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Published in: Annals of Surgical Oncology 6/2007

01-06-2007

α1,2Fucosylation Is a Superior Predictor of Postoperative Prognosis for Colorectal Cancer Compared with Blood Group A, B, or Sialyl Lewis X Antigen Generated within Colorectal Tumor Tissues

Authors: Kaori Tsuboi, MD, Takayuki Asao, MD, PhD, Munenori Ide, MD, PhD, Shinji Hashimoto, MD, Kasumi Noguchi, PhD, Yoshihiko Kominato, MD, PhD, Abby R. Saniabadi, PhD, Hiroyuki Kuwano, MD, PhD, Shin Yazawa, PhD

Published in: Annals of Surgical Oncology | Issue 6/2007

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Abstract

Background

We have previously demonstrated tumor-specific α1,2fucosylation, which is associated with resistance of tumor cells to anticancer treatment in human colorectal tumor tissues. By using the YB-2 monoclonal antibody, the resulting products have been identified as Y, Leb, and H type 2 antigens in colorectal tumor tissues.

Methods

Immunohistochemical analyses of colorectal cancer tissues (74 specimens) were performed with a newly established mouse monoclonal antibody, YB-3 specifically recognizing H disaccharide (Fucα1,2Galβ) structures, and anti-A, anti-B, YB-2, and anti–sialyl Lewis X (SLX) antibodies, together with the analyses of glycosyltransferases involved in the synthesis of ABH antigens in the same tissues.

Results

The YB-3 antibody enabled us to detect colorectal tumors, particularly tumors in the distal large intestine and the rectum, with high sensitivity (74.3%) and specificity (100%). From immunohistochemical and enzymatic analyses of colorectal tissues, we found that once α1,2fucosylation had proceeded in tumor tissues, blood group A or B antigen was also synthesized in approximately half of the tissues of A or B blood type, but not in their normal tissues. A correlation of survival rate with immunostaining of tissues was found only by YB-3 antibody and not by anti-A, anti-B, or anti-SLX antibody.

