MUC2 mucin is a major carrier of the cancer-associated sialyl-Tn antigen in intestinal metaplasia and gastric carcinomas

Glycobiology

Volumn 20, Issue 2, 2009, Pages 199-206

  Conze, Tim ^a   Carvalho, Ana Sofia ^b   Landegren, Ulf ^a   Almeida, Raquel ^b,c   Reis, Celso A ^b,c   David, Leonor ^b,c   Söderberg, Ola ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY OF PORTO   (Portugal)

^c University of Porto   (Portugal)

Author keywords

Gastric cancer; Glycosylation; In situ proximity ligation assay; Intestinal metaplasia; Sialyl Tn

Indexed keywords

MUCIN 2; TN ANTIGEN; MONOCLONAL ANTIBODY; MUC2 PROTEIN, HUMAN; SIALOSYL TN ANTIGEN; SIALOSYL-TN ANTIGEN; TUMOR ANTIGEN; TUMOR MARKER;

ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTESTINE METAPLASIA; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STOMACH CARCINOMA; BIOSYNTHESIS; CHEMISTRY; IMMUNOLOGY; INTESTINE; METAPLASIA; PATHOLOGY; STOMACH TUMOR;

ANTIBODIES, MONOCLONAL; ANTIGENS, NEOPLASM; ANTIGENS, TUMOR-ASSOCIATED, CARBOHYDRATE; HUMANS; IMMUNOHISTOCHEMISTRY; INTESTINES; METAPLASIA; MUCIN-2; STOMACH NEOPLASMS; TUMOR MARKERS, BIOLOGICAL;

EID: 77649216263     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwp161     Document Type: Article

References (66)

