Biological significance of cancer-associated sialyl-Tn antigen: Modulation of malignant phenotype in gastric carcinoma cells

Cancer Letters

Volumn 249, Issue 2, 2007, Pages 157-170

  Pinho, Sandra ^a   Marcos, Nuno T ^a   Ferreira, Bibiana ^a   Carvalho, Ana S ^a   Oliveira, Maria J ^a   Santos Silva, Filipe ^a,b   Harduin Lepers, Anne ^c   Reis, Celso A ^a,b  

^a UNIVERSITY OF PORTO   (Portugal)

^b University of Porto   (Portugal)

^c UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

Author keywords

Adhesion; Gastric carcinoma; Invasion; Malignant phenotype; Sialyl Tn; Sialyltransferase

Indexed keywords

ACTIN; ANTIBODY; CARBOHYDRATE; GLYCAN; SIALYL TN ANTIGEN; TN ANTIGEN; UNCLASSIFIED DRUG;

ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CANCER GROWTH; CARCINOMA CELL; CELL ADHESION; CELL AGGREGATION; CELL CYCLE; CELL FUNCTION; CELL INVASION; CELL MOTILITY; CELL STRUCTURE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GLYCOSYLATION; HUMAN; HUMAN CELL; IMMUNOMODULATION; PHENOTYPE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; STOMACH CARCINOMA;

ANTIGENS, NEOPLASM; ANTIGENS, TUMOR-ASSOCIATED, CARBOHYDRATE; APOPTOSIS; CARCINOMA; CELL ADHESION; CELL AGGREGATION; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; HUMANS; MUCINS; NEOPLASM INVASIVENESS; PHENOTYPE; SIALYLTRANSFERASES; STOMACH NEOPLASMS;

EID: 33947423328     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2006.08.010     Document Type: Article

References (68)