Conclusions

As a predictor of postoperative prognosis of patients with colorectal cancer, immunodetection of α1,2fucosylated antigens with the YB-3 antibody seemed to be superior to blood groups A, B, or SLX antigen in colorectal tumor tissues.
Literature
1.
go back to reference Hakomori S. Antigen structure and genetic basis of histo-blood groups A, B and O: their changes associated with human cancer. Biochim Biophys Acta 1999;1473:247–66PubMed Hakomori S. Antigen structure and genetic basis of histo-blood groups A, B and O: their changes associated with human cancer. Biochim Biophys Acta 1999;1473:247–66PubMed
2.
go back to reference Le Pendu J, Marionneau S, Cailleau-Thomas A, et al. ABH and Lewis histo-blood group antigens in cancer. APMIS 2001;109:9–31PubMedCrossRef Le Pendu J, Marionneau S, Cailleau-Thomas A, et al. ABH and Lewis histo-blood group antigens in cancer. APMIS 2001;109:9–31PubMedCrossRef
3.
go back to reference Varki A. Glycosylation changes in cancers. In: Varki A, Cummings R, Esko J, Freeze H, Hart G, Marth J, eds. Essentials of Glycobiology, Cold Spring Harbor NY: Cold Spring Harbor Press, 1999;537–49 Varki A. Glycosylation changes in cancers. In: Varki A, Cummings R, Esko J, Freeze H, Hart G, Marth J, eds. Essentials of Glycobiology, Cold Spring Harbor NY: Cold Spring Harbor Press, 1999;537–49
4.
go back to reference Yazawa S, Nishihara S, Iwasaki H, et al. Genetic and enzymatic evidence for Lewis enzyme expression in Lewis-negative cancer patients. Cancer Res 1995;55:1473–8PubMed Yazawa S, Nishihara S, Iwasaki H, et al. Genetic and enzymatic evidence for Lewis enzyme expression in Lewis-negative cancer patients. Cancer Res 1995;55:1473–8PubMed
5.
go back to reference Nakamura J, Mogi A, Asao T, Nagamachi Y, Yazawa S. Evidence that the aberrant αl→2fucosyltransferase found in colorectal carcinoma may be encoded by Fuc-TIII (Le) gene. Anticancer Res 1997;17:4563–9PubMed Nakamura J, Mogi A, Asao T, Nagamachi Y, Yazawa S. Evidence that the aberrant αl→2fucosyltransferase found in colorectal carcinoma may be encoded by Fuc-TIII (Le) gene. Anticancer Res 1997;17:4563–9PubMed
6.
go back to reference Ørntoft TF, Greenwell P, Clausen H, Watkins WM. Regulation of the oncodevelopmental expression of type 1 chain ABH and Lewis(b) blood group antigens in human colon by alpha-2-L-fucosylation. Gut 1991;32:287–93PubMed Ørntoft TF, Greenwell P, Clausen H, Watkins WM. Regulation of the oncodevelopmental expression of type 1 chain ABH and Lewis(b) blood group antigens in human colon by alpha-2-L-fucosylation. Gut 1991;32:287–93PubMed
7.
go back to reference Yazawa S, Akamatsu S, Tachikawa T, et al. Development and characterization of a novel anti-fucosylated antigen monoclonal antibody YB-2 and its usefulness in the immunohistochemical diagnosis of colorectal cancer. Jpn J Cancer Res 1993;84:641–8PubMed Yazawa S, Akamatsu S, Tachikawa T, et al. Development and characterization of a novel anti-fucosylated antigen monoclonal antibody YB-2 and its usefulness in the immunohistochemical diagnosis of colorectal cancer. Jpn J Cancer Res 1993;84:641–8PubMed
8.
go back to reference Akamatsu S, Yazawa S, Tachikawa T, et al. α2→3sialyltransferase associated with the synthesis of CA 19-9 in colorectal tumors. Cancer 1996;77:1694–700PubMed Akamatsu S, Yazawa S, Tachikawa T, et al. α2→3sialyltransferase associated with the synthesis of CA 19-9 in colorectal tumors. Cancer 1996;77:1694–700PubMed
9.
go back to reference Naitoh H, Nakajima T, Nagamachi Y, Yazawa S. A clinicopathological evaluation of anti-fucosylated antigens antibody (YB-2) in colorectal carcinoma. Glycosylation Dis 1994;1:31–6CrossRef Naitoh H, Nakajima T, Nagamachi Y, Yazawa S. A clinicopathological evaluation of anti-fucosylated antigens antibody (YB-2) in colorectal carcinoma. Glycosylation Dis 1994;1:31–6CrossRef
10.