1. Audie JP, Janin A, Porchet N, Copin MC, Gosselin B and Aubert JP. 1993. Expression of human mucin genes in respiratory, digestive, and reproductive tracts ascertained by in situ hybridization. J Histochem Cytochem. 41:1479-1485.
2. Baeckstrom D, Hansson GC, Nilsson O, Johansson C, Gendler SJ and Lindholm L. 1991. Purification and characterization of a membrane-bound and a secreted mucin-type glycoprotein carrying the carcinoma-associated sialyl-Lea epitope on distinct core proteins. J Biol Chem. 266:21537-21547.
3. Baeckstrom D, Nilsson O, Price MR, Lindholm L and Hansson G C. 1993. Discrimination of MUC1 mucins from other sialyl-Le(a)-carrying glycoproteins produced by colon carcinoma cells using a novel monoclonal antibody. Cancer Res. 53:755-761.
4. Baeckstrom D, Zhang K, Asker N, Ruetschi U, Ek M and Hansson GC. 1995. Expression of the leukocyte-associated sialoglycoprotein CD43 by a colon carcinoma cell line. J Biol Chem. 270:13688-13692.
5. Bobek LA, Tsai H, Biesbrock AR and Levine MJ. 1993. Molecular cloning, sequence, and specificity of expression of the gene encoding the low molecular weight human salivary mucin (MUC7). J Biol Chem. 268:20563-20569.
6. Carneiro F, Amado M, David L, Clausen H and Sobrinho-Simoes M. 1994. Glycosylation features of gastric carcinoma initiation and progression. A review with emphasis on simple mucin-type carbohydrates and histo-blood group antigens of the Lewis system. Eur J Cancer Prev. 3(Suppl 2):39-46.
7. Carneiro F, David L and Sobrinho-Simoes M. 1994. Sialyl-Tn expression in gastric carcinoma. Eur J Cancer. 30A:1398-1399.
8. Carrato C, Balague C, de Bolos C, Gonzalez E, Gambus G, Planas J, Perini JM, Andreu D and Real FX. 1994. Differential apomucin expression in normal and neoplastic human gastrointestinal tissues. Gastroenterology. 107:160-172.
9. Correa P. 1988. A human model of gastric carcinogenesis. Cancer Res. 48:3554-3560.
10. Correa P. 1992. Human gastric carcinogenesis: A multistep and multifactorial process-First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res. 52:6735-6740.
11. David L, Nesland JM, Clausen H, Carneiro F and Sobrinho-Simoes M. 1992. Simple mucin-type carbohydrate antigens (Tn, sialosyl-Tn and T) in gastric mucosa, carcinomas and metastases. APMIS Suppl. 27:162-172.
12. De Bolos C, Garrido M and Real FX. 1995. MUC6 apomucin shows a distinct normal tissue distribution that correlates with Lewis antigen expression in the human stomach. Gastroenterology. 109:723-734.
13. Dufosse J, Porchet N, Audie JP, Guyonnet Duperat V, Laine A, Van-Seuningen I, Marrakchi S, Degand P and Aubert J P. 1993. Degenerate 87-base-pair tandem repeats create hydrophilic/hydrophobic alternating domains in human mucin peptides mapped to 11p15. Biochem J. 293(Pt 2):329-337.
14. Fernandez-Rodriguez J, Dwir O, Alon R and Hansson GC. 2001. Tumor cell MUC1 and CD43 are glycosylated differently with sialyl-Lewis a and x epitopes and show variable interactions with E-selectin under physiological flow conditions. Glycoconj J. 18:925-930.
15. Ferreira B, Marcos NT, David L, Nakayama J and Reis CA. 2006. Terminal alpha1,4-linked N-acetylglucosamine in Helicobacter pylori-associated intestinal metaplasia of the human stomach and gastric carcinoma cell lines. J Histochem Cytochem. 54:585-591.
16. Fredriksson S, Gullberg M, Jarvius J, Olsson C, Pietras K, Gustafsdottir SM, Ostman A and Landegren U. 2002. Protein detection using proximity-dependent DNA ligation assays. Nat Biotechnol. 20:473-477.
17. Gambus G, de Bolos C, Andreu D, Franci C, Egea G and Real FX. 1993. Detection of the MUC2 apomucin tandem repeat with a mouse monoclonal antibody. Gastroenterology. 104:93-102.