1. Hakomori S. Tumor malignancy defined by aberrant glycosylation and sphingo(glyco)lipid metabolism. Cancer Res. 56 (1996) 5309-5318
2. Kannagi R. Carbohydrate-mediated cell adhesion involved in hematogenous metastasis of cancer. Glycoconj. J. 14 (1997) 577-584
3. Collard J.G., Schijven J.F., Bikker A., La Riviere G., Bolscher J.G., and Roos E. Cell surface sialic acid and the invasive and metastatic potential of T-cell hybridomas. Cancer Res. 46 (1986) 3521-3527
4. Lin S., Kemmner W., Grigull S., and Schlag P.M. Cell surface α2,6-sialylation affects adhesion of breast carcinoma cells. Exp. Cell Res. 276 (2002) 101-110
5. Sawada M., Moriya S., Saito S., Shineha R., Satomi S., Yamori T., Tsuruo T., Kannagi R., and Miyagi T. Reduced sialidase expression in highly metastatic variants of mouse colon adenocarcinoma 26 and retardation of their metastatic ability by sialidase overexpression. Int. J. Cancer 97 (2002) 180-185
6. Baldus S.E., and Hanisch F.G. Biochemistry and pathological importance of mucin-associated antigens in gastrointestinal neoplasia. Adv. Cancer Res. 79 (2000) 201-248
7. David L., Nesland J.M., Clausen H., Carneiro F., and Sobrinho-Simoes M. Simple mucin-type carbohydrate antigens (Tn, sialosyl-Tn and T) in gastric mucosa, carcinomas and metastases. APMIS Suppl. 27 (1992) 162-172
8. Victorzon M., Nordling S., Nilsson O., Roberts P.J., and Haglund C. Sialyl-Tn antigen is an independent predictor of outcome in patients with gastric cancer. Int. J. Cancer 65 (1996) 295-300
9. Itzkowitz S.H., Bloom E.J., Kokal W.A., Modin G., Hakomori S., and Kim Y.S. Sialosyl-Tn. A novel mucin antigen associated with prognosis in colorectal cancer patients. Cancer 66 (1990) 1960-1966
10. Kobayashi H., Terao T., and Kawashima Y. Serum sialyl-Tn as an independent predictor of poor prognosis in patients with epithelial ovarian cancer. J. Clin. Oncol. 10 (1992) 95-101
11. Leivonen M., Nordling S., Lundin J., von Boguslawski K., and Haglund C. STn and prognosis in breast cancer. Oncology 61 (2001) 299-305
12. Yonezawa S., Tachikawa T., Shin S., and Sato E. Sialosyl-Tn antigen. Its distribution in normal human tissues and expression in adenocarcinomas. Am. J. Clin. Pathol. 98 (1992) 167-174
13. Kim G.E., Bae H.I., Park H.U., Kuan S.F., Crawley S.C., Ho J.J., and Kim Y.S. Aberrant expression of MUC5AC and MUC6 gastric mucins and sialyl-Tn antigen in intraepithelial neoplasms of the pancreas. Gastroenterology 123 (2002) 1052-1060
14. Nakagoe T., Sawai T., Tsuji T., Jibiki M.A., Nanashima A., Yamaguchi H., Yasutake T., Ayabe H., Arisawa K., and Ishikawa H. Predictive factors for preoperative serum levels of sialyl Lewis(x), sialyl Lewis(a) and sialyl-Tn antigens in gastric cancer patients. Anticancer Res. 22 (2002) 451-458
15. Werther J.L., Rivera-MacMurray S., Bruckner H., Tatematsu M., and Itzkowitz S.H. Mucin-associated sialosyl-Tn antigen expression in gastric cancer correlates with an adverse outcome. Br. J. Cancer 69 (1994) 613-616
16. Werther J.L., Tatematsu M., Klein R., Kurihara M., Kumagai K., Llorens P., Guidugli N.J., Bodian C., Pertsemlidis D., Yamachika T., Kitou T., and Itzkowitz S. Sialosyl-Tn antigen as a marker of gastric cancer progression: an international study. Int. J. Cancer 69 (1996) 193-199
17. Itzkowitz S.H., Bloom E.J., Lau T.S., and Kim Y.S. Mucin associated Tn and sialosyl-Tn antigen expression in colorectal polyps. Gut 33 (1992) 518-523
18. Karlen P., Young E., Brostrom O., Lofberg R., Tribukait B., Ost K., Bodian C., and Itzkowitz S. Sialyl-Tn antigen as a marker of colon cancer risk in ulcerative colitis: relation to dysplasia and DNA aneuploidy. Gastroenterology 115 (1998) 1395-1404
