Identification of new cancer biomarkers based on aberrant mucin glycoforms by in situ proximity ligation

Journal of Cellular and Molecular Medicine

Volumn 16, Issue 7, 2012, Pages 1474-1484

  Pinto, Rita ^a   Carvalho, Ana S ^a   Conze, Tim ^b   Magalhães, Ana ^a   Picco, Gianfranco ^c   Burchell, Joy M ^c   Taylor Papadimitriou, Joyce ^c   Reis, Celso A ^a,d   Almeida, Raquel ^a,d   Mandel, Ulla ^e   Clausen, Henrik ^e   Söderberg, Ola ^b   David, Leonor ^a,d  

^a UNIVERSITY OF PORTO   (Portugal)

^b UPPSALA UNIVERSITY   (Sweden)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d University of Porto   (Portugal)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Cancer biomarkers; Glycosylation; In situ proximity ligation assay (in situ PLA); Mucins; Post translational modifications (PTMs)

Indexed keywords

5 ACETYLNEURAMINYL (2 3) GALACTOSYL (1 4) (FUCOPYRANOSYL (1 3)) N ACETYLGLUCOSAMINE; 5-ACETYLNEURAMINYL-(2-3)-GALACTOSYL-(1-4)-(FUCOPYRANOSYL-(1-3))-N-ACETYLGLUCOSAMINE; GANGLIOSIDE; MUC1 PROTEIN, HUMAN; MUC2 PROTEIN, HUMAN; MUC5AC PROTEIN, HUMAN; MUC6 PROTEIN, HUMAN; MUCIN 1; MUCIN 2; MUCIN 5AC; MUCIN 6; OLIGOSACCHARIDE; SIALOSYL TN ANTIGEN; SIALOSYL-TN ANTIGEN; SIALYL LE(A) GANGLIOSIDE; TN ANTIGEN; TUMOR ANTIGEN; TUMOR MARKER;

ARTICLE; BREAST; COLLOID CARCINOMA; COLON; FLUORESCENT ANTIBODY TECHNIQUE; GLYCOSYLATION; HUMAN; IMMUNOHISTOCHEMISTRY; LUNG; METABOLISM; NEOPLASM; PATHOLOGY;

ADENOCARCINOMA, MUCINOUS; ANTIGENS, TUMOR-ASSOCIATED, CARBOHYDRATE; BREAST; COLON; FLUORESCENT ANTIBODY TECHNIQUE; GANGLIOSIDES; GLYCOSYLATION; HUMANS; IMMUNOHISTOCHEMISTRY; LUNG; MUCIN 5AC; MUCIN-1; MUCIN-2; MUCIN-6; NEOPLASMS; OLIGOSACCHARIDES; TUMOR MARKERS, BIOLOGICAL;

EID: 84863091545     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2011.01436.x     Document Type: Article

References (33)