go back to reference Yazawa S, Nakamura J, Asao T, et al. Aberrant α1→2 fucosyltransferases found in human colorectal carcinoma involved in the accumulation of Leb and Y antigens in colorectal tumors. Jpn J Cancer Res 1993;84:989–95PubMed Yazawa S, Nakamura J, Asao T, et al. Aberrant α1→2 fucosyltransferases found in human colorectal carcinoma involved in the accumulation of Leb and Y antigens in colorectal tumors. Jpn J Cancer Res 1993;84:989–95PubMed
11.
go back to reference Yazawa S, Nishimura T, Ide M, et al. Tumor-related expression of α 1,2fucosylated antigens on colorectal carcinoma cells and its suppression by cell-mediated priming using sugar acceptors for α1,2fucosyltransferase. Glycobiology 2002;12:545–53PubMedCrossRef Yazawa S, Nishimura T, Ide M, et al. Tumor-related expression of α 1,2fucosylated antigens on colorectal carcinoma cells and its suppression by cell-mediated priming using sugar acceptors for α1,2fucosyltransferase. Glycobiology 2002;12:545–53PubMedCrossRef
12.
go back to reference Sun J, Thurin J, Cooper HS, et al. Elevated expression of H type GDP-L-fucose: β-D-galactoside α-2-L-fucosyltransferase is associated with human colon adenocarcinoma progression. Proc Natl Acad Sci U S A 1995;92:5724–8PubMedCrossRef Sun J, Thurin J, Cooper HS, et al. Elevated expression of H type GDP-L-fucose: β-D-galactoside α-2-L-fucosyltransferase is associated with human colon adenocarcinoma progression. Proc Natl Acad Sci U S A 1995;92:5724–8PubMedCrossRef
13.
go back to reference Orlow I, Lacombe L, Pellicer I, et al. Genotype and phenotypic characterization of the histoblood groups ABO(H) in primary bladder tumors. Int J Cancer 1998;75:819–24PubMedCrossRef Orlow I, Lacombe L, Pellicer I, et al. Genotype and phenotypic characterization of the histoblood groups ABO(H) in primary bladder tumors. Int J Cancer 1998;75:819–24PubMedCrossRef
14.
go back to reference Iwamoto S, Withers DA, Handa K, Hakomori S. Deletion of A-antigen in a human cancer cell line is associated with reduced promoter activity of CBF/NF-Y binding region, and possibly with enhanced DNA methylation of A transferase promoter. Glycoconjugate J 1999;16:659–66CrossRef Iwamoto S, Withers DA, Handa K, Hakomori S. Deletion of A-antigen in a human cancer cell line is associated with reduced promoter activity of CBF/NF-Y binding region, and possibly with enhanced DNA methylation of A transferase promoter. Glycoconjugate J 1999;16:659–66CrossRef
15.
go back to reference Kominato Y, Hata Y, Takizawa H, Tsuchiya T, Tsukada J, Yamamoto F. Expression of human histo-blood group ABO genes is dependent upon DNA methylation of the promoter region. J Biol Chem 1999;274:37240–50PubMedCrossRef Kominato Y, Hata Y, Takizawa H, Tsuchiya T, Tsukada J, Yamamoto F. Expression of human histo-blood group ABO genes is dependent upon DNA methylation of the promoter region. J Biol Chem 1999;274:37240–50PubMedCrossRef
16.
go back to reference Gao S, Worm J, Guldberd P, et al. Genetic and epigenetic alteration of the blood group ABO gene in oral squamous cell carcinoma. Int J Cancer 2004;109:230–7PubMedCrossRef Gao S, Worm J, Guldberd P, et al. Genetic and epigenetic alteration of the blood group ABO gene in oral squamous cell carcinoma. Int J Cancer 2004;109:230–7PubMedCrossRef
17.
go back to reference Ichikawa D, Handa K, Withers DA, Hakomori S. Histo-blood group A/B versus H status of human carcinoma cells as correlated with haptotactic cell motility: approach with A and B gene transfection. Cancer Res 1997;57:3092–6PubMed Ichikawa D, Handa K, Withers DA, Hakomori S. Histo-blood group A/B versus H status of human carcinoma cells as correlated with haptotactic cell motility: approach with A and B gene transfection. Cancer Res 1997;57:3092–6PubMed
18.