19. Holmberg L.A., Oparin D.V., Gooley T., Lilleby K., Bensinger W., Reddish M.A., MacLean G.D., Longenecker B.M., and Sandmaier B.M. Clinical outcome of breast and ovarian cancer patients treated with high-dose chemotherapy, autologous stem cell rescue and Theratope STn-KLH cancer vaccine. Bone Marrow Transplant. 25 (2000) 1233-1241
20. Holmberg L.A., Oparin D.V., Gooley T., and Sandmaier B.M. The role of cancer vaccines following autologous stem cell rescue in breast and ovarian cancer patients: experience with the STn-KLH vaccine (Theratope(R)). Clin. Breast Cancer 3 Suppl. 4 (2003) S144-S151
21. Holmberg L.A., and Sandmaier B.M. Vaccination with Theratope (STn-KLH) as treatment for breast cancer. Expert. Rev. Vaccines 3 (2004) 655-663
22. Kagan E., Ragupathi G., Yi S.S., Reis C.A., Gildersleeve J., Kahne D., Clausen H., Danishefsky S.J., and Livingston P.O. Comparison of antigen constructs and carrier molecules for augmenting the immunogenicity of the monosaccharide epithelial cancer antigen Tn. Cancer Immunol. Immunother. 54 (2005) 424-430
23. Soares M.M., Mehta V., and Finn O.J. Three different vaccines based on the 140-amino acid MUC1 peptide with seven tandemly repeated tumor-specific epitopes elicit distinct immune effector mechanisms in wild-type versus MUC1-transgenic mice with different potential for tumor rejection. J. Immunol. 166 (2001) 6555-6563
24. Vlad A.M., Muller S., Cudic M., Paulsen H., Otvos Jr. L., Hanisch F.G., and Finn O.J. Complex carbohydrates are not removed during processing of glycoproteins by dendritic cells: processing of tumor antigen MUC1 glycopeptides for presentation to major histocompatibility complex class II-restricted T cells. J. Exp. Med. 196 (2002) 1435-1446
25. Vlad A.M., and Finn O.J. Glycoprotein tumor antigens for immunotherapy of breast cancer. Breast Dis. 20 (2004) 73-79
26. Miles D.W., and Taylor-Papadimitriou J. Mucin based breast cancer vaccines. Expert. Opin. Investig. Drugs 7 (1998) 1865-1877
27. Taylor-Papadimitriou J., Burchell J., Miles D.W., and Dalziel M. MUC1 and cancer. Biochim. Biophys. Acta 1455 (1999) 301-313
28. Brockhausen I., Yang J., Dickinson N., Ogata S., and Itzkowitz S.H. Enzymatic basis for sialyl-Tn expression in human colon cancer cells. Glycoconj. J. 15 (1998) 595-603
29. Ikehara Y., Kojima N., Kurosawa N., Kudo T., Kono M., Nishihara S., Issiki S., Morozumi K., Itzkowitz S., Tsuda T., Nishimura S.I., Tsuji S., and Narimatsu H. Cloning and expression of a human gene encoding an N-acetylgalactosamine-α2,6-sialyltransferase (ST6GalNAc I): a candidate for synthesis of cancer-associated sialyl-Tn antigens. Glycobiology 9 (1999) 1213-1224
30. Kono M., Tsuda T., Ogata S., Takashima S., Liu H., Hamamoto T., Itzkowitz S.H., Nishimura S., and Tsuji S. Redefined substrate specificity of ST6GalNAc II: a second candidate sialyl-Tn synthase. Biochem. Biophys. Res. Commun. 272 (2000) 94-97
31. Samyn-Petit B., Krzewinski-Recchi M.A., Steelant W.F., Delannoy P., and Harduin-Lepers A. Molecular cloning and functional expression of human ST6GalNAc II. Molecular expression in various human cultured cells. Biochim. Biophys. Acta 1474 (2000) 201-211
32. Marcos N.T., Pinho S., Grandela C., Cruz A., Samyn-Petit B., Harduin-Lepers A., Almeida R., Silva F., Morais V., Costa J., Kihlberg J., Clausen H., and Reis C.A. Role of the human ST6GalNAc-I and ST6GalNAc-II in the synthesis of the cancer-associated sialyl-Tn antigen. Cancer Res. 64 (2004) 7050-7057
