). Выводы: �становлена зависи��ость �ровня анти-PFdi IgG от оп�холевойPFdi IgG от оп�холевой IgG от оп�холевой
про�рессии, что по�тверж�ает их �частие в пато�енезе злокачественных новообразований ор�анов жел��очно-кишечно�о
тракта. �еобхо�и��ы �альнейшие иссле�ования по опре�елению приро�ных ��ишеней �ля антител, роли в развитии �р��их
заболеваний и про�ностическо�� значении при онколо�ической патоло�ии.
Ключевые слова: GalNAc бета1-3GalNAc бета, Пара — Форс��анн, полиакрила��и�-�ликоконъю�аты, IgG антитела, ракGalNAc бета1-3GalNAc бета, Пара — Форс��анн, полиакрила��и�-�ликоконъю�аты, IgG антитела, рак бета1-3GalNAc бета, Пара — Форс��анн, полиакрила��и�-�ликоконъю�аты, IgG антитела, ракGalNAc бета, Пара — Форс��анн, полиакрила��и�-�ликоконъю�аты, IgG антитела, рак бета, Пара — Форс��анн, полиакрила��и�-�ликоконъю�аты, IgG антитела, ракIgG антитела, рак антитела, рак
жел��ка, рак кишечника.
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