18. Gendler SJ, Lancaster CA, Taylor-Papadimitriou J, Duhig T, Peat N, Burchell J, Pemberton L, Lalani EN and Wilson D. 1990. Molecular cloning and expression of human tumor-associated polymorphic epithelial mucin. J Biol Chem. 265:15286-15293.
19. Gum JR, Byrd JC, Hicks JW, Toribara NW, Lamport DT and Kim YS. 1989. Molecular cloning of human intestinal mucin cDNAs. Sequence analysis and evidence for genetic polymorphism. J Biol Chem. 264:6480-6487.
20. Gum JR Jr, Hicks JW, Crawley SC, Dahl CM, Yang SC, Roberton AM and Kim YS. 2003. Initiation of transcription of the MUC3A human intestinal mucin from a TATA-less promoter and comparison with the MUC3B amino terminus. J Biol Chem. 278:49600-49609.
21. Hanski C, Hanski ML, Zimmer T, Ogorek D, Devine P and Riecken EO. 1995. Characterization of the major sialyl-Lex-positive mucins present in colon, colon carcinoma, and sera of patients with colorectal cancer. Cancer Res. 55:928-933.
22. Ho SB, Niehans GA, Lyftogt C, Yan PS, Cherwitz DL, Gum ET, Dahiya R and Kim YS. 1993. Heterogeneity of mucin gene expression in normal and neoplastic tissues. Cancer Res. 53:641-651.
23. Hoff SD, Matsushita Y, Ota DM, Cleary KR, Yamori T, Hakomori S and Irimura T. 1989. Increased expression of sialyl-dimeric LeX antigen in liver metastases of human colorectal carcinoma. Cancer Res. 49:6883-6888.
24. Ho JJ, Siddiki B and Kim YS. 1995. Association of sialyl-Lewis(a) and sialyl-Lewis(x) with MUC-1 apomucin in a pancreatic cancer cell line. Cancer Res. 55:3659-3663.
25. Isshiki S, Kudo T, Nishihara S, Ikehara Y, Togayachi A, Furuya A, Shitara K, Kubota T, Watanabe M, Kitajima M et al. 2003. Lewis type 1 antigen synthase (beta3Gal-T5) is transcriptionally regulated by homeoproteins. J Biol Chem. 278:36611-36620.
26. Itoh Y, Kamata-Sakurai M, Denda-Nagai K, Nagai S, Tsuiji M, Ishii-Schrade K, Okada K, Goto A, Fukayama M and Irimura T. 2008. Identification and expression of human epiglycanin/MUC21: A novel transmembrane mucin. Glycobiology. 18:74-83.
27. Itzkowitz SH, Bloom EJ, Kokal WA, Modin G, Hakomori S and Kim YS. 1990. Sialosyl-Tn. A novel mucin antigen associated with prognosis in colorectal cancer patients. Cancer. 66:1960-1966.
28. Itzkowitz SH, Bloom EJ, Lau TS and Kim YS. 1992. Mucin associated Tn and sialosyl-Tn antigen expression in colorectal polyps. Gut. 33:518-523.
29. Jarvius M, Paulsson J, Weibrecht I, Leuchowius KJ, Andersson AC, Wahlby C, Gullberg M, Botling J, Sjoblom T, Markova B et al. 2007. In situ detection of phosphorylated platelet-derived growth factor receptor beta using a generalized proximity ligation method. Mol Cell Proteomics. 6:1500-1509.
30. Karlen P, Young E, Brostrom O, Lofberg R, Tribukait B, Ost K, Bodian C and Itzkowitz S. 1998. Sialyl-Tn antigen as a marker of colon cancer risk in ulcerative colitis: Relation to dysplasia and DNA aneuploidy. Gastroenterology. 115:1395-1404.
31. Kim GE, Bae HI, Park HU, Kuan SF, Crawley SC, Ho JJ and Kim YS. 2002. Aberrant expression of MUC5AC and MUC6 gastric mucins and sialyl Tn antigen in intraepithelial neoplasms of the pancreas. Gastroenterology. 123:1052-1060.
32. Kim YS, Gum J, Jr and Brockhausen I. 1996. Mucin glycoproteins in neoplasia. Glycoconj J. 13:693-707.
33. Kjeldsen T, Clausen H, Hirohashi S, Ogawa T, Iijima H and Hakomori S. 1988. Preparation and characterization of monoclonal antibodies directed to the tumor-associated O-linked sialosyl-2-6 alpha-N-acetylgalactosaminyl (sialosyl-Tn) epitope. Cancer Res. 48:2214-2220.
34. Kobayashi H, Terao T and Kawashima Y. 1992. Serum sialyl Tn as an independent predictor of poor prognosis in patients with epithelial ovarian cancer. J Clin Oncol. 10:95-101.