33. Sewell R., Backstrom M., Dalziel M., Gschmeissner S., Karlsson H., Noll T., Gatgens J., Clausen H., Hansson G.C., Burchell J., and Taylor-Papadimitriou J. The ST6GalNAc-I sialyltransferase localizes throughout the Golgi and is responsible for the synthesis of the tumor-associated sialyl-Tn O-glycan in human breast cancer. J. Biol. Chem. 281 (2006) 3586-3594
34. Brockhausen I., Yang J., Lehotay M., Ogata S., and Itzkowitz S. Pathways of mucin O-glycosylation in normal and malignant rat colonic epithelial cells reveal a mechanism for cancer-associated Sialyl-Tn antigen expression. Biol. Chem. 382 (2001) 219-232
35. Dall'Olio F., and Chiricolo M. Sialyltransferases in cancer. Glycoconj. J. 18 (2001) 841-850
36. Feizi T. Carbohydrate-mediated recognition systems in innate immunity. Immunol. Rev. 173 (2000) 79-88
37. Crocker P.R., and Varki A. Siglecs in the immune system. Immunology 103 (2001) 137-145
38. Hughes R.C. Galectins as modulators of cell adhesion. Biochimie 83 (2001) 667-676
39. Liotta L.A., and Kohn E.C. The microenvironment of the tumour-host interface. Nature 411 (2001) 375-379
40. Trusolino L., Bertotti A., and Comoglio P.M. A signaling adapter function for α6β4 integrin in the control of HGF-dependent invasive growth. Cell 107 (2001) 643-654
41. Ogata S., Maimonis P.J., and Itzkowitz S.H. Mucins bearing the cancer-associated sialosyl-Tn antigen mediate inhibition of natural killer cell cytotoxicity. Cancer Res. 52 (1992) 4741-4746
42. Marcos N.T., Cruz A., Silva F., Almeida R., David L., Mandel U., Clausen H., Mensdorff-Pouilly S., and Reis C.A. Polypeptide GalNAc-transferases, ST6GalNAc-transferase I, and ST3Gal-transferase I expression in gastric carcinoma cell lines. J. Histochem. Cytochem. 51 (2003) 761-771
43. Boteborg T., Bracke M.E., Bruyneel E.A., and Mareel M.M. Cell aggregation assays. In: Brooks S.A., and Shumacher U. (Eds). Metastasis Research Protocols: Analysis of Cell Behavior In Vitro and In Vivo vol. 2 (2000), Humana Press, Totowa, NJ 33-45
44. Taylor-Papadimitriou J., Peterson J.A., Arklie J., Burchell J., Ceriani R.L., and Bodmer W.F. Monoclonal antibodies to epithelium-specific components of the human milk fat globule membrane: production and reaction with cells in culture. Int. J. Cancer 28 (1981) 17-21
45. Adams J.C. Cell-matrix contact structures. Cell Mol. Life Sci. 58 (2001) 371-392
46. Hall A. Rho GTPases and the actin cytoskeleton. Science 279 (1998) 509-514
47. Dickeson S.K., Mathis N.L., Rahman M., Bergelson J.M., and Santoro S.A. Determinants of ligand binding specificity of the α(1)β(1) and α(2)β(1) integrins. J. Biol. Chem. 274 (1999) 32182-32191
48. Brown E.J., and Goodwin J.L. Fibronectin receptors of phagocytes. Characterization of the Arg-Gly-Asp binding proteins of human monocytes and polymorphonuclear leukocytes. J. Exp. Med. 167 (1988) 777-793
49. Veiga S.S., Chammas R., Cella N., and Brentani R.R. Glycosylation of β-1 integrins in B16-F10 mouse melanoma cells as determinant of differential binding and acquisition of biological activity. Int. J. Cancer 61 (1995) 420-424
50. Clement M., Rocher J., Loirand G., and Le Pendu J. Expression of sialyl-Tn epitopes on β1 integrin alters epithelial cell phenotype, proliferation and haptotaxis. J. Cell Sci. 117 (2004) 5059-5069
51. Burchell J., Gendler S., Taylor-Papadimitriou J., Girling A., Lewis A., Millis R., and Lamport D. Development and characterization of breast cancer reactive monoclonal antibodies directed to the core protein of the human milk mucin. Cancer Res. 47 (1987) 5476-5482
52. Girling A., Bartkova J., Burchell J., Gendler S., Gillett C., and Taylor-Papadimitriou J. A core protein epitope of the polymorphic epithelial mucin detected by the monoclonal antibody SM-3 is selectively exposed in a range of primary carcinomas. Int. J. Cancer 43 (1989) 1072-1076