1. Reis CA, Osório H, Silva L, et al. Alterations in glycosylation as biomarkers for cancer detection. J Clin Pathol. 2010; 63: 611-8.
2. Srensen AL, Reis CA, Tarp MA, et al. Chemoenzymatically synthesized multimeric Tn/STn MUC1 glycopeptides elicit cancer-specific anti-MUC1 antibody responses and override tolerance. Glycobiology. 2006; 16: 96-107.
3. Burchell J, Gendler S, Taylor -Papadimitriou J, et al. Development and characterization of breast cancer reactive monoclonal antibodies directed to the core protein of the human milk mucin. Cancer Res. 1987; 47: 5476-82.
4. Reis CA, Srensen T, Mandel U, et al. Development and characterization of an antibody directed to an alpha-N-acetyl-D-galactosamine glycosylated MUC2 peptide. Glycoconj J. 1998; 15: 51-62.
5. Blixt O, Cló E, Nudelman AS, et al. A high-throughput O-glycopeptide discovery platform for seromic profiling. J Proteome Res. 2010; 9: 5250-61.
6. Wandall HH, Blixt O, Tarp MA, et al. Cancer biomarkers defined by autoantibody signatures to aberrant O-glycopeptide epitopes. Cancer Res. 2010; 70: 1306-13.
7. Söderberg O, Gullberg M, Jarvius M, et al. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods. 2006; 3: 995-1000.
8. Weibrecht I, Leuchowius KJ, Clausson CM, et al. Proximity ligation assays: a recent addition to the proteomics toolbox. Expert Rev Proteomics. 2010; 7: 401-9.
9. Conze T, Carvalho AS, Landegren U, et al. MUC2 mucin is a major carrier of the cancer-associated sialyl-Tn antigen in intestinal metaplasia and gastric carcinomas. Glycobiology. 2010; 20: 199-206.
10. Edge SB, Byrd DR, Compton CC, et al., editors. AJCC Cancer staging manual. 7th ed. New York: Springer-Verlag; 2010.
11. Itzkowitz SH, Yuan M, Montgomery CK, et al. Expression of Tn, sialosyl-Tn, and T antigens in human colon cancer. Cancer Res. 1989; 49: 197-204.
12. Inoue M, Ton SM, Ogawa H, et al. Expression of Tn and sialyl-Tn antigens in tumour tissues of the ovary. Am J Clin Pathol. 1991; 96: 711-6.
13. Tashiro Y, Yonezawa S, Kim YS, et al. Immunohistochemical study of mucin carbohydrates and core proteins in human ovarian tumours. Hum Pathol. 1994; 25: 364-72.
14. Werther JL, Rivera -MacMurray S, Bruckner H, et al. Mucin-associated sialosyl-Tn antigen expression in gastric cancer correlates with an adverse outcome. Br J Cancer. 1994; 69: 613-6.
15. Terada T, Nakanuma Y. Expression of mucin carbohydrate antigens (T, Tn and sialyl Tn) and MUC-1 gene product in intraductal papillary-mucinous neoplasm of the pancreas. Am J Clin Pathol. 1996; 105: 613-29.
16. Cao Y, Schlag PM, Karsten U. Immunodetection of epithelial mucin (MUC1, MUC3) and mucin-associated glycotopes (TF, Tn, and sialosyl-Tn) in benign and malignant lesions of colonic epithelium: apolar localization corresponds to malignant transformation. Virchows Arch. 1997; 431: 159-66.
17. Ghazizadeh M, Ogawa H, Sasaki Y, et al. Mucin carbohydrate antigens (T, Tn, and sialyl-Tn) in human ovarian carcinomas: relationship with histopathology and prognosis. Hum Pathol. 1997; 28: 960-6.
18. Freire T, Medeiros A, Reis CA, et al. Biochemical characterization of soluble Tn glycoproteins from malignant effusions of patients with carcinomas. Oncol Rep. 2003; 10: 1577-85.
19. Freire T, Bay S, von Mensdorff-Pouilly S, et al. Molecular basis of incomplete O-glycan synthesis in MCF-7 breast cancer cells: putative role of MUC6 in Tn antigen expression. Cancer Res. 2005; 65: 7880-7.
20. Marcos NT, Pinho S, Grandela C, et al. Role of the human ST6GalNAc-I and ST6GalNAc-II in the synthesis of the cancer-associated sialyl-Tn antigen. Cancer Res. 2004; 64: 7050-7.
21. Pinho S, Marcos NT, Ferreira B, et al. Biological significance of cancer-associated sialyl-Tn antigen: modulation of malignant phenotype in gastric carcinoma cells. Cancer Lett. 2007; 249: 157-70.
22. Sewell R, Bäckstrm M, Dalziel M, et al. The ST6GalNAc-I sialyltransferase localizes throughout the Golgi and is responsible for the synthesis of the tumour-associated sialyl-Tn O-glycan in human breast cancer. J Biol Chem. 2006; 281: 3586-94.
23. Powlesland AS, Hitchen PG, Parry S, et al. Targeted glycoproteomic identification of cancer cell glycosylation. Glycobiology. 2009; 19: 899-909.
24. Kumar SR, Sauter ER, Quinn TP, et al. Thomsen-Friedenreich and Tn antigens in nipple fluid: carbohydrate biomarkers for breast cancer detection. Clin Cancer Res. 2005; 11: 6868-71.
25. Deutscher SL, Dickerson M, Gui G, et al. Carbohydrate antigens in nipple aspirate fluid predict the presence of atypia and cancer in women requiring diagnostic breast biopsy. BMC Cancer. 2010; 10: 519.
26. Sakamoto S, Watanabe T, Tokumaru T, et al. Expression of Lewisa, Lewisb, Lewisx, Lewisy, siayl-Lewisa, and sialyl-Lewisx blood group antigens in human gastric carcinoma and in normal gastric tissue. Cancer Res. 1989; 49: 745-52.
27. Zhou H, Schaefer N, Wolff M, et al. Carcinoma of the ampulla of Vater: comparative histologic/immunohistochemical classification and follow-up. Am J Surg Pathol. 2004; 28: 875-82.
28. Inata J, Hattori N, Yokoyama A, et al. Circulating KL-6/MUC1 mucin carrying sialyl Lewisa oligosaccharide is an independent prognostic factor in patients with lung adenocarcinoma. Int J Cancer. 2007; 120: 2643-9.
29. Sikut R, Zhang K, Baeckström D, et al. Distinct sub-populations of carcinoma-associated MUC1 mucins as detected by the monoclonal antibody 9H8 and antibodies against the sialyl-Lewis a and sialyl-Lewis x epitopes in the circulation of breast-cancer patients. Int J Cancer. 1996; 66: 617-23.
30. Burdick MD, Harris A, Reid CJ, et al. Oligosaccharides expressed on MUC1 produced by pancreatic and colon tumour cell lines. J Biol Chem. 1997; 272: 24198-202.
31. Hanski C, Drechsler K, Hanisch FG, et al. Altered glycosylation of the MUC-1 protein core contributes to the colon carcinoma-associated increase of mucin-bound sialyl-Lewis(x) expression. Cancer Res. 1993; 53: 4082-8.
32. Hanski C, Hanski ML, Zimmer T, et al. Characterization of the major sialyl-Lex-positive mucins present in colon, colon carcinoma, and sera of patients with colorectal cancer. Cancer Res. 1995; 55: 928-33.
33. Schallmeiner E, Oksanen E, Ericsson O, et al. Sensitive protein detection via triple-binder proximity ligation assays. Nat Methods. 2007; 4: 135-7.