go back to reference Ichikawa D, Handa K, Hakomori S. Histo-blood group A/B antigen deletion/ reduction vs. continuous expression in human tumor cells as correlated with their malignancy. Int J Cancer 1998;76:284–9PubMedCrossRef Ichikawa D, Handa K, Hakomori S. Histo-blood group A/B antigen deletion/ reduction vs. continuous expression in human tumor cells as correlated with their malignancy. Int J Cancer 1998;76:284–9PubMedCrossRef
19.
go back to reference Gao S, Bennett EP, Reibel J, et al. Histo-blood group ABO antigen in oral potentially malignant lesions and squamous cell carcinoma-genotypic and phenotypic characterization. APMIS 2004;112:11–20PubMedCrossRef Gao S, Bennett EP, Reibel J, et al. Histo-blood group ABO antigen in oral potentially malignant lesions and squamous cell carcinoma-genotypic and phenotypic characterization. APMIS 2004;112:11–20PubMedCrossRef
20.
go back to reference Graziano SL, Tatum AH, Gonchoroff NJ, Newman NB, Kohman LJ. Blood group antigen A and flow cytometric analysis in resected early-stage non–small cell lung cancer. Clin Cancer Res 1997;3:87–93PubMed Graziano SL, Tatum AH, Gonchoroff NJ, Newman NB, Kohman LJ. Blood group antigen A and flow cytometric analysis in resected early-stage non–small cell lung cancer. Clin Cancer Res 1997;3:87–93PubMed
21.
go back to reference Yazawa S, Takeya A, Hosomi O, et al. Use of synthetic H disaccharides as acceptors for detecting activities of UDP-GalNAc:Fuc αl→2Gal β-R α1→3-N-acetylgalactosaminyltransferase in plasma samples from blood group A subgroups. Clin Chem 1992;38:2392–5PubMed Yazawa S, Takeya A, Hosomi O, et al. Use of synthetic H disaccharides as acceptors for detecting activities of UDP-GalNAc:Fuc αl→2Gal β-R α1→3-N-acetylgalactosaminyltransferase in plasma samples from blood group A subgroups. Clin Chem 1992;38:2392–5PubMed
22.
go back to reference Sobin LH, Wittekind C, eds. TNM: Classification of Malignant Tumours. 6th ed. New York: Wiley-Liss, 2002 Sobin LH, Wittekind C, eds. TNM: Classification of Malignant Tumours. 6th ed. New York: Wiley-Liss, 2002
23.
go back to reference Yazawa S, Madiyalakan R, Izawa H, et al. Cancer-associated elevation of α(l→3)-L-fucosyltransferase activity in human serum. Cancer 1988;62:516–520PubMedCrossRef Yazawa S, Madiyalakan R, Izawa H, et al. Cancer-associated elevation of α(l→3)-L-fucosyltransferase activity in human serum. Cancer 1988;62:516–520PubMedCrossRef
24.
go back to reference Yazawa S, Asao T, Izawa H, et al. The presence of CA19-9 in serum and saliva from Lewis blood-group negative cancer patients. Jpn J Cancer Res 1988;79:538–43PubMed Yazawa S, Asao T, Izawa H, et al. The presence of CA19-9 in serum and saliva from Lewis blood-group negative cancer patients. Jpn J Cancer Res 1988;79:538–43PubMed
25.
go back to reference Akamatsu S, Yazawa S, Zenita K, et al. Elevation of an α(l,3)fucosyltransferase activity correlated with apoptosis in human colon adenocarcinoma cell line, HT-29. Glycoconj J 1996;13:985–93CrossRef Akamatsu S, Yazawa S, Zenita K, et al. Elevation of an α(l,3)fucosyltransferase activity correlated with apoptosis in human colon adenocarcinoma cell line, HT-29. Glycoconj J 1996;13:985–93CrossRef
26.
go back to reference Nishihara S, Hiraga T, Ikehara Y, et al. Molecular mechanisms of expression of Lewis b antigen and other type 1 Lewis antigens in human colorectal cancer. Glycobiology 1999;9:607–16PubMedCrossRef Nishihara S, Hiraga T, Ikehara Y, et al. Molecular mechanisms of expression of Lewis b antigen and other type 1 Lewis antigens in human colorectal cancer. Glycobiology 1999;9:607–16PubMedCrossRef
27.
go back to reference Fujitani N, Liu Y, Toda S, et al. Expression of H type 1 antigen of ABO histo-blood group in normal colon and aberrant expressions of H type 2 and H type 3/4 antigens in colon cancer. Glycoconjugate J 2000;17:331–8CrossRef Fujitani N, Liu Y, Toda S, et al. Expression of H type 1 antigen of ABO histo-blood group in normal colon and aberrant expressions of H type 2 and H type 3/4 antigens in colon cancer. Glycoconjugate J 2000;17:331–8CrossRef