35. Lan MS, Batra SK, Qi WN, Metzgar RS and Hollingsworth MA. 1990. Cloning and sequencing of a human pancreatic tumor mucin cDNA. J Biol Chem. 265:15294-15299.
36. Lapensee L, Paquette Y and Bleau G. 1997. Allelic polymorphism and chromosomal localization of the human oviductin gene (MUC9). Fertil Steril. 68:702-708.
37. Lauren P. 1965. The two histological main types of gastric carcinoma: Diffuse and so-called intestinal-type carcinoma. An attempt at a histo-clinical classification. Acta Pathol Microbiol Scand. 64:31-49.
38. Leivonen M, Nordling S, Lundin J, von Boguslawski K and Haglund C. 2001. STn and prognosis in breast cancer. Oncology. 61:299-305.
39. Ligtenberg MJ, Vos HL, Gennissen AM and Hilkens J. 1990. Episialin, a carcinoma-associated mucin, is generated by a polymorphic gene encoding splice variants with alternative amino termini. J Biol Chem. 265:5573-5578.
40. Machado JC, Nogueira AM, Carneiro F, Reis CA and Sobrinho-Simoes M. 2000. Gastric carcinoma exhibits distinct types of cell differentiation: An immunohistochemical study of trefoil peptides (TFF1 and TFF2) and mucins (MUC1, MUC2, MUC5AC, and MUC6). J Pathol. 190:437-443.
41. Marcos NT, Pinho S, Grandela C, Cruz A, Samyn-Petit B, Harduin-Lepers A, Almeida R, Silva F, Morais V, Costa J et al. 2004. Role of the human ST6GalNAc-I and ST6GalNAc-II in the synthesis of the cancer-associated sialyl-Tn antigen. Cancer Res. 64:7050-7057.
42. Meezaman D, Charles P, Daskal E, Polymeropoulos MH, Martin BM and Rose MC. 1994. Cloning and analysis of cDNA encoding a major airway glycoprotein, human tracheobronchial mucin (MUC5). J Biol Chem. 269:12932-12939.
43. Mesquita P, Jonckheere N, Almeida R, Ducourouble MP, Serpa J, Silva E, Pigny P, Silva FS, Reis C, Silberg D et al. 2003. Human MUC2 mucin gene is transcriptionally regulated by Cdx homeodomain proteins in gastrointestinal carcinoma cell lines. J Biol Chem. 278:51549-51556.
44. Morgan SM, Samulowitz U, Darley L, Simmons DL and Vestweber D. 1999. Biochemical characterization and molecular cloning of a novel endothelial-specific sialomucin. Blood. 93:165-175.
45. Nakagoe T, Sawai T, Tsuji T, Jibiki MA, Nanashima A, Yamaguchi H, Yasutake T, Ayabe H, Arisawa K and Ishikawa H. 2002. Predictive factors for preoperative serum levels of sialy Lewis(x), sialyl Lewis(a) and sialyl Tn antigens in gastric cancer patients. Anticancer Res. 22:451-458.
46. Nielsen PA, Mandel U, Therkildsen MH and Clausen H. 1996. Differential expression of human high-molecular-weight salivary mucin (MG1) and low-molecular-weight salivary mucin (MG2). J Dent Res. 75:1820-1826.
47. Pinho S, Marcos NT, Ferreira B, Carvalho AS, Oliveira MJ, Santos-Silva F, Harduin-Lepers A and Reis CA. 2007. Biological significance of cancer-associated sialyl-Tn antigen: Modulation of malignant phenotype in gastric carcinoma cells. Cancer Lett. 249:157-170.
48. Pinto-de-Sousa J, David L, Reis CA, Gomes R, Silva L and Pimenta A. 2002. Mucins MUC1, MUC2, MUC5AC and MUC6 expression in the evaluation of differentiation and clinico-biological behaviour of gastric carcinoma. Virchows Arch. 440:304-310.
49. Porchet N, Nguyen VC, Dufosse J, Audie JP, Guyonnet-Duperat V, Gross MS, Denis C, Degand P, Bernheim A and Aubert JP. 1991. Molecular cloning and chromosomal localization of a novel human tracheo-bronchial mucin cDNA containing tandemly repeated sequences of 48 base pairs. Biochem Biophys Res Commun. 175:414-422.
50. Reis CA, David L, Carvalho F, Mandel U, de Bolos C, Mirgorodskaya E, Clausen H and Sobrinho-Simoes M. 2000. Immunohistochemical study of the expression of MUC6 mucin and co-expression of other secreted mucins (MUC5AC and MUC2) in human gastric carcinomas. J Histochem Cytochem. 48:377-388.