53. Hollingsworth M.A., and Swanson B.J. Mucins in cancer: protection and control of the cell surface. Nat. Rev. Cancer 4 (2004) 45-60
54. Reis C.A., Hassan H., Bennett E.P., and Clausen H. Characterization of a panel of monoclonal antibodies using GalNAc glycosylated peptides and recombinant MUC1. Tumour. Biol. 19 Suppl. 1 (1998) 127-133
55. Burdick M.D., Harris A., Reid C.J., Iwamura T., and Hollingsworth M.A. Oligosaccharides expressed on MUC1 produced by pancreatic and colon tumor cell lines. J. Biol. Chem. 272 (1997) 24198-24202
56. Ligtenberg M.J., Buijs F., Vos H.L., and Hilkens J. Suppression of cellular aggregation by high levels of episialin. Cancer Res. 52 (1992) 2318-2324
57. Satoh S., Hinoda Y., Hayashi T., Burdick M.D., Imai K., and Hollingsworth M.A. Enhancement of metastatic properties of pancreatic cancer cells by MUC1 gene encoding an anti-adhesion molecule. Int. J. Cancer 88 (2000) 507-518
58. Wesseling J., van der Valk S.W., and Hilkens J. A mechanism for inhibition of E-cadherin-mediated cell-cell adhesion by the membrane-associated mucin episialin/MUC1. Mol. Biol. Cell 7 (1996) 565-577
59. Julien S., Lagadec C., Krzewinski-Recchi M.A., Courtand G., Bourhis X.L., and Delannoy P. Stable expression of sialyl-Tn antigen in T47-D cells induces a decrease of cell adhesion and an increase of cell migration. Breast Cancer Res. Treat. 90 (2005) 77-84
60. Julien S., Krzewinski-Recchi M.A., Harduin-Lepers A., Gouyer V., Huet G., Le B., and Delannoy X.P. Expression of sialyl-Tn antigen in breast cancer cells transfected with the human CMP-Neu5Ac: GalNAc α2,6-sialyltransferase (ST6GalNac I) cDNA. Glycoconj. J. 18 (2001) 883-893
61. Takenaka Y., Fukumori T., and Raz A. Galectin-3 and metastasis. Glycoconj. J. 19 (2004) 543-549
62. Kjeldsen T., Clausen H., Hirohashi S., Ogawa T., Iijima H., and Hakomori S. Preparation and characterization of monoclonal antibodies directed to the tumor-associated O-linked sialosyl-2-6 α-N-acetylgalactosaminyl (sialosyl-Tn) epitope. Cancer Res. 48 (1988) 2214-2220
63. Clausen H., Stroud M., Parker J., Springer G., and Hakomori S. Monoclonal antibodies directed to the blood group A associated structure, galactosyl-A: specificity and relation to the Thomsen-Friedenreich antigen. Mol. Immunol. 25 (1988) 199-204
64. Young Jr. W.W., Portoukalian J., and Hakomori S. Two monoclonal anticarbohydrate antibodies directed to glycosphingolipids with a lacto-N-glycosyl type II chain. J. Biol. Chem. 256 (1981) 10967-10972
65. Magnani J.L., Nilsson B., Brockhaus M., Zopf D., Steplewski Z., Koprowski H., and Ginsburg V. A monoclonal antibody-defined antigen associated with gastrointestinal cancer is a ganglioside containing sialylated lacto-N-fucopentaose II. J. Biol. Chem. 257 (1982) 14365-14369
66. Fukushi Y., Hakomori S., Nudelman E., and Cochran N. Novel fucolipids accumulating in human adenocarcinoma. II. Selective isolation of hybridoma antibodies that differentially recognize mono-, di-, and tri-fucosylated type 2 chain. J. Biol. Chem. 259 (1984) 4681-4685
67. Fukushi Y., Nudelman E., Levery S.B., Hakomori S., and Rauvala H. Novel fucolipids accumulating in human adenocarcinoma. III. A hybridoma antibody (FH6) defining a human cancer-associated difucoganglioside (VI3NeuAcV3III3Fuc2nLc6). J. Biol. Chem. 259 (1984) 10511-10517
68. Abe K., McKibbin J.M., and Hakomori S. The monoclonal antibody directed to difucosylated type 2 chain (Fuc α1 leads to 2Gal β1 leads to 4[Fuc α1 leads to 3]GlcNAc; Y determinant). J. Biol. Chem. 258 (1983) 11793-11797