28.
go back to reference Hakomori S. Tumor malignancy of defined by aberrant glycosylation and sphingo-(glyco)lipid metabolism. Cancer Res 1996;56:5309–18PubMed Hakomori S. Tumor malignancy of defined by aberrant glycosylation and sphingo-(glyco)lipid metabolism. Cancer Res 1996;56:5309–18PubMed
29.
go back to reference Lee JS, Ro JY, Sahin AA, et al. Expression of blood-group antigen-A—a favorable prognostic factor in non–small-cell lung cancer. N Engl J Med 1991;324:1084–90PubMedCrossRef Lee JS, Ro JY, Sahin AA, et al. Expression of blood-group antigen-A—a favorable prognostic factor in non–small-cell lung cancer. N Engl J Med 1991;324:1084–90PubMedCrossRef
30.
go back to reference Dabelsteen E. ABO blood group antigens in oral mucosa. What is new? J Oral Pathol Med 2002;31:65–70PubMed Dabelsteen E. ABO blood group antigens in oral mucosa. What is new? J Oral Pathol Med 2002;31:65–70PubMed
31.
go back to reference Marionneau S, Le Moullac-Vaidve B, Le Pendu J. Expression of histo-blood group A antigen increases resistance to apoptosis and facilitates escape from immune control of rat colon carcinoma cells. Glycobiology 2002;12:851–6PubMedCrossRef Marionneau S, Le Moullac-Vaidve B, Le Pendu J. Expression of histo-blood group A antigen increases resistance to apoptosis and facilitates escape from immune control of rat colon carcinoma cells. Glycobiology 2002;12:851–6PubMedCrossRef
32.
go back to reference Nakagoe T, Nanashima A, Sawai T, et al. Expression of blood group antigens A, B and H in carcinoma tissue correlates with a poor prognosis for colorectal cancer patients. J Cancer Res Clin Oncol 2000;126:375–82PubMedCrossRef Nakagoe T, Nanashima A, Sawai T, et al. Expression of blood group antigens A, B and H in carcinoma tissue correlates with a poor prognosis for colorectal cancer patients. J Cancer Res Clin Oncol 2000;126:375–82PubMedCrossRef
33.
go back to reference Nakagoe T, Fukushima K, Nanashima A, et al. Comparison of the expression of ABH/Lewis-related antigens in polypoid and non-polypoid growth types of colorectal carcinoma. J Gastroenterol Hepatol 2001;16:176–83PubMedCrossRef Nakagoe T, Fukushima K, Nanashima A, et al. Comparison of the expression of ABH/Lewis-related antigens in polypoid and non-polypoid growth types of colorectal carcinoma. J Gastroenterol Hepatol 2001;16:176–83PubMedCrossRef
34.
go back to reference Sakuma Y, Kubishiro K, Tsukazaki K, Nozawa S. Involvement of H type 1 carbohydrate antigen in cell adhesion to vascular endothelial cells of human endometrial cancer. Anticancer Res 2003;23:1277–82PubMed Sakuma Y, Kubishiro K, Tsukazaki K, Nozawa S. Involvement of H type 1 carbohydrate antigen in cell adhesion to vascular endothelial cells of human endometrial cancer. Anticancer Res 2003;23:1277–82PubMed
35.
go back to reference Nakamura M, Kudo T, Narimatsu H, et al. Single glycosyltransferase, core 2 β1→6-N-actylglucosaminyltransferase, regulates cell surface sialyl-Lex expression level in human pre-B lymphocytic leukemia cell line KM3 treated with phorbolester. J Biol Chem 1998;273:26779–89PubMedCrossRef Nakamura M, Kudo T, Narimatsu H, et al. Single glycosyltransferase, core 2 β1→6-N-actylglucosaminyltransferase, regulates cell surface sialyl-Lex expression level in human pre-B lymphocytic leukemia cell line KM3 treated with phorbolester. J Biol Chem 1998;273:26779–89PubMedCrossRef
36.
go back to reference Mathieu S, Prorol M, Benoliel A, et al. Transgene expression of α(l,2)-fucosyltransfease-I (FUT1) in tumor cells selectively inhibits sialyl-Lewis x expression and binding to E-selectin without affecting synthesis of sialyl-Lewis or binding to P-selecin. Am J Pathol 2004;164:371–83PubMed Mathieu S, Prorol M, Benoliel A, et al. Transgene expression of α(l,2)-fucosyltransfease-I (FUT1) in tumor cells selectively inhibits sialyl-Lewis x expression and binding to E-selectin without affecting synthesis of sialyl-Lewis or binding to P-selecin. Am J Pathol 2004;164:371–83PubMed