51. Reis CA, David L, Correa P, Carneiro F, de Bolos C, Garcia E, Mandel U, Clausen H and Sobrinho-Simoes M. 1999. Intestinal metaplasia of human stomach displays distinct patterns of mucin (MUC1, MUC2, MUC5AC, and MUC6) expression. Cancer Res. 59:1003-1007.
52. Reis CA, David L, Nielsen PA, Clausen H, Mirgorodskaya K, Roepstorff P and Sobrinho-Simoes M. 1997. Immunohistochemical study of MUC5AC expression in human gastric carcinomas using a novel monoclonal antibody. Int J Cancer. 74:112-121.
53. Reis CA, David L, Seixas M, Burchell J and Sobrinho-Simoes M. 1998. Expression of fully and under-glycosylated forms of MUC1 mucin in gastric carcinoma. Int J Cancer. 79:402-410.
54. Reis CA, Sorensen T, Mandel U, David L, Mirgorodskaya E, Roepstorff P, Kihlberg J, Hansen JE and Clausen H. 1998. Development and characterization of an antibody directed to an alpha-N-acetyl-D-galactosamine glycosylated MUC2 peptide. Glycoconj J. 15:51-62.
55. Robbe-Masselot C, Herrmann A, Carlstedt I, Michalski JC and Capon C. 2008. Glycosylation of the two O-glycosylated domains of human MUC2 mucin in patients transposed with artificial urinary bladders constructed from proximal colonic tissue. Glycoconj J. 25:213-224.
56. Schallmeiner E, Oksanen E, Ericsson O, Spangberg L, Eriksson S, Stenman UH, Pettersson K and Landegren U. 2007. Sensitive protein detection via triple-binder proximity ligation assays. Nat Methods. 4:135-137.
57. Shankar V, Pichan P, Eddy RL Jr, Tonk V, Nowak N, Sait SN, Shows TB, Schultz RE, Gotway G, Elkins RC et al. 1997. Chromosomal localization of a human mucin gene (MUC8) and cloning of the cDNA corresponding to the carboxy terminus. Am J Respir Cell Mol Biol. 16:232-241.
58. Söderberg O, Gullberg M, Jarvius M, Ridderstrale K, Leuchowius KJ, Jarvius J, Wester K, Hydbring P, Bahram F, Larsson LG et al. 2006. Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods. 3:995-1000.
59. Sternberg LR, Byrd JC, Yunker CK, Dudas S, Hoon VK and Bresalier RS. 1999. Liver colonization by human colon cancer cells is reduced by antisense inhibition of MUC2 mucin synthesis. Gastroenterology. 116:363-371.
60. Toribara NW, Roberton AM, Ho SB, Kuo WL, Gum E, Hicks JW, Gum JR Jr, Byrd JC, Siddiki B and Kim YS. 1993. Human gastric mucin. Identification of a unique species by expression cloning. J Biol Chem. 268:5879-5885.
61. Wang F, Goto M, Kim YS, Higashi M, Imai K, Sato E and Yonezawa S. 2001. Altered GalNAc-alpha-2,6-sialylation compartments for mucin-associated sialyl-Tn antigen in colorectal adenoma and adenocarcinoma. J Histochem Cytochem. 49:1581-1592.
62. Werther JL, Rivera-MacMurray S, Bruckner H, Tatematsu M and Itzkowitz SH. 1994. Mucin-associated sialosyl-Tn antigen expression in gastric cancer correlates with an adverse outcome. Br J Cancer. 69:613-616.
63. Werther JL, Tatematsu M, Klein R, Kurihara M, Kumagai K, Llorens P, Guidugli Neto J, Bodian C, Pertsemlidis D, Yamachika T et al. 1996. Sialosyl-Tn antigen as a marker of gastric cancer progression: An international study. Int J Cancer. 69:193-199.
64. Wreschner DH, Hareuveni M, Tsarfaty I, Smorodinsky N, Horev J, Zaretsky J, Kotkes P, Weiss M, Lathe R, Dion A et al. 1990. Human epithelial tumor antigen cDNA sequences. Differential splicing may generate multiple protein forms. Eur J Biochem. 189:463-473.
65. Yin BW and Lloyd KO. 2001. Molecular cloning of the CA125 ovarian cancer antigen: Identification as a new mucin, MUC16. J Biol Chem. 276:27371-27375.
66. Yonezawa S, Tachikawa T, Shin S and Sato E. 1992. Sialosyl-Tn antigen. Its distribution in normal human tissues and expression in adenocarcinomas. Am J Clin Pathol. 98:167-174.