37.
go back to reference Labarrière N, Pian JP, Otry C, et al. H blood group antigen carried by CD44V modulates tumorigenicity of rat colon carcinoma cells. Cancer Res 1994;54:6275–81PubMed Labarrière N, Pian JP, Otry C, et al. H blood group antigen carried by CD44V modulates tumorigenicity of rat colon carcinoma cells. Cancer Res 1994;54:6275–81PubMed
38.
go back to reference Goupille C, Hallouin F, Meflah K, Le Pendu J. Increase of rat colon carcinoma cells tumorigenicity by α(l-2)fucosyltransferase gene transfection. Glycobiology 1997;7:221–9PubMedCrossRef Goupille C, Hallouin F, Meflah K, Le Pendu J. Increase of rat colon carcinoma cells tumorigenicity by α(l-2)fucosyltransferase gene transfection. Glycobiology 1997;7:221–9PubMedCrossRef
39.
go back to reference Hallouin F, Goupille C, Bureau V, Meflah K, Le Pendu J. Increased tumorigenicity of rat colon carcinoma cells after 2-fucosyltranferase FTA anti-sense cDNA transfection. Int J Cancer 1999;80:601–11CrossRef Hallouin F, Goupille C, Bureau V, Meflah K, Le Pendu J. Increased tumorigenicity of rat colon carcinoma cells after 2-fucosyltranferase FTA anti-sense cDNA transfection. Int J Cancer 1999;80:601–11CrossRef
40.
go back to reference Cordel S, Goupille C, Hallouin F, et al. Role of α1,2fucosyltransferase and histo-blood group H antigen type 2 in resistance of rat colon carcinoma cells to 5-fluorouracil. Int J Cancer 2000;85:142–8PubMedCrossRef Cordel S, Goupille C, Hallouin F, et al. Role of α1,2fucosyltransferase and histo-blood group H antigen type 2 in resistance of rat colon carcinoma cells to 5-fluorouracil. Int J Cancer 2000;85:142–8PubMedCrossRef
41.
go back to reference Goupille C, Marionneau S, Bureau V, et al. α1,2Fucosyltransferase increases resistance to apoptosis of rat colon carcinoma cells. Glycobiology 2000;10:375–82PubMedCrossRef Goupille C, Marionneau S, Bureau V, et al. α1,2Fucosyltransferase increases resistance to apoptosis of rat colon carcinoma cells. Glycobiology 2000;10:375–82PubMedCrossRef
42.
go back to reference Zerfaoui M, Fukuda M, Sbarra V, Lombardo D, El-Battari A. α(l,2)-Fucosylation prevents sialyl Lewis x expression and E-selectin–mediated adhesion of fucosyltransferase VII-transfected cells. Eur J Biochem 2000;267:53–60PubMedCrossRef Zerfaoui M, Fukuda M, Sbarra V, Lombardo D, El-Battari A. α(l,2)-Fucosylation prevents sialyl Lewis x expression and E-selectin–mediated adhesion of fucosyltransferase VII-transfected cells. Eur J Biochem 2000;267:53–60PubMedCrossRef
43.
go back to reference Chihara Y, Sugano K, Kobayashi A, et al. Loss of blood group A antigen expression in bladder cancer caused by allelic loss and/or methylation of the ABO gene. Lab Invest 2005;85:895–907PubMedCrossRef Chihara Y, Sugano K, Kobayashi A, et al. Loss of blood group A antigen expression in bladder cancer caused by allelic loss and/or methylation of the ABO gene. Lab Invest 2005;85:895–907PubMedCrossRef
Metadata
Title
α1,2Fucosylation Is a Superior Predictor of Postoperative Prognosis for Colorectal Cancer Compared with Blood Group A, B, or Sialyl Lewis X Antigen Generated within Colorectal Tumor Tissues
Authors
Kaori Tsuboi, MD
Takayuki Asao, MD, PhD
Munenori Ide, MD, PhD
Shinji Hashimoto, MD
Kasumi Noguchi, PhD
Yoshihiko Kominato, MD, PhD
Abby R. Saniabadi, PhD
Hiroyuki Kuwano, MD, PhD
Shin Yazawa, PhD
Publication date
01-06-2007
Publisher
Springer-Verlag
Published in
Annals of Surgical Oncology / Issue 6/2007
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-007-9363